Eastern Mediterranean Health Journal [2017; Vol.23, Issue 6]

Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale Volume 23 / No. 6 June/Juin 6 ددع / نوشرعلاو ثلاثلا دلجلما ناريزح/وينوي2017 Contents V o lu m e 2 3 N u m b er 6 Ju n e 2 0 1 7 In 2015, tuberculosis still remained one of the top 10 causes of death worldwide. However, significant progress has been made in the Region over the last two decades, achieving the STOP TB Strategy target of halving the TB mortality rate since 1990. In November 2017, WHO is organizing the first global ministerial conference to support a multisectoral approach to End TB, which will take place in Moscow, Russian Federation. Editorial What would it take to eliminate tuberculosis in the Eastern Mediterranean Region? .........................................393 Research articles Surveillance of communicable diseases for decision-making in Egypt: 2006–2013 ............................................395 The relation between pica and iron deficiency in children in Zanjan, Islamic Republic of Iran: a case–control study ................................................................................................................................................ 404 Disease and treatment-related factors associated with tuberculosis treatment default in Khartoum State, Sudan: a case–control study ........................................................................................................ 408 Health labour market requirements of health professional education in Yemen .................................................415 Delays in diagnosis and treatment among children with cancer: Egyptian perspective ......................................422 Reviews The impact of antimicrobial stewardship strategies on antibiotic appropriateness and prescribing behaviours in selected countries in the Middle East: a systematic review ............................................................430 Determinants of caesarean birth on maternal demand in the Islamic Republic of Iran: a review ....................... 441 Short communication Governing the Lebanese health system: strengthening the national response to the burden of Syrian refugees ..........................................................................................................................................................449 WHO events addressing public health priorities Fostering national bioethics committees: first regional summit in the Eastern Mediterranean Region/Arab States Region ...................................................................................................................................... 453 Cover 23-06 (2).indd 5-7 8/16/2017 1:23:32 PM EASTERN MEDITERRANEAN HEALTH JOURNAL IS the official health journal published by the Eastern Mediterranean Regional Office of the World Health Organization. It is a forum for the presentation and promotion of new policies and initiatives in health services; and for the exchange of ideas, con‑ cepts, epidemiological data, research findings and other information, with special reference to the Eastern Mediterranean Region. It addresses all members of the health profession, medical and other health educational institutes, interested NGOs, WHO Col‑ laborating Centres and individuals within and outside the Region. LA REVUE DE SANTÉ DE LA MÉDITERRANÉE ORIENTALE EST une revue de santé officielle publiée par le Bureau régional de l’Organisation mondiale de la Santé pour la Méditerranée orientale. Elle offre une tribune pour la présentation et la promotion de nouvelles politiques et initiatives dans le domaine des ser‑vices de santé ainsi qu’à l’échange d’idées, de concepts, de données épidémiologiques, de résultats de recherches et d’autres informations, se rapportant plus particulièrement à la Région de la Méditerranée orientale. Elle s’adresse à tous les professionnels de la santé, aux membres des instituts médicaux et autres instituts de formation médico‑sanitaire, aux ONG, Centres collabora‑ teurs de l’OMS et personnes concernés au sein et hors de la Région. EMHJ is a trilingual, peer reviewed, open access journal and the full contents are freely available at its website: http://www/emro.who.int/emhj.htm EMHJ information for authors is available at its website: http://www.emro.who.int/emh-journal/authors/ EMHJ is abstracted/indexed in the Index Medicus and MEDLINE (Medical Literature Analysis and Retrieval Systems on Line), ISI Web of knowledge, the Cumulative Index to Nursing and Allied Health Literature (CINAHL), Embase, Lexis Nexis, Scopus and the Index Medicus for the WHO Eastern Mediterranean Region (IMEMR). © World Health Organization (WHO) 2017. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO licence (https://creativecommons.org/licenses/by-nc-sa/3.0/igo). Disclaimer. The designations employed and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of WHO concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted and dashed lines on maps represent approximate border lines for which there may not yet be full agreement. The mention of specific companies or of certain manufacturers’ products does not imply that they are endorsed or recommended by WHO in preference to others of a similar nature that are not mentioned. Errors and omissions excepted, the names of proprietary products are distinguished by initial capital letters. All reasonable precautions have been taken by WHO to verify the information contained in this publication. However, the published material is being distributed without warranty of any kind, either expressed or implied. The responsibility for the interpretation and use of the material lies with the reader. In no event shall WHO be liable for damages arising from its use. The authors alone are responsible for the views expressed in this publication and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated. If authors are staff members of the World Health Organization, the authors alone are responsible for the views expressed in this publication and do not necessarily represent the decisions, policy or views of the World Health Organization. ISSN 1020‑3397 تاسايسلا ميدقتل برنم ىهو .ةيلماعلا ةحصلا ةمظنمب طسوتلما قشرل ىميلقلإا بتكلما نع ردصت ىتلا ةيمسرلا ةلجلما ىه يرغو ثاحبلأا جئاتنو ةيئابولا تايطعلماو ميهافلماو ءارلآا لدابتلو ،اله جيوترلاو ةيحصلا تامدلخا فى ةديدلجا تاردابلماو تايلكلاو ،ةيحصلا نهلما ءاضعأ لك لىإ ةهجوم ىهو .طسوتلما قشر ميلقإب اهنم قلعتي ام ةصاخو ،تامولعلما نم كلذ دارفلأاو ةيلماعلا ةحصلا ةمظنم عم ةنواعتلما زكارلماو ،ةينعلما ةيموكلحا يرغ تماظنلما اذكو ،ةيميلعتلا دهاعلما رئاسو ةيبطلا .هجراخو ميلقلإا فى ةحصلاب ينمتهلما طسوتلما قشرل ةيحصلا ةلجلما Correspondence Editor-in-chief Eastern Mediterranean Health Journal WHO Regional Office for the Eastern Mediterranean P.O. Box 7608 Nasr City, Cairo 11371 Egypt Tel: (+202) 2276 5000 Fax: (+202) 2670 2492/(+202) 2670 2494 Email: emrgoemhj@who.int طسوتلما قشرل ةيلماعلا ةحصلا ةمظنلم ةيميلقلإا ةنجللا ءاضعأ نادلبلا ةيملاسلإا ناريإ ةيروهجم . ايبيل . سنوت . نيرحبلا . ناتسكاب . ةدحتلما ةيبرعلا تاراملإا . ناتسناغفأ . ندرلأا صرم . نانبل . تيوكلا . رطق . ينطسلف . نماُع . قارعلا . لاموصلا . نادوسلا . تيوبيج . نميلا . ةيروسلا ةيبرعلا ةيروهملجا ةيدوعسلا ةيبرعلا ةكلملما . برغلما Members of the WHO Regional Committee for the Eastern Mediterranean Afghanistan . Bahrain . Djibouti . Egypt . Islamic Republic of Iran . Iraq . Jordan . Kuwait . Lebanon Libya . Morocco . Oman . Pakistan . Palestine . Qatar . Saudi Arabia . Somalia . Sudan . Syrian Arab Republic . Tunisia . United Arab Emirates . Yemen Membres du Comité régional de l’OMS pour la Méditerranée orientale Afghanistan . Arabie saoudite . Bahreïn . Djibouti . Égypte . Émirats arabes unis . République islamique d’Iran Iraq . Libye . Jordanie . Koweït . Liban . Maroc . Oman . Pakistan . Palestine . Qatar . République arabe syrienne Somalie . Soudan . Tunisie . Yémen Subscriptions and Permissions Publications of the World Health Organization can be obtained from Knowledge Sharing and Production, World Health Organization, Regional Office for the Eastern Mediterranean, PO Box 7608, Nasr City, Cairo 11371, Egypt (tel: +202 2670 2535, fax: +202 2670 2492; email: emrgoksp@who.int). Requests for permission to reproduce, in part or in whole, or to translate publications of WHO Regional Office for the Eastern Mediterranean – whether for sale or for noncommercial distribution – should be addressed to WHO Regional Office for the Eastern Mediterranean, at the above address; email: emrgoegp@who.int. Cover 23-06 (2).indd 8-10 8/16/2017 1:23:32 PM Contents La Revue de Santé de la Méditerranée orientale Eastern Mediterranean Health Journal Vol. 23 No. 6 6 ددع نوشرعلاو ثلاثلا دلجلما• 2017 • Editorial What would it take to eliminate tuberculosis in the Eastern Mediterranean Region? Mohamed Abdel Aziz, Samiha Baghdadi and Rana Hajjeh ...................................................................................................................................................................................................... 393 Research articles Surveillance of communicable diseases for decision-making in Egypt: 2006–2013 Madiha S.M. Abdel-Razik, Hoda I.I. Rizk and Mahmoud H.M. Hassan ............................................................................................................................................................................. 395 The relation between pica and iron deficiency in children in Zanjan, Islamic Republic of Iran: a case–control study Mansour Sadeghzadeh Parisa Khoshnevisasl and Sina Sadeghzadeh ..................................................................................................................................................................................... 404 Disease and treatment-related factors associated with tuberculosis treatment default in Khartoum State, Sudan: a case–control study Ahmed O.A. Ali and Martin H. Prins ................................................................................................................................................................................................................................................. 408 Health labour market requirements of health professional education in Yemen Taha Almahbashi, Syed Mohamed Aljunid and Aniza Ismail .................................................................................................................................................................................................... 415 Delays in diagnosis and treatment among children with cancer: Egyptian perspective Suzy Abdelmabood, Shaimaa Kandil, Ahmed Megahed, Ashraf Fouda ................................................................................................................................................................................. 422 Reviews The impact of antimicrobial stewardship strategies on antibiotic appropriateness and prescribing behaviours in selected countries in the Middle East: a systematic review Ziad Nasr, Bridget Paravattil and Kyle J. Wilby ............................................................................................................................................................................................................................... 430 Determinants of caesarean birth on maternal demand in the Islamic Republic of Iran: a review Fatemeh Darsareh, Teamur Aghamolaei, Minoo Rajaei, Abdoulhossain Madani ............................................................................................................................................................... 441 Short communication Governing the Lebanese health system: strengthening the national response to the burden of Syrian refugees Alessio Santoro and Martin McKee ...................................................................................................................................................................................................................................................... 449 WHO events addressing public health priorities Fostering national bioethics committees: first regional summit in the Eastern Mediterranean Region/Arab States Region ................................ 453 Book 23-06.indb 391 8/16/2017 1:24:12 PM Mahmoud Fikri, Editor-in-chief Editorial Board Zulfiqar Bhutta Mahmoud Fahmy Fathalla Rita Giacaman Ahmed Mandil Ziad Memish Arash Rashidian Sameen Siddiqi Huda Zurayk International Advisory Panel Mansour M. Al-Nozha Fereidoun Azizi Rafik Boukhris Majid Ezzati Hans V. Hogerzeil Mohamed A. Ghoneim Alan Lopez Hossein Malekafzali El-Sheikh Mahgoub Hooman Momen Sania Nishtar Hikmat Shaarbaf Salman Rawaf Editors Phillip Dingwall Guy Penet (French) Eva Abdin, Fiona Curlet, Cathel Kerr, Marie-France Roux (Freelance) Manar Abdel-Rahman, Ahmed Bahnassy, Abbas Rahimiforoushani (Statistics) Graphics Suhaib Al Asbahi, Diana Tawadros Administration Nadia Abu-Saleh, Yasmeen Sedky, Iman Fawzy Cover designed by Diana Tawadros Internal layout designed by Emad Marji and Diana Tawadros Printed by WHO Regional Office for the Eastern Mediterranean Book 23-06.indb 392 8/16/2017 1:24:12 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 393 Editorial What would it take to eliminate tuberculosis in the Eastern Mediterranean Region? Mohamed Abdel Aziz 1, Samiha Baghdadi 1 and Rana Hajjeh 1 Twenty-five years ago, tuberculosis (TB) was declared a global health emergency by the World Health Or- ganization (WHO) (1). However, TB still remained one of the top 10 causes of death worldwide in 2015 (2). In 2014, the World Health As- sembly (WHA) had approved a new global strategy to end TB that builds on successes achieved by the DOTS and the Stop TB Strategy (3). The End TB Strategy 2016–2035 envisions a world free of TB by pursuing policies that promote prevention and care, and encourage research and innovation (4), which is in line with the Sustainable Development Goals (SDGs) calling for the TB epidemic to end by 2030 (5). In 2002, the Global Fund to fight AIDS, Tuberculosis and Malaria – a partnership between governments, civil society, private sector and patients – was launched to raise significant funds to support programmes in countries and communities most in need (6). The Eastern Mediterranean Region (EMR) covers 22 countries, many of which are facing major humanitarian crises and significant challenges in the fight to eliminate TB in the next two decades. Following the commemora- tion of World TB Day on 24 March, it is important to examine key challenges and successes from the Region, and present the strategies needed to suc- cessfully eliminate TB. In 2015, more than 10 million people globally were estimated to have developed acute TB, of whom 480 000 had drug-resistant TB (MDR-TB) and 1.4 million had died (7). In the EMR, significant progress has been made over the last two decades, with TB mortality decreasing from 38/100 000 popula- tion in 2000 to 12/100 000 in 2015, and achieving the Stop TB target of halving the mortality rate (compared to 1990) (8). Success rate for treated patients with susceptible TB reached 91% in 2016, and 68% for MDR-TB — the highest of all WHO Regions (8). However, an estimated 749 000 TB cases (116/100 000 population) still occurred in 2016, with only 63% reported, and only 21% of MDR-TB cases detected and treated (8). Experience in some countries shows that prevention and successful control of TB is feasible. Compared to 1990, in- cidence decreased drastically in 2015 in Egypt, Oman, Islamic Republic of Iran and Sudan (8). In Afghanistan, restruc- turing of the national TB programme and integrating TB treatment into pri- mary health care allowed the country to achieve most of its disease control targets (9). New diagnostic tools such as Gene-Xpert and Line probe assays are increasingly used in the Region, and their use is being scaled up mainly in Pakistan to cover most hospitals by end of 2018 (10). As for planning, most countries have updated their national strategic plan (NSP) in line with SDGs and End TB Strategy. A few countries with low disease burden are targeting TB elimination, and all countries’ key staff have been trained on the new MDR-TB management guidelines (8). Three major challenges need to be highlighted in the fight to eliminate TB in the Region: suboptimal political commitment, low case detection, and humanitarian emergencies. Although political commitment is difficult to measure, adequate human and financial resources and supportive policies can serve as indicators. The Global Fund to fight AIDS, Tuberculosis and Malaria provides significant and highly appreci- ated support to the 11 eligible countries. However, national TB programmes in most countries have insufficient staff, and except for the Gulf Cooperation Council countries (GCC) and Islamic Republic of Iran, policies mandating timely reporting of TB cases are either non-existent or rarely enforced (8). In 2015, only 30% of available funds for TB were from domestic sources, while 50% came from international sources, creating a high dependence on external donors, and is unsustainable (8). In 2015, 37% of estimated TB cases were missed or not reported. Five coun- tries are responsible for 90% of these missed cases, namely Pakistan (67%), Afghanistan (9%), Sudan (7%), Somalia (6%) and Djibouti (1%) (11). In Paki- stan, the majority of missed cases (62%) resided in Punjab Province, suggesting that targeted efforts can significantly improve regional case identification rate (11). As most unreported cases are treated in the private sector, with ques- tionable quality of drugs and regimens used, serious concerns exist about poor outcome and increased resistance. The Region has been suffering from many conflicts and major humanitarian emergencies, resulting in breakdown of public services and infrastructure, and disruption of logistic and societal 1 Department of Communicable Diseases, Prevention and Control, WHO Regional Office for the Eastern Mediterranean, Cairo, Egypt. Book 23-06.indb 393 8/16/2017 1:24:12 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 394 References 1. World Health Organization. Statement from Dr Marion Rav- iglione, WHO Director, Stop TB Department. Geneva: World Health Organization; 2017 (http://www.who.int/tb/features_ archive/mr_statement/en/, accessed 26 July 2017). 2. World Health Organization. Tuberculosis fact sheet. Geneva: World Health Organization; 2017 (http://www.who.int/me- diacentre/factsheets/fs104/en/, accessed 26 July 2017). 3. World Health Organization. Global strategy and targets for tuberculosis prevention, care and control after 2015. Geneva: World Health Organization; 2014 (http://apps.who.int/gb/ ebwha/pdf_files/EB134/B134_R4-en.pdf?ua=1, accessed 26 July 2017). 4. World Health Organization. The End TB Strategy. Geneva: World Health Organization; 2015 (http://www.who.int/tb/ strategy/end-tb/en/, accessed 26 July 2017). 5. United Nations. Sustainable Development Goal 3: Ensure healthy lives and promote wellbeing for all at all ages. New York: United Nations; 2016 (https://sustainabledevelopment. un.org/sdg3, accessed 26 July 2017). 6. The Global Fund (https://www.theglobalfund.org/en/, ac- cessed 26 July 2017). 7. World Health Organization. Definitions and reporting frame- work for tuberculosis – 2013 revision (updated December 2014). Geneva: World Health Organization; 2013 (http://apps. who.int/iris/bitstream/10665/79199/1/9789241505345_eng. pdf, accessed 26 July 2017). 8. World Health Organization. Global tuberculosis report 2016. Geneva: World Health Organization; 2016 (http://www.who. int/tb/publications/global_report/en/, accessed 26 July 2017). 9. Seddiq K, Enarson DA, Shah K, Zaeem H, Khan W. Implement- ing a successful tuberculosis programme within primary care services in a conflict area using the stop TB strategy: Afghani- stan case study Confl Health. 2014;8:3. (https://conflictand- health.biomedcentral.com/articles/10.1186/1752-1505-8-3, accessed 26 July 2017). 10. World Health Organization. Rapid diagnostic test and shorter, cheaper treatment signal new hope for multidrug-resistant tu- berculosis patients. Geneva: World Health Organization; 2016 (http://www.who.int/mediacentre/news/releases/2016/ multidrug-resistant-tuberculosis/en/, accessed 26 July 2017). 11. World Health Organization. Assessing tuberculosis under- reporting through inventory studies. Geneva: World Health Organization; 2012 (http://www.who.int/tb/publications/ inventory_studies/en/, accessed 26 July 2017). 12. Zignol M, Dean A, Falzon D, van Gemert W, Wright A, van Deun A, et al. Twenty years of global surveillance of anti-tuber- culosis drug resistance. N Engl J Med. 2016;375:1081-9 (http:// www.nejm.org/doi/full/10.1056/NEJMsr1512438#t=article, accessed 26 July 2017). 13. WHO Regional Office for the Eastern Mediterranean. Tubercu- losis control in complex emergencies. Cairo: WHO Regional Office for the Eastern Mediterranean; 2015 (http://applica- tions.emro.who.int/dsaf/EMROPUB_2015_EN_1913.pdf?ua=1, accessed 26 July 2017). networks, which has significantly affect- ed TB control. The interruption of drug supplies results in irregular drug intake by TB patients, leading to a low cure rate, high relapse rates, and increased risk of MDR-TB. The presence of many organizations providing healthcare ser- vices, including United Nations agen- cies and multiple non-governmental organizations, is helpful but can un- fortunately result in erratic and poorly coordinated care, which is often not consistent with national guidelines and can lead to suboptimal treatment and adherence. To meet the End TB Strategy objec- tives by 2030, the Region needs to reach three ambitious targets: 90% reduction in TB deaths, 80% reduction in TB in- cidence rate, and no affected families facing “catastrophic costs” due to TB. A regional strategic plan has been devel- oped based on three pillars: integrated, patient-centered care and prevention; bold policies and supportive systems; and intensified research and innovation. Midterm targets were set for 2016 – 2020, which are 40% reduction in TB deaths in each country, and 20% reduc- tion in incidence rate. Almost all EMR countries have updated their NSPs in line with the regional plan. To achieve the regional targets, notification should increase from 63% to 90% of all estimated cases and from 21% to 80% for MDR-TB by 2020. This could be achieved through better implementation of public/private mix, enforcing laws on obligatory notifica- tion of TB, rigorous contact investiga- tion, and use of new diagnostic tools for early detection. The Region should also sustain a treatment success rate at 91% or higher for all TB cases, and 65% or higher for MDR-TB by 2020, while increasing the proportion of MDR-TB treated from 78% to 100% by 2020. Major efforts are needed to ensure drug supply is available and well man- aged and that TB control activities are adequately implemented in complex emergencies (12,13). Can TB in the Region be eliminated, despite all challenges? The answer re- mains open. In November 2017, WHO is organizing the first global ministerial conference to support a multisectoral approach to End TB, which will take place in Moscow, Russian Federation. National commitment at the highest level is essential, but with strong com- mitment from donors, sound imple- mentation of strategies, and the new diagnostic techniques, the Region should be well placed to eliminate TB in 2035 and hopefully earlier. Book 23-06.indb 394 8/16/2017 1:24:13 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 395 1Department of Public Health, Faculty of Medicine, Cairo University, Cairo, Egypt (Correspondence to: Hoda I.I. Rizk: hoda.rizk@kasralainy.edu. eg). 2Central Epidemiology and Surveillance unit, Ministry of Health and Population, Cairo, Egypt. Received: 30/09/15; accepted: 01/11/16 Surveillance of communicable diseases for decision- making in Egypt: 2006–2013 Madiha S.M. Abdel-Razik 1, Hoda I.I. Rizk 1 and Mahmoud H.M. Hassan 2 Surveillance des maladies transmissibles en vue de la prise de décision en Égypte : 2006-2013 RÉSUMÉ Le système de surveillance du ministère de la Santé et de la Population égyptien fournit des données sur les maladies transmissibles à déclaration obligatoire. La présente étude avait pour objectif d’orienter la prise de décision visant à réduire la charge des maladies transmissibles en Égypte au moyen de l’analyse des données de surveillance entre 2006 et 2013, ainsi qu’à identifier les tendances de l’incidence des maladies par gouvernorat, saison, âge et sexe. Les scores de l’indice de risque composite ont permis de classer les 27 gouvernorats égyptiens en trois groupes : risque élevé, risque modéré, risque faible. Les 15 maladies ayant l’incidence la plus élevée était les maladies d’origine alimentaire et les maladies à transmission hydrique (cinq maladies), les maladies à prévention vaccinale (sept maladies) et d'autres maladies, telles que l’infection à hépatite C. La diarrhée sanglante et la typhoïde avaient l’incidence la plus élevée entre 2006 et 2013. On comptait 11 gouvernorats à haut risque, et Ismaïlia affichait le score d’indice de risque le plus élevé. Les résultats suggèrent un besoin d’interventions spécifiques en matière d’assainissement de l’environnement, ainsi que l’amélioration des programmes de vaccination des enfants, en particulier dans les gouvernorats à haut risque. 2013-2006 :صرم في رارقلا عنص ضارغلأ ةيراسلا ضارملأا دصرت نسح دوممح ،قزر ىده ،قزارلا دبع ةيحدم فدـلها لـّثتمو .اـهنع غاـبلإا يـغبني يـتلا ةيراـسلا ضارـملأا نـع تاـنايب ةـيصرلما ناكـسلاو ةـحصلا ةرازو في دـصترلا ماـظن رـّفوي :ةـصلالخا لاـ خ نـ م كـ لذو صرـ م في ةيراـ سلا ضارـ ملأا ءبـ ع ضـ فخ لـ جأ نـ م رارـ قلا ذاـ تخا ضارـ غلأ تاـ مولعم رـ فوت في ةـ ساردلا هذـ ه نـ م مـسولماو ةـظفاحلما بـسح ةمـسقم ضارـملأاب ةـباصلإا في ةـماعلا تاـهاتجلاا دـيدتحو ،2013 - 2006 نـب اـم ةترـفلل دـصترلا تاـنايب لـيلتح ثاـث لىإ ةـظفامح 27 اـهددع غـلابلا ةـيصرلما تاـظفاحلما فـينصت لىإ بـكرلما رـطاخلما شرؤـم تاـجرد تارـيدقت تراـشأو .سـنلجاو رـمعلاو :ةــ باصلإا تلادــ عم ىــ عأ تلجــ س يــ تلا شرــ ع ةــ سملخا ضارــ ملأا تءاــ جو .ةــ ضفخنمو ةطــ سوتمو ةــ عفترم :رــ طاخلما بــ سح تاــ عوممج ضارـمأو )ضارـمأ ةعبـس( مـيعطتلاب اـهنم ةـياقولا نـكمي يـتلا ضارـملأاو ،)ضارـمأ ةـسخم( هاـيلماب ةـلوقنلما ضارـملأاو ةـيئاذغلا ضارـملأا .2013-2006 نـب اـم ةترـفلا في ةـباصلإا تلادـعم ىـعأ دوـفيتلاو يوـمدلا لاهـسلإا لجـسو .C دـبكلا باـهتلا سورـف ىودـع لـثم ىرـخأ ءارـجإ ةروضر لىإ جـئاتنلا رـشتو .رـطاخلما شرؤـم ىـع ةـجرد ىـعأ ةيليعاـسلإا ةـظفامح تلجـس ،رـطاخلما ةـعفترم ةـظفامح 11 نـب نـمو .رـطاخلما ةـيلاعلا تاـظفاحلما في ايـس لا ،لاـفطلأا مـيعطت جـمارب نـستحو يـئيبلا حاـحصلإاب قـلعتت ةددـمح تاـخدت ABSTRACT The Egyptian Ministry of Health and Population surveillance system provides data about notifiable communicable diseases. This study aimed to provide information for decision-making to reduce the burden of communicable diseases in Egypt by analysis of the surveillance data for 2006–2013 to identify trends in the incidence of the diseases by governorate, season, age and sex. Composite risk-index scores were estimated to rank the 27 Egyptian governorates into 3 groups: high, medium and low risk. The 15 diseases with the highest incidence were food and waterborne diseases (5 diseases), vaccine-preventable diseases (7 diseases) and others, e.g. hepatitis C infection. Bloody diarrhoea and typhoid had the high incidence for 2006–2013. There were 11 high-risk governorates; Ismailia had the highest risk-index score. The findings suggest the need for specific interventions related to environmental sanitation and improving the childhood immunization programme, particularly in the high-risk governorates. Book 23-06.indb 395 8/16/2017 1:24:13 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 396 Introduction Public health surveillance is one of the essential features of epidemiological practice. It provides the scientific and factual data essential to allow public health practitioners to assess and moni- tor population health and make recom- mendations for action (1). As a result, decision-makers are able to set policies and strategies for public health preven- tion and control programmes for com- municable diseases (2). Promoting the use of information in decision-making is pivotal for managing infectious diseases at national and international levels (3). The final link in the surveillance chain is the application of data for prevention and control. Therefore, the main purpose of public health surveil- lance is to provide actionable health information to public health staff, gov- ernment leaders and the public to guide public health policy and programmes towards specific actions. Public health surveillance can also be used to assess public health status, provide early warn- ing of outbreaks, define public health priorities, design and plan public health programmes, evaluate interventions and conduct research studies (4,5). A surveillance system for communi- cable diseases has been in operation in Egypt for about a century with frequent interventions for improvement being made during this period (6). In 1999, in collaboration with the World Health Organization (WHO), United States Naval Medical Research Unit No. 3 and the Center for Disease Control and Prevention, Atlanta, United States of America, a comprehensive surveillance system was developed to collect infor- mation on 26 notifiable communicable diseases for the purpose of their control (7). In 2006, the Central Epidemiology and Surveillance Unit of the Ministry of Health and Population (MoHP) in Egypt developed an electronic system for reporting those diseases (National Electronic Disease Surveillance Sys- tem); as a result, the list of diseases under surveillance changed in view of the identified pattern of diseases (8). Other surveillance systems for specific communicable diseases are operating in Egypt, such as sentinel surveillance for influenza like illness and severe acute respiratory infection (9) and a vertical programme for tuberculosis, HIV/AIDs and malaria. The vertical surveillance programmes are included as sources of data for the communicable disease surveillance system (10). The annual reports on communi- cable diseases published by the MoHP provide a large amount of data and information about selected communi- cable diseases (11). The reports pro- vide background on the activities of the MoHP for prevention and control of those diseases. In addition, the reports show trends over time for different dis- eases at the national level. However, the reports do not provide information about the pattern of communicable dis- eases by: month, age and sex of cases, and governorate. Furthermore, there is no feedback to governorates about the level of risk of the various communica- ble diseases in the governorate so as to allocate resources to high–risk areas. The aim of this study therefore was to provide information in those areas and identify the priority areas for intervention, with the overall goal of re- ducing the incidence of communicable diseases in Egypt. The specific objectives were to: 1. Describe the epidemiological pro- file (person, time and place) for the 15 communicable diseases with the highest incidence in Egypt (2006– 2013) 2. Categorize the governorates in Egypt according to their incidence of the 15 diseases as high, medium or low risk. Methods Study setting and design The study was conducted in the Central Epidemiology and Surveillance Unit of the MoHP and was a retrospective review of communicable disease sur- veillance data from 2006 to 2013 by age, sex and governorate. Data collection and management The MoHP National Electronic Dis- eases Surveillance System for Commu- nicable Diseases (2006–2013) was the source of the data on cases of communi- cable diseases. Cases are date-stamped based on the date of notification. The 2007–2014 reports of the Central Agency for Public Mobilization and Statistics were the source of total popu- lation data per year per governorate, and the population data by age and sex (12). The 27 governorates in Egypt are categorized into 4 types: urban (Al- exandria, Cairo, Port Said and Suez); Lower Egypt (Beheira, Dakahlia, Dami- etta, Gharbia, Ismailia, Kafr El–Sheikh, Menoufia, Qalyubia and Sharqia); Up- per Egypt (Assiut, Aswan, Beni Suef, Fayoum, Giza, Luxor, Minia, Qena and Sohag); and Frontier Governorates (Matrouh, New Valley, North Sinai, Red Sea and South Sinai). All communicable disease surveil- lance data for the year 2006 for all Egypt were reviewed (160 861 records) to identify the 15 communicable diseases with the highest incidence (Table 1). The surveillance data for these 15 dis- eases for the 8-year period 2006–2013 for the 27 governorates of Egypt were then reviewed and analysed (361 055 records). Data were entered into Excel, version 2010. The incidence of each disease was estimated by year, age (< 15 and ≥ 15 years), sex, month and governorate. Total case rates (crude rates without categorization by age, sex or governorate) are given per 100 000 Book 23-06.indb 396 8/16/2017 1:24:13 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 397 persons (the number of reported cases divided by the mid–year population for that year multiplied by 100 000). Governorates were ranked (1–27) according to the incidence rate for each year over the period 2006–2013. The incidence rates per 100 000 persons for each year from 2006 to 2013 were ranked (1–27), which represented a score for communicable disease risk. Score 1 was given to the governorate with the lowest incidence in a specific year and score 27 to the governorate with the highest incidence. The magnitude of the communica- ble disease burden for each governorate was further measured and ranked ac- cording to an estimated composite risk index that considered time (8 years) and all 15 diseases. First, the risk index score for 15 diseases was calculated for each governorate by summing its ranking scores for each disease. The maximum risk index for a governorate for the 15 disease was therefore 405, assuming a ranking score of 27 for all the diseases (15 × 27). The composite risk index score for each governorate was calculated as a percentage of the maximum risk index level (405) to give the magnitude of risk for each governo- rate. Based on the composite risk index percentages, the governorates were categorized into 3 risk groups: high, medium and low. To determine the cut-off points for the groups, the range of the composite risk–index score was divided by 3; this was added to the low- est limit, to get the range of the lowest risk governorates and so on. Ethical considerations The study was approved by the Coun- cil of the Public Health Department, Faculty of Medicine, Cairo University, and MoHP staff. The data on reported cases in the surveillance records are anonymous. Results With total records for year 2006 (160 861 records), the diseases with lowest incidence were excluded from the study and 58 079 records were included. The excluded records were for the following diseases: encephalitis, HIV/AIDs, diphtheria, malaria, plague, tetanus neonatorum, acute food poi- soning, botulism, viral haemorrhagic fever, Rift Valley Fever, cholera, swine flu, anthrax, pertussis, schistosomiasis, leprosy, fascioliasis, filariasis, and animal bites. The 15 diseases with the highest incidence in 2006 were: undifferenti- ated acute hepatitis, bloody diarrhoea (dysentery), typhoid/paratyphoid, brucellosis, hepatitis A, tuberculosis, rubella, meningitis, hepatitis C, measles, rabies, acute flaccid paralysis, hepatitis B, avian influenza and mumps. Trend in incidence of the 15 communicable diseases, 2006–2013. The diseases were grouped into 5 categories: 1) undifferentiated (acute hepatitis); 2) food- and waterborne infections without preventable vac- cines (bloody diarrhoea/dysentery and brucellosis), foodborne infections with preventable vaccines (acute flac- cid paralysis/poliomyelitis (compul- sory immunization to children) and typhoid fever (compulsory TAB vac- cine for food handlers and hepatitis A Table 1 Incidence per 100 000 population of the top 15 notifiable communicable diseases in Egypt, 2006−2013 Communicable disease 2006 Rank 2006 2007 2008 2009 2010 2011 2012 2013 Mean Rank 2006- 2013 Undifferentiated acute hepatitis 17.8 15 7.9 12.6 6.9 7.5 5.0 6.3 6.4 8.8 13 Bloody diarrhoea (dysentery) 16.8 14 13.9 17.8 14.6 16.1 13.3 9.8 7.4 13.7 15 Typhoid/paratyphoid 12.7 13 9.8 10.5 10.3 7.9 6.5 6.9 7.2 9.0 14 Brucellosis 8.7 12 6.9 7.4 5.5 4.7 4.5 6.1 5.0 6.1 12 Hepatitis A 4.3 11 2.2 2.7 5.5 1.8 1.4 3.6 3.7 3.2 9+ Tuberculosis 4.1 10 2.9 4.1 3.1 3.4 2.6 3.9 3.6 3.5 10 Rubella 3.9 9 14.4 1.5 0.1 0.1 0.1 0.1 0.1 2.5 8 Meningitis 3.3 8 2.2 2.5 1.8 1.7 1.5 2.0 1.8 2.1 7 Hepatitis C 2.4 7 1.2 1.1 1.8 0.5 0.5 0.5 0.6 1.1 4 Measles 2.0 6 4.2 1.1 0.4 0.3 0.4 0.9 1.0 1.3 6 Rabies 1.7 5 0.8 0.2 0.1 0.1 0.2 0.0 0.1 0.4 2 Acute flaccid paralysis 0.9 4 0.8 0.9 0.7 0.9 0.8 0.9 0.9 0.9 3 Hepatitis B 0.8 3 0.3 0.3 0.7 0.2 0.2 0.2 0.2 0.4 1 Avian influenza 0.7 2 1.7 1.9 4.6 0.4 0.3 0.4 0.2 1.3 5 Mumps 0.7 1 0.6 0.5 0.2 0.2 0.5 15.2 22.2 5.0 11 Total 5.4 4.7 4.3 3.8 3.1 2.5 3.8 4.0 3.9 Book 23-06.indb 397 8/16/2017 1:24:13 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 398 Ta bl e 2 S um m ar y of th e ra nk o rd er o f g ov er no ra te s by c om po si te ri sk in de x of c om m un ic ab le d is ea se s, E gy pt , 2 0 0 6− 20 13 G ov er no ra te U nd if- fe re nt i- at ed a cu te he pa ti ti s Bl oo dy di ar rh oe a (d ys en te ry ) Ty ph oi d/ pa ra ty ph oi d Br uc el lo si s H ep at it is A Tu be rc ul os is Ru be lla M en in gi ti s H ep at i- ti s C M ea sl es Ra bi es A cu te fla cc id pa ra ly - si s H ep at i- ti s B A vi an in flu - en za M um ps To ta l sc or e C om - po si te ri sk in de x (% ) Is m ai lia 15 10 27 14 19 26 24 21 9 26 7 20 21 21 26 28 6 71 M at ro uh 22 3 19 20 6 27 23 23 17 27 2 22 20 9 18 25 8 64 M en ou fia 21 7 18 26 18 3 11 27 16 16 24 16 12 24 13 25 2 62 Be he ira 18 19 21 25 17 16 16 22 19 10 16 7 17 18 7 24 8 61 Ka fr El -S he ik h 11 27 14 17 14 17 12 13 21 17 20 19 9 25 4 24 0 59 Sh ar qi a 6 8 23 19 16 7 13 26 11 19 22 26 8 20 12 23 6 58 A ss iu t 17 12 16 18 1 25 8 24 26 4 25 9 26 6 19 23 6 58 G iz a 14 22 2 15 10 15 18 18 23 21 10 17 16 13 22 23 6 58 M in ia 3 4 22 27 12 19 6 19 13 15 23 27 13 23 9 23 5 58 Q al yu bi a 13 21 24 23 13 10 19 10 15 14 11 15 15 16 16 23 5 58 Su ez 25 24 20 7 27 12 22 17 18 2 6 1 18 11 21 23 1 57 C ai ro 12 25 1 5 25 8 15 16 20 23 12 3 24 14 25 22 8 56 G ha rb ia 19 11 6 16 4 13 17 25 7 18 14 25 5 27 15 22 2 55 D am ie tta 27 9 15 12 8 18 27 8 4 24 3 14 1 26 24 22 0 54 D ak ah lia 9 14 10 10 24 21 20 1 22 8 19 18 14 22 3 21 5 53 N ew V al le y 26 18 26 22 21 9 14 2 27 9 1 5 22 1 11 21 4 53 So ut h Si na i 7 26 8 2 22 5 7 20 25 12 13 12 23 2 27 21 1 52 Q en a 8 15 12 9 20 24 1 6 12 5 26 23 25 17 6 20 9 52 A le xa nd ria 1 2 3 13 26 23 26 7 24 7 8 4 27 19 17 20 7 51 Fa yo um 10 5 4 24 5 14 10 14 14 11 27 24 11 12 2 18 7 46 N or th S in ai 16 20 5 3 3 1 21 15 3 25 18 21 2 4 23 18 0 44 A sw an 24 17 7 8 9 11 9 9 8 6 9 13 19 10 20 17 9 44 Be ni S ue f 5 16 11 21 7 6 2 12 10 22 21 10 7 5 10 16 5 41 Po rt S ai d 20 1 13 4 23 20 25 3 1 20 4 11 3 7 5 16 0 40 So ha g 2 13 9 11 2 22 5 11 6 3 17 6 10 15 8 14 0 35 Re d Se a 4 23 17 1 15 4 4 5 2 13 15 2 6 3 14 12 8 32 Lu xo r 23 6 25 6 11 2 3 4 5 1 5 8 4 8 1 11 2 28 To ta l h ig h ris k 16 5 15 7 20 6 21 1 15 3 17 7 17 2 22 0 18 8 17 1 16 6 17 9 17 5 18 6 16 7 26 93 44 % 42 % 54 % 56 % 40 % 47 % 46 % 58 % 50 % 45 % 44 % 47 % 46 % 49 % 44 % 47 % Re d = hi gh ri sk ; y el lo w = m ed iu m ri sk ,; gr ee n = lo w ri sk . Book 23-06.indb 398 8/16/2017 1:24:13 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 399 virus vaccination for at–risk groups); 3) droplet infections with preventable vac- cines (tuberculosis, rubella, meningitis, measles, mumps) and droplet infections without preventable vaccines (avian in- fluenza); 4) bloodborne infections with preventable vaccines (hepatitis B) and bloodborne infections without prevent- able vaccines (hepatitis C virus); and 5) contact infection with preventable vaccines (rabies). As can be seen from the table, the 3 diseases with the high- est incidence rates in 2006 were undif- ferentiated hepatitis (17.8/100 000), bloody diarrhoea (16.8/100 000) and typhoid fever (12.7/100 000). In ad- dition, these 3 diseases had the highest mean incidence throughout the 8-year period, 2006–2013. Mumps emerged as a health problem in 2012 (incidence 15.2/100 000) with a further increase in the reported cases in 2013 (incidence 22.2/100 000 population). The top 5 diseases for 2006 were undifferentiated acute hepatitis, bloody diarrhoea (dysentery), typhoid, bru- cellosis and hepatitis A. Together they accounted 60.3 cases/100 000 popula- tion in 2006 and 29.7 cases/100 000 in 2013 with an estimated reduction in incidence of 51%. Indeed throughout the period 2006–2013, bloody diar- rhoea and typhoid/paratyphoid ranked the first and second diseases with the highest incidence The diseases categorized as prevent- able because there is compulsory im- munization of children against were: tuberculosis, rubella, measles, acute flac- cid paralysis, and hepatitis B. (Although mumps has a compulsory vaccination, we categorized it as re-emerging dis- eases because in 2006 its incidence was < 1 per 100 000 but in 2012 and 2013 it was 15.2 and 22.2 per 100 000 respectively). The estimated combined incidence rate of these diseases was 11.7 cases/100 000 in 2006 and 5.8 cases/100 000 in 2013, an estimated reduction in incidence of 50%. Incidence of the 15 communicable diseases by governorate, 2006–2013 Table 2 shows the Egyptian governo- rates ranked according to the magni- tude of the incidence of the 15 diseases for 2006–2013 and their composite risk index scores. For comparative purposes, the composite index score was assigned a risk status: green = low risk, yellow = medium risk and red = high risk. To divide the set of data into 3 groups the range of composite risk–index score was divided by 3 (71–28%/3 = 14%). Adding 14% to the lowest limit (i.e. 28%), the lowest risk governorates had composite index score of 28–28%/3 = 14%). Adding 14% to the lowest limit (i.e. 28%), the lowest risk governorates had composite index score of 28–42% (5 governorates). The medium risk governorates had composite risk index scores between 42% and 56% (11 gov- ernorates). The high risk governorates had composite risk index scores be- tween 57% and 71% (11 governorates). Ismailia governorate had the highest composite risk index for communicable diseases (71%), followed by Matrouh (a frontier governorate with very low population density), Menoufia, and Be- heira. Luxor had the lowest composite risk index (28%). The total risk score for communicable diseases for the 27 governorates was 5670 and the risk score for the 11 high-risk governorates (41% of governorates) was 2693, i.e. 47% of total risks for all the Egyptian governorates. Therefore efforts directed at the high–risk governorates could reduce the risk of infectious diseases by 47% (from 40% for hepatitis A to 58% for meningitis). Table 3 shows the epidemiological pattern of the 15 diseases according to age and sex of the cases, governorate and month. The cases were categorized by age into 2 groups: young dependent group < 15 years and older group ≥ 15 years. The incidence rates of undif- ferentiated acute hepatitis, bloody diar- rhoea, hepatitis A, meningitis, measles, acute flaccid paralysis and mumps were higher in the younger group < 15 years. The incidence rates of typhoid, brucel- losis and tuberculosis were higher in the older group ≥ 15 years. The reported in- cidence rates for 9 diseases were higher for males than females. A higher propor- tion of cases were in the summer and early autumn months. The incidence of most of the diseases decreased over time, the incidence of tuberculosis and acute flaccid paralysis was unchanged, and the incidence mumps increased. Figure 1 shows that throughout the period 2006–2013 there was an overall decline in the incidence of communica- ble diseases in Egypt. Discussion Our study addresses health policy, health systems, programmatic and com- munity issues related to the epidemiol- ogy of communicable diseases in Egypt. The study capitalized on the available data in a well-established surveillance system in the MOHP. This allowed us to provide public health information related to place, person and time (health informatics) (13). The study empha- sizes the importance of using country data after processing and aggregation of indicators for public health decision- making, a method advocated in other studies (14). This systematic processing of national level data allows informa- tion to be disseminated to the service providers involved in reporting cases to the surveillance system (15). This could prepare them to anticipate rather than react to an outbreak. Furthermore, simulation tools that use environmen- tal, epidemiological and molecular (related to microbiology, genetics and vaccine preparations) data could help manage and analyse risks and inform appropriate actions by public health authorities (16). Our study described the situ- ation in Egypt regarding the com- m u n i c a b l e d i s e a s e s w i t h t h e Book 23-06.indb 399 8/16/2017 1:24:13 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 400 Ta bl e 3 In ci de nc e of 1 5 co m m un ic ab le d is ea se s in E gy pt in 2 0 13 b y ag e an d se x, a nd b y tr en d 20 0 6– 20 13 D is ea se Se x, 20 13 A ge g ro up (y ea rs ), 20 13 M on th s (2 0 0 6– 20 13 )5 Tr en d ov er ti m e6 G ov er no ra te w it h th e hi gh es t ri sk s co re s fo r th e di se as e (2 0 0 6– 20 13 ) M al e1 Fe m al e2 < 15 3 ≥ 15 4 Ja n Fe b M ar A pr il M ay Ju ne Ju ly A ug Se p O ct N ov D ec U nd iff er en tia te d ac ut e he pa tit is 7 5 11 .0 5. 0 ↓ D am ie tta Bl oo dy d ia rr ho ea (d ys en te ry ) 7 8 11 .0 5. 7 ↓ Ka fr El sh ei k Ty ph oi d/ pa ra ty ph oi d 7 7 3. 3 9. 7 ↓ Is m ai lia Br uc el lo si s 6 4 1.0 8. 0 ↓ M in ia H ep at iti s A 4 3 6. 3 1.7 ↑ Su ez Tu be rc ul os is 5 2 0 .3 6. 7 ← ® M at ro uh Ru be lla 0 .1 0 .1 0 .4 0 .0 ↓ D am ie tta M en in gi tis 2 1 4. 7 1.7 ↓ M en ou fia H ep at iti s C 0 .8 0 .4 0 .0 1.3 ↓ N ew V al le y M ea sl es 1 1 3. 3 0 .3 ↓ M at ro uh Ra bi es 0 .1 0 .0 0 .1 0 .0 ↓ Fy ou m A cu te fl ac ci d pa ra ly si s 1 1 3. 3 0 .0 ← ® M in ia H ep at iti s B 0 .3 0 .1 0 .0 0 .3 ↓ A le xa nd ria A vi an in flu en za 0 .2 0 .3 0 .2 0 .4 ↓ G ha rb ia M um ps 28 16 30 .3 9. 7  So ut h Sa in i 1 N o. o f c as es /1 00 0 00 m al es ; 2 N o. o f c as es /1 00 0 00 fe m al es ; 3 N o. o f c as es /1 00 0 00 < 15 y ea rs ; 4 N o. o f c as es /1 00 0 00 ≥ 15 y ea rs ). 5 T he b la ck b lo ck s s ho w th e m on th s w ith th e re po rt ed h ig he st in ci de nc e of th e di se as e th ro ug ho ut 2 00 6− 20 13 . 6 ↓ D ec re as e, ↑ In cr ea se , ← ® U nc ha ng ed ,  R e- em er gi ng . Book 23-06.indb 400 8/16/2017 1:24:13 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 401 highest reported incidence from 2006 to 2013. Compared with the list of cata- strophic infectious diseases (17) (i.e. plague, viral haemorrhagic fevers, mea- sles, smallpox, yellow fever, influenza, cholera, sleeping sickness, HIV, severe acute respiratory syndrome and dengue haemorrhagic fever), only measles and influenza were among the 15 communi- cable diseases with the highest reported incidence in Egypt in the past 8 years. Our list of the top 15 communicable diseases is specific to Egypt in a certain time period. Other countries have dif- ferent priority communicable diseases. For example, the health statistical year book in Saudi Arabia, which includes information about 30 notifiable com- municable diseases, showed that the top reported communicable diseases in 2011 in Saudi Arabia were chickenpox, hepatitis B, brucellosis, dengue fever, hepatitis C, amoebic dysentery, salmo- nellosis, measles and hepatitis A (18). In Jordan in 2008, the top reported com- municable diseases were chickenpox, animal bites, non-meningococcal men- ingitis, hepatitis A, food poisoning, cu- taneous leishmaniasis, mumps, bloody diarrhoea, schistosomiasis and measles (19). In Oman, for the period 2006– 2012, the top reported communicable diseases were influenza-like illness, fe- ver and rash illnesses, malaria, mumps, hepatitis A, food poisoning, unspecified viral hepatitis, pertussis and HIV/AIDS (20). In Lebanon, the top reported communicable diseases in 2012 were hepatitis A, typhoid fever, food poison- ing, dysentery, meningitis, hepatitis B, brucellosis, pertussis, hepatitis C and malaria (21). The top 5 communicable disease in Egypt (Table 1) were related to in- sanitary water and food supply, with the exclusion of mumps which was a re-emerging disease in 2012–2013 (22). This highlights the need for a mul- tispectral approach to the prevention of communicable diseases. A number of the reported diseases are preventable because there is a compulsory immu- nization programme for children; these include tuberculosis, rubella, measles, mumps, acute flaccid paralysis and hep- atitis B (23). Their high incidence high- lights 2 challenging issues: obstacles for the health system to reach and provide coverage of children with effective vac- cines at the primary health care level, and increasing the demand for compul- sory immunization at the community level. The observed high incidence rates of mumps in 2012 (15.2/100 000) and 2013 (22.2/100 000) after years of low incidence is of concern. The re-emer- gence of such infections pose a threat at both national and international levels and is an issue that has been discussed within the concept of the global burden of infectious diseases (24). The use of modelling in public health to compare interventions and costs is helpful to guide policy-making (25). Our study suggests that modelling could include 2 major interventions: strengthening the immunization system and improving water and food sanita- tion. The results of our study provide evidence of the epidemiology of com- municable diseases in Egypt regarding trend, place and person and seasonal variations, and highlight the importance of using different methods to guide decision-making towards specific prior- ity areas for intervention. The ranking method in the current study was used to develop composite risk indices. Such methods for ranking communicable diseases have been considered in other studies (26,27). A systematic review that provided an evidence-based frame- work for identifying priority health interventions added an economic 5.4 4.7 4.3 3.8 3.1 2.5 3.8 4.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 2006 2007 2008 2009 2010 2011 2012 2013 In ci d en ce p er 1 0 0 0 0 0 p op ul at io n Figure 1 Trend in incidence (number of cases per 100 000 population) of 15 communicable diseases in Egypt 2006–2013 Book 23-06.indb 401 8/16/2017 1:24:13 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 402 References 1. Gilbert R, Cliiffe SJ. Public health surveillance. In: Regmi K, Gee I, editors. Public health intelligence: issues of measure and method. Switzerland: Springer; 2016:91–110. 2. German RR, Lee LM, Horan JM, Milstein RL, Pertowski CA, Waller MN; Guidelines Working Group Centers for Disease Control and Prevention (CDC). Updated guidelines for evalu- ating public health surveillance systems: recommendations from the Guidelines Working Group. MMWR Recomm Rep. 2001;50(RR-13):1–35. 3. Mphande FA. Infectious diseases and rural livelihood in devel- oping countries. Singapore: Springer; 2016. 4. Thacker SB. Historical Development. In: Teutsch SM, Churchill RE, editors. Principles and Practice of Public Health Surveil- lance. 2nd ed. Oxford: Oxford University Press; 2000. 5. Abdallah S, Panjabi R. Epidemiology and surveillance. In: Rand EC, editor. The Johns Hopkins and Red Cross Red Crescent: public health guide for emergencies. 2nd ed. Geneva: Inter- national Federation of Red Cross and Red Crescent Societies; 2008:220–69 6. Preventive health instructions. Cairo: Ministry of Health and Population; 2001 [In Arabic]. 7. Periodic bulletin of Egyptian notifiable communicable disease surveillance. Cairo: Ministry of Health and Population; 2012 [In Arabic]. 8. National guidelines for communicable disease surveillance, NEDSS. Cairo: Ministry of Health and Population; 2006 [In Arabic]. 9. Centers for Disease Control and Prevention. Influenza Division International Program: Arab Republic of Egypt; 2011. (http:// www.cdc.gov/flu/pdf/international/program/egypt.pdf, ac- cessed 2 April 2017). 10. Mankoula WA, Omara MA, Abdelwahab M, Kandil Y, Etman A, Amin M, et al. [Rapid assessment of the National Egyptian Disease Surveillance System. NEDSS.] Cairo: Ministry of Health and Population; 2012 [In Arabic]. 11. Communicable disease annual bulletin. 6th issue, Cairo: Central Agency for Public Mobilization and Statistics; 2013 [In Arabic]. 12. Statistical year books, Egypt (9 books). Cairo: Central Agency for Public Mobilization and Statistics (CAPMAS); 2007–2014. parameter, especially useful in low and middle income countries (28). Our study added another dimen- sion to the surveillance system by grouping the governorates into high, medium and low risk for the priority communicable diseases. We identified the governorates with the highest bur- den of communicable diseases. These 11 governorates comprise 51% of the Egyptian population. This information could help policy-makers direct efforts to reducing the burden in these gover- norates and this could reduce the risk of infectious diseases in Egypt by 47% (range 40–58%). Ismailia was the governorate with the highest risk index and hence the governorate that should have the high- est priority for interventions to reduce the incidence of communicable dis- eases. Ismailia is one of the lower Egypt governorates and lies between Port Said and Suez. Certain environmental parameters could explain why it has a higher risk than other Suez Canal cities (Port Said and Suez) (29). Half of the population of Ismailia lives in rural ar- eas, while Port Said and Suez are urban governorates. Ismailia has no access to either the Mediterranean Sea (as Port Said) or the Red Sea (as Suez). It is situated on El-Temsah Lake, where un- managed sewage is disposed of and fish- ing takes place. Adding sewage with rich organic matter that consumes oxygen to the salt lake could cause fish to die; these are then easy to collect and are widely consumed. In our study, Ismailia was ranked the highest risk governorate for reported cases of typhoid/paratyphoid throughout the period 2006–2013. These findings indicate a persistence of an environmental risk of infection. Governors of the 27 governorates and health authorities involved in the surveillance programme at all levels could use the information derived from our study to direct interventions to re- duce the incidence of these 15 diseases and the overall burden of communica- ble diseases in Egypt. There are some limitations to our study. Findings derived from the study on the ranking of communicable diseas- es by severity or incidence rate cannot be generalized outside of Egypt to other countries However, the methodology could be replicated in other countries. The data included in our analysis are de- rived from MoHP surveillance system. The accuracy of the reporting of the notifiable diseases according to the set diagnosis depends on the efficiency and effectiveness of the surveillance system in monitoring data at the peripheral and central levels. The surveillance systems capture cases occurring and reported to the health authorities. Some cases of disease are not reported to the public health authorities (under-reporting). The pattern of this underreporting var- ies by disease and governorate; it is a complex mix of health care-seeking behaviour, access to health services, re- porting practices by doctors and others, and the performance of the surveillance system at the local level. Conclusion Proper analysis and presentation of sur- veillance data are essential in order to provide meaningful information neces- sary for decision-making so as to prevent and control communicable diseases at central and governorate levels. Our analysis suggests the need for specific interventions related to environmental sanitation and improving the childhood immunization programme. Funding: None. Competing interests: None declared. Book 23-06.indb 402 8/16/2017 1:24:14 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 403 13. Haque SN, Dixon BE, Grannis SJ. Public health informatics. In: Finnell JT, Dixon B, editors. Clinical informatics study guide: text and review. Switzerland: Springer International Publishing; 2016:501–20. 14. Rothwell CJ, Freedman MA, Weed JA. The national vital statistics system. In: Magnuson JA, Fu Jr PC, editors. Public health informatics and information systems. London: Springer; 2014:309–27. 15. Thomas RK. In sickness and in health: disease and disability in contemporary America. New York: Springer; 2016:51–70. 16. Han BA, Drake JM. Future directions in analytics for infectious disease intelligence: Toward an integrated warning system for emerging pathogens. EMBO Rep. 2016;17(6):785–9. 17. Mphande FA. Infectious diseases and rural livelihood in devel- oping countries. Singapore: Springer; 2016:35–53. 18. Ministry of Health, Saudi Arabia. Health statistical year book; 2011 (http://www.moh.gov.sa/Ministry/MediaCenter/News/ Documents/healthybook.pdf, accessed 2 April 2017). 19. Jordan-MOH. (2009) Annual Report; 2008 [Online], Avail- able: http://www.dcd.gov.jo/images/Upload/y2008.pdf [1 February 2015]. 20. Ministry of Health, Oman. Incidence of communicable dis- eases, 1996–2012 (http://www.cdscoman.org/uploads/ cdscoman/Incidence%20of%20Diseases%20yearly.pdf, ac- cessed 2 Aril 2017). 21. Republic of Lebanon. Ministry of Public Health. Statistical Bulletin 2012 (http://www.moph.gov.lb/en/Pages/8/327/ statistical-bulletins, accessed 2 May 2017). 22. Bad bug book. Foodborne pathogenic microorganisms and natural toxins. 2nd ed. Silverspring (MD): Food and Drug Ad- ministration; 2012. 23. Brenzel L, Wolfson LJ, Rushby JF, Miller M, Halsey NA. Vaccine- preventable diseases. In: Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, et al., editors. Disease control priorities in developing countries. 2nd ed. Washington (DC): World Bank; 2006. 24. Pinheeiro P, Mathers CD, Kramer A. The global burden of in- fectious diseases. In: Krämer A, Kretzschmar M, Krickeberg K, editors. Modern infectious diseases epidemiology. Concepts, methods, mathematical models, and public health. New York: Springer-Verlag; 2010:3–21. 25. Briggs ADM, Smith A, Scarborough P. Modelling in pub- lic health. In: Regmi K, Gee I, editors. Public health intelli- gence: issues of measure and method. Switzerland: Springer; 2016:67–90. 26. Best practices in ranking emerging infectious disease threats. Stockholm; European Centre for Disease Prevention and Con- trol; 2015. 27. Boedeke W, Klindworth H. Prioritization of diseases for work- related health monitoring by multidimensional ranking. J Pub- lic Health (Bangkok). 2011 April;19(2):113–20. 28. Wiseman V, Mitton C, Doyle-Waters MM, Drake T, Conteth L, Newall AT, et al. Using Economic Evidence to Set Healthcare Priorities in Low-Income and Lower Middle –Income Coun- tries: A Systematic Review of Methodological Frameworks. Health Econ. 2016;25 Suppl.1:140–61. 29. Environmental profile of Ismailia governorate. Cairo: Egyptian Environmental Affairs Agency; 2007 [In Arabic]. Book 23-06.indb 403 8/16/2017 1:24:14 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 404 1Zanjan Metabolic Disease Research Centre; 2Zanjan University of Medical Sciences, Zanjan, Islamic Republic of Iran (Correpondence to: Parisa Khoshnevisasl: khoshnevis@zums.ac.ir). 3NODET High School, Zanjan, Islamic Republic of Iran. Received: 22/03/16; accepted: 11/07/16 The relation between pica and iron deficiency in children in Zanjan, Islamic Republic of Iran: a case– control study Mansour Sadeghzadeh 1 Parisa Khoshnevisasl 2 and Sina Sadeghzadeh 3 Lien entre le pica et les carences en fer chez les enfants à Zanjan, République islamique d’Iran : étude cas- témoin RÉSUMÉ La présente étude cas-témoin avait pour objectif de déterminer la fréquence du pica et son lien avec les carences en fer chez les enfants de Zanjan. Nous avons sélectionné 872 enfants de manière aléatoire et déterminé la fréquence du pica. Nous avons choisi des élèves en bonne santé du même âge, sexe et de la même classe que nos cas afin de servir de groupe témoin. Les cas et les témoins ont été examinés pour détecter une anémie ferriprive. Parmi les 57 élèves (6,7 %) souffrant de pica, il n’existait pas de lien significatif avec le sexe (p > 0,05). Les types les plus connus de pica étaient la géophagie (62,3 %) et l’ingestion de papier (31,2 %). La fréquence de l’anémie parmi les cas était plus élevée que chez les témoins, mais la différence n’était pas statistiquement significative. Le ratio de la capacité de fixation du fer sérique/fer total, inférieur ou égal à 0,15, ne différait pas significativement entre les deux groupes. Nous n’avons trouvé aucune association entre le pica et l’anémie et/ou les carences en fer (p > 0,05). ةطباض ةلاح ةسارد :ةيملاسلإا ناريإ ةيروهجم ،ناجناز ةظفامح في لافطلأا في ديدلحا صقنو اكيبلا ينب ةقلاعلا هداز قداص انيس ،لصا سيونشوخ اسيرب ،هداز قداص روصنم ةـظفامح في لاـفطلأا في دـيدلحا صـقنب اـهتقاعو اكـيبلا راـشتنا لدـعم دـيدتح في هذـه ةـطباضلا ةـلالحا ةـسارد نـم فدـلها لـ َّثتم :ةـصلالخا ةــ حصلاب نوــ عتمتي ًلااــ فطأ فيازــ ج لكــ شب اــ نترخاف .اكــ يبلا راــ شتنا لدــ عم اــ نددحو ًاــ فط 872 نــ م ةيئاوــ شع ةــ نيع اــ نترخا دــ قو .ناــ جناز تلااـلحاو تلااـلحا مـييقت ىرـجو .ةـطباض ةـعومجمك مهمادختـسلا تلااـلحاك سيردـلما فـصلا سـفن نـمو سـنلجاو رـمعلا سـفن نـم ًاــ بلاط 57 مــ هددع غــ لابلاو اكــ يبلا ضرــ مب نــ باصلما باــ طلا نــ ب نــ مو .دــ يدلحا صــ قن نــ ع مــ جانلا مدــ لا رــ قف ساــ سأ ىــ ع ةــ طباضلا قروــ لاو )% 62.3( باترــ لا لواــ نت ًاعويــ ش اكــ يبلا عاوــ نأ رــ ثكأ ءاــ جو .)p> 0.05( ضــ يرلما ســ نجب ةــ للاد تاذ ةــ قاع يأ تــ بثت لم ،)% 6.7( لمو .ةـ يئاصحإ ةـ للاد فاـتخلاا اذـله نـكي لم نإو ،ةـطباضلا تلااـلحا في اـهنم رـكأ تلااـلحا نـب مدـلا رـقف راـشتنا لدـعم ءاـجو .)31.2( طاـبترا يأ دـجن لمو .نـتعومجلما نـب ةـللاد اذ ًاـفاتخا 0.1 ≤ مدـلا في دـيدلحا ىوتـسلم ةـطبارلا ةردـقلا/مدلاب دـيدلحا ىوتـسم ةبـسن فـلتتخ عاـبتاب صيوـي ،اكـيبلا كولـسل لـماوعلا ةددـعتلما ةـعيبطلا لىإ رـظنلابو .)p> 0.05( دـيدلحا صـقن وأ/و مدـلا رـقفو اكـيبلا ضرـمب ةـباصلإا نـب .تاـصصختلا ددـعتم جـنه ABSTRACT The aim of this case–control study was to determine the frequency of pica and its relationship with iron deficiency in children in Zanjan. We selected 872 children and determined the frequency of pica. We selected students who did not have pica of the same age and sex, and in the same class as our cases as a control group. Both groups were evaluated for iron deficiency anaemia. Among the 57 students (6.7%) who had pica, there was no significant relationship with sex (P > 0.05). The most common types of pica were soil (62.3%) and paper (31.2%). The frequency of anaemia among cases was greater than in controls, although the difference was not statistically significant. The serum iron/total iron binding capacity ratio ≤ 0.15 did not differ significantly between the 2 groups. We did not find any association between pica and anaemia and/or iron deficiency (P > 0.05). Book 23-06.indb 404 8/16/2017 1:24:14 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 405 Introduction Pica is defined as the compulsive eat- ing of non-food material persisting for more than 1 month (1). There are many substances considered as pica such as soil, ice, plaster, cinder, etc. This may vary by ethnicity, culture, race or geographic region (2). There are several theories to ex- plain pica; one is hunger (3), but given that patients usually consume small quantities of non-food substances be- tween meals, this theory is not fully supported (4). The protection theory maintains that pica is a defensive prac- tice that protects the gastrointestinal tract from absorbing pathogens and chemical substances. Although clay is an effective substance for this (3), more studies are needed to determine this relationship. A protective response to psychological stress is another the- ory proposed to explain pica (3). The American Psychological Association believes that pica is a psychopathology that needs therapeutic interventions. Some studies show that pica is usually associated with a number of psycho- logical disorders (4). Another theory for pica is micronu- trient deficiency, e.g. iron, zinc, seleni- um and calcium. There have been many studies on the validity of this hypoth- esis (1,3,5). According to this theory, the patients’ taste towards the deficient material changes (3). Furthermore, it seems that culture plays a major role in some societies (6). For instance clay is used for fertility and childbearing in Turkey, Africa and Australia (7). Pica may have consequences like gastro- intestinal disturbances; lead, mercury or arsenic intoxication; parasitic in- festation; or potassium abnormalities (8). The frequency of pica varies from place to place, however, it appears to be more common in children, women, black people, people residing in ru- ral areas and pregnant women (9). Its frequency in the United States of America ranges from 4% among men to 68% in pregnant women and 18.5% in children (10). Despite the widespread preva- lence of pica and its association with multiple health issues, little is known about its causes and consequences. Many researchers have studied the relationship between pica and iron deficiency (11–14); nevertheless, the etiology is still a matter of debate. The frequency of pica and its related factors have not yet been studied in the north- western regions of Iran such as the city of Zanjan. The aim of this study was to determine the frequency of pica and its relationship with iron deficiency in children in Zanjan. Methods This case–control study was con- ducted on students aged 6–15 years in Zanjan in 2012. We selected 872 chil- dren from Zanjan elementary schools: 580 girls (66.5%) and 292 boys (33.5 %) were randomly selected from a total of 13 529 students (8228 boys, 5301 girls) by multistage probability sam- pling. The sampling was carried out in 3 steps. The total number of students in grades 1–5 of elementary schools was determined. The proportion of children in each class was calculated. Assuming that each class has 40 stu- dents we determined the number of classes in each age group and based on the percentage of the total specimens, the number of clusters was assigned. We selected 32 clusters (40 students in each class) by simple randomization. The sample size was calculated using the formula: n = z2 × p × q/d2, where: p = prevalence, d = 0.005, z = 1.96, q = 1–p. Sample size was calculated at 860. For the control group we randomly choose students who did not have pica of the same age and sex and from the same class as our cases. We distributed about 1200 ques- tionnaire and 872 were filled in com- pletely by the parents. As participation was voluntary, we did not record rea- sons for non-participation. Parents gave written informed consent and completed a questionnaire about their children’s pica. After collecting the completed questionnaires, the pica- positive students (according to par- ents) were selected as the case group and a student of the same sex and age in the same class was chosen randomly as control group. We considered about 10 more students in control group. From 872 students only 57 students had pica according to the question- naires but only 45 students accepted to participate. The control group was 65 students but only 45 accepted to do blood tests. Both the cases and controls were examined by the researchers and their probable signs and symptoms were re- corded. Blood samples were collected and tested for haemoglobin, haema- tocrit, serum iron and total iron bind- ing capacity. Anaemia was defined as haemoglobin level ≤ 11 /dL and iron deficiency as serum iron to total iron binding capacity ratio ≤ 15% (15–17). Discrete variables are expressed as counts (%) and compared using the chi-squared test. Statistical analysis was performed by independent t-test and Pearson correlation using SPSS 16.0. Differences were considered statisti- cally significant at P-value < 0.05. The ethics committee at Zanjan University of Medical Sciences ap- proved this study. Results A total of 872 students participated in this study, 580 girls (66.5%) and 292 boys (33.5%). The characteristics of the participants are shown in Table 1. The children were divided into 3 age groups (6–9 years, > 9–11 years and > 11 years) with mean age 9.40 (stand- ard deviation 2.89) years. Fifty seven students (6.7%) had pica, 36 (63.2%) girls and 21 (36.8%) boys (Table 1). Book 23-06.indb 405 8/16/2017 1:24:14 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 406 We did not find a significant relation- ship between sex and pica (P > 0.05). The reported types of pica were soil in 33 children (3.8%), paper in 17 (1.94%), hair in 10 (1.14%), plaster in 5 (0.57%), cotton thread in 5 (0.57%), plastic materials in 5 (0.57%), cinder in 1 (0.11%) and stone in 1 (0.11%). Pica of paint was not found in our cases. The most common type of pica was soil (62.3% of the cases) followed by paper (31.2% of the cases). Only 45 of the 57 children in the case group, i.e. those with pica, agreed to have blood tests and continued the study (30 girls and 15 boys); each of these children was randomly matched with another student in their class who did not have pica of the same sex and age as a control group. The propor- tion of children with pica increased with age, but there was no significant relationship between pica and age (P > 0.05). The most frequent symptom re- ported in both the pica case group who agreed to have blood tests and the control group was irritability. Other frequent symptoms included: weak- ness, paleness and loss of appetite. We did not find any statistically significant difference between the 2 groups in symptoms reported (P > 0.05). The laboratory results for the blood testing are shown in Table 2. The fre- quency of anaemia in cases was greater than in the controls although the dif- ference was not statistically significant. There were 3 cases and 2 controls with serum iron < 50 μg/dL and 5 cases and 1 control with serum total iron bind- ing capacity greater than the expected 400 μg/dL, but the serum iron:total iron binding capacity ratio ≤ 0.15 did not differ significantly between the 2 groups. Discussion In this study from Zanjan, north- western Islamic Republic of Iran, the frequency of pica in 872 students was 6.7%. The type and prevalence of pica may depend on cultural and ethnic factors (18). In a study on children in Egypt, the prevalence of pica was 7.2%, which is similar to our study (19). Our result is in contrast with a report from Madagascar with 53% geophagy and 85% amylophagy. In the observed population pica was not regarded as stigmatized culture, rather a divergent behaviour (20). In studies from the United States of America the prevalence of pica in children ranged between 10.0% and 18.5% (7,10). The differences may be explained by the distinct definitions of pica and the parents’ unwillingness to declare their child’s behaviour abnormal. As in other studies, the most com- mon type of pica in this study was geophagia (62.3%). In a study of Zam- bian children, 74.4% practiced some form of geophagia (21). In a study in Egypt, clay (43.1%) and dust (25.9%) were the most common type of pica (19). We did not find a significant as- sociation between sex and pica. This is concurrent with the findings of Ivascu et al. (21) in a study on patients with sickle cell disease but disagrees with the findings of Nchito et al. which showed a significant incidence of pica in girls in their study from Zambia (22). Table 1 Demographic characteristics of schoolchildren (case and control groups), Zanjan, 2012 Characteristic Total (n = 872) Cases with pica (n = 57) No. % No. % Sex a Male 292 33.5 21 7.2 Female 580 66.5 36 6.2 Age (years) a 6–9 401 45.9 16 35.5 > 9–11 425 48.9 24 53.4 > 11 46 5.2 5 11.1 *Only 45 participants agreed to the blood testing. aRelationship between pica and sex and pica and age not significant (P > 0.05). Table 2 Results for blood tests for anaemia or iron deficiency in children in Zanjan, 2012. Variable Cases (n = 45) Controls (n = 45) P-value No. % No. % Hb ≤ 11 g/dL 6 13.3 2 4.4 > 0.05 Hb > 11 g/dL 39 86.7 43 95.6 HCT ≤ 34% 8 17.7 3 6.6 > 0.05 HCT > 34% 37 82.3 42 93.4 SI ≤ 50 μg/dL 3 6.6 2 4.4 > 0.05 SI >50 μg/dL 42 93.4 43 95.6 TIBC ≤ 400 μg/dL 5 11.1 1 2.2 > 0.05 TIBC < 400 μg/dL 40 88.9 44 97.8 SI/TIBC ≤ 0.15 7 15.5 8 16.7 > 0.05 SI/TIBC > 0.15 38 84.5 37 82.3 Hb = haemoglobin, HCT = haematocrit, SI = serum iron, TIBC = total iron binding capacity. Book 23-06.indb 406 8/16/2017 1:24:14 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 407 We did not find any association between pica and anaemia and/or iron deficiency (P > 0.05). These findings differ from those of some other stud- ies (3,19,23,24). But at least 2 double blind controlled studies did not find any relationship between iron therapy and pica behaviour (10). This is prob- ably because pica is more a cultural be- haviour than a result of iron deficiency. On the other hand, some other studies have shown that pica was common in patients with sickle cell anaemia; these patients usually have high iron levels (22,25). It should be taken into account that pica may also be seen in zinc or other micronutrient deficiency. A limitation of this study was not measuring the concentration of other micronutrients such as zinc, calcium and selenium. Acknowledgements We would like to thank all the children and their families for their participation in this study. Funding: This study was based on a thesis for a medical degree and was funded by the Research Department of Zanjan University of Medical Sciences. Competing interests: None declared. References 1. Bay A, Dogan M, Bulan K, Kaba S, Demir N, Öner AF. A study on the effects of pica and iron-deficiency anemia on oxidative stress, antioxidant capacity and trace elements. Hum Exp Toxi- col. 2013;32(9 ):895–903. PMID:23444335 2. Barton JC, Barton JCl, Bertoli LF. Pica associated with iron deficiency or depletion: clinical and laboratory correlates in 262 non-pregnant adult outpatients. BMC Blood Disord 2010;10:9. PMID:21176208 3. Young S L, Wilson MJ, Miller D, Hillier S. Toward a compre- hensive approach to the collection and analysis of pica sub- stances, with emphasis on geographical material. PLOS One 2008;3(9):e3147. PMID:18773081 4. Placek CD, Hagen EH. A test of three hypotheses of pica and amylophagy among pregnant women in Tamil Nadu, India. Am J Hum Biol. 2013;25(6):803–13. PMID:24130118 5. Lumish RA, Young SL, Lee S, Cooper EM, Pressman E, O’Brien KO. Pica behavior is prevalent and associated with low iron status in pregnant adolescents. FASEB J. 2013;27:634.11 6. Kawai K, Saathoff E, Antelman G, Msamanga G, Fawzi WW. Geophagy (soil-eating) in relation anaemia and helminth in- fection among HIV-infected pregnant women in Tanzania. Am J Trop Med Hyg. 2009;80(1):36–43. PMID:19141837 7. Blinder, Barton J, Blinder BJ, Salama C. An update on pica: prevalence, contributing causes, and treatment. Psychiatric Times. 2008;25(6):66–70. 8. Mishori R, McHale. Pica: an age-old eating disorder that’s often missed. J Fam Pract. 2014 Jul;63(7):E1-4. PMID:25198212 9. Mathee A, Kootbodien T, Mahuma T, Nkomo P, Naik I. A cross- sectional analytical study of geophagia practices and blood metal concentrations in pregnant women in Johannesburg, South Africa. S Afr Med J. 2014;104(8):568–73. PMID:25213850 10. Miao D, Sera L, Young CD, Golden A. Meta-analysis of pica and micronutrient status. Am J Hum Biol. 2015;27:84–93. PMID:25156147 11. Nafil H, Tazi I, Mahmal L. Prevalence of pica in iron deficiency anemia in Marrakech (Morocco). Med Sante Trop. 2015;24 [Epub ahead of print] [in French]. PMID:26103958 12. Rabel A, Leitman SF, Miller JL. Ask about ice, then consider iron. J Am Assoc Nurse Pract. 2015;5 [Epub ahead of print]. PMID:25943566 13. Uchida T, Kawati Y. Pagophagia in iron deficiency anemia. Rinsho Ketsueki. 2014;55(4):436–9. PMID:24850454 14. Reilly C, Henry J. Geophagia: why do humans consume soil? Nutr Bull. 2000;25:141–4. 15. Kliegman RM, Stanton BF, St Geme JW, Schor NF, Behrman RE. Nelson textbook of pediatrics, 19th ed. Philadelphia: WB Saunders Company; 2011:2017. 16. Oski FA, Brugnara C, Nathan DG. A diagnostic approach to the anemic patients. In: Nathan DG, Orkin SH, eds. Nathan and Oski’s hematology of infancy and childhood, 7th ed. Philadel- phia: WB Saunders Company; 2008:Appendix 11. 17. Ghasemi F, Valizadeh F, Taee N. Iron-deficiency anemia in children with febrile seizure: a case–control study. Iran J Child Neurol. 2014 Spring;8(2):38–44. PMC4058064 18. Kettaneh A, Eclache V, Fain O, Sontag C, Uzan M, Carbillon L, et al. Pica and food craving in patients with iron-defi- ciency anemia: a case- control study in France. Am J Med. 2005;118(2):185–8. PMID:15694906 19. El Nemer FM, Alian DM, Salah Eldin M, Moustafa Khalil H. Prevalence of pica among children attending pediatrics clinic at El-Menoufiya University Hospital. Am J BioScience. 2014;2(4):147–52. 20. Golden CD, Rasolofoniaina BJR, Benjamin R, Young SL. Pica and amylophagy are common among Malagasy men, women and children. PLoS ONE 2012;7(10):e47129. PMID:23082143 21. Ivascu NS, Sarnaik S, McCrae J, Whitten-Shurney W, Thom- as R, et al. Characterization of pica prevalence among pa- tients with sickle cell disease. Arch Pediatr Adolesc Med. 2001;155(11):1243–47. PMID: 11695934. 22. Nchito M, Geissler PW, Mubila L, Friis H, Olsen A. Effects of iron and multimicronutrient supplementation on geophagy: a two-by-two factorial study among Zambian school children in Lusaka. Trans R Soc Trop Med Hyg. 2004;98(4):218–27. PMID:15049460 23. Gupta N, Sood S. The serum level of iron, zinc, calcium and selenium in children with pica. Int J Basic & Applied Physiol- ogy. 2014;3(1):151–15. 24. Shruti S, Bhatia MS, Rusia U, Rusia A. Iron profile estima- tion in children of behavioural disorders. Delhi Psychiatry J. 2010;13(2):339–40. 25. O’Callaghan ET, Gold JI. Pica in children with sickle cell dis- ease: two case reports. J Paediatric Nursing. 2012;27(6):e65– e70. PMID:22917881 Book 23-06.indb 407 8/16/2017 1:24:14 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 408 1General Directorate of Infectious Disease Control, Ministry of Health, Riyadh, Saudi Arabia (Correspondence to: Ahmed O.A. Ali: abuoosmann@ yahoo.com). 2Department of Epidemiology, Maastricht University Medical Centre, Maastricht, the Netherlands. Received: 28/06/16; accepted: 11/09/16 Disease and treatment-related factors associated with tuberculosis treatment default in Khartoum State, Sudan: a case–control study Ahmed O.A. Ali 1 and Martin H. Prins 2 Facteurs pathologiques et thérapeutiques entraînant un abandon du traitement de la tuberculose dans l’État de Khartoum, Soudan : étude cas-témoin RÉSUMÉ L’abandon du traitement de la tuberculose (TB) demeure un défi dans la lutte antituberculeuse. La présente étude cas-témoin avait pour objectif d’identifier les déterminants de l’abandon de traitement parmi les patients atteints de tuberculose pris en charge dans des centres de traitement dans l’État de Khartoum entre mai et juillet 2011. Les cas comprenaient des patients atteints de tuberculose et ayant abandonné leur traitement, et les témoins étaient ceux ayant mené leur traitement à terme. Sur les 2727 patients atteints de tuberculose traités dans les centres, 328 (14 %) avaient abandonné le traitement. Sur ce nombre, 185 avaient repris le traitement avant la collecte des données, et 143 étaient restés sans traitement et étaient donc éligibles comme cas. Sur les 143, 27 n’ont pu être tracés et 11 ont refusé de participer. Ainsi, 105 cas et 210 témoins ont été inclus et interrogés. Les variables associées de façon significative avec l’abandon de traitement étaient le fait d’habiter en zone rurale (OR = 2,68 ; IC à 95 % I 1,51-4,73), la non participation à un programme DOTS (traitement de brève durée sous surveillance directe) (OR = 2,53 ; IC à 95 % 1,49-4,30), le développement d’effets secondaires (OR = 1,94 ; IC à 95 % 1,14-3,29) et des antécédents de tuberculose (rechute, tuberculose multirésistante ou échec du traitement) (OR = 5,11 ; IC à 95 % 2,69-9,6). Une attention devrait être accordée à ces groupes à risque d’abandon de façon à encourager l’observance et la poursuite du traitement. ةطباض ةلاح ةسارد :نادوسلا ،موطرلخا ةيلاو في لسلا جلاع نع فلختلا لىإ يدؤت يتلا جلاعلاو ضرلماب ةطبترلما لماوعلا نيرب كيردنه نترام ،ىع دحمأ ناثع دحمأ ةـلاح ةـسارد تـيرجأو .نادوـسلاب موـطرلخا ةـيلاو في لـسلا ضىرـم نـب جاـعلا نـع فـلختلا تادّدـمح دـيدتح لىإ ةـساردلا هذـه فدـته :ةـصلالخا تاداـيعلا لىإ رـح دـقلو .»ةـطباض صراـنع« جاـعلا اولمكتـسا نـيذلا ضىرـلماو »تلااـح« جاـعلا نـع اوـفلتخ نـيذلا ضىرـلما اـهيف رـُتعا ةـطباض ًاضيرم 328 عـطقنا نـح في مـهجاع )% 86( ًاـضيرم 2399 لمكتـسا ،ضىرـلما ءلاؤـه نـب نـمو .لـسلاب ًاـضيرم 2727 ةـساردلا ةترـف لاـخ ةكراـشلما غلابلاو مـهجاع اولمكتـسا نـيذلا ضىرـلما ةـساردلا في جرُدأ ،كـلذ نـع ًاـضفو .مـهعم تاـباقم ءارـجإو ةـلاح 105 يـّفقت مـتو .جاـعلا نـع )% 14( “فـيرلا في نكـسلا“ : يـي اـم جذوـمنلا في ةـمئاق تـلظ يـتلا تارـغتلما تـنمضت ،تارـغتلما ددـعتلما لـيلحتلا راـطإ فيو .ًاـضيرم 210 مـهددع ثودــ ح“و ،)OR= 2.53; 95% CI 1.49-4.30( “شراــ بلما فاشرلاا تــ تح جاــ علا“ جــ مانرب في ةكراــ شلما مدــ ع،)OR= 2.68; 95% CI 1.51-4.73( “جاــ علا لــ شف وأ ةددــ عتم ةــ يودلأ مواــ قلما لــ سلاب ةــ باصلاا ددــ تجو ثودــ ح“و ، )OR= 1.94; 95% CI 1.14-3.29 ( “جاــ علل ةــ يبناج راــ ثآ ضىرلم ةيعرفلا تاـعومجلما ضـعب نـب اـتهاجرد ىـعأ في نوـكت جاـعلا نـع فـلختلا رـطامخ نأ لىإ جـئاتنلا رـشتو .)OR= 5.11; 95% CI 2.69-9.69( .جاعلاب ضىرـلما ءلاؤـه مازـتلاب ماـتهلاا ردـيجو اهديدتح لهـسي يـتلا لـسلا ABSTRACT Defaulting on tuberculosis (TB) treatment remains a challenge to controlling TB. This case-control study aimed to identify determinants of treatment default among TB patients attending treatment clinics in Khartoum State from May to July 2011. Cases were TB patients who defaulted on treatment and controls were those who completed treatment. Of the 2727 TB patients attending the clinics, 328 (14%) had defaulted. Of these, 185 had resumed treatment before data collection and 143 had not and were eligible as cases. Of the 143, 27 could not be traced and 11 declined to participate. Thus, 105 cases and 210 controls were included and interviewed. The variables significantly associated with treatment default were: rural residence (OR: 2.68; 95% CI: 1.51–4.73), not being on a DOTS programme (OR: 2.53; 95% CI: 1.49–4.30), having side-effects from treatment (OR: 1.94; 95% CI: 1.14–3.29), and having a history of TB (relapse, multidrug-resistant TB or treatment failure) (OR: 5.11; 95% CI: 2.69–9.69). Attention should be paid to these groups at risk of defaulting to encourage treatment adherence and continuation. Book 23-06.indb 408 8/16/2017 1:24:14 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 409 Introduction Tuberculosis (TB) has been known for a long time and is still a major public health problem (1). Worldwide TB kills more young and middle-aged adults than any other infectious disease, al- though it is a curable and preventable disease (2). The World Health Organi- zation (WHO) estimates that currently about 9.6 million new TB cases occur each year and that about 1.5 million deaths annually are related to TB (3,4). In 2010, it was estimated that the prevalence of TB cases in Sudan was 209 per 100 000 population with an an- nual incidence of new cases of 119 per 100 000, resulting in about 37 000 new cases each year in Sudan. Hence, Sudan has about 15% of the TB burden in the WHO Eastern Mediterranean Region and the second highest active TB preva- lence of the countries in this region. In addition, the estimated death rate related to TB, including HIV-infected TB patients, was 24 per100 000 per year (5). Successful treatment of TB in- volves taking anti-TB drugs for at least 6 months (6,7). The therapeutic regimens given under direct observa- tion short course therapy (DOTS) as recommended by WHO have been shown to be highly effective for both preventing and treating TB (8,9). The health authority of Sudan follows the strategies for TB prevention and treat- ment recommended by WHO. Despite the efforts that had been made by health authorities, some patients still do not follow their TB treatment and do not complete the intensive stage of treat- ment. As defined by WHO, patients who fail to collect their TB treatment for 2 consecutive months are reported as defaulters (10). Defaulting on TB medication is a major barrier to its local and global control. In addition, default- ing increases the risk of drug resistance, relapse and death, and may prolong infectiousness (11–15). The TB patient treatment default rate is about 10% in Sudan (5) and 14% in Khartoum State (16). The high rate of default on TB treatment in Khartoum State makes the identification of the risk factors leading to patients to default essential. In a previous paper, we reported on the sociodemographic factors as- sociated with non-adherence to TB treatment (17). In the present paper we identify the disease- and treatment-re- lated determinants of treatment default among TB patients in Khartoum State. This information could help to suggest actions that could lead to a reduction of TB treatment defaulting. Methods Study design This was an observational case–control study. Cases were TB patients who defaulted from treatment and controls were those who completed treatment. Setting This study was conducted in Khartoum State. In 1993, the Ministry of Health in Khartoum State established a TB control programme. The decentralized health care system in Khartoum is di- vided into 7 districts and 19 health areas. Its health facilities include 43 hospitals, 147 health centres, 185 centres run by nongovernmental organizations, 235 dispensaries and 365 primary health care units. TB services are available in 53 of the primary health care cen- tres in Khartoum State and is where TB patients receive their treatment (16). A registered nurse is designated responsible for TB treatment and fol- low up of continuation of treatment in the primary health care unit. This primary health care unit is the basic unit of management and reporting of the TB programme. Staff at the primary health care unit responsible for TB services include a medical assistant, a laboratory technician and a clerk. The programme provides care through the DOTS strat- egy as recommended by WHO. Population Our cases and controls were drawn from all TB patients attending the 53 treatment clinics in Khartoum State. The inclusion criteria for both cases and controls were: patients over 15 years who were clinically and laboratory diagnosed with TB and registered at the treatment units in Khartoum State. Cases were those patients identified as having defaulted on TB treatment dur- ing the data collection period. Following identification of each case (defaulter), without exclusion criteria, the next 2 patients who had completed their treat- ment without defaulting were included as controls, without exclusion criteria. They were attending the clinics because they had been requested to come for follow up, in the same TB treatment unit or the nearest one in the same area, either to do the final sputum smear or to collect the smear results. Patients were excluded from the study if they were too ill for interview, had a psychiatric illness or had given an incorrect address and could not be traced. The interview process was done from 1 May 2011 to 15 July 2011, but in order to reach the target defaulted group for the interviews, we used clinic records for the patients registered from May 2010 to May 2011. TB and treatment definitions The following definitions were applied. A pulmonary TB patient was one with TB disease involving the lung paren- chyma. An extra-pulmonary TB patient was one with TB of organs other than the lungs (e.g. pleura, lymph nodes, ab- domen, genitourinary tract, skin, joints and bones and meninges). A patient in whom both pulmonary and extra- pulmonary TB were diagnosed was classified as pulmonary TB (10). Treatment default was defined as an interruption of TB treatment for 2 or more consecutive months during the intended treatment period. Relapse was defined as a patient previously treated Book 23-06.indb 409 8/16/2017 1:24:15 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 410 for TB who has been declared cured or has completed treatment and is di- agnosed with bacteriologically positive (smear or culture) TB. Treatment fail- ure was defined as a patient who is spu- tum smear positive at 5 months or later during treatment. Multidrug resistant (MDR) TB was defined as TB resist- ance to at least isoniazid and rifampicin. Side-effects of treatment were defined according to a patient’s complaint and as identified by doctors and taken from the records (5,18–20). Drug regimen was defined as a drug or several drugs given in certain doses for a stated duration, as described by the treating doctor according to the na- tional TB control programme. All new TB patients should receive the category 1 (CAT1) regimen for 6 months, which includes rifampicin, isoniazid, pyrazina- mide and ethambutol. The category 2 (CAT2) treatment regimen is used for retreatment of TB patients; it lasts for 8 months and includes streptomycin in the first 2 months (5,10,19). DOTS is directly observed treat- ment, or watching the patient take his/ her medication to ensure medications are taken in the right combination and for the correct duration (10,19). Data collection Information on disease-related and treatment-related factors was retrieved from the medical records of the patients. In addition, face-to-face interviews were held, using a structured questionnaire, by trained interviewers to obtain infor- mation on the various factors possibly associated with treatment default. The questionnaire was pretested on 35 patients and, based on the results, was used without any major changes. All TB patients who had defaulted prior to the data collection period were identified and their address retrieved from patient records. Then, the interviewers used the following sequence of contact attempts: telephone calls, first to the patient and then to known family members or friends, and then home visits, first to patient and then to known family mem- bers or friends. If there was no telephone number on record, home visits were made. Data on the following variables were collected: sociodemographic charac- teristics including age, sex, residence (urban/rural); and disease- and treat- ment-related factors including BCG vaccination status, sputum smear result, treatment regimen, on a DOTS pro- gramme or not, chest X-ray, response to treatment, side-effects from treat- ment, sputum smear after 2 months, previous history of TB (including re- lapse, treatment failure and MDR-TB), other treatments sought, and other chronic diseases, e.g. diabetes mellitus (1,4,11,16,20–22). Statistical analysis The sample size was calculated accord- ing to Fleiss (1981) (23–25) assuming a two-sided type one error of 0.05, a power of 80% and the ability to detect an odds ratio (OR) of 2.0 with an ex- posure frequency of 30% in the control group and a ratio of cases to controls of 1:2. This gave a sample size of 105 cases and 210 controls. Data were reviewed for consistency and completeness. Data analysis was performed in SPSS, version 16. The de- mographic characteristics of the cases and controls were compared using the chi-squared test for qualitative vari- ables and Student t-test for continuous variables. Univariate and multivariate analyses were done. Descriptive statis- tics were calculated for the dependent variable (treatment default). Logistic regression analysis was done to calcu- late the ORs and its 95% confidence in- tervals (CI). Variables that were related to treatment default with a P-value less than 0.20 were entered in a multivariate model, using a backward selection. Ethical considerations Ethical approval was obtained from the ethics committee of the Ministry of Health, Khartoum State. Permission was granted by public committee lead- ers (senior health officers at the local- ity: director of health services, health team coordinator and PHC director) in the localities through official letters. Informed verbal consent was obtained from every eligible patient included in the study before the interview. Prior to the interview, all relevant aspects of the study were explained to the participants, including the purpose of the study, inter- view process and potential benefits. The interviews took place at the TB units in a suitable and separate room. The inter- viewers introduced themselves to the participants and outlined the scope of the interview and its approximate length at the beginning of each interview. The participants were informed that partici- pation was entirely voluntary, and that privacy and confidentially would be maintained during data processing and reporting. Potential respondents also were informed that they had the right to decline to participate, or to end the interview at any time without jeopard- izing their right for care and treatment. Privacy and confidentially were maintained and the information was used only for this study and will not be used by any other person for any other purposes. Results Cases and controls There were 2 727 TB patients who at- tended the 53 TB treatment clinics in Khartoum State during the study pe- riod. Out of these, 2 399 patients (86%) had completed their treatment while 328 patients (14%) had interrupted treatment. The 328 patients were di- vided into 2 categories: 1) 143 who had defaulted and never come back until the time of data collection, who were be eligible to be included as cases; and 2) 185 who had defaulted but were traced and came back to continue treatment before the start of data collection, who were excluded. Book 23-06.indb 410 8/16/2017 1:24:15 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 411 Of the 143 eligible cases, 15 had given a wrong address and 12 had moved away from Khartoum State and could not be interviewed. A further 11 patients declined the interview. None of the cases was too ill for interview or had a psychiatric illness. Hence, 105 cases were traced and interviewed. In addition, 210 patients who had com- pleted their treatment were included as controls; none declined to participate. Demographic characteristics of the cases and controls The demographic characteristics of the cases and controls are given in Table 1. Among the cases, 70.5% were males compared with 60.9% among the controls. The mean ages and standard deviations (SD) were 32.8 (SD14.4) years for the cases and 34.6 (SD 14.9) years for the controls; 53.3% of the cases and 47.6% of the controls were aged 15 to 30 years. Among the cases, 61.0% were urban residents while 80.5% of the controls were urban residents. Disease and treatment characteristics of the cases and controls The disease and treatment characteris- tics of the cases and controls are given in Table 1. Cases and controls had a simi- lar BCG vaccination status (61.9% and 53.3% had had the BCG vaccination respectively) and sputum smear results at the beginning of treatment (71.4% and 74.8% were positive respectively) as well as after 2 months (10.5% and 6.1% were positive respectively). How- ever, more cases had a previous his- tory of TB (37.1%), including relapse, failure and MDR-TB, compared with controls (10.0%). Hence, more cases (45.7%) received the CAT2 treatment regimen than controls (22.9%). Fewer cases were on DOTS (36.2%) than the controls (59.5%) and fewer had a good response to treatment (76.2%) compared with controls (88.6%). In ad- dition, more cases (52.4%) developed side-effects from treatment than the controls (31.0%) and more also sought traditional remedies (28.6%) than the controls (12.9%) (Table1). Risk factors for defaulting In the univariate analysis the following disease- and treatment-related factors were statistically significant associated with defaulting (P < 0.01): rural resi- dence (OR: 2.64; 95% CI: 1.57–4.44), CAT2 regimen (OR: 2.84; 95% CI: 1.72–4.69), not being on a DOTS programme (OR: 2.59; 95% CI: 1.59– 4.201), poor response to treatment (OR: 2.42; 95% CI: 1.305–4.49), hav- ing side-effects from treatment (OR: 2.45; 95% CI: 1.52–3.97), previous history of TB (relapse, treatment failure and MDR-TB) (OR: 5.32; 95% CI: 2.92–9.69) and seeking traditional rem- edies (OR: 2.71; 95% CI: 1.51–4.87) (Table 1). The multiple logistic regression analysis and adjusted ORs (aOR) and 95% CIs are shown in Table 2. The variables that remained in the model were: rural residence (aOR: 2.68; 95% CI: 1.51–4.73), not being on a DOTS programme (aOR: 2.53; 95% CI:1.49– 4.30), having side-effects from treat- ment (aOR: 1.94; 95% CI:1.14–3.29) and previous history of TB (aOR: 5.11; 95% CI: 2.69–9.69) (Table 2). Discussion In our study, the overall prevalence of TB treatment default among the patients who attended TB treatment clinics during the study period was 14%, which is similar to that reported in other studies conducted in Khartoum State (5,16). A high default rate on TB treat- ment has also been reported in other developing countries in Africa and Asia, e.g. 22.88% in Ethiopia and 10.33% in India (26,27). Our study showed that DOTS re- duced default rates as those not on a DOTS programme had 2.5-times high- er odds of default. This agrees with the results of previous studies conducted in both developed and developing coun- tries (20,22,28–30). Rural residence was strongly associ- ated with TB default which concurs with the findings of other studies in Ethiopia (31), and South Africa (32). TB treatment default was also strongly associated with having side-effects from the TB medication and having a his- tory of TB (relapse, failure and MDR- TB), which concurs with other studies (6,11,33–36). However, our findings are in contrast to those reported from Malaysia where residence, medicine side-effects and history of TB were not associated with TB treatment default (20). Furthermore, in contrast to the findings of our study, a study in Estonia found that urban residence was posi- tively associated with TB default (37). The findings of our study might help doctors and policy-makers in Khartoum State and other developing countries in planning and policy development to strengthen TB control programmes in general. Although we highlight the relation between disease and treat- ment-related factors and defaulting TB treatment, further exploration of precipitating factors for defaulting are needed. To combat the TB spread in com- munities, WHO launched the DOTS strategy in 1993. Since that time, DOTS implementation has achieved good results by increasing patient compli- ance with treatment and decreasing treatment interruption in communities of both low and high socioeconomic status (28,29). The Ministry of Health in Khartoum State adopted a DOTS strategy when it was recommended by the WHO in 1993 (5). To make the access of TB services available, the Ministry of Health set up more than 50 TB units (microscopic and treatment centres) distributed all over the State, according to geography and population density (16). Despite these efforts, TB treatment default remains high. Book 23-06.indb 411 8/16/2017 1:24:15 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 412 Table1 Distribution of disease and treatment related factors in the tuberculosis (TB) patients Disease and treatment related factors Cases (n = 105) Controls (n = 210) P-value OR 95% CI No. (%) No. (%) Age (years) 15−30 (ref) 56 (53.3) 100 (47.6) > 30 49 (46.7) 110 (52.4) 0.34 0.80 0.50−1.27 Sex Male 74 (70.5) 128 (61.0) 0.098 1.53 0.93−2.53 Female (ref) 31 (29.5) 82 (39.0) Residence Urban (ref) 64 (61.0) 169 (80.5) Rural 41 (39.0) 41 (19.5) < 0.0001 2.64 1.57−4.44 Site of TB Pulmonary 92 (87.6) 180 (85.7) 0.643 1.18 0.60−2.37 Extra-pulmonary (ref) 13 (12.4) 30 (14.3) Sputum smear at the beginning Positive 75 (71.4) 157 (74.8) 0.52 0.84 0.50−1.43 Negative (ref) 30 (28.6) 53 (25.2) Chest X-ray Normal 80 (76.2) 173 (82.4) 0.19 0.68 0.39−1.21 Positive (ref) 25 (23.8) 37 (17.6) Treatment regimen CAT1 (ref) 57 (54.3) 162 (77.1) CAT2 48 (45.7) 48 (22.9) < 0.0001 2.84 1.72−4.69 On DOTS Yes (ref) 38 (36.2) 125 (59.5) No 67 (63.8) 85 (40.5) < 0.0001 2.59 1.59−4.21 Response to treatment Good (ref) 80 (76.2) 186 (88.6) Poor 25 (23.8) 24 (11.4) 0.004 2.42 1.30−4.49 Sputum smear after 2 months Positive 11 (10.5) 13 (6.1) 0.166 1.82 0.78−4.27 Not done 23 (21.9) 44 (21.0) 0.686 1.13 0.63−2.01 Negative (ref) 71 (67.6) 153 (72.9) Had side-effects to TB treatment Yes 55 (52.4) 65 (31.0) < 0.0001 2.45 1.52−3.97 No (ref) 50 (47.6) 145 (69.0) Previous history of TB No: new case (ref) 66 (62.9) 189 (90.0) Yesa 39 (37.1) 21 (10.0) < 0.0001 5.32 2.92−9.69 Sought traditional remedies Yes 30 (28.6) 27 (12.9) 0.001 2.71 1.51−4.87 No (ref) 75 (71.4) 183 (87.1) Had BCG vaccine Yes 65 (61.9) 112 (53.3) 0.149 1.42 0.88−2.29 No (ref) 40 (38.1) 98 (46.7) Have chronic diseases Yes 10 (9.5) 35 (16,7) 0.06 0.53 0.25−1.11 No (ref) 95 (90.5) 175 (83.3) aIncluding relapse, treatment failure and multidrug-resistant TB. OR = odds ratio; CI = confidence intervals. ref = reference category. Book 23-06.indb 412 8/16/2017 1:24:15 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 413 In view of our findings, in order to reduce TB treatment default further, attention should be paid to more ad- equate follow-up of patients, treatment of their side-effects, increasing the num- ber of health units that use DOTS and tracing defaulters, particularly among rural patients who may face barriers to continuing treatment, and among those with a history of TB (those who have relapsed, experienced treatment failure and those with MDR-TB). An objective of the TB control programme in Khar- toum State is to provide tracing teams for defaulters in all TB units, which are responsible for contacting defaulting patients, encouraging them to come back to continue their treatment and visiting them at their home if they do not reply so as to identify the barriers and advise them on how to overcome them when they first start to default. The fact that this does not appear to be happening, at least up to our study pe- riod, may indicate that the programme and its allocated resources need to be reassessed. The introduction of a re- vised retrieval system in Saudi Arabia significantly improved the retrieval of non-attenders and reduced the dropout rate (38). In terms of the generalizability of our findings, some methodological aspects of our study need to be considered. First, our study was conducted in Khar- toum State, which is the most popu- lated state in Sudan. Its population may represent the whole country as most of the inhabitants come from various parts of Sudan. In addition, the TB patients included in this study were selected from all TB treatment units in the State. Thus, our findings can be generalized to the total TB population in the State and also Sudan as well as to communities with similar settings. Second, recall bias was minimized by using a standardized questionnaire during the interview and by cross-checking patients’ responses for each study variable against their medical records. Third, the reliability of the information gathered from each pa- tient could not be counter-checked but questions about sensitive issues were carefully handled to maximize the accu- racy of the responses obtained. Fourth, possible confounders were taken into consideration in the design (by restrict- ing the diagnosis criteria) and in the analysis by using logistic regression analysis. Lastly, the major problem we faced during the study was how to reach the defaulting patients (cases). This problem was tackled in 3 steps. First, the patient medical records were traced and identified and all contact information was reviewed. Then, study personnel first tried to telephone the patient and, failing that, to telephone known family members or friends. If telephone con- tact failed or if there was no telephone number on record, home visits were made, first to the patient and then to known family members or friends. Interestingly, we found that many of the defaulting patients did not have access to any phone (mobile or landline), a risk factor not previously described or evaluated in our study. The interview- ers made an average of 3 attempts to contact each defaulter before recording a defaulter was a non-respondent. Due to the number of eligible cases who could not be traced and interviewed (27 of 143), generalizing the findings to the whole population of patients with TB should be done with caution. In conclusion, our study shows that living in a rural area, not being on a DOTS programme, developing side- effects to treatment and having a history of TB (relapse, MDR-TB or treatment failure) increased the likelihood of de- faulting on treatment. These findings may help guide improvement in the current TB treatment delivery in Sudan and similar developing countries. Acknowledgements We would like to thank our colleagues at Ministry of Health, Khartoum State, and TB control Programme. We are further grateful to all TB coordinators and health care workers at TB units for their cooperation. Funding: None. Competing interests: None declared. Table 2 Multivariate analysis of the disease and treatment risk factors for defaulting on tuberculosis (TB) treatment Disease and treatment related factors Adjusted OR 95% CI P-value Rural residence 2.68 1.51−4.73 0.001 Not on DOTS 2.53 1.49−4.30 0.001 Side-effects from TB treatment 1.94 1.14−3.29 0.015 Previous history of TBa 5.11 2.69−9.69 < 0.0001 aIncluding relapse, treatment failure and multidrug-resistant TB. OR = odds ratio; CI = confidence intervals. Book 23-06.indb 413 8/16/2017 1:24:15 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 414 References 1. Katia S, Tachfouti N, Obtel M, Nejjari C. Factors associated with treatment default by tuberculosis patients in Fez, Morocco. East Mediterr Health J. 2013;19(8):687–93. 2. TB advocacy, a practical guide. Geneva: World Health Organi- zation; 1999. 3. Global tuberculosis report. 20th ed. Geneva: World Health Organization; 2015. 4. Lönnroth K, Castro GK, Chakaya JM, Chauhan LS, Floy K, Glaziou P, et al. Tuberculosis control and elimination 2010–50: cure, care, and social development. Lancet. 2010;375(9728):1755–7. 5. Federal Ministry of Health. General Directorate of Primary Health Care. Sudan: National Tuberculosis Control Programme; 2011. 6. Muture B, Keraka M, Kimuu P, Kabiru E, Ombeka V, Oguya F. Factors associated with default from treatment among tubercu- losis patients in Nairobi province, Kenya: A case control study. BMC Public Health. 2011;11(696):1–10. 7. Munro SA, Lewin SA, Smith HJ, Engel ME, Fretheim A, Volmink J. Patient adherence to tuberculosis treatment: a systematic re- view of qualitative research. PLoS Med 2007, 4(7):e238. 8. Addington WW. Patient compliance: The most serious remain- ing problem in the control of tuberculosis in the United States. Chest. 1979;76:741–3. 9. Chhaya M, Gupta SC. Noncompliance to DOTS: How it can be decreased. Indian J Community Med. 2011;36(1):27–30. 10. Operational guide for national tuberculosis control pro- grammes on the introduction and use of fixed-dose combina- tion drugs. Geneva: World Health Organization; 2002. 11. Chuah SY. Factors associated with poor patient compliance with antituberculosis therapy in Northwest Perak, Malaysia. Tubercle. 1991;72:261–4. 12. Menzies R, Rochert I, Vissandjee B. Factors associated with compliance in treatment of tuberculosis. Tuber Lung Dis. 1993;74:32–7. 13. Wilkinson D. High-compliance tuberculosis treatment pro- gramme in a rural community. Lancet 1994, 343:647. 14. William JB, Cohn DL, Rietmeijer CA, Judson FN, Sbarbaro JA, Reves RR. Noncompliance with directly observed therapy for tuberculosis: epidemiology and effect on the outcome of treat- ment. Chest. 1997;111:1168–73. 15. Jasmer RM, Seaman CB, Gonzalez LC, Kawamura LM, Osmond DH, Daley CL. Tuberculosis treatment outcomes: directly ob- served therapy compared with self-administered therapy. Am J Respir Crit Care Med. 2004;170(5):561–6. 16. Suleiman MMA, Sodemann M. Evaluation of tuberculosis con- trol programme in Khartoum State for the year 2006. Scand J Public Health. 2009;37:101–8. 17. Ali AOA, Prins MH. Patient non adherence to tuberculosis treat- ment in Sudan: socio demographic factors influencing non ad- herence to tuberculosis therapy in Khartoum State. Pan Afr Med J. 2016;25:80 doi:10.11604/pamj.2016.25.80.9447. 18. Awofeso N. Anti-tuberculosis medication side-effects consti- tute major factor for poor adherence to tuberculosis treatment. Bull World Health Organ. 2008;86(3):B-D. 19. What is DOTS? A guide to understanding the WHO-rec- ommended TB control strategy known as DOTS. Geneva: World Health Organization; 1999 (http://apps.who.int/iris/ bitstream/10665/65979/1/WHO_CDS_CPC_TB_99.270.pdf, accessed 20 March 2017). 20. Nyi NN, Catherine D, Abdul Rahman I, Rosemi S, Noraini B, Mohd RM. Factors contributing to poor compliance with anti- TB treatment among tuberculosis patients. Southeast Asian J Trop Med Public Health. 2001;32(2):369–82. 21. Sabate E. WHO Adherence to long-term therapies: policy for action. Geneva: World Health Organization; 2001 (http:// www.who.int/chp/knowledge/publications/adherencerep. pdf, accessed 20 March 2017). 22. Jaggarajamma K, Sudha G, Chandrasekaran V, Nirupa C, Thom- as A, Santha T, et al. Reasons for non-compliance among patients treated under Revised National Tuberculosis Control Programme (RNTCP), Tiruvallur District, South India. Indian J Tuberc. 2007;54:130–5. 23. Fleiss LJ. Statistical methods for rates and proportions. 2nd ed. Hoboken, NJ: John Wiley & Sons Ltd; 1981:35–48. 24. Kelsey JL, Whittemore AS, Thomson WD, Evans AS. Methods in observational epidemiology. 2nd ed. New York: Oxford Uni- versity Press; 1986. 25. Riegalman RK, Hirsch RP. Studying a study and testing a test. How to read the medical literature. 2nd ed. Boston: Little, Brown and Company; 1989. 26. Demeke D, Legesse M, Bati J. Trend of tuberculosis and treat- ment outcomes in Gambella region with special emphasize on Gambella Regional Hospital, Western Ethiopia. J Mycobac Dis. 2013;3(2). 27. Pardeshi GS. Time of default in tuberculosis patients on directly observed treatment. J Glob Infect Dis. 2010;2(3):226–30. 28. Marlucia DSG, Maria LP, Toma MP. Porcuna, Alexandra B S, et al. Factors associated with tuberculosis treatment default in an endemic area of the Brazilian Amazon: a case control-study. PLoS One. 2012;7(6):e39134. 29. Robert MJ, David CS, Jussi JS, Philip CH. etal. Short-Course Rifampin and Pyrazinamide Compared with soniazid for Latent Tuberculosis Infection: A Cost-Effectiveness Analysis Based on a Multicenter Clinical Trial. Clin Infect Dis. 2004;38:363–9. 30. Ifebunandu NA, Ukwaja KN. Tuberculosis treatment default in a large tertiary care hospital in urban Nigeria: prevalence, trend, timing and predictors. J Infect Public Health. 2012;5(5):340–5. 31. Wondimu T, W/Michael K, Kassahun W, Getachew S. Delay in initiating tuberculosis treatment and factors associated among pulmonary tuberculosis patients in East Wollega, Western Ethiopia. Ethiopian J Health Dev. 2007;21(2):148. 32. Ndwandwe ZSI, Mahomed S, Lutge E, Knight SE. Factors affect- ing nonadherence to tuberculosis treatment in uMgungund- lovu Health District in 2010. South Afr J Infect Dis 2014;29(2):56. 33. Pandi NT, Choudhary SK. A study of treatment compliance in directly observed therapy for tuberculosis. Indian J Community Med. 2006;31(4):241–3. 34. Sanchez PE, Marquer C, Kalon S, Qayyum S, Hayrapetyan A, Varaine F, et al. Reasons for defaulting from drug-resistant tu- berculosis treatment in Armenia: a quantitative and qualitative study. Int J Tuberc Lung Dis. 2014;18(2):160–7. 35. Slama K, Tachfouti N, Obtel M, Nejjari C. Factors associated with treatment default by tuberculosis patients in Fez, Morocco. East Mediterr Health J. 2013;19(8):687–93. 36. Lalor MK, Greig J, Allamuratova S, Althomsons S, Tigay Z, Khaem- raev A, et al. Risk factors associated with default from multi- and extensively drug-resistant tuberculosis treatment, Uzbekistan: a retrospective cohort analysis. PLoS One. 2013;8(11):e78364. 37. Kliiman K, Altraja A. Predictors and mortality associated with treatment default in pulmonary tuberculosis. Int J Tuberc Lung Dis. 2010 Apr;14(4):454–63. 38. Chaudhry LA, Al-Tawfiq J, Ba-Essa E, Robert AA. Low rate of non-compliance to antituberculous therapy under the banner of directly observed treatment short course (DOTS) strategy and well organized retrieval system: a call for implementation of this strategy at all DOTS centers in Saudi Arabia. Pan Afr Med J. 2015;21:267. Book 23-06.indb 414 8/16/2017 1:24:15 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 415 1High Institute of Health Sciences, Ministry of Public Health and Population, Sana’a, Republic of Yemen (Correspondence to: T. Almahbashi: almahbashi@gmail.com). 2Department of Health Policy & Management, Faculty of Public Health, Health Science Center, Kuwait University, Safat, Kuwait. 3Community Health Department, University Kebangsaan Malaysia Medical Centre, Kuala Lumpar, Malaysia Received: 30/05/16; accepted: 16/11/16 Health labour market requirements of health professional education in Yemen Taha Almahbashi 1, Syed Mohamed Aljunid 2 and Aniza Ismail 3 Exigences du marché du travail de la santé et éducation des professionnels de la santé au Yémen RÉSUMÉ Il est important d’associer l’éducation des professionnels de la santé aux besoins en matière de services de santé du marché du travail privé et public, de façon à répondre aux aspirations du secteur de la santé. Ainsi, l’objectif premier de la présente étude était d’identifier les exigences du marché du travail actuel afin d’améliorer les résultats des instituts de formation en santé. Une étude qualitative a été menée parmi des professionnels des soins de santé de différentes spécialisations et diverses parties prenantes dans la ville de Sanaa, au Yémen. Six groupes de discussion ont été constitués pour 42 diplômés et 20 entretiens approfondis ont été conduits en collaboration avec des partenaires du développement sanitaire et des employeurs publics et privés. Les résultats des instituts de formation en santé restent en deçà des exigences du marché du travail de la santé, et ne comblaient pas les lacunes en anglais ou en matières de compétences cliniques. La survie de l’éducation des professionnels de la santé dépend des évolutions futures qui seront opérées en vue de répondre aux exigences du marché du travail, grâce à la collaboration entre les parties prenantes clés, une mise à jour régulière des programmes, et le développement professionnel constant des équipes de formation. نميلا في يحصلا ينهلما ميلعتلا نم يحصلا لمعلا قوس تاجايتحا ليعاسإ ةزينأ ،دينلجا ديس ،شيبحلما هط عاـطقلا طـطخ ذـيفنتل ماـعلاو صاـلخا لـمعلا يقوـس في ةـيحصلا تاـمدلخا تاـجايتحاب يـحصلا يـنهلما مـيلعتلا طـبر مـهلما نـم :ةـصلالخا بـيردتلا دـهاعم تاـجرمخ قـيقتح لـجأ نـم ةـيلالحا لـمعلا قوـس تاـجايتحا دـيدتح ىـع ًاـساسأ ةـساردلا هذـه تزـّكر ،مـث نـمو .يـحصلا ءاـعنص ةـنيدم في ةـينعلما فارـطلأا فـلتمخو ةـيحصلا ةـياعرلا لاـمج في نـيئاصخلأا نـم عوـنتم جـيزم نـب ةـيعون ةـسارد تـيرجُأو .ةـيحصلا باـبرأو ةـيحصلا ةـيمنتلا ءاكشر عـم ةـقّمعم ةـلباقم 20 تـيرجأ اـك ،ًاـيجرخ 42 هـعوممج اـلم ةـيرؤب ةـيعاجم تاـشقانم تـس تـيرجأو .نـميلاب تاوـجفلا دـ ِّست لمو ،يـحصلا لـمعلا قوـس تاـعقوت نود يـحصلا بـيردتلا دـهاعم تاـجرمخ تـناكو .صاـلخاو ماـعلا نـعاطقلا نـم لـمع ةـيبلتل لبقتـسلما في هرـيوطت ىـع يـنهلما يـحصلا مـيلعتلا رارمتـسا دـمتعيو .ةـيريسرلا تاراـهلماو ةـيزيلجنلإا ةـغللا ناـقتإ لاـمج في ةـمئاقلا يـنهلما رـيوطتلاو ،ةـمظتنم ةروـصب يـميلعتلا جـهنلما ثـيدتحو ،ةيـسيئرلا ةـينعلما فارـطلأا نـب نواـعتلا لاـخ نـم لـمعلا قوـس تاـجايتحا .سـيردتلا ةـئيه ءاـضعلأ رمتـسلما ABSTRACT It is important to link health professional education to the health service needs of the private and public labour market so as to meet the plans of the health sector. Thus, the main focus of this study was to identify the present labour market requirements for the outcomes of health training institutes. A qualitative study was carried out among mixed healthcare professionals and various stakeholders in Sana’a City, Yemen. Six focus group discussions were formed for 42 graduates and 20 in-depth interviews were undertaken with health development partners and public and private employers. Outcomes of the health training institutes were still below the expectations of the health labour market, and did not fill the existing gaps in English-language proficiency and clinical skills. The survival of health professional education depends on future development to meet labour market demands through collaboration between key stakeholders, regular updating of the curriculum, and constant professional development of the teaching staff. Book 23-06.indb 415 8/16/2017 1:24:15 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 416 Introduction In Yemen and many other parts of the world, there is a growing concern about the fitness of healthcare graduates to provide quality professional services, and the capacity of educational pro- grammes to give nurses and midwives the right set of competencies and ethical and professional values (1–3). In pre- paring the workforce, the curriculum is expected to meet standards that are often defined as core competencies. The curriculum must also be responsive to changes in health knowledge as well as the needs and demands emerging from health systems. A complete picture of the health labour market includes pro- ductivity and performance. Productiv- ity measures the units of care or service that workers provide. Performance is often measured by examining what the health workers are trained to do and how their performance utilizes that training. Performance of health workers includes the quality of their work, the technical skills they use, the care they deliver and the impact of their work on health outcomes (4). Employers are critical that most of the graduates lack the necessary core skills needed to be successful at work, which is attributed to the traditional teaching and learning processes in the education system (5). A lot of health-related suffering in Yemen is prevented, alleviated or cured by nurses and paramedics, as well as physicians. Most training for health professionals in Yemen is provided by the High Institute of Health Sciences (HIHS), Sana’a and Aden, which is af- filiated to the Ministry of Public Health and Population. HIHS has a branch in almost every governorate, and the educational programmes are estab- lished according to the needs of the community and capacity of health train- ing institutes. Capacity in pre-service training includes physical infrastructure (e.g., classrooms, laboratories, libraries, clinics for internships, and campus resi- dencies); human resources (quantity and quality of instructors and auxiliary staff); financial resources; organization- al and operational capacity (manage- rial structure and processes); and other non-infrastructure physical inputs (e.g., reference books, journals and computer equipment [1]). There are scant data at the national level in the Middle Eastern Region re- garding the needs of the health labour market and the response of health pro- fessional education. This is believed to be the first study in Yemen in the area of health professional education. The unique nature of the study lies in the participation of various players: health- care professionals (graduates), health development partners, and public and private employers. We used focus group discussions and interviews to identify the needs of the health labour market. Finally, the study links the performance of health professionals with the satisfac- tion of health development partners and public and private health sector employers. Methods This study was carried out from No- vember 2013 to February 2014. Sana’a, the capital city of Yemen, was selected from among the 21 administrative divi- sions because it has the largest hospitals and numerous national employers and international health partners. Major public and private hospitals as well as health development partners were selected to generalize the study at the national level. Interviews Twenty in-depth interviews were conducted with the main stakeholders. There were two types of stakehold- ers: public and private employers and developmental partners who have a direct relationship with health profes- sional education and health institutes. The health development partners who were interviewed were programme and project managers at their organizations and had experience in dealing with the health training institutes. Participants were United Nations and international organizations that have health projects in Yemen (Table 1). The employers’ in-depth individual interviews were conducted with representatives in the public and private health sectors that benefit from graduates of the health training institutes (Table 2). An audio- tape in-depth interview was conducted through an interview guide that aimed to explore: 1) stakeholders’ opinions about the professionalism of graduates of health training institutes and the relevance of healthcare professionals to the labour market; and 2) stakehold- ers’ views of any shortcomings in the healthcare professionals, both in quality and quantity. Discussion groups Six discussion groups were formed for 42 (27 male and 15 female) healthcare professionals: 3 for healthcare profes- sionals working in 3 public referral hos- pitals and 3 for healthcare professionals working in 3 major private hospitals in Sana’a (Table 3). The characteristics of the healthcare professionals are shown in Table 4. The discussions focused on the healthcare professionals’ opinions on the following open-ended questions: 1) How will they prepare academically and professionally to hold their first job in the area of their specialization? 2) How do they see the development of their career after graduation? The discussions were audiotaped with permission from the participants. The discussion moderator was supported by a note-taker during each session. These notes served as supplementary docu- mentation of the discussion, as well as a back-up. A summary of the points discussed in each group session was emailed to participants to verify that the findings were their own views and not those of the researcher. Immediately after each focus group discussion, the moderator, note-taker and researcher Book 23-06.indb 416 8/16/2017 1:24:15 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 417 met for a debriefing session to discuss overall findings. Data analysis To make the data manageable and use- ful, they were simplified into significant themes and categories that described the phenomena being studied. Accord- ing to the content analysis, the transcript was read repeatedly for familiarization and then categorized into words and phrases to find meaningful relationships between the categories and emergent themes. The themes that emerged were then related to the study objectives. Tri- angulation used multiple perspectives to interpret a single set of data to check the validity of the information gathered. A simple method of triangulation was for two colleagues to read and analyse the same set of transcripts and then compare notes. If the notes agreed, then the information was credible. Results The major themes identified from the interviews and the focus group discussions are summarized in Table 5, namely professional performance, career development, academic prepara- tion and linking the outcomes to the needs of the health sector. Professional performance Most employers and health develop- ment partners had the opinion that the professional performance of the healthcare professionals was good and satisfactory/good, with some negative observations. These included that Yem- eni health professionals demonstrated impatience towards their patients, which differed from the attitude of In- dian and Filipino nurses. There was a consensus among all respondents that shortcomings were mainly in the practi- cal skills in all specializations, which was attributed to the limited practical train- ing and inability to deal with modern equipment. These shortcomings were particularly evident in the specializa- tions of radiography and in emergency, intensive care nursing. There were also deficiencies in occupational ethics and safety. Career development Some interviewees were of the opin- ion that the qualifications offered by the health training institutes were not suitable for the needs of the labour market. This resulted in 33 of 42 (78%) healthcare professionals stating that they were not satisfied with their career development. They believed that the de- grees or certificates issued by the health training institutes did not enable them to improve their positions because they could not continue their studies to bachelor degree and above. Academic preparation Most of the healthcare professionals (35/42, 83%) were not satisfied with their academic and professional prepa- ration to hold their first job in their area of specialization. Twenty-eight of 42 (67%) participants expressed satisfac- tion with the theoretical content of their course. However, 39 of 42 (93%) participants thought that there was a deficiency in their practical training. There was a weakness in coordination between the educational institutes and the health facilities where practi- cal training was undertaken, and there was a shortage and lack of updating of equipment and tools required for practical training. Some thought that they encountered situations that were more advanced than those studied and Table 1 Health development partners interviewed Entity Designation Main fields of partnership with the health training institutes EU Project Member of the technical team of the project Capacity building in reproductive health WHO Health System Programmes Officer Capacity building and curriculum development UNFPA Advocacy and Stimulus Programmes Officer in Reproductive Health Capacity building and infrastructure support UNICEF Nutrition Projects Officer Capacity building in nutrition USAID MCHIP Manager Midwifery curriculum development SFD Health Projects Officer Capacity building and education system support Health and Population Project, the World Bank Project Manager Capacity building in midwifery GIZ Deputy Programme Manager Quality improvement programme in health institutes EU = European Union; GIZ = Gesellschaft für Internationale Zusammenarbeit; SFD = Social Fund for Development; UNFPA = United Nations Population Fund; UNICEF = United Nations Children’s Fund; USAID = United States Agency for International Development; WHO = World Health Organization. Book 23-06.indb 417 8/16/2017 1:24:15 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 418 practiced during training, and that they only learned theoretically and practi- cally after graduation. Linking the outcomes to the needs of the health sector Most interviewees (15/20) stated that the graduates did not cover the needs of the labour market, particularly in remote tribal areas of Yemen, where access to health services is difficult and the availability of health service provid- ers is rare. They also stated that there was a shortage of female healthcare professionals, especially in radiography and anaesthetics. Respondents thought that healthcare professionals needed to enhance their linguistic skills, especially English. Others stressed the necessity of acquiring the practical rather than lan- guage skills that would be needed in later professional practice. Continued professional development for health care professionals was referred to by most of the participants, with one stat- ing that it made no sense for graduates of health training institutes to continue depending on what they learned 20 years ago. One respondent stated that when the population size and the number of workers are taken into consideration, there is still a need for educational institutions to train more healthcare professionals. Some partici- pants emphasized the need to link the outcomes of health training institutes to the needs of the health sector, but this was not happening at present. One participant stressed the importance of responding to the needs of the health sector market, and raised the challenge of how we can match outcomes to our expectations of the health system. Discussion The perspectives of graduates and em- ployers have been used in several stud- ies to investigate the needs of the labour market in health profession education (4,5). Lack of proficiency in English lan- guage was behind the unemployment of 8000 nursing graduates in Malaysia who had not secured jobs, which in- dicates that a special English course is needed for the nursing profession (6). The importance of English language in the labour market has been indicated in several studies (7,8). The low per- formance in clinical skills is attributed to several reasons; one of which is that Table 3 Characteristics of hospitals that hosted discussion groups Hospital Type No. of beds Teaching status Al-Jomhori Teaching Hospital Public 367 Major Al-Thawra Modern General Hospital Public 500 Major Dr. Abdulkader Al-Mutawakel Specialized Hospital Private 150 Moderate to limited Saudi German Hospital Private 420 Moderate University Kuwait Hospital Public 297 Major University of Science and Technology Hospital Private 350 Major Source: Ministry of Public Health and Population. Annual health statistical report 2014. Sana’a Yemen. 2014. http://www.mophp-ye.org/arabic/docs/Report2014.pdf. Table 2 Health employers interviewed Entity Title Military Hospital in Sana’a Head of the Nursing Department Al-Jomhori Teaching Hospital Deputy for Academic Affairs Al-Thawra Modern General Hospital Head of Nursing Staff Health and Population Office, Al-Tahrir District, Municipality Secretariat Office Director Health and Population Office – Sana’a Governorate Reproductive Health Manager Hospital of the University of Science and Technology Administrative Manager The Yemeni German Hospital Technical and Administrative Director – Vice-Chairman of the Yemen Association for Private Hospitals Dr. Abdulkader Al-Mutawakel Specialized Hospital General Manager Ibn-Sina Hospital General Manager Azal Hospital Deputy Technical Director and Head of Radiology Department Book 23-06.indb 418 8/16/2017 1:24:15 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 419 the teaching and training approaches at health training institutions are still teacher- rather than student-centred. According to the interviewed partners in our study, updating the curricula is the main key to improv- ing the performance of health service providers; however, private employers said that this approach is outdated and has several shortcomings. Updating the curriculum was addressed in the recent National Strategy of Human Resources for Halth in Yemen (2014–2020) as a prominent challenge for the pre-service education sector (9). The World Health Organization (WHO) has reported that health professionals’ education and training institutions should consider adapting curricula to population needs, through identifying and defining the core competencies that are required to meet the evolving needs of their popula- tions (1). This seems to explain why the curricula lag behind the real needs of the market and are sometimes not adapted to the capacity of the students. Budget allocations remain an impor- tant unresolved concern for curricular development. Some partners have pro- vided financial support to health train- ing institutes for development of some curricula, but there are still some that need updating. It is reported that the level of financial support directly affects curricular development (10). Thus, lack of experience, less productivity and fi- nancial shortage are behind the slow pace of curricular development. In our focus group discussions, the graduates agreed that the teaching aids used at their health training institutions were out of date. Problems occurred when they went to work at hospitals and found things different from what they had studied. This might be attributed to two main reasons: timetable misman- agement, which meant that students had no time to access the library or repeat their training sessions in a skills laboratory; or lack of finance to renew or provide new technology. Such results are consistent with a Kenyan study that showed that providing students with ap- propriate learning resources increased the quality of university graduates (11). Education, according to the human science model (12), builds a knowl- edge and theoretical base that can be transferred and used in other areas to continue growth and learning. In health Table 4 Characteristics of health care professionals Specialization Gender Mean age, yr Average years of experienceMale Female Nursing 8 5 32 8 Medical assistant 4 2 27 4 Health statistics 3 1 30 6 Operating Theatre 2 0 37 11 Radiography 3 1 27 4 Medical laboratories 5 2 26 3 Midwifery 0 4 28 5 Public health 2 0 33 9 Table 5 Themes emerging from interviews with stakeholders and focus group discussions with healthcare professionals Major themes identified Key findings Professional performance • Impatience toward patients • Limited practical skills • Inability to deal with modern equipment • Deficiency in job ethics and occupational safety Career development • Diploma program is not matching needs • Diploma holders are in need of upgrading • Healthcare professionals are not satisfied with their career development Academic preparation • Weakness of academic and professional preparation • Deficiency in practical training • Shortage of and lack of updating to equipment and tools of practical training Linking the outcomes to the needs of the health sector • Remote governorates not covered • Shortage of female healthcare providers • Inadequate linguistic competencies • Outcomes of the health training institutes are not linked to the plans of the health sector Book 23-06.indb 419 8/16/2017 1:24:16 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 420 care, education focuses on personal development as well as training in the necessary skills and procedures with which health professionals must be fa- miliar. The educational process forms a continuous cycle that involves 2 inde- pendent players, the teacher and learn- ers (13). The present study showed that graduates were not satisfied with the performance of their teachers and the teaching methods. The employers also commented that teaching staff did not update their knowledge and need to be trained in teaching methodology. Some teachers may believe that being a good clinician or scientist is sufficient qualification to be a good teacher (14, 15). Without formal preparation for the teaching role, teachers may lack the con- fidence needed to use unfamiliar teach- ing techniques. WHO recommends that health professionals’ education and training institutions should consider de- signing and implementing continuous development programmes for teaching staff (1). There is substantial evidence that educators of health professionals are insufficiently prepared in terms of knowledge and skills (16). Another fac- tor that may contribute to poor perfor- mance of teaching staff is the selection criteria, and there is not much evidence for strategies or requirements for faculty selection. A major problem is that there is a shortage of educators, particularly in the geographically peripheral areas. Globally, health education institutions have heavy teaching loads and a short- age of educators, while in poorer coun- tries, the major constraint is a scarcity of qualified medical educators to teach the next generation of professionals (17). Although the study achieved its aims, there were some limitations. First, because of the time limit, this study was conducted only in the capital city of Yemen. Second, some health profes- sionals were not involved in the focus groups due to their work commitments during the study. Third, the targeted interviewees were the health develop- ment partners who had collaborative activities with the health training insti- tutes, while other health sector partners were not involved. Conclusion Monitoring entry into the health workforce requires a high level of col- laboration between key stakeholders, including ministries of health, education and finance, health training institutions, professional regulatory bodies and the private sector. We conclude that updat- ing the curricula in practical aspects is essential and should be conducted regularly in health training institutes for labour market adaptation. It is particu- larly interesting to note that graduates provided similar opinions to employers regarding insufficient speaking and writ- ing skills in English, which are important features of nursing, midwifery and other disciplines. Our findings reveal that the teaching staff are in constant need of learning modern teaching principles, particularly with the development and improvement of needs-based teaching. Funding: None. Competing interests: None declared. References 1. Transforming and scaling up health professionals’ educa- tion and training: World Health Organization guidelines. Geneva: World Health Organization; 2013 (http://apps.who. int/iris/bitstream/10665/93635/1/9789241506502_eng.pdf, accessed 22 March 2017). 2. Sousa A, Scheffler RM, Nyoni J, Boerma T. A comprehen- sive health labour market framework for universal health coverage. Bull World Health Organ. 2013 Nov 1;91:892–4. PMID:24347720 3. Global standards for the initial education of professional nurses and midwives. Geneva: World Health Organization; 2009 (WHO/HRH/HPN/08.6; http://apps.who.int/iris/ bitstream/10665/44100/1/WHO_HRH_HPN_08.6_eng.pdf, accessed 22 March 2017). 4. Asiyai RI. Challenges of quality higher education in Nigeria in the 21st century. Int J Educ Plan Admin. 2013;3(2):159–72 (https://www.ripublication.com/ijepa/ijepav3n2_07.pdf). 5. Arumugam N, Kaur N. Needs analysis on the importance of English communication skills for medical assistants. J Inst Res S E Asia. 2011;9(1):67–77. 6. Nalini A, Xavier T, Laura CD, Mahendran M. Unemployment among graduate nurses in Malaysia: a case study. Asian Soc Sci. 2014;10(9): 227–33 (http://www.ccsenet.org/journal/ index.php/ass/article/view/36594/20579). 7. Herath HMTS, Ranasinghe A. Labour Market Prospects for Business Graduates in Sri Lanka. Int J Soc Sci Humanit. 2011 May;1(1): 26–30 (http://www.ijssh.org/papers/5-H00086. pdf). 8. Mohammad M. Hussainat, Qasem M. The impact of unem- ployment on young people in the community: a case study from unemployed perspective. Asian Soc Sci. 2013;9(1):155–64 (http://www.ccsenet.org/journal/index.php/ass/article/ view/23542/15039). 9. Badr E. National Human Resources for Health Strategy for Yemen 2014–2020. An extended executive summary. Sana’a: Yemen Ministry of Public Health and Population; 2014. 10. Yates L. From curriculum to pedagogy and back again: Knowl- edge, the person and the changing world. Pedagogy Cult Soc. 2009;17(1):17–28. 11. Gudo C, Olel M. Oanda, I. University expansion in Kenya and issues of quality education: challenges and opportunities. Int J Bus Soc Sci. 2011;2(20):203–14 (http://www.ijbssnet.com/ journals/Vol_2_No_20_November_2011/22.pdf). 12. Huitt W. Humanism and open education. Educ Psychol Inter- act. 2009 (http://www.edpsycinteractive.org/topics/affect/ humed.html). 13. Carpenter JA, Bell SK. What do nurses know about teach- ing patients? J Nurses Staff Dev. 2002 May-Jun;18(3):157–61. PMID:12189998 14. DaRosa DA, Skeff K, Friedland JA, Coburn M, Cox S, Pol- lart S, et al. Barriers to effective teaching. Acad Med. 2011 Apr;86(4):453–9. PMID:21346500 Book 23-06.indb 420 8/16/2017 1:24:16 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 421 15. Hafler JP, Ownby AR, Thompson BM, Fasser CE, Grigsby K, Haidet P, et al. Decoding the learning environment of medical education: a hidden curriculum perspective for faculty devel- opment. Acad Med. 2011 Apr;86(4):440–4. PMID:21346498 16. Holmboe ES, Ward DS, Reznick RK, Katsufrakis PJ, Leslie KM, Patel VL, et al. Faculty development in assessment: The missing link in competency-based medical education. Acad Med. 2011 Apr;86(4):460–7. PMID:21346509 17. Frenk J, Chen L, Bhutta ZA, Cohen J, Crisp N, Evans T, et al. Health professionals for a new century: transforming educa- tion to strengthen health systems in an interdependent world. Lancet. 2010;376(9756):1923–58. PMID:21112623 Book 23-06.indb 421 8/16/2017 1:24:16 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 422 1Hematology/Oncology Unit (Correspondence to: A. Fouda: ashraf_foda@mans.edu.eg), 2Pediatric Department, Mansoura University Children’s Hospital, Faculty of Medicine, Mansoura University, Mansoura, Egypt. Received: 29/12/15; accepted: 06/11/16 Delays in diagnosis and treatment among children with cancer: Egyptian perspective Suzy Abdelmabood 1, Shaimaa Kandil 2, Ahmed Megahed 2, Ashraf Fouda 1 Délais de diagnostic et de traitement chez les enfants atteints de cancer : perspective égyptienne RÉSUMÉ Les délais de diagnostic constituent l’un des facteurs contribuant à des taux de guérison moins élevés du cancer dans les pays à revenu faible. La présente étude transversale a été menée auprès de 138 enfants atteints de cancer et traités dans l’Unité d’oncologie pédiatrique du Centre d’oncologie de l’Université de Mansoura, en Égypte. Cent-seize patients avaient été mal diagnostiqués à l’origine. Le délai total médian était de 37 jours, avec un délai patient/parent médian de trois jours et un délai médecin médian de 28 jours. Le type de cancer avait une influence significative sur le délai de diagnostic. Le sexe du patient, le niveau d’éducation des parents et le lieu de résidence n’affectaient pas significativement le délai total médian. En revanche, les patients de moins de cinq ans et ceux avec un diagnostic de cancer provisoire posé initialement bénéficiaient du délai total médian le plus court. Nous suggérons de mettre en place des programmes de formation médicale continue, d’améliorer l’accès aux services de diagnostic, et de faciliter l’orientation-recours de façon à donner la priorité aux patients suspects de cancer et ainsi raccourcir le délai de diagnostic. يصرم روظنم :ناطسرلاب ينباصلما لافطلأا جلاعو صيخشت في رخأتلا ةدوف فشرأ ،دهامج دحمأ ،ليدنق ءايش ،دوبعلما دبع يزوس .لـخدلا ةـضفخنلما نادـلبلا في ناـطسرلا نـم ءافـشلا تلادـعم ضـفخ في مهـست يـتلا لـماوعلا دـحأ صيخـشتلا رـخأت ل ِّكـشي :ةـصلالخا ةــ عماج ماروأ زــ كرمب ،لاــ فطلأا ماروأ ةدــ حو في جاــ علل عــ ضخ ناــ طسرلاب ًاــ باصم ًاــ فط 138 ىــ ع ةــ يعطقلما ةــ ساردلا هذــ ه تــ يرجأ دــ قو كـلذ في اـب ،ًاـموي 37 يكـلا رـخأتلا نـمز طـسوتم غـلبو .ةـ يادبلا في ئـطاخ صيخـشتل اوـضرعت دـق ًاـضيرم 160 ناكو .صرـم ،ةروـصنلما ىـع رـبك رـثأت ناـطسرلا عوـنل ناكو .ًاـموي 28 هـتدم ءاـبطلأل رـخأت نـمز طـسوتمو ماـيأ ةـثاث هـتدم ءاـبلآا/ضىرملل رـخأت نـمز طـسوتم في ،يكـلا رـخأتلا نـمز طـسوتم ىـع ًارـبك ًارـثأت هـتماقإ لـمحو هـيدلاو مـيلعت ىوتـسمو ضـيرلما سـنج رـثؤي لم نـح في .صيخـشتلا رـّخأت ذـيفنت حترـقنو .يك رـخأت نـمز طـسوتم صرـقأ ناـطسرلاب مـهتباصإ يـئدبلما صيخـشتلا تـبثأ نـمم وأ تاونـس 5 قوـف ضىرـلما لّجـس نـح ناـطسرلاب مـهتباصإ في هبتـشلما لىإ ةـيولولأا حـنلم ةـلاحلإا رـسيتو ،صيخـشتلا قـفارم لىإ لوـصولا نـستحو ،رمتـسلما يـبطلا مـيلعتلل جـمارب .ناـطسرلا صيخـشت في قرغتـسلما نـمزلا راـصتخلا ABSTRACT Delayed diagnosis is one of the contributing factors to lower cure rates for cancer in low-income countries. This was a cross-sectional study of 138 children with cancer who were treated at the Pediatric Oncology Unit, Oncology Center of Mansoura University, Egypt. One hundred and sixteen patients were initially misdiagnosed. The median total delay was 37 days, including median patient/parent delay of 3 days and median physician delay of 28 days. The type of cancer significantly influenced the diagnostic delay. Patients’ sex, level of parents’ education, and residence did not significantly affect the median total delay, while patients aged < 5 years and those who had an initial provisional diagnosis of cancer had the shortest median total delay. We suggest implementation of continuing medical education programmes, improving access to diagnostic facilities, and facilitating referral to give priority to those with suspected cancer to shorten the time for cancer diagnosis. Book 23-06.indb 422 8/16/2017 1:24:16 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 423 Introduction Overall, cancer remains a rare diagnosis in children. In developed countries, childhood cancer represents < 1% of all cases of cancer; however, in low- resource or developing countries, where children may make up half the popula- tion, the proportion of childhood can- cer can be 5 times higher in comparison. Cancer remains an important cause of childhood mortality, with an estimated 80 000 cancer-related deaths per year worldwide. Although overall survival rates for childhood cancer are ~80% in high-income countries, they may be as low as 10% in developing countries. This may be due to the lack of proper diagnosis, delayed detection and slow referral for treatment (1). Diagnosis of childhood cancer as early as possible is crucial to reduce mortality. Children with cancer have improved response to treatment compared to those who are older, but childhood cancer progresses faster in the absence of treatment than in older individuals (2). High cure rate in cancer needs right diagnosis, quick referral to medical care system, and finishing the required treatment. Cure rates are at least 30% lower in low-income than higher-income countries (3), which may be due to delay in diagnosis (ad- vanced stage of cancer), more fatal tox- icities, incomplete or abandonment of treatment (4). Few studies have been published on determinants and impacts of diagnostic delay in childhood cancer. Practical new strategies to reduce diagnostic delay are needed and require study and un- derstanding of diagnostic delays and their impact on the prognosis of can- cer (5). To the best of our knowledge, few studies have been conducted in Egypt to assess diagnostic delay in child- hood cancer. We evaluated different factors resulting in diagnostic delay in 138 children aged 1 month to 17 years, who were diagnosed with cancer or referred to the Pediatric Oncology Unit, Oncology Center of Mansoura Uni- versity, Egypt. Our Oncology Center is a regional tertiary referral centre for children with cancer in the Egyptian Delta Region, which has ~5.5 million inhabitants. Methods Setting This was a cross-sectional study of chil- dren diagnosed with cancer at our insti- tution from November 2013 to January 2015. Of the 168 patients approached, 138 agreed to participate. There were 77 boys (55.8%) and 61 girls (44.2%), with a male to female ratio of 1.0: 0.8 and age range of 1 month to 17 years. Data collection Data were collected from parent inter- views upon admission to the Pediatric Oncology Unit. All referral documents (letters, imaging and laboratory study reports) were reviewed and examined to establish approximate dates of initial medical contact, diagnostic tests and initial diagnosis. We estimated the time in days from the onset of patients’ symptoms to the beginning of cancer treatment (total delay). Different com- ponents of delay were obtained from the date of onset of symptoms until the first medical contact (patient/parent delay); time from initial medical con- tact until the patient was assessed by an oncologist (referral delay); time from referral to an oncologist until the final diagnosis of cancer (diagnostic delay); and time from diagnosis of cancer until the start of treatment (treatment delay) (Figure 1). The term misdiagnosis was used when another benign disease was diagnosed provisionally and cancer was not suspected. The patients’ characteristics in- cluded: age at diagnosis, sex, parental educational level, residence, duration of illness at diagnosis, type of malignancy, initial symptoms, initial diagnosis by a healthcare professional, and initial phy- sicians’ notes before the final diagnosis of malignancy was recorded. The most common malignancies were: leukaemia (including acute lymphoblastic leukae- mia and acute myeloid leukaemia), lym- phoma [Hodgkin’s disease (HD) and non-Hodgkin’s lymphoma (NHL)], Wilms’ tumour, neuroblastoma (NB), rhabdomyosarcoma (RMS), bone tumours (Ewing sarcoma and osteo- sarcoma), germ cell tumours (GCTs), brain tumours, and histiocyte disorders. Statistical analysis Data were analysed using SPSS version 21.0 (Chicago, IL, USA). Numerical data were presented as mean (standard deviation; SD) if normally distributed and as median and interquartile range (IQR) (25th–75th centiles) if not normally distributed. Delay times were mostly right-skewed, so nonparametric tests were used. The Mann–Whitney U test was used to compare between 2 groups and the Kruskal–Wallis test to compare among >2 groups. Categorical data were compared using the χ2 test. P < 0.05 was considered to indicate statistical significance. Results Sex, age at diagnosis, level of parents’ education, residence, initial provisional suspicion of malignancy and type of malignancy, and their relationship to the total delay in cancer diagnosis are shown in Table 1. Sex and level of par- ents’ education did not significantly af- fect median total delay. In contrast, age at diagnosis had a significant effect on total delay, as patients aged < 5 years at diagnosis had the shortest median total delay. When malignancy was initially suspected, the median total delay for these patients was significantly shorter. The median total delay was significantly influenced by the type of cancer; the shortest delay was observed among Book 23-06.indb 423 8/16/2017 1:24:16 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 424 patients with Wilms’ tumour, followed by acute leukaemia and NHL. Most of the patients were diagnosed at an advanced stage of malignancy as follows: NHL: 1, 14 and 7 patients had stage I, III and IV, respectively; NB: 3, 4 and 8 patients had stage II, III and IV, respectively; HD: 1, 1, 2 and 1 patient had stage I, II, III and IV, respectively); Wilms’ tumour: 2, 3, 4 and 1 patient had stage I, II, III and IV, respectively); bone tumours (Ewing sarcoma and osteosar- coma): 2, 6, 2 and 2 patients had stage T1N0M0, T2N0M0, T2N1M1 and T3N1M0, respectively. Median total delay for all patients was 37.0 days (IQR 21.5–67.0 days, range 1.0–417.0 days). Median patient/ parent diagnostic delay was 3.0 days (IQR 1.0–7.0 days, range 1.0–365.0 days). The shortest delay was in patients with Wilms’ tumour, hepatoblastoma, Langerhans cell histocytosis (LCH), leukaemia and NB. The longest delay was 101.0 days in patients with HD. Median physician delay (referral + di- agnostic delay) was 28.0 days (IQR 15.0–51.0 days, range 1.0–312.0 days). The shortest delay was in patients with GCT, NHL, brain tumours and leukaemia. Median referral delay was 14.5 days (IQR 3.0–30.0 days, range 1.0–300.0 days). The shortest delay was in patients with GCT, Wilms’ tu- mour, NHL and leukaemia. Median diagnostic delay was 12.0 days (IQR 8.0–17.25 days, range 1.0–120.0 days). The shortest delay was in patients with hepatoblastoma, leukaemia, brain tu- mours and RMS. Median treatment delay was 1.0 day (IQR 0–1.0 day, range 1.0-60.0 days). The median treatment delay was 1.0–2.5 days for different types of tumours. Median health system delay (physician + treatment delays) was 30.0 days (IQR 16.0–54.0 days, range 7.0–313.0 days). The shortest duration was in patients with GCT, Wilms’ tumour, NHL and leukaemia. Different components of delay lengths for each type of cancer: patient/parent delay, referral delay, diagnostic delay, physician delay, treatment delay and health system delay are shown with the mean age at the start of symptoms (Table 2). Common initial presenting symp- toms for our patients were: fever, which was the most common initial symptom in 44 patients, followed by bone aches, limping or difficulty walking in 26 cases, abdominal symptoms (pain, enlarge- ment and mass) in 20 patients and pal- lor in 16 patients (Table 3). Diagnostic clues suggestive for initial provisional diagnosis of cancer (according to different types of cancer) were: complete blood count, which was helpful for suspecting malignancy in 41.3% of cases; imaging such as ab- dominal ultrasound, X ray, computed tomography and magnetic resonance imaging was suggestive of cancer in 29.7, 9.4, 2.9 and 8.0% of cases, respec- tively (Table 3). Biopsies were essential to differentiate malignancy from other benign conditions in 8.7% of patients. In an attempt for physicians to reach a diagnosis or explain their patients’ complaints, provisional initial diagnoses ranged from everyday minor problems (e.g., common cold/pharyngitis and tonsillitis) to more serious diagnoses such as arthritis, myositis, osteomyeli- tis or juvenile rheumatoid arthritis to explain symptoms like fever and feeling unwell, bone pain and limb swelling. Pallor and anaemia were interpreted as iron deficiency anaemia (14 patients) or favism (1 patient). Abdominal Figure 1 Schematic representation of different delay variables Total delay Health care delay Physician delay Patient/parent delay Referral delay Diagnosis delay Treatment delay Onset of symptoms Initial health care contact Assessment by oncologist Final diagnosis Start treatment Book 23-06.indb 424 8/16/2017 1:24:16 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 425 symptoms were misdiagnosed as gas- troenteritis/gastritis, parasitic infesta- tion or even hepatitis (Table 3). Initial healthcare providers con- tacted were paediatricians (47.1% of patients), general practitioners (13.8% of patients) and internal medicine physicians (15.9% of patients). Some patients initially contacted physicians in other specialties due to different disease presentations: for example, orthopae- dics (for arthralgia, arthritis or bone pain) or ophthalmology (for proptosis or raccoon eyes). There was no signifi- cant difference in physician diagnostic delay regardless of whether the first physician contacted was a paediatrician (P = 0.959). One hundred and sixteen (84.1%) patients were initially wrongly diagnosed (cancer was not suspected), and 22 patients (15.9%) were provi- sionally suspected of having cancer from the start of seeking medical advice (Table 3). Malignancy was correctly suspected in 10 of 64 patients with leu- kaemia, 6 of 10 with Wilms’ tumour, 3 of 22 with NHL, 2 of 3 with GCT, and 1 of 15 with NB. None of the patients with bone tumours (12 patients), HD (5 patients) , RMS (2 patients), brain tumors (2 patients), LCH (2 patients) or hepatoblastoma (1 patient) were correctly suspected to have malignancy. Most of the patients (13 of 22; 59.1%) correctly suspected for malignancy, were first seen by a paediatrician. Table 1 Total delay in relation to different patients’ characteristics Patients characteristics No. of patients (%) Total delay (d) Median (IQR: 25th–75th) P Sex Male 77 (55.8%) 29.0 (19.0–48.0) 0.590 Female 61 (44.2%) 42.0 (25.0–76.5) Age 0–5 years 77 (55.8%) 29.0 (19.0–50.5) 0.038* 5–10 years 28 (20.3%) 39.0 (25.5–66.5) >10 years 33 (23.9%) 45.0 (27.5–145.5) Parents level of education No education (illiterate) 22 (15.9%) 39.50 (26.75–64.5) 0.727 Low education (below high school) 98 (71.0%) 35.50 (20.0–70.25) High education 18 (13%) 33.0 (15.5–75.5) Patient residence Urban area 63 (45.7%) 32 (19.0–64.0) 0.564 Rural area 75 (54.3%) 39 (22.0–71.0) Initial provisional diagnosis Correct (suspected cancer) 22 (15.9%) 19.50 (12.75–39.0) 0.039* Wrong diagnosis 116 (84.1%) 38.0 (24.25–70.45) Type of malignancy Leukaemia (ALL+AML) 64 (45.7%) 31.0 (19.0–46.5) 0.026* Hodgkin’s disease 5 (3.5%) 240.0 (44.5–368.5) Non-Hodgkin’s lymphoma 22 (15.9%) 32.0 (23.75–55.25) Neuroblastoma 15 (10.5%) 39.0 (28.0–70.0) Wilms’ tumour 10 (7.0%) 22.50 (13.5–32.5) Rhabdomyosarcoma 2 (1.4%) 88.5 (40.0–137.0) Ewing sarcoma 6 (4.4%) 72.50 (60.75–173.25) Osteosarcoma 6 (4.4%) 130.50 (62.0–205.25) GCT 3 (2.2%) 12.0 (1.0–15.0) LCH 2 (1.4%) 39.50 (24.0–55.0) Brain tumour 2 (1.4%) 44.0 (7.0–81.0) Hepatocellular carcinoma 1 (0.7%) 187.0 *Significant at P < 0.05 (Mann–Whitney U test to compare between two groups, and Kruskal–Wallis to compare among > 2 groups). ALL = acute lymphoblastic leukaemia; AML: acute myeloid leukaemia; GCT = germ cell tumour; LCH = Langerhans cells histocytosis. Book 23-06.indb 425 8/16/2017 1:24:16 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 426 Discussion Although the outcomes of childhood cancer are better to some extent than those of adult cancer, the tumours grow at a faster rate unless they are treated. This can be partially overcome by early diagnosis (2). In this study, the median total delay was 37 days, which was shorter than that reported by a recent study from Egypt (47 days) (6). However, our delay was longer than in previous Canadian (7) and South African (2) studies that reported a me- dian total diagnostic delay of 30 and 34 days, respectively. Differences in healthcare systems, physician attitudes and concerns about childhood cancer, and socioeconomic and cultural factors may have been responsible for the dif- ferent results. The median patient/parent delay was 3 days, which is shorter than in pre- vious Egyptian (6), Canadian (7) and South African (2) studies (8, 9 and 5 days, respectively). This may have been because 55.8% of the study population that had the shortest parent delay was aged < 5 years. The median physician delay was 28 days, which was longer than in previous studies from Canada, South Africa and Turkey (8, 20 and 23 days, respectively) (2,7,8). This may have been due to dif- ficulties facing the physicians or lack of awareness of presentation and diag- nosis of childhood cancer. It might also be explained by the presence of other major concerns for the physicians in developing countries, like malnutrition, infectious disease and parasitic infec- tions rather than suspecting malignan- cies in children. It may also have been due to lack of facilities and equipment for diagnosis of cancer in developing countries. Sex of the patients did not signifi- cantly affect the time to diagnosis. This agrees with previous studies (2,6–8), although other studies (9–11) have Ta bl e 2 Le ng th o f d el ay a nd a ge a t c lin ic al o ns et b y ty pe s of tu m ou r Ty pe o f t um ou r N o. o f p at ie nt s (% ) A ge a t s ta rt o f sy m pt om s, y r M ea n (S D ) Pa ti en t/ pa re nt s d el ay M ed ia n (IQ R) Re fe rr al d el ay M ed ia n (IQ R) D ia gn os is d el ay M ed ia n (IQ R) Tr ea tm en t d el ay M ed ia n (IQ R) Ph ys ic ia n de la y M ed ia n (IQ R) H ea lt h sy st em de la y M ed ia n (IQ R) Le uk ae m ia 64 (4 6. 4% ) 6. 11 (4 .2 ) 3. 0 (1 .0 –9 .5 ) 14 .5 (3 .5 –3 0 .0 ) 9. 5 (7 –1 2) 1.0 (0 –1 .0 ) 27 .0 (1 3. 25 –3 9. 0 ) 27 .5 (1 3. 25 –3 9. 0 ) H od gk in ’s di se as e 5 (3 .6 % ) 8. 8 (4 .14 ) 10 1.6 (4 .5 –2 42 .0 ) 30 .0 (1 4. 5– 19 5. 0 ) 21 .0 (1 3. 0 –3 0 .0 ) 1.0 (0 –1 .0 ) 51 .0 (3 6. 5– 21 6. 0 ) 52 .0 (3 6. 5– 21 6. 0 ) N H L 22 (1 5. 9% ) 7.2 3 (4 .19 ) 5. 0 (1 .0 –7 .0 ) 10 .0 (3 .5 –3 1.5 ) 14 .0 (1 0 .0 –1 9. 5) 1.0 (0 –2 .0 ) 26 .0 (1 6. 0 –4 5. 0 ) 26 .0 (1 6. 0 –4 5. 0 ) H ep at ob la st om a 1 ( 0 .7 % ) 14 .0 1.0 18 0 .0 5. 0 2. 0 18 5. 0 18 7.0 Br ai n tu m ou r 2 (1. 4% ) 9. 75 (6 .0 1) 15 .0 (1 .0 –3 0 .0 ) 15 .5 ( 1.0 –3 0 .0 ) 11 .0 (1 .0 –2 1.0 ) 2. 5 (1. 0 –5 .0 ) 26 .5 (2 .0 –5 1.0 ) 29 .0 (7 .0 –5 1.0 ) RM S 2 (1. 4% ) 7.0 (0 ) 11 .5 0 (2 .0 –2 1.0 ) 61 .0 (2 .0 –1 20 .0 ) 13 .5 (1 3. 0 –1 4. 0 ) 2. 5 (1. 0 –4 .0 ) 74 .5 (1 5. 0 –1 34 .0 ) 77 .0 (1 9. 0 –1 35 .0 ) Bo ne tu m ou ra 12 (8 .6 % ) 11 .5 8 (4 .3 1) 7.0 (7 .0 –8 2. 5) 37 .5 (3 0 .0 –9 0 .0 ) 20 .0 (1 4. 25 –2 8. 5) 1.0 (1 .0 –1 .5 ) 62 .0 (3 8. 75 –1 31 .2 5) 62 .0 (4 5. 5– 13 2. 75 ) G C T 3 (2 .1% ) 8. 33 (6 .4 2) 15 .0 (1 .0 –2 4. 0 ) 1.0 (1 .0 –2 .0 ) 14 .0 (7 .0 –1 5. 0 ) 1.0 (0 –1 .0 ) 15 .0 (8 .0 –1 7.0 ) 15 .0 (8 .0 –1 7.0 ) W ilm s’ tu m ou r 10 (7 .0 % ) 3. 65 (2 .7 9) 0 .5 (1 .0 –1 .2 5) 2. 0 (1 .0 –1 0 .5 ) 15 .0 (1 0 .5 –2 1.0 ) 1.0 (0 –1 .2 5) 22 .0 (1 2. 5– 30 .7 5) 22 .0 (1 2. 25 –3 1.2 5) N eu ro bl as to m a 15 (1 0 .9 % ) 2. 42 (1 .4 9) 3. 0 (1 .0 –7 .0 ) 14 .0 (4 .0 –4 0 .0 ) 15 .0 (1 1.0 –2 1.0 ) 1.0 (0 –1 .0 ) 34 .0 (1 7.0 –7 0 .0 ) 36 .0 (1 7.0 –7 0 .0 ) LC H 2 (1. 4% ) 2. 0 (1 .4 1) 1.5 (1 .0 –2 .0 ) 21 .0 (2 .0 –4 0 .0 ) 17 .0 (1 4. 0 –2 0 .0 ) 1.0 (0 –1 .0 ) 38 .0 (2 2. 0 –5 4. 0 ) 38 .0 (2 2. 0 –5 4. 0 ) To ta l c as es m ed ia n (IQ R) [m in –m ax ] 13 8 (1 0 0 % ) 6. 39 (4 .5 1) 3. 0 (1 .0 –7 .0 ) [1 –3 65 ] 14 .5 (3 .0 –3 0 .0 ) [1 –3 0 0 ] 12 .0 (8 .0 –1 7.2 5) [1 –1 20 ] 1.0 (0 –1 .0 ) [1 –6 0 ] 28 .0 (1 5. 0 –5 1.0 ) [1 –3 12 ] 30 .0 (1 6. 0 –5 4. 0 ) [7 –3 13 ] Re su lts p re se nt ed a s d ay s u nl es s s ta te d ot he rw is e. a O st eo sa rc om a + Ew in g sa rc om a. G C T = ge rm ce ll tu m ou r; IQ R = in te rq ua rt ile ra ng e; L C H = L an ge rh an s c el ls h is to cy to si s; N H L = no n- H od gk in ’s ly m ph om a; R M S = rh ab do m yo sa rc om a. Book 23-06.indb 426 8/16/2017 1:24:16 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 427 reported a significantly longer delay for male patients. Patients aged < 5 years had the shortest diagnostic delay, which was similar to a previous systematic review that showed that time to diagnosis was significantly shorter for younger chil- dren (12). Probable interpretations are that younger children have better medi- cal care, observation and examination by their parents /physicians than older children are, and many older children might be unwilling to reveal their com- plaints and symptoms. Also, different tumour types vary with regard to growth patterns in different age groups. Some slow-growing tumours (ganglioglioma or localized Ewing sarcoma) are more common in older children in compari- son to some rapid-growing aggressive tumours (nephroblastoma, leukaemia or choroid plexus carcinoma), which are common in younger age groups (12). Unexpectedly, the level of parents’ education did not significantly influ- ence the diagnostic delay. This can be explained by the small number of parents with higher educational levels in our study (n = 18; 13%), which was similar to a South African study with a low numbers of highly educated par- ents, which did not affect the delay sig- nificantly (2). These results differ from a Canadian study reporting a greater percentage of highly educated parents (41.8%) who had a significantly shorter median total delay (6). Whether the patients were from a rural or urban area did not significantly affect total delay time. This may have been due to the small surface area of the Delta Region that is covered by our hospital, as the patients can reach most healthcare facilities (university hospi- tals, regional local hospitals or private clinics) within a short period of time. This finding was similar to another study from the Egyptian Delta (6). The diagnostic delay was signifi- cantly influenced by the type of tumour. The shortest delay was observed for Wilms’ tumour (median 22.5 days) followed by acute leukaemia (31 days) and NHL (32 days). This may have been due to the younger age at the time of symptom onset among Wilms’ tu- mour patients and the large abdominal mass in relation to small body size mak- ing the tumour easily recognizable. Our results were consistent with most of the previous studies that found shorter diagnostic delay for leukaemia, renal tumours, NB and NHL; intermediate delay for HD, RMS, GCT and retino- blastoma; and longer delay for brain tumours, bone tumours and soft-tissue sarcoma (5,7,12,13). This also may be Table 3 Common presentations of cancer, diagnostic clues and initial misdiagnoses Different clinical and diagnostic parameters Total no. of patients (%) Main initial presenting symptoms Fever 44 Bone pain/limping/difficulty walking 26 Abdominal pain/enlargement/mass 20 Pallor 16 Lymph node swelling 15 Constipation/diarrhoea, vomiting 8 Swelling (jaw, skull or legs) 7 Bleeding (hematemesis/melena, vaginal bleeding, epistaxis) 5 Cough/respiratory distress 4 Rare: testicular swelling, eye (proptosis), jaundice, priapism, polyphagia/polysomnia 3, 2, 1, 1, 1 Diagnostic clues suggestive of cancer diagnosis Complete blood count 57 (41.3%) X ray 13 (9.4%) Abdominal ultrasonography 41 (29.7%) Computed tomography 4 (2.9%) Magnetic resonance imaging 11 (8.0%) Biopsy 12 (8.7%) Misdiagnosis initially (cancer was not suspected) 116 (84.1%) Common cold/pharyngitis/tonsillitis 17 Arthritis/myositis 15 Anaemia (iron deficiency/favism) 15 Infections (UTI, typhoid, appendicitis, osteomyelitis, septicaemia) 14 Gastroenteritis/gastritis 7 Parasitic infestation (worms) 7 Lymphadenitis 6 Bronchitis/bronchial asthma 4 Radiculitis/disc prolapse/GBS/post-injection injury 4 Hepatitis 3 Bleeding tendency/normal menarche 3 Functional constipation/food poisoning 2 Correctly suspected (malignancy suspected initially) 22 (15.9%) GBS = Guillain–Barré syndrome; UTI = urinary tract infection. Book 23-06.indb 427 8/16/2017 1:24:16 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 428 References 1. The International Agency for Research on Cancer. Interna- tional Childhood Cancer Day: much remains to be done to fight childhood cancer. 15 February 2016 (http://www.iarc.fr/ en/media-centre/pr/2016/pdfs/pr241_E.pdf, accessed on 23 March 2016). 2. Stefan DC, Siemonsma F. Delay and causes of delay in the diagnosis of childhood cancer in Africa. Pediatr Blood Cancer. 2011 Jan;56(1):80–5. PMID:21108442 3. Bonilla M, Moreno N, Marina N, deReyes G, Shurtleff SA, Downing JR, et al. Acute lymphoblastic leukemia in a devel- explained by different tumour growth patterns: slowly growing patterns tu- mours, such as low-grade astrocytoma, ganglioglioma or localized Ewing sarco- ma are diagnosed more slowly, whereas aggressive fast-growing tumours such as Wilms’ tumour, leukaemia and NHL are diagnosed more quickly (12). The median total delay for leukaemia was 31 days, which was the same as in a South African study (2), while the median diagnosis delay in a Canadian study was 18 days (7). The shortest median physi- cian delay for leukaemia was in Canada (3 days) (7), while it was 27 days in the current study and 22 days in the South African study (2). Reasons for this large difference could be that the physicians may have had difficulty suspecting and recognizing symptoms of leukaemia, or unavailability of diagnostic facilities such as bone marrow examination and flow cytometry. The longest total delay in the current study was for diagnosis of HD and bone tumours. This may have been partly related to the quiescent nature of HD, making the patient/parent delay long (median 101 days). Also, bone tumour diagnosis was characterized by long physician delay, which may have been because of the slow growing nature of these tumours, wrong initial diagnoses and lack of facilities for diagnosis (imag- ing or open bone biopsy). Eighty-four percent of our patients were initially misdiagnosed and only 16% were suspected to have cancer at the time of their first visit to a physician. More than half of those suspected to have cancers initially (59.1%) were seen by a paediatrician, which indicated the awareness of paediatricians (to some ex- tent) for cancer occurrence in children. Most of the correctly suspected patients had leukaemia and Wilms’ tumour. Leukaemia was suspected because of prolonged fever, pallor, bleeding ten- dency and abdominal enlargement. Wilms’ tumour was the only tumour with a higher percentage of initial cor- rect diagnoses compared to other tu- mours, which may be for the reasons mentioned before. This differs from another study from Egypt that reported that misdiagnosis was initially recorded in 39.5% of patients (6), but was similar to previous studies (13–15) showing that diagnostic delay was significantly longer when patients were seen for the first time by a general practitioner rather than a paediatrician. Common presentations of cancer in our study were fever, bone pain, dif- ficulty walking and abdominal enlarge- ment/pain, which denote that previous such complaints may be serious. With presentation of fever, especially when it is prolonged or of unknown origin, malignancy should be included in the differential diagnosis, which requires thorough clinical examination and further investigation. Abdominal pain, although it is a common paediatric problem, may signify serious illness, es- pecially when it is persistent, interfering with daily activities or accompanied by abdominal enlargement, which may necessitate abdominal ultrasonography. Our study had several limitations. First, the small sample size and that most of the patients were from the Egyptian Delta Region. Second, recall bias was an issue when questioning about the beginning of symptoms, but we attempted to achieve accuracy by reviewing dates of referral letters and ini- tial written suspected diagnoses. Third, there was difficulty in evaluating the socioeconomic status of parents due to cultural issues, as most of the parents refused to give information when they were asked about their income. In conclusion, we suggest shorten- ing diagnostic delay through the im- plementation of continuing medical education programmes for healthcare providers, which is not obligatory yet in Egypt, and specialty medical training about childhood cancer and the mode of cancer presentation. Parents should be encouraged to seek medical advice from specialists, such as paediatricians, to help with early recognition of alarm signs. This will improve the diagnostic skills of the physicians, their index of suspicion, and facilitate and enhance the healthcare system to minimize the time to referral for a child with possible cancer. Also, facilitating referral to give priority to those with suspected cancer diagnosis, while improving access to diagnostic facilities, will help to shorten the time to final diagnosis of cancer. Acknowledgements We would like to thank Dr. Lesleigh Abbott, MD, FRCPC, Assistant Pro- fessor, Hematologist/Oncologist, The Children’s Hospital of Eastern Ontario (CHEO), Ottawa, Ontario, Canada, for English language review and correction of the manuscript. We would also like to thank Dr. Soha Aly Elmorsy, MD, PhD, Research Consult- ant, KAMC, Saudi Arabia, for statistical revision of the study. Funding: None. Competing interests: None declared. Book 23-06.indb 428 8/16/2017 1:24:17 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 429 oping country: preliminary results of a nonrandomized clini- cal trial in El Salvador. J Pediatr Hematol Oncol. 2000 Nov-Dec;22(6):495–501. PMID:11132215 4. Howard SC. Wilimas JA. Delays in diagnosis and treatment of childhood cancer: where in the world are they important? Pediatr Blood Cancer. 2005 Apr;44(4):303–4. PMID:15486952 5. Dang-Tan T, Franco EL. Diagnosis delays in childhood cancer: a review. Cancer. 2007 Aug 15;110(4):703–13. PMID:17620277 6. Abdelkhalek E, Sherief L, Kamal N, Soliman R. Factors associ- ated with delayed cancer diagnosis in egyptian children. Clin Med Insights Pediatr. 2014 Sep 4;8:39–44. PMID:25232287 7. Dang-Tan T, Trottier H, Mery LS, Morrison HI, Barr RD, Green- berg ML, et al. Delays in diagnosis and treatment among chil- dren and adolescents with cancer in Canada. Pediatr Blood Cancer. 2008 Oct;51(4):468–74. PMID:18454472 8. Araz NC, Guler E. Delays in diagnosis of childhood cancer in southeastern Turkey and the associated factors. Pediatr Hema- tol Oncol. 2015 Mar;32(2):153–63. PMID:24498898 9. Halperin EC, Watson DM, George SL. Duration of symptoms prior to diagnosis is related inversely to presenting disease stage in children with medulloblastoma. Cancer. 2001 Apr 15;91(8):1444–50. PMID:11301391 10. Crawford JR, Zaninovic A, Santi M, Rushing EJ, Olsen CH, Keating RF, et al. Primary spinal cord tumors of childhood: effects of clinical presentation, radiographic features, and pathology on survival. J Neurooncol. 2009 Nov;95(2):259–69. PMID:19521666 11. Widhe B, Widhe T. Initial symptoms and clinical features in osteosarcoma and Ewing sarcoma. J Bone Joint Surg Am. 2000 May;82(5):667–74. PMID:10819277 12. Brasme JF, Morfouace M, Grill J, Martinot A, Amalberti R, Bons-Letouzey C, et al. Delays in diagnosis of paediatric cancers: a systematic review and comparison with expert testimony in lawsuits. Lancet Oncol. 2012 Oct;13(10):e445–59. PMID:23026830 13. Loh AH, Aung L, Ha C, Tan AM, Quah TC, Chui CH. Diagnostic delay in pediatric solid tumors: a population based study on determinants and impact on outcomes. Pediatr Blood Cancer. 2012 Apr;58(4):561-5. PMID:22052842 14. Haimi M, Peretz Nahum M, Ben Arush MW. Delay in diag- nosis of children with cancer: a retrospective study of 315 children. Pediatr Hematol Oncol. 2004 Jan-Feb;21(1):37–48. PMID:14660305 15. Haimi M, Perez-Nahum M, Stein N, Ben Arush MW. The role of the doctor and the medical system in the diagnostic delay in pediatric malignancies. Cancer Epidemiol. 2011 Feb;35(1):83–9. PMID:20685192 Book 23-06.indb 429 8/16/2017 1:24:17 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 430 1College of Pharmacy, Qatar University, Qatar (Correspondence to: Ziad Nasr: znasr@qu.edu.qa). Received: 03/6/16; accepted: 16/11/16 Review The impact of antimicrobial stewardship strategies on antibiotic appropriateness and prescribing behaviours in selected countries in the Middle East: a systematic review Ziad Nasr,1 Bridget Paravattil 1 and Kyle J. Wilby 1 L’impact des stratégies de gestion des antimicrobiens sur la pertinence des antibiotiques et les comportements en matière de prescription au Moyen-Orient : analyse systématique RÉSUMÉ La résistance aux antimicrobiens est un problème de santé mondial et la gestion des antimicrobiens constitue une composante essentielle des politiques hospitalières dans le monde. Pourtant, il existe actuellement peu d’informations sur l'efficacité des stratégies de mise en œuvre au Moyen-Orient. Nous avons passé en revue des études conduites dans la région utilisant différentes stratégies de gestion des antimicrobiens afin d’évaluer la pertinence des antimicrobiens et les comportements en matière de prescription. Une recherche dans Medline, Embase, International Pharmaceutical Abstracts, Google et Google Scholar a été effectuée. Vingt articles répondaient au critère d’inclusion, deux études évaluaient les stratégies incluant des audits prospectifs avec rétro-information, tandis que 18 autres évaluaient des stratégies incluant des analyses comparatives de l’utilisation des antimicrobiens par rapport aux procédures. Les recommandations en matière de mise en œuvre de la gestion des antimicrobiens au Moyen-Orient soulignaient l’importance de développer et de mettre à jour les politiques locales de prescription des antimicrobiens, et de recourir à des approches interdisciplinaires collaboratives, si l’on veut assurer le succès des programmes. في اـهفصو تايكولـسو ةـيويلحا تاداـضلما ةـمءلام ىدـم ىـع تاـبوركيلما تاداـضمب ةـقلعتلما ةرادلإا تايجيتارـسا رـثأ يـجهنم ضارعتـسا :طـسولأا قرـلا يبليو .ج لياك ،ليتافاراب تيجديرب ،صرن دايز تايفـشتسلما تاـسايس في ًايـساسأ ًاصرنع تابوركيلما تاداـضم ةرادإ لـثتمو ،ةـيلماع ةيحص ةلكـشم تاـبوركيلما تاداـضم ةـمواقم لـّثتم :ةـصلالخا ًاضارعتـسا اـنيرجأ دـقو .طـسولأا قشرـلا في لاـّعفلا ذـيفنتلا تايجيتاترـسا نأـشب تاـمولعلما نـم رـثكلا دـجوي لا هـنأ لاإ ،لماـعلا ءاـحنأ عـيجم في تاداضم ةـمءام ىدـم مييقت لجأ نـم تاـبوركيلما تاداـضم ةرادلإ ةـفلتمخ تايجيتاترـسا تـقبُط ثـيح ةـقطنلما هذـه في تذـ ِّفُن يـتلا تاـساردلل ثحبلا يـكرمحو ،ةيلودلا ةـينلاديصلا تاـصالخاو EMBASEو MEDLINE تاـنايب دـعاوق ىـع ثـحب ىرـجُأو .اـهفصو تايكولـسو تاـبوركيلما ءارـجإ نـمضتت يـتلا تايجيتاترـسلاا مـييقتب ناتـسارد تـينُعف ؛ضارعتـسلاا في جاردلإا رـياعم ًلااـقم 20 فىوتـساو .Google Scholarو Google تاداـضم مادختـسا ةـنراقم نـمضتت يـتلا تايجيتاترـسلاا مـييقت لىإ ىرـخأ ةـسارد 18 تدـمع نـح في ،تاـقيلعت رـفوت عـم ةـيعّلطت ةـعجارم ةـصالخا تاـسايسلا ثـيدتحو دادـعإ ةـيهمأ طـسولأا قشرـلا في فاشرلإا ذـيفنتب ةـقلعتلما تاـيصوتلا تزرـبأو .ةـيهيجوتلا ئداـبلماب تاـبوركيلما .حاـجنلا قـيقحتل تاـصصختلا ةددـعتم ةـينواعت جُـُنه مادختـساو يـحلما ىوتـسلما ىـع تاـبوركيلما تاداـضم فـصوب ABSTRACT Antimicrobial resistance is a global health problem and antimicrobial stewardship is an essential component of hospital policies worldwide yet little is known regarding effective implementation strategies in the Middle East. We conducted a review of studies carried out in this region that deployed different antimicrobial stewardship strategies to assess antimicrobial appropriateness and prescribing behaviours. A search of MEDLINE, EMBASE, International Pharmaceutical Abstracts, Google and Google Scholar was conducted. Twenty articles met the inclusion criteria; 2 studies evaluated strategies including prospective audit with feedback, while 18 others evaluated strategies including benchmarking antimicrobial utilization against guidelines. Recommendations for implementation of stewardship in the Middle East highlighted the importance of developing and updating local antimicrobial prescribing policies and using collaborative interdisciplinary approaches for success. Book 23-06.indb 430 8/16/2017 1:24:17 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 431 Introduction Antimicrobial resistance is known to be one of the major threats to global health, mainly due to the prevalence of injudicious and overzealous use of an- timicrobials (1). The world has reached a post-antibiotic era where major and even minor injuries can lead to multi- drug-resistant infections and result in mortality, as available antibiotic options may not be available for treatment (1). This is alarming, especially that resistant bacterial illnesses increases the cost of treatment and extends the course of therapy. As such, the duration of hospi- talizations, the overall health care costs and the economic burden on families and societies worldwide will increase (1). In fact, the World Health Organi- zation (WHO) states that multidrug- resistant bacterial infections have led to more than 8 million additional hospital stays and currently cost the health care system in excess of US$ 20 billion (2). Antimicrobial stewardship refers to a set of coordinated strategies that focus on promoting appropriate antibi- otic use in inpatient health care settings while improving patient outcomes, ensuring patient safety, reducing phar- macy cost for antibiotics and decreasing antimicrobial resistance and the spread of infections caused by multidrug-re- sistant organisms (3,4). Antimicrobial stewardship programmes are typically hospital-based programmes designed to ensure that patients receive the right antibiotic, at the right dose, at the right time and for the right duration (5–7). An effective programme is one that has committed leadership and necessary human, financial and information tech- nology resources. The literature shows that successful programmes are those that are led by a coalition between phy- sicians and clinical pharmacists (8–10). While most research conducted is re- ported from centres in North America and Europe, international guidelines are currently being developed and dis- seminated. However, institutions in the Middle East and the Persian Gulf region still lack firm and clear guidelines for proper antimicrobials use, which are essential for the success of local pro- grammes due to regional variations in antibiotic utilization and prevalence of resistant organisms (10). Antimicrobial stewardship interven- tions can only be successful if they meet the specific needs of the health care institution with dedicated multifaceted, multidisciplinary teams (physicians, pharmacists and nurses), administra- tors and policy-makers (9). These in- terventions include: prospective audits with intervention and feedback; im- plementation of formulary restriction programmes and pre-authorization requirements for specific antimicrobials within individual institutions; educa- tion; compliance with local/national guidelines and dissemination of clinical pathways; antimicrobial cycling and order forms; streamlining or therapy de-escalation; use of combination anti- microbial therapy; and dose optimiza- tion, or the switch from the intravenous route of administration to oral when indicated (7). In general, such interven- tions typically require essential compo- nents such as stakeholder buy-in, review of documentation systems, navigation of prescriber–pharmacist relationships and national/institutional prescribing policies (11,12). In order to address the unique needs of individual institutions through implementation of a proactive antimi- crobial stewardship programme and to provide guidance for future programme development, we conducted a review of studies that adopted different anti- microbial stewardship strategies in the Middle East region to assess antimi- crobial utilization and evaluate antimi- crobial prescribing behaviours within hospitals. A secondary objective was to determine core recommendations for programme development in the Middle Eastern context. Methods A search of MEDLINE (1948–Feb- rua ry 2 01 6), E MBASE (1980– F e b r u a r y 2 0 1 6 ) , I n t e r n a t i o n a l Pharmaceutical Abstracts (1970– February 2016), Google and Google Scholar was conducted for articles assessing prescribing patterns of antibi- otics and evaluating the use of antimi- crobials within health care institutions in selected countries in the Middle East region. Search terms included combina- tions of ‘antimicrobial’, ‘antimicrobial stewardship’, ‘prescribing’, ‘utilization’, ‘resistance’, and ‘Middle East’, ‘Bahrain’, ‘Iraq’, ‘Jordan’, ‘Kuwait’, ‘Lebanon’, ‘Oman’, ‘Palestine’, ‘Qatar’, ‘Saudi Ara- bia’, ‘Syria’, ‘United Arab Emirates’ and ‘Yemen’. The reference lists of the arti- cles identified were manually searched for pertinent articles that were not iden- tified in the electronic search. Identified abstracts were included if the study was published in English and had at least 1 antibiotic prescribing pattern or its use was assessed or evaluated in a hos- pital inpatient setting. All populations were included. Articles were excluded if they were done in a community setting (including health centres or primary health clinics), addressed general drug prescribing patterns with no focus on antibiotics or if they did not assess use against guidelines or defined local insti- tutional or national policies. After title and abstract review, the full text versions of identified articles were downloaded for review. After as- sessment against inclusion criteria, a total of 20 articles were included in this narrative review. Data extracted from identified studies included study design, setting, interventions, comparators and results. If provided by the article, rec- ommendations regarding programme development or implementation were also extracted. Book 23-06.indb 431 8/16/2017 1:24:17 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 432 Results Strategies for implementation of successful antimicrobial stewardship programmes All 20 studies collected data through patients’ chart s and medical file review, either retrospectively (11 studies) or prospectively (9 studies). All studies provided recommendations for suc- cessful programme development and/ or implementation. Table 1 summarizes the studies in regard to the adoption by institutions of interventional strategies in order to assess and enhance antimi- crobial use and prescribing behaviours by physicians (13–32). Two studies used proactive core strategies in the form of prospective audit or point prevalence survey fol- lowed by education and feedback (13,14) to evaluate the appropriateness of antimicrobial prescribing and utili- zation. Amer et al. compared the pre- scribing appropriateness of the empiric antibiotic therapy before and after the implementation of the antimicrobial stewardship programme at their institu- tion in Saudi Arabia (13). The primary aim of the programme was to optimize the appropriateness of antimicrobials use and thus prevent the emergence of antimicrobial resistance associated with inappropriate use. Through tar- geting the 5 most commonly used broad-spectrum antibiotics (piperacil- lin/tazobactam, imipenem/cilastatin, meropenem, vancomycin, tigecycline) in the intensive care unit setting, they prospectively compared patients who were put under the active antimicrobial stewardship programme arm with other patients who had been admitted to the same unit at that institution before the implementation of the programme in 2011 over a 6-month period during the same season. Appropriateness of empirical antibiotics was assessed by the stewardship team and evaluated according to the institution’s internally developed criteria, including formu- lary restrictions, and following reliable international infectious diseases clinical guidelines. Recommendations were then communicated in a verbal fashion to the intensive care unit team. The ap- propriateness of empirical antibiotics improved from 30.6% (15/49) in the historical control arm to 100% (24/24) in the proactive antimicrobial steward- ship programme arm; the difference was statistically significant (P < 0.05). The rate of inappropriate antimicrobial use was reduced to 0% upon implementing the programme. There was also a signifi- cant reduction in the antibiotic utiliza- tion and direct costs in the antimicrobial stewardship programme arm. On the other hand, there was no significant clinical difference between the 2 arms of the study in terms of Clostridium difficile infection rate. A total of 27 interven- tions were made with an acceptance rate of 96.3% (13). However, this study had a number of limitations, including lack of randomization, small sample size, short follow-up duration and single institution’s experience, thus affecting the generalizability of the results. After performing a point prevalence survey over a 3-month period to assess vancomycin prescribing compliance with the Centers for Disease Control and Prevention (CDC) guidelines, Dib et al. evaluated feedback and performed an educational intervention to enhance adherence to local policies at their in- stitution in Saudi Arabia (14). In the pre-intervention period, vancomycin utilization was deemed appropriate in only 65% (48/74) of adult patients. The investigators then implemented a continuous education and active feed- back approach targeting compliance with CDC recommendations. During the post-intervention period, compli- ance with guidelines for vancomycin utilization increased significantly for all indicators from 65% (48/74) in the pre- intervention phase to 91% (31/34) in the post-intervention phase (P = 0.004). In addition, compliance with vancomy- cin trough level monitoring increased from 35% to 67.7% (P = 0.0002). The study concluded that audit and feed- back and/or educational approaches are effective in improving compliance with guidelines for antimicrobials utili- zation (14). Eighteen additional studies evalu- ated prescribing patterns and antimi- crobial utilization within hospitals in the Middle East area (15–32) by as- sessing compliance with local/national institutional policies or internationally endorsed clinical guidelines. Eleven (61.1%) of these reported unwarranted and inappropriate use (typically over- use) of antimicrobials. The majority of the studies concluded that prescribing habits were to blame for the discrep- ancies observed, and that physicians were not prescribing according to lo- cal policies and guidelines (16–26). Conversely, 6 (33.3%) studies reported adherence to guidelines and local institutional policies (27–32). These studies deemed prescribing patterns to be rational and in line with local and international standards. The reasons be- hind this are recorded as being the result of institutional policies, implementa- tion of protocols or prescribing aids, or adoption of international guidelines from North America and/or Europe. Some of these studies also reported that antimicrobial stewardship initiatives (restrictive measures, antimicrobial cy- cling, antimicrobial switch, etc.) likely influenced adherence rates (15,24,32). Recommendations for programme development and implementation Specific recommendations extracted from each study are given in Table 1. All the studies we examined provided recommendations that are considered to be crucial for further enhancement of antimicrobial usage through imple- mentation of successful antimicrobial stewardship programmes. Eight studies mentioned the importance of imple- menting local guidelines and policies (13,16,18,21,24,25–27). It was also sug- gested that these should be supported Book 23-06.indb 432 8/16/2017 1:24:17 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 433 by an infection control committee (17,23). Other studies recommended that these policies should be updated regularly and must be readily available and disseminated throughout the insti- tution (17,20,23,24,26). Other approaches were also mentioned. These included annual surveillance; infectious diseases team consultations (17,23,24,32) focusing on interdisciplinary collaboration; and good cross-departmental communica- tion (22,23). In the majority of studies training of health care professionals, public health awareness and continuing medical education were considered to be important components that further enhance health care professionals’ knowledge, and thus improve antibiot- ics use and overall prescribing appropri- ateness (13–15,19,21,24–26). Others highlighted the importance of the role of the clinical pharmacist in monitoring prescriptions (i.e. dosage and frequency adjustments), intervening when appro- priate, and the implementation of such interventions if deemed reasonable (17,18,21,23,29,30,32). Lastly, some studies reflected upon the need for con- tinuous use of guidelines (13,28,31) and the increased need for drug utiliza- tion reviews, audits, or strategies that include restriction policies, order forms, pharmacodynamics dose optimization and antimicrobial cycling and rotating (13–15,17,21,23,24). Discussion To our knowledge, this is the first review to summarize published antimicrobial stewardship interventions in the Middle Eastern context and to extract recom- mendations from past studies for future programme implementation. The re- sults provide excellent background in- formation for institutions in the region attempting to improve antimicrobial use and an insight for programme de- velopment and implementation. A total of 20 studies were identified that have assessed at least one type of antimicro- bial stewardship intervention. Two of these studies reported the use of proac- tive core interventions which positively affected prescribing behaviours through audit and feedback. The remaining 18 papers primarily described adherence of antimicrobial prescribing patterns to institutional, local/national, or interna- tional policies and guidelines. The end result from the studies we examined in this review was that antimicrobial utili- zation is a problem in the Middle East and more-proactive strategies should be developed in order to further improve the appropriateness of therapy. The 2 papers describing proactive core strategies must be closely exam- ined to determine how results can be applied in other settings in the region (13,14). These studies are very impor- tant, in that they demonstrate that a pro- spective audit and feedback approach is effective in the region, and their findings suggest that prescribers were receptive and an audit and feedback model can be established. While this approach is a core component of antimicrobial stewardship programmes in North America and Europe, there may be cul- tural considerations in the Middle East (physician attitudes, acceptance of col- laborative practices, acceptance of phar- macist recommendations, etc.) that could limit effectiveness (8,33). These cultural differences should be further explored and any associated impact on effectiveness of programmes should be assessed. In addition, a key finding was that education seems to be central in the implementation of any programme and perhaps is important for those institu- tions developing programmes in areas of the Middle East where antimicrobial stewardship is considered a novel con- cept (34). A number of key recommendations were extracted from the studies includ- ed in our review that provide insight into future programme development and implementation; many themes emerged from these recommendations that warrant discussion. First, develop- ment of local policies was recommend- ed by a large majority of the studies. The importance of this point cannot be stressed enough as antimicrobial resistance patterns vary greatly between settings and even between institutions. Therefore, antibiograms and prescrib- ing protocols and policies are essential for continuous monitoring of outcomes at the institutional level (11,35). It is also important to note that any guide- line established from other settings (i.e. North America or Europe) must be carefully reviewed for applicability be- fore adoption in a new context. Secondly, any policy or prescribing protocol developed must be continually updated based on current epidemio- logical data, including infection preva- lence and antimicrobial resistance. This should be done at least annually in order to ensure guidelines and recommenda- tions remain valid over time. A third point that emerged from the recommendations was the importance of the collaborative approach within a multidisciplinary team. Physicians and clinical pharmacists are typically considered to be the core members of antimicrobial stewardship programme leadership (in addition to information technology personnel), however col- laboration with other disciplines such as nursing, laboratory personnel, ad- ministrators and home care services will only improve stakeholder buy in and promote a culture of antimicrobial stewardship within the institution itself (9,10,36). Considering the points discussed above, we urge institutions in the Mid- dle East to consider the following points for programme development and im- plementation. First, it is important to ensure adequate baseline surveillance data is obtained, in order to guide the most appropriate type of interventions and stewardship strategies. This can be obtained through laboratory data, drug utilization trends and point prevalence surveys. In addition, it is important for Book 23-06.indb 433 8/16/2017 1:24:17 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 434 Ta bl e 1. S um m ar y of tw en ty s tu di es d es cr ib in g an ti m ic ro bi al s te w ar ds hi p st ra te gi es in th e M id dl e Ea st St ud y C ou nt ry D es ig n Se tt in g (N o. o f p at ie nt s) Ev al ua te d co m po ne nt C om pa ra to r O ut co m e Re co m m en da ti on s A m er e t a l. 20 13 Sa ud i A ra bi a C om pa ra tiv e, hi st or ic al ly co nt ro lle d st ud y us in g pr os pe ct iv e au di t w ith fe ed ba ck H os pi ta l (7 3) A pp ro pr ia te ne ss of p re sc rib in g th e em pi ric al a nt ib io tic th er ap y Pr e/ po st an tim ic ro bi al st ew ar ds hi p pr og ra m m e im pl em en ta tio n A pp ro pr ia te ne ss im pr ov ed fr om 3 0 .6 % to 10 0 % (P < 0 .0 5) C on tin uo us h ig he r a dm in is tr at io n su pp or t M ul tid is ci pl in ar y te am a pp ro ac h C on tin uo us u se o f s up pl em en ta l st ra te gi es , i nc lu di ng e du ca tio n, gu id el in es , a nt im ic ro bi al o rd er fo rm s, d os e op tim iz at io n an d cy cl in g D ib e t a l. 20 0 9 Sa ud i A ra bi a Pr os pe ct iv e ch ar t a ud it (p oi nt pr ev al en ce su rv ey ) w ith e du ca tio na l in te rv en tio n H os pi ta l (7 4) A pp ro pr ia te ne ss o f an tib io tic u se a nd ef fe ct o f e du ca tio na l in te rv en tio n on it s ut ili za tio n C om pl ia nc e w ith C D C -a da pt ed cr ite ria a nd th e ho sp ita l c on tr ol pr ac tic es Si gn ifi ca nt im pr ov em en t i n us e po st -in te rv en tio n C om pl ia nc e w ith gu id el in es im pr ov ed fro m 2 1% p re - in te rv en tio n to 8 5% po st -in te rv en tio n (P = 0 .0 0 0 1) Em ph as is o n im po rt an ce o f ac tiv e st ra te gi es , i nc lu di ng c ha rt au di t, ph ys ic ia n’ s f ee db ac k an d ed uc at io na l e ffo rt s t o de cr ea se in ap pr op ria te a nt ib io tic u sa ge A l-T aw fiq e t a l. 20 15 Sa ud i A ra bi a Se le ct iv e an d re st ric tiv e re po rt in g of te st ed an tim ic ro bi al su sc ep tib ili tie s f or ke y pa th og en s i n an a nt im ic ro bi al st ew ar ds hi p in iti at iv e, in cl ud in g an ed uc at io na l in te rv en tio n be fo re th e la un ch of th e re po rt in g in iti at iv e H os pi ta l Ef fe ct o f e du ca tio na l in te rv en tio n (c ha ng e in c as ca de a nd re st ric tiv e re po rt in g) in en ha nc in g an tim ic ro bi al st ew ar ds hi p pr og ra m m es an d ut ili za tio n of an tim ic ro bi al a nd cl in ic al p re sc rib in g pa tte rn s b y ph ys ic ia ns C om pl ia nc e w ith lo ca l a nt ib io gr am s (tr ac ki ng a nt ib io tic su sc ep tib ili tie s) , ph ar m ac ok in et ic fa ct or s a nd ID SA re co m m en da tio ns In cr ea se d su sc ep tib ili ty ra te s to so m e an tib io tic s w ith re du ce d ra te s o f C . d iffi ci le in fe ct io n fro m 0 .11 to 0 .0 7 pe r 10 0 0 p at ie nt d ay s En co ur ag em en t o f u se o f a ct iv e st ra te gi es su ch a s r es tr ic tiv e re po rt in g to fu rt he r i nfl ue nc e cl in ic al pr es cr ib in g an d to p er m it la bo ra to ry - ba se d co nt rib ut io n to w ar ds im pl em en ta tio n of a n an tim ic ro bi al st ew ar ds hi p pr og ra m m e O ng oi ng su pp or t f ro m p hy si ci an s is u lti m at el y ne ed ed a nd th ey m us t be p ro vi de d w ith e du ca tio na l in te rv en tio ns , i nc lu di ng se m in ar s, w ar d vi si ts , t el ep ho ne te ac hi ng a nd af te r- ho ur s d is cu ss io n A l-M om an y et a l. 20 0 9 Jo rd an Pr os pe ct iv e ev al ua tio n of pa tie nt s’ m ed ic al fil es H os pi ta l (2 36 ) D eg re e of a dh er en ce fo r a nt im ic ro bi al pr op hy la xi s p ra ct ic e in ca rd ia c su rg er y C om pl ia nc e w ith in te rn at io na l gu id el in es A dh er en ce is fa r fro m o pt im al a nd in ap pr op ria te ad m in is tr at io n of an tib io tic s i n te rm s o f ch oi ce (1 % ), du ra tio n (3 9. 4% ), do se (2 7.9 % ) an d do si ng in te rv al (1 3% ) D ev el op in g lo ca l h os pi ta l g ui de lin es G iv in g th e ph ar m ac is t a c en tr al ro le in th e ad m in is tr at io n, m on ito rin g an d in te rv en tio n of a nt im ic ro bi al pr op hy la xi s Book 23-06.indb 434 8/16/2017 1:24:17 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 435 Ta bl e 1. S um m ar y of tw en ty s tu di es d es cr ib in g an ti m ic ro bi al s te w ar ds hi p st ra te gi es in th e M id dl e Ea st (c on ti nu ed ) St ud y C ou nt ry D es ig n Se tt in g (N o. o f p at ie nt s) Ev al ua te d co m po ne nt C om pa ra to r O ut co m e Re co m m en da ti on s A l-A br i e t a l. 20 12 O m an Re tr os pe ct iv e ev al ua tio n of co m pu te riz ed pa tie nt s’ c as e no te s H os pi ta l (1 72 ) Q ua lit y of c ar e fo r c om m un ity - ac qu ire d pn eu m on ia m an ag em en t C om pl ia nc e w ith G C C c om m un ity - ac qu ire d pn eu m on ia gu id el in es Po or a dh er en ce to gu id el in es in te rm s of p re ve nt io n, di ag no si s a nd se ve rit y as se ss m en t D ev el op m en t a nd im pl em en ta tio n of a lo ca lly b as ed in te gr at ed c ar e pa th w ay El H as sa n et a l. 20 15 U ni te d A ra b Em ira te s Re tr os pe ct iv e ev al ua tio n of pa tie nt re co rd s H os pi ta l (2 50 ) Su rg eo ns ’ a dh er en ce in te rm s o f p re sc rib in g, se le ct io n, d os in g an d du ra tio n of an tim ic ro bi al s C om pl ia nc e w ith lo ca l s ur gi ca l an tim ic ro bi al pr op hy la xi s gu id el in es Po or a dh er en ce to gu id el in es (3 2. 1% ) Pr ot oc ol im pl em en ta tio n A w ar en es s a nd c on tin ui ng m ed ic al ed uc at io n to ta rg et a nt im ic ro bi al pr op hy la xi s C lin ic al p ha rm ac y se rv ic es C yc lic a ud iti ng D ep lo ym en t o f c lin ic al p ha rm ac is ts in su rg ic al w ar ds A ly e t a l. 20 12 Ku w ai t Re tr os pe ct iv e ev al ua tio n of pa tie nt re co rd s G ov er nm en t ho sp ita l (1 11 2) Ph ys ic ia ns ’ a dh er en ce to a nt im ic ro bi al ad m in is tr at io n C om pl ia nc e w ith lo ca l a nt ib io tic po lic y gu id el in es Po or a dh er en ce to gu id el in es (5 2. 7% of p re sc rip tio ns m at ch in g th e po lic y an d 30 .4 % fu ll ad he re nc e to a nt ib io tic ad m in is tr at io n) O pt im iz in g ad he re nc e by u pd at in g po lic ie s H am m ud a et a l. 20 13 Q at ar Po in t p re va le nc e su rv ey in th e fo rm of p at ie nt c ha rt au di t C an ce r h os pi ta l (5 8) A pp ro pr ia te ne ss o f u se of a nt im ic ro bi al a ge nt s in c an ce r p op ul at io n C om pl ia nc e w ith lo ca l a nt im ic ro bi al pr es cr ib in g po lic ie s a nd fe br ile ne ut ro pe ni a gu id el in es Po or a dh er en ce to p ol ic ie s a nd gu id el in es . H ig h pr ev al en ce o f an tim ic ro bi al m is us e: 57 .6 % o f p re sc rip tio ns w er e or de re d by a n ap pr ov ed pr es cr ib er w ith o nl y 33 % a dh er en ce to fe br ile n eu tr op en ia gu id el in es In te rd is ci pl in ar y co lla bo ra tio n an d de ve lo pm en t o f a nt im ic ro bi al st ew ar ds hi p pr og ra m m es Kh an e t a l. 20 12 Q at ar Re tr os pe ct iv e ev al ua tio n of pa tie nt m ed ic al re co rd s H os pi ta l (5 96 ) A pp ro pr ia te ne ss o f u se of a b ro ad -s pe ct ru m an tib io tic C om pl ia nc e w ith lo ca l g ui de lin es a nd an nu al su rv ei lla nc e pe rio di ca lly up da te d by co ns en su s a m on g ex pe rt s In ju di ci ou s u se o f an tib io tic s: u nj us tifi ed pr es cr ip tio ns ; in ap pr op ria te e m pi ric pr es cr ip tio ns (5 7% ); in ap pr op ria te d ru g m od ifi ca tio n ba se d on th e re su lts o f m ic ro bi al c ul tu re s a nd an tib io gr am s ( 22 % ) D is se m in at io n of th e im pl em en te d lo ca l g ui de lin es v ia st af f e du ca tio n an d w id es pr ea d pu bl ic at io n Ra tio na liz at io n of u se in d iff er en t ho sp ita l u ni ts v ia a pp ro pr ia te ne ss in in iti al e m pi ric a nd m od ifi ca tio n of th er ap y po st -c ul tu re re su lts O ng oi ng a nn ua l s ur ve ill an ce Re st ric tiv e m ea su re s s uc h as m an da to ry in fe ct io us d is ea se te am co ns ul ta tio n Book 23-06.indb 435 8/16/2017 1:24:17 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 436 Ta bl e 1. S um m ar y of tw en ty s tu di es d es cr ib in g an ti m ic ro bi al s te w ar ds hi p st ra te gi es in th e M id dl e Ea st (c on ti nu ed ) St ud y C ou nt ry D es ig n Se tt in g (N o. o f p at ie nt s) Ev al ua te d co m po ne nt C om pa ra to r O ut co m e Re co m m en da ti on s H an ss en s e t a l. 20 0 5 Q at ar Pr os pe ct iv e ob se rv at io n an d ev al ua tio n of pa tie nt s c ha rt s H os pi ta l (7 1) A pp ro pr ia te ne ss o f u se of a nt im ic ro bi al s a nd pr es cr ib in g pa tte rn s o f ph ys ic ia ns C om pl ia nc e w ith lo ca l h os pi ta l gu id el in es , in te rn at io na l gu id el in es a nd cl in ic al ju dg m en t an d ex pe rie nc e In ap pr op ria te an tib io tic m an ag em en t ( 52 % po si tiv e cu ltu re s in 7 6% o f p at ie nt s w ith p re su m ed o r pr ov en in fe ct io n w ith on ly 5 2% c ha ng e in em pi ric th er ap y po st se ns iti vi ty re su lts ) Lo w p ot en tia l f or m ic ro bi ol og ic al di ag no st ic p ro ce du re s an d in ap pr op ria te m ic ro bi ol og ic al in ve st ig at io ns U rg en t n ee d fo r u pd at ed e m pi ric an d lo ca l h os pi ta l t re at m en t gu id el in es in a dd iti on to th e ne ed fo r a re vi ew o f a nt ib io tic p re sc rib in g po lic ie s M on ito rin g of a nt ib io tic u sa ge Ro le o f c lin ic al p ha rm ac is t i n as su rin g ju st ifi ed u se o f c on tin uo us an tib io tic s Im pl em en ta tio n of e m pi ric al an tib io tic tr ea tm en t w ith ou t a ny de la y, b as ed o n cl in ic al ju dg m en t, gu id ed b y lo ca l a nt ib io gr am s a nd an tib io tic re si st an ce p at te rn s a nd o n de -e sc al at in g an tib io tic st ra te gy Ro ta tin g em pi ric al a nt ib io tic sc he du le to li m it em er ge nc e of re si st an ce p at te rn s G oo d co m m un ic at io n am on g he al th ca re p ro fe ss io na ls Im pl em en ta tio n of in fe ct io us c on tr ol pr ac tic es to re du ce re si st an ce a nd th e sp re ad o f n os oc om ia l i nf ec tio ns Fu tu re d ru g ut ili za tio n re vi ew s t o as se ss a nt i-i nf ec tio us m an ag em en t A l-T aw fiq , 2 0 12 Sa ud i A ra bi a Re tr os pe ct iv e ob se rv at io n of an d ev al ua tio n of th e ph ar m ac y re gi st er o f t he an nu al m ed ic at io n ut ili za tio n H os pi ta l A pp ro pr ia te ne ss o f u se of a nt im ic ro bi al s C om pl ia nc e w ith W H O g ui de lin es fo r de fin ed d ai ly d os e of a nt im ic ro bi al s In cr ea se d an d un ex pl ai ne d us ag e of in tr av en ou s an tib io tic s; e sp ec ia lly flu or oq ui no lo ne s (fr om 3 .5 to 8 2. 64 3 de fin ed d ai ly do se /1 0 0 p at ie nt da ys ) l ea di ng to em er ge nc e of flu or oq ui no lo ne - re si st an t b ac te ria l st ra in s Sp ec ifi c un it an tim ic ro bi al co ns um pt io n da ta to b e ab le to co m pa re w ith b en ch m ar ki ng d at a su ch a s t he N H SN Ed uc at io n an d im pl em en ta tio n of a nt im ic ro bi al st ew ar ds hi p pr og ra m m e to c on tr ol th e us e of an tib io tic s Book 23-06.indb 436 8/16/2017 1:24:17 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 437 Ta bl e 1. S um m ar y of tw en ty s tu di es d es cr ib in g an ti m ic ro bi al s te w ar ds hi p st ra te gi es in th e M id dl e Ea st (c on ti nu ed ) St ud y C ou nt ry D es ig n Se tt in g (N o. o f p at ie nt s) Ev al ua te d co m po ne nt C om pa ra to r O ut co m e Re co m m en da ti on s A l H ar bi , 1 99 8 Sa ud i A ra bi a Re tr os pe ct iv e ev al ua tio n of c as e re co rd s H os pi ta l (8 88 ) A pp ro pr ia te ne ss of p re sc rib in g pr ac tic es o f s ur ge on s fo r a nt im ic ro bi al pr op hy la xi s i n th e su rg ic al w ar d C om pl ia nc e w ith th e ho sp ita l lo ca l a nt ib io tic pr es cr ib in g po lic y U nw ar ra nt ed an d ov er us e of pr op hy la ct ic a ge nt s (≤ 7 0 % o f p at ie nt s) w ith in cr ea se d co st to th e ho sp ita l St ric t e nf or ce m en t o f t he lo ca l p ol ic y St ric t s ur ve ill an ce a nd p ro ph yl ac tic an tib io tic a ud it Su pe rv is io n by h ea lth c ar e te am in cl ud in g in fe ct io us d is ea se sp ec ia lis t, cl in ic al m ic ro bi ol og is t an d cl in ic al p ha rm ac is t f or th e ap pr op ria te u se o f a nt ib io tic s Fo rm ul ar y re st ric tio ns Pr ep rin te d st an di ng o rd er s Re vi si on o f c om pl ia nc e w ith th e pr in ci pl es o f p ro ph yl ac tic ad m in is tr at io n by th e in fe ct io n co nt ro l c om m itt ee Se no k et a l. 20 0 9 Ba hr ai n Re tr os pe ct iv e ev al ua tio n of pa tie nt s’ c as e fil es H os pi ta l (1 84 ) A pp ro pr ia te ne ss of a nt im ic ro bi al pr es cr ib in g pa tte rn s o f ph ys ic ia ns C om pl ia nc e w ith th e A A P, C D C a nd th e ID SA g ui de lin es fo r t he tr ea tm en t o f up pe r r es pi ra to ry tr ac t i nf ec tio ns A nt ib io tic o ve ru se D ev el op m en t o f n at io na l g ui de lin es ba se d on lo ca l k no w le dg e of c lin ic al pr es en ta tio n an d an tim ic ro bi al re si st an ce p at te rn s In te gr at io n of g ui de lin es in to st ru ct ur ed c on tin ui ng m ed ic al ed uc at io n co ur se s Pu bl ic h ea lth a w ar en es s c am pa ig ns ac tiv el y su pp or te d by o pi ni on le ad er s M us m ar e t a l. 20 14 Pa le st in e O bs er va tio na l no n- in te rv en tio na l pr os pe ct iv e co ho rt G ov er nm en t ho sp ita l (4 0 0 ) Su rg eo ns ’ A dh er en ce in te rm s o f p re sc rib in g pa tte rn , s el ec tio n, do si ng a nd d ur at io n of a nt im ic ro bi al s a fte r su rg er y C om pl ia nc e w ith th e A SH P gu id el in es Ve ry lo w c om pl ia nc e in a ll as pe ct s ( 2% co m pl ia nc e fo r st ud ie d pa ra m et er s w ith si gn ifi ca nt p- va lu es ) A do pt in g gu id el in es fo r p ro ph yl ax is ; Tr ai ni ng a ll he al th c ar e pr ov id er s A l-B al us hi e t a l. 20 14 O m an Re tr os pe ct iv e cr os s- se ct io na l re vi ew o f pr es cr ip tio ns us in g m ed ic al fi le s H os pi ta l (4 99 ) A pp ro pr ia te ne ss of a nt im ic ro bi al pr es cr ib in g pa tte rn s o f ph ys ic ia ns C om pl ia nc e w ith C D C a nd W H O d efi ni tio n of “a pp ro pr ia te an tib io tic pr es cr ip tio n pr ac tic es “ Si m ila r r es ul ts w ith st ud ie s c on du ct ed in de ve lo pe d co un tie s (N or th A m er ic a, Eu ro pe a nd A si a) En co ur ag em en t o f g ui de lin e- ba se d an tib io tic p re sc rip tio n pr ac tic es Im pl em en ta tio n of a u ni fo rm an tib io tic p re sc rib in g po lic y ba se d on lo ca l s en si tiv ity p at te rn s Book 23-06.indb 437 8/16/2017 1:24:17 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 438 Ta bl e 1. S um m ar y of tw en ty s tu di es d es cr ib in g an ti m ic ro bi al s te w ar ds hi p st ra te gi es in th e M id dl e Ea st (c on ti nu ed ) St ud y C ou nt ry D es ig n Se tt in g (N o. o f p at ie nt s) Ev al ua te d co m po ne nt C om pa ra to r O ut co m e Re co m m en da ti on s Ze en ny e t a l. 20 14 Le ba no n Re tr os pe ct iv e ev al ua tio n of pa tie nt m ed ic al re co rd s H os pi ta l (1 85 ) A pp ro pr ia te ne ss o f u se of a b ro ad -s pe ct ru m an tib io tic C om pl ia nc e w ith ID SA g ui de lin es Ju st ifi ed p re sc rip tio n fo r t he in te nd ed u se in ge ne ra l; an tim ic ro bi al cy cl in g an d sc he du le d an tim ic ro bi al sw itc h (8 6% o f t he c as es w ith p= 0 .0 28 ); In ap pr op ria te ne ss in do si ng fr eq ue nc y an d do sa ge a dj us tm en t in p at ie nt s w ith re na l f ai lu re (3 4. 1% in ap pr op ria te ne ss m ai nl y du e to in ap pr op ria te d os e ad ju st m en t w ith P < 0 .0 5) H ig hl ig ht in g up on th e im po rt an ce of th e ro le o f a c lin ic al p ha rm ac is t an d hi s c ru ci al p re se nc e in e ve ry ho sp ita l w ar d fo r d os ag e an d fre qu en cy a dj us tm en t w he n ne ce ss ar y; Im pl em en ta tio n of cl in ic al p ha rm ac is ts ’ i nt er ve nt io ns ; C on tin ui ng e du ca tio n ac tiv iti es / in -s er vi ce s t o th e m ed ic al te am ; M an da to ry su pe rv is io n of a nt ib io tic us e by in fe ct io us d is ea se sp ec ia lis ts ; D ev el op m en t o f l oc al a nt im ic ro bi al st ew ar ds hi p pr og ra m m e Jo hn e t a l. 20 14 U ni te d A ra b Em ira te s Pr os pe ct iv e cr os s- se ct io na l r ev ie w o f m ed ic al re co rd s H os pi ta l (2 38 ) A pp ro pr ia te ne ss of a nt im ic ro bi al pr es cr ib in g pa tte rn s o f ph ys ic ia ns C om pl ia nc e w ith W H O g ui de lin es fo r up pe r r es pi ra to ry tr ac t i nf ec tio ns Ra tio na l p ra ct ic es in pr es cr ib in g an tib io tic s En co ur ag em en t o f c on tin uo us u se of th er ap eu tic g ui de lin es b as ed o n se ns iti vi ty p at te rn s t o op tim iz e th e us e of a nt im ic ro bi al a ge nt s Ka bb ar a et a l. 20 15 a Le ba no n Pr os pe ct iv e ob se rv at io n an d ev al ua tio n of el ec tr on ic c ha rt s H os pi ta l (1 18 ) A pp ro pr ia te ne ss o f u se of fl uo ro qu in ol on es C om pl ia nc e w ith ID SA g ui de lin es , m an uf ac tu re r pa ck ag e in se rt s a nd cl in ic al ju dg m en t A pp ro pr ia te pr es cr ip tio ns fo r in te nd ed u se (9 3. 2% ); In ap pr op ria te ne ss in du ra tio n of th er ap y (5 7.6 % ) a nd d os ag e ad ju st m en t i n re na l fa ilu re p at ie nt s ( 57 .1% ) H ig hl ig ht in g up on th e im po rt an ce of th e ro le o f a c lin ic al p ha rm ac is t in d e- es ca la tin g tr ea tm en t w he n in di ca te d po st -c ul tu re re su lts a nd in sp ar in g th e us e of b ro ad -s pe ct ru m flu or oq ui no lo ne s Re hm an i e t a l. 20 14 Sa ud i A ra bi a Q ua si - ex pe rim en ta l pr os pe ct iv e st ud y H os pi ta l (1 59 ) A pp ro pr ia te ne ss of in iti al a nt ib io tic th er ap y an d tim e fro m re co gn iti on o f s ev er e se ps is /s ep tic sh oc k to fi rs t a nt ib io tic d os e de liv er y C om pl ia nc e w ith lo ca l e m pi ric an tib io tic gu id el in es ; l oc al ly w rit te n se ps is pr ot oc ol (p re /p os t in te rv en tio n) Im pr ov ed ti m in g an d ap pr op ria te ne ss of in iti al e m pi ric an tim ic ro bi al th er ap y (o ve ra ll re du ct io n of 7 2 m in ut es fr om tim e se ve re se ps is is re co gn iz ed to d el iv er y of a nt ib io tic s) ; im pr ov em en t b y 37 % in a nt ib io tic us e po st -p ro to co l im pl em en ta tio n En co ur ag em en t o f t he c on tin uo us us e of lo ca l p ro to co ls a nd lo ca l m ic ro bi ol og ic al d at a w hi ls t t ry in g to ac tiv at e th e pr ot oc ol d ur in g th e ea rly “t ria ge “ p ha se Book 23-06.indb 438 8/16/2017 1:24:17 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 439 Ta bl e 1. S um m ar y of tw en ty s tu di es d es cr ib in g an ti m ic ro bi al s te w ar ds hi p st ra te gi es in th e M id dl e Ea st (c on cl ud ed ) St ud y C ou nt ry D es ig n Se tt in g (N o. o f p at ie nt s) Ev al ua te d co m po ne nt C om pa ra to r O ut co m e Re co m m en da ti on s Ka bb ar a et a l. 20 15 b Le ba no n Re tr os pe ct iv e ev al ua tio n of pa tie nt s’ m ed ic al re co rd s H os pi ta l (1 0 0 ) A pp ro pr ia te ne ss o f u se of a b ro ad -s pe ct ru m an tib io tic C om pl ia nc e w ith th e ID SA g ui de lin es , th e Su rv iv in g Se ps is C am pa ig n gu id el in es , d ru g in fo rm at io n ha nd bo ok d os ag e re co m m en da tio ns an d cl in ic al ju dg m en t A pp ro pr ia te pr es cr ip tio ns fo r t he in te nd ed u se a nd go od a dh er en ce w ith na tio na l g ui de lin es (a pp ro pr ia te u se in 9 7.2 % o f c as es em pi ric al ly , a nd 9 7.2 % po st -c ul tu re ) d ue to im pl em en ta tio n of re st ric tio n po lic ie s: w ith in 2 4 ho ur s, re je ct o r a ut ho riz e us e af te r e va lu at io n of ap pr op ria te ne ss ) In ap pr op ria te u se re la te d to d os e ad ju st m en t i n pa tie nt s w ith re na l f ai lu re H ig hl ig ht in g up on th e im po rt an ce of th e ro le o f a c lin ic al p ha rm ac is t in te rm s o f: tim el y pa tie nt fo llo w -u p to a pp ro pr ia te ly a dj us t d os es w he n ne ce ss ar y, a nd to e du ca te o th er he al th c ar e pr of es si on al s t o im pr ov e pa tie nt o ut co m es AA P: A m er ic an A ca de m y of P ed ia tr ic s; A SH P: A m er ic an S oc ie ty fo r H os pi ta l P ha rm ac is ts ; C D C : C en te rs fo r D is ea se P re ve nt io n an d Co nt ro l; G CC : G ul f C oo pe ra tio n Co un ci l; ID SA : I nf ec tio us D is ea se s S oc ie ty o f A m er ic a; N H SN : N at io na l H ea lth ca re S af et y N et w or k; W H O : W or ld H ea lth O rg an iz at io n. institutions to evaluate any antimicro- bial stewardship initiative on a regular basis (e.g. annually) in order to assess the impact and seek opportunities for improvement. Second, any adapted policy or guideline originating from an- other context must be locally validated to ensure appropriateness and applica- bility for the setting. While international guidelines do provide evidence-based recommendations, stewardship must be adapted to each local context and culture. Lastly, we strongly urge clini- cians and researchers working in this area to disseminate their findings in the form of abstracts and publications. As demonstrated by this review, there is a great lack of data for guidance of stew- ardship in the Middle Eastern context, and sharing of experiences and knowl- edge will only work towards improving patient outcomes through appropriate use of antimicrobials. Conclusions Our findings show antimicrobial stew- ardship programmes are in their infancy in the region but that work is currently being done to further develop these programmes. 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Antimicrobial stewardship ward rounds and a dedicated chart reduce antibiotic consumption and pharmacy costs without affecting inpatient mortality or re-admission rates. PLoS One. 2013;8(12):e7974. PMID:24348995 Book 23-06.indb 440 8/16/2017 1:24:18 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 441 1Social Determinants in Health Promotion Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Islamic Republic of Iran (Correspondence to: T. Aghamolaei: teaghamolaei@gmail.com). 2Hormozgan Fertility and Infertility Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Islamic Republic of Iran. Received: 25/01/15; accepted: 30/10/16 Review Determinants of caesarean birth on maternal demand in the Islamic Republic of Iran: a review Fatemeh Darsareh 1, Teamur Aghamolaei 1, Minoo Rajaei 2, Abdoulhossain Madani 1 Analyse des déterminants des naissances par césarienne sur demande de la mère en République islamique d’Iran RÉSUMÉ Le phénomène des naissances par césarienne sur demande fait l’objet de discussions, notamment parce qu’une première césarienne est hautement prédictive d’autres césariennes lors des naissances suivantes. L’identification des raisons d’un accouchement par césarienne sur demande est importante de façon à planifier des interventions efficaces. À ce titre, la présente analyse fait état, sur la base d’études menées en République islamique d’Iran, des facteurs impliqués dans la tendance qu’ont les femmes de recourir à un accouchement par césarienne. Plusieurs mots clés incluant « naissance par césarienne », « accouchement », « causes », « demande/ exigence de la mère », ainsi que « choix de la patiente » ont été utilisés pour effectuer des recherches dans Medline, PubMed, Ovid, Scientific Information Database, Magiran, Google et Google Scholar. La recherche a été menée à partir d’articles en persan et en anglais, sans limitation de temps. À l’aide d’une analyse de contenu, les facteurs influençant le recours à une césarienne ont été divisés en trois catégories : les facteurs liés à la mère, les facteurs sociaux, et ceux liés aux dispensateurs de soins. Eu égard à la prévalence élevée de césariennes, il est important de concevoir et de mettre en œuvre des programmes et des interventions efficaces prenant en compte les raisons principales qui conduisent les femmes à opter pour une césarienne non nécessaire. ةعجارم :ةيملاسلإا ناريإ ةيروهجم في ملأا بلط بسح ةيصريقلا ةدلاولا تاددمح نيدم نسلحا دبع ،يئاجر ونيم ،ياماقآ روميت ،هراسرد ةمطاف ىع يوـق شرؤـم ةـباثمب نوـكت لىولأا ةـيصريقلا ةدلاوـلا نأو ايـس لا ،ماـتهلاا بـلطلا بـسح ةـيصريقلا ةدلاوـلا ةرـهاظ تبطقتـسا :ةـصلالخا تاـخدتلا طـيطختل بـلطلا بـسح ةـيصريقلا ةدلاوـلا ءارو ةـنماكلا بابـسلأا دـيدتح مـهلما نـمو .ةـقحلا ةـيصريق تادلاوـل ملأا عوـضخ تـيرجأ تاـسارد لىإ ًادانتـسا ،ةـيصريقلا ةدلاوـلا ءارـجإ لىإ ءاـسنلا لـيم في مهـست يـتلا لـماوعلا ضارعتـسلاا اذـه دروـي ،هـيلعو .ةـلاعفلا تاراـيتخاو ،ملأا بـلطو ،بابـسلأاو ،عـضولاو ،ةـيصريقلا ةدلاوـلا اـهنم ةيـسيئر تاـلك ةدـع تمدخُتـساو .ةيماـسلإا نارـيإ ةـيروهجم في و Googleو Magiran ثــ حبلا تاكرــ محو ،ةــ يملعلا تاــ نايبلا ةدــ عاقو Ovidو PubMedو Medline تاــ نايبلا دــ عاوق ىــ ع ثــ حبلل ،ضــ يرلما ،ىوــ تحلما لــ يلتح مادختــ سابو .ةــ ينمز دوــ يق نود ،ةــ يزيلجنلإاو ةيــ سرافلا ةــ غللاب ةــ بوتكم تلااــ قم في ثــ حبلا يرــ جأو .Google Scholar قـلعتت لـماوعو ،ةـيعاتجا لـماوعو ،لـمالحا ملأا ّصـتخ لـماوع :تاـئف 3 لىإ ةـيصريقلا ةدلاوـلا راـيتخا ىـع رـثؤت يـتلا لـماوعلا تمـسُق ةاعارم عـم ةـلاّعف تاـّخدتو جـمارب ذـيفنتو مـيمصت مـهلما نـم ،ةـيصريقلا تادلاوـلا راـشتنا لدـعم عاـفترلا ًارـظنو .ةـيحصلا ةـياعرلا مّدـقمب .يـعاد اـب ةـيصريقلا ةدلاوـلا راـيتخا لىإ ءاـسنلا عـفدت يـتلا ةيـسيئرلا بابـسلأا ABSTRACT The phenomenon of caesarean birth on demand has gained attention, particularly as a first caesarean birth appears to be strongly predictive of subsequent caesareans. Identification of reasons behind caesarean birth on demand is important for planning effective interventions. Therefore, this review reports the factors involved in the tendency of women to undergo caesarean birth, based on studies in the Islamic Republic of Iran. Several keywords including caesarean delivery, childbirth, causes, maternal request/demand, and patient choice were used to search Medline, PubMed, Ovid, Scientific Information Database, Magiran, Google and Google Scholar. The search was conducted on Persian and English language articles, with no time limitation. Using content analysis, the factors influencing caesarean section were divided into 3 categories: maternal, social and healthcare giver. According to the high prevalence of caesarean section, it is important to design and implement effective programmes and interventions with consideration of the key reasons that lead women to opt for unnecessary caesarean section. Book 23-06.indb 441 8/16/2017 1:24:18 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 442 Introduction Caesarean section rates are on the rise worldwide (1). Based on a recent study in the Islamic Republic of Iran, the rate of caesarean section is 49% nationwide (2). Caesarean birth on maternal de- mand (CBMD) is responsible for some increase in the overall rate. In developed countries, conservative estimates of CBMD range from 4% to 18% of all caesarean deliveries (3). Although the rate of CBMD in the Islamic Republic of Iran remains unclear because of poor documentation, the total rate of cae- sarean birth is unfortunately high (4). CBMD is defined as elective caesarean delivery for singleton pregnancy on maternal request at term in the absence of any medical or obstetric indications (5). It is now recognized that perform- ing a caesarean section with no medical indication offers no health advantages for the mother and infant, and has in- creased health risks, from both physical and emotional perspectives, compared to vaginal birth (6). The problem is that caesarean birth is associated with an increase in ma- ternal and infant mortality and mor- bidity, and increased healthcare costs. Theoretically, maternal outcomes of fever, infection, pneumonia and throm- boembolism are consistently increased with medically indicated caesarean birth and would also be present in instances of CBMD (7). The issue of cost must also be considered in the broader con- text of burden to the already stressed healthcare system and the impact on finite resources (6). CBMD has received increasing at- tention in the social science literature, with a focus on women’s motivations. The reasons for CBMD are complex and it appears to have interrelated fac- tors that are not easily explained. As the literature review revealed, elective caesarean section is related to personal, psychological and social factors such as autonomy, self-control, perceptions of safety, fear of childbirth, sexuality, and perceived quality of obstetric care (8). Limited information is available about how the decision for elective caesarean section comes about in the clinical en- vironment (9,10). CBMD is clinically relevant because of the increasing num- bers of women choosing this mode of delivery, the health risks to the mother and infant, and the increased cost as- sociated with the procedure. There is a need to gather informa- tion about the factors involved in the tendency of women to opt for caesar- ean section, based on studies that have been conducted in the Islamic Republic of Iran. The ultimate goal is to devise interventions to reduce the number of maternal requests for caesarean sec- tions, thereby reducing their associated mortality, morbidity and healthcare costs. Many studies have investigated the reasons for CBMD in the Islamic Republic of Iran. However, these studies have been in a particular geographical area. Hence, there is a need to identify and summarize the different causes in different regions of the country, and the results could be used to design and implement appropriate national plans and interventions to reduce unneces- sary caesarean sections. Methods This study was a review of the litera- ture regarding elective caesarean birth without specific medical indications. We searched the following databases: Medline, PubMed, Ovid, Google and Google Scholar. To access Iranian studies published in Persian, we also searched Scientific Information Da- tabase, Iran Medex and Magiran. We searched using the terms caesarean delivery, childbirth and birth, maternal request/demand, and patient choice for published articles in Persian and English languages, with no time limit. We re- viewed articles from all over the Islamic Republic of Iran because of the ethnic and cultural diversity in the country. Approximately 126 articles were ini- tially obtained including abstracts, quantitative and qualitative research, governmental reports, comprehensive reviews, and opinion/editorial articles. We restricted the search to peer- reviewed full-text articles that explained only CBMD without any medical indications. After excluding irrelevant or repeated articles, experimental and quasi-experimental studies, we ana- lysed 29 articles (24 quantitative and 5 qualitative) related to the objectives of the study. All studies were performed from 2002 to 2014. Selected articles were studied extensively to extract the required information (Figure 1) and we identified the factors influencing the decision for caesarean section. Results Several factors influenced women to opt for caesarean birth, which can be divided into 3 groups: maternal, social and healthcare provider. Maternal fac- tors included demographic factors such as age, education, job status and place of living; psychological factors such as fear and anxiety; and other factors such as perception and attitude toward childbirth that was mostly related to individual behaviour and comprehen- sion. The reviewed studies showed that factors influencing women to choose caesarean section included advanced maternal age, high educational level, living in the city, fear of vaginal birth pain, concerns about infant safety, fear of urogenital trauma during vaginal birth, and prior complicated normal childbirth. The second group were social fac- tors. In some cases CBMD was based on the recommendation of family and friends. Social status was also an influ- encing factor and women with higher social status were more likely to have an elective caesarean birth. The third group were healthcare provider factors. Recommendations Book 23-06.indb 442 8/16/2017 1:24:18 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 443 from obstetricians and midwives were the main reasons behind CBMD in some cases. The results are summarized in Table 1. Discussion Historically, the management of preg- nancy and labour has been primarily associated with high expectation, and until recently, the concept of requesting a caesarean birth was not recognized as a possibility for women. To request a caesarean section is a difficult decision for women planning childbirth, and ac- cording to previous studies, too many factors are involved in this decision- making process. The aim of this review was to identify the main factors behind this increased tendency of women to re- quest a caesarean section in the Islamic Republic of Iran. We found that CBMD was influenced by maternal, social and healthcare giver factors. Maternal factors Caesarean section among older women (> 35 years old) is more frequent than in younger women (11–13). Consistent research findings indicate that women who choose elective caesarean tend to be older (14). Maternal age has been reported as an independent risk fac- tor for caesarean delivery. The reasons for this increased risk remain unclear, but other studies have suggested that it may be due to physician and patient concern over pregnancy outcomes in older women (15). Advanced maternal age places women in a risk category in which screening and diagnostic tests for chromosomal abnormalities are routinely offered and is associated with infertility and assisted reproductive technology (16). These factors may contribute to a maternal viewpoint of the pregnancy as being high risk and requiring additional medical interven- tion, which leads to elective caesarean section (17). Caesarean section among women with higher education is more frequent than among those with lower education (11,12,18). This is consistent with some studies that have reported an increased tendency for caesarean section among women with higher educational level (19) but inconsistent with other reports that more educated women choose vaginal delivery (20). Although some studies have indicated that women who live in a city and who are in employment are more likely to choose caesarean sec- tion (13,21,22), these factors have less effect than other demographic factors on choosing caesarean section. Psychological factors, especially fear of vaginal birth and its associated pain, are related to the demand for caesar- ean birth (23–32). Anxiety and fear of childbirth have consistently been as- sociated with maternal request for elec- tive caesarean section (33–36). Severe fear of childbirth can lead to pregnancy complications (37), which is thought to increase the percentage of women who demand elective caesarean birth. Hofberg and Brockington described a condition known as tokophobia, a fear of death in childbirth, preceding pregnancy (38). Women with this condition are afraid that they will die if they give birth vaginally. It is reported that about half of women with toko- phobia choose an elective caesarean section (38). The emotional status of women during pregnancy and delivery may be associated with interpretation, expectations and decisions concerning the delivery process. Pregnancy-related depression, stress or anxiety may con- tribute to lessened confidence, fear and dissatisfaction with the birthing process (39), which can encourage women to opt for caesarean section. Another important factor is negative past experiences – both with regard to pregnancy and childbirth – and this is currently considered to be one of the main causes of fear of childbirth that might lead to elective caesarean section (12,23,28,40). Women who have had a negative previous birth experience con- tinue to feel fear in subsequent births, especially in relation to labour pain. Labour pain is one of the most stressful episodes in childbirth (41) and a signifi- cant association with elective caesarean section has been reported (34,42). Almost all pregnant women are concerned about the well-being of the fetus and want to provide a safe uterine environment. They desire a type of birth that is safe for the infant. Although there is no evidence to support that caesarean birth with no medical indication offers health advantages for the mother and infant, many women believe that elec- tive caesarean section is safer for the fetus (6). Concerns about fetal safety have been reported in different quali- tative studies as a reason for CBMD (43–48). Many women are concerned about retaining function of their urogenital organs after childbirth. Although there is no consensus that planned caesarean birth preserves the pelvic floor or pre- vents urinary incontinence or anorectal dysfunction, some women are afraid that having vaginal birth will damage these internal organs (23,24,39). One study has indicated that some women tend to elective caesarean section because they want their baby to be born on a particular day (27). Studies in Australia and Turkey have suggested that women may opt for cae- sarean delivery because they can plan for the time of day or week that meets the needs of the obstetricians’ and their own schedules (49,50). This practice is more common in private health care where women have more flexibility and financial strength to schedule delivery. Social factors The support of family and friends is associated with CBMD (24,26,27). Sharing childbirth experiences within the family may affect a woman’s deci- sion about the method of birth. Women who benefit from the support of family and friends take a more active role in the Book 23-06.indb 443 8/16/2017 1:24:18 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 444 Table 1 Summary of reviewed studies Authors Type of research Participants Results Aram et al. (2002) (22) Cross-sectional 500 parturients Fearing vaginal delivery pain , doctor’s recommendation , concern about infant health and mother’s fitness , associated disease , high educational level, having job were associated with caesarean section. Shareat et al. (2002) (61) Cross-sectional 824 parturients 13.5% of caesarean sections were due to fear of vaginal delivery pain, or doctor’s recommendation. Alimohamadian et al. (2003) (62) Cross-sectional 824 parturients Mother’s request or doctor’s recommendation was the main reason for caesarean section. Moradan (2004) (31) Cross-sectional 400 pregnant women The most common cause of tendency to caesarean section was fear from pain during vaginal delivery. Mobaraki et al. (2005) (59) Cross-sectional 7649 parturients Doctor’s recommendation, fear of vaginal delivery pain, and mother’s request were the factors leading to elective caesarean section. Mohammad et al. (2006) (13) Cross-sectional 1473 parturients Older age of women, higher level of education, higher socioeconomic status and hospitalization in private hospitals were associated with caesarean section. Khosrovi et al. (2006) (55) Cross-sectional 473 parturients Caesarean section was more common in women with a better job, higher educational level and living in a city. Seyed Noori et al. (2006) (46) Cross-sectional 210 pregnant women Infant health, fear of vaginal delivery pain , mother’s safety, infant’s safety, and friend’s recommendation were the main factors leading to elective caesarean section. Negahban et al. (2006) (21) Cross-sectional 256 pregnant women Fearing vaginal delivery pain , tube ligation , fearing infant’s harm , fearing harm to female reproductive system , maternal health, views of partner and family, and living in a city were the factors associated with caesarean section. Tabande & Kashani (2007) (40) Cross-sectional 187 pregnant women Low pain , fearing harm to female reproductive system, concern about infant safety, medical condition, and negative experience from previous childbirth were the factors leading to elective caesarean section. Mohammaditabar et al. (2009) (30) Cross-sectional 618 primiparous Fear of labour pain and medical staff play a role in high caesarean section rate. Mohammad et al. (2009) (58) Cross-sectional 250 pregnant women Doctor’s recommendation, fearing vaginal delivery pain, previous caesarean section, and care given by private physician were the main factors leading to elective caesarean section. Alavije et al. (2010) (32) Cross-sectional 342 parturients Lower pain , infant’s health, maternal health and friends’ opinion were associated with elective caesarean section. Sharghi et al. (2010) (60) Cohort study 396 pregnant women Caesarean section was chosen as the most popular method for delivery. The most effective factor in decision-making was physician’s suggestion. Atghaei & Nouhi (2010) (29) Cross-sectional 400 pregnant women Fear of vaginal delivery pain was the main factor for elective caesarean section. Fathian et al. (2010) (57) Cross-sectional 195 parturients Doctor’s persistence , personal belief and mother’s persistence were the factors leading to elective caesarean section. Bahonar et al. (2010) (18) Case–control 210 parturients High educational level and family recommendation were associated with elective caesarean section. Naseh et al. (2010) (12) Cross-sectional 1500 parturients Old age and education, and previous delivery experience were associated with elective caesarean section. Moeini et al. (2011) (44) Cross-sectional 346 pregnant women Doctor’s opinion, low pain , infant’s safety, awareness of delivery time, and partner’s suggestion were the factors leading to elective caesarean section. Ghooshchian et al. (2011) (28) Descriptive– analytical 300 pregnant women Fearing vaginal delivery pain, advanced age, and negative previous childbirth experience led to elective caesarean section. Book 23-06.indb 444 8/16/2017 1:24:18 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 445 birth process, and women without such support are more fatalistic about their role in the birth process (51). Some research has shown that women who receive social support in pregnancy and during labour have lower rates of caesar- ean section (52). Another social factor that might influence the type of birth decision is so- cial status. Some studies have suggested that caesarean sections are more likely in women of higher social status (53). In contrast, one retrospective study of a large number of caesarean sections in England stratified by social status found that caesarean sections were not more likely in women of higher social status (54). Healthcare provider factors Recommendation by physicians and midwives is one of the main reasons for caesarean section (4,55–61). Traditionally, the role of obstetricians has been paternalistic, and women have complied with their recommendations based on the balance of power in the physician–patient relationship. Many complex factors may contribute to ob- stetricians’ viewpoint about maternal choice and elective caesarean birth, and attitudes among obstetrician appear to be changing. Several studies have examined maternal choice of caesarean section from the obstetricians’ point of view and found that physicians may play an important role in promoting elective caesarean delivery to individual women (62,63). Physicians may push their patients toward requesting caesarean section with remarks that imply that it may be needed. The result of one Eu- ropean study exploring the attitudes of obstetricians showed that > 75% of German and British obstetricians accepted CBMD, as did even 22% of obstetricians in the Netherlands where the caesarean rate was lowest (64). Wax and colleagues found that 8.3% of obste- tricians surveyed cited convenience as a reason for giving birth by CBMD. Tim- ing of caesarean deliveries is important to physicians. Lo has suggested that an increased rate of caesarean sections in the United States of America may occur in the last week of December so parents can take advantage of a tax deduction (65). Physicians have to juggle office visits, surgeries and deliveries during the day. Vaginal deliveries and emergency caesarean deliveries may keep a physi- cian awake all night and result in signifi- cant fatigue. Planned elective caesarean deliveries can improve the schedule of the physician who schedules deliveries at their convenience (66). A caesarean section takes about 30 minutes com- pared to assisting with vaginal birth, Table 1 Summary of reviewed studies (concluded) Authors Type of research Participants Results Bagheri et al. (2012) (45) Qualitative study 11 pregnant women Fearing vaginal delivery pain led to elective caesarean section. Movahed et al. (2012) (11) Cross-sectional 600 pregnant women Significant relation among these factors (age, age at marriage, education, spouse’s education, occupational status, place of birth, social status, previous childbirth method, record of barrenness, place of previous childbirth, place of pregnancy care, record of caesarean in family and attitude toward caesarean (with choice of caesarean having been approved. Shahraki Sanavi et al. (2012) (27) Qualitative study 200 pregnant women in third trimester Fear of pain, inability to withstand vaginal childbirth pain, encouragement from family members, partner’s and physician’s confidence about the infant’s safety, and earlier preparation knowledge of exact time of delivery were the main reasons to have elective caesarean section. Davari et al. (2012) (54) Cross-sectional 459 Nulliparous women High educational level and social status were associated with elective caesarean section. Abbaspoor et al. (2014) (25) Qualitative study 18 pregnant and postnatal women Fear of normal childbirth process and concern about normal delivery complications resulted in most participants deciding to have caesarean section. Akbari & Ahmadi (2014) (24) Cross-sectional 200 primiparous women Major reasons declared by mothers in the caesarean group were fear of vaginal delivery pain, concerns about vaginal delivery complications, and recommendation of friends and their delivery method. Faisal et al. (2014) (23) Qualitative study 14 primigravidae Reasons for requesting a caesarean section were related to fear of childbirth (labour pain, injury to mother or infant), complications after vaginal delivery (vaginal prolapse, urinary incontinence or sexual dysfunction), trust in obstetricians, and lack of trust in maternity ward staff. Book 23-06.indb 445 8/16/2017 1:24:18 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 446 which may take up to 12 hours or more (67). In summary, physicians play an important role in a woman’s decision to request a caesarean section. Conveni- ence, physician fatigue and legal issues play a role in the attitude of physicians to encourage women to request a cae- sarean section. Study limitations There were some limitations to this review. First, the quality of studies that were analysed in this review was not examined. Second, some of the studies evaluated women’s preferences and not actual demand for caesarean section. Therefore, the actual factor behind CBMD cannot be inferred from those data. Conclusion This review may have implications for the health system, researchers and clini- cians. The results suggest that the fol- lowing factors may influence women’s childbirth decisions: fear of vaginal birth pain, concern about infant safety, fear of urogenital trauma during vaginal birth, prior complicated vaginal childbirth, recommendation of family and friends, and opinion of healthcare providers (obstetricians or midwives). Consider- ing the key reasons for caesarean sec- tion, providing effective interventions such as educational programmes to gain appropriate knowledge, enhancing the quality of vaginal birth services, and so- lutions to reduce the healthcare provid- ers’ recommendation for unnecessary and not-indicated caesarean sections are important. Acknowledgements Funding: This study was supported by Hormozgan University of Medical Sciences, Islamic Republic of Iran. Competing interests: None declared. Records identified through database searching (n = 121) Sc re en in g In cl ud ed El ig ib ili ty Id en tifi ca tio n Additional records identified through other sources (n = 8) Total records retrieved (n = 129 ) Records screened (n = 98) Records excluded Unrelated (n = 54) Not obtainable (n = 5) Editorials/notes/abstracts (n = 7) Full-text articles assessed for eligibility (n = 32) Full -text articles excluded, Duplicate data (n = 3) Studies included in synthesis (n = 29) Duplicates removed (n = 31 ) Figure 1. PRISMA flow diagram for systematic review Book 23-06.indb 446 8/16/2017 1:24:19 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 447 References 1. Caesarean Section. Clinical guideline [CG132]. London: Na- tional institute for Health and Care Excellence; 2012 (https:// www.nice.org.uk/guidance/cg132, accessed 5 April 2017). 2. Azami-Aghdash S, Ghojazadeh M, Dehdilani N, Mohammadi M, Asl Amin Abad R. Prevalence and causes of cesarean sec- tion in Iran: systematic review and meta-analysis. Iran J Pub Health. 2014;43(5):545-555. 3. Cesarean delivery on maternal request. NIH Consensus and State-of-the-Science Statements . 2006 27–29 Mar;23(1):1–29. Bethesda, MD: National Institutes of Health; 2006 (http:// consensus.nih.gov/2006/cesareanstatement.pdf, accessed 15 April 2017) 4. Ahmad-Nia S, Delavar B, Eini-Zinab H, Kazemipour S, Mehryar AH, Naghavi M. Caesarean section in the Islamic Repub- lic of Iran: prevalence and some sociodemographic corre- lates. East Mediterr Health J. 2009 Nov-Dec;15(6):1389–98. PMID:20218129 5. Caesarean delivery on maternal request (CDMR). C-Obs 39. The Royal Australian and New Zealand College of Obstetri- cians and Gynaecologists; 2010 (https://www.ranzcog.edu. au/RANZCOG_SITE/media/DOCMAN-ARCHIVE/Caesar- ean%20Delivery%20on%20Maternal%20Request%20(C- Obs%2039)%20Review%20Nov13.pdf, accessed 5 April 2017). 6. Armson BA. Is planned caesarean childbirth a safe alternative? CMAJ. 2007 Feb 13;176(4):475–6. PMID:17296960 7. Lavender T, Hofmeyr GJ, Neilson JP, Kingdon C, Gyte GM. Caesarean section for non-medical reasons at term. Cochrane Database Syst Rev. 2012 Mar 14;3:CD004660. PMID:22419296 8. McCourt C, Weaver J, Statham H, Beake S, Gamble J, Creedy DK. Elective cesarean section and decision making: a criti- cal review of the literature. Birth. 2007 Mar;34(1):65–79. PMID:17324181 9. Fenwick J, Staff L, Gamble J, Creedy DK, Bayes S. Why do wom- en request caesarean section in a normal, healthy first preg- nancy? Midwifery. 2010 Aug;26(4):394–400. PMID:19117644 10. Kingdon C, Baker L, Lavender T. Systematic review of nul- liparous women’s views of planned cesarean birth: the missing component in the debate about a term cephalic trial. Birth. 2006 Sep;33(3):229–37. PMID:16948723 11. Movahed M, Enayat H, Ghaffarinasab E, Alborzi S, Mozafari R. 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Identification of factors related to elective cesar- ean labor: a theory-based study. Daneshvar. 2010;19(96):1–11 (in Persian) Book 23-06.indb 447 8/16/2017 1:24:19 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 448 33. Poikkeus P, Saisto T, Unkila-Kallio L, Punamaki R, Repokari L, Vilska S, et al. Fear of childbirth and pregnancy-related anxi- ety in women conceiving with assisted reproduction. Obstet Gynecol. 2006 Jul;108:70–6. PMID:16816058 34. Waldenstrom U, Hildingsson I, Ryding E. Antenatal fear of childbirth and its association with subsequent caesarean sec- tion and experience of childbirth. BJOG. 2006 Jun;113(6):638– 46. PMID:16709206 35. Nerum H, Halvorsen L, Sorlie T, Oian P. Maternal request for cesarean section due to fear of birth: Can it be changed through crisis-oriented counseling? Birth. 2005 Sep;33(3):221– 8. PMID:16948722 36. Saisto T, Salmela AK, Nurmi JE, Kononen T, Halmesmaki E. A randomized controlled trial of intervention in fear of childbirth. Obstet Gynecol. 2001 Nov;98(5 Pt 1):820–6. PMID:11704175 37. Saisto T, Halmesmaki E. Fear of childbirth: A neglected di- lemma. Acta Obstet Gynecol Scand. 2003 Mar;82(3):201–8. PMID:12694113 38. Hofberg K, Brockington I. Tokophobia: an unreasoning dread of childbirth. A series of 26 cases. Br J Psychiatry. 2000 Jan;176:83–5. PMID:10789333 39. Ip WY, Martin CR. Does confidence in labor predict the occurrence of postnatal depression? J Reprod Infant Psy- chol. 2008;26:270–1 (http://www.tandfonline.com/doi/ abs/10.1080/02646830802224440). 40. Tabande A, Kashani E. The prevalency of cesarean among em- ployed educated women of medical science groups in Gorgan (2005). J Gorgan Univ Med Sci. 2007 Summer;9(2):67–70 (in Persian) (http://goums.ac.ir/journal/browse.php?a_ id=265&slc_lang=en&sid=1&ftxt=1) 41. Lally JE, Murtagh MJ, Macphail S, Thomson R. More in hope than expectation: a systematic review of women’s expectations and experience of pain relief in labor. BMC Med. 2008 Mar 14;6:7. PMID:18366632 42. Weaver J, Statham H, Richards M. Are there “unnecessary“ cesarean sections? Perceptions of women and obstetricians about cesarean sections for nonclinical indications. Birth. 2007 Mar;34(1):32–41. PMID:17324176 43. Moeini B, Allahverdipour H, Mahjoub H, Bashirian S. Assessing pregnant women’s beliefs, behavioral intention and predictive factors for cesarean section in Hamadan. Iran J Obstet Gynecol Infertil. 2011 Aug-Sep;14(3):37–44 (in Persian). 44. Bagheri A, Masoodi Alavi N, Abbaszade F. Effective factors for choosing the delivery method among the pregnant women in Kashan. FEYZ. 2012;16(2):146–53. 45. Seyed Noori T, Jamshidi Aranaki F. Survey the relationship between knowledge and attitude of pregnant women request- ing cesarean section referred to Rasht health centers and their choice reasons. J Guilan Univ Med Sci. 2006;15(59):75–84 (in Persian). 46. Bryant J, Porter M, Tracy SK, Sullivan EA. Caesarean birth: Con- sumption, safety, order, and good mothering. Soc Sci Med. 2007 Sep;65(6):1192–201. PMID:17590252 47. Cheung NF, Mander R, Cheng L, Chen VV, Yang XQ. Caesar- ean decision-making: negotiation between Chinese women and healthcare professionals. Evid Based Midwifery. 2006 Jul;4(1):24 (https://www.rcm.org.uk/learning-and-career/ learning-and-research/ebm-articles/caesarean-decision- making-negotiation-between). 48. 48. Weaver J, Stratham H. Wanting a caesarean section: the decision process. Br J Midwifery. 2005;13(6):370–3. 49. Gezer A, Sximsek YO, Altinok TA. Elective cesarean sec- tion: evolution of obstetrician to technician. Birth. 2007 Dec;34(4):357–9. PMID:18021154 50. Kassak KM, Ali Abdallah AM. Opting for a cesarean: what deter- mines the decision? Public Admin Manag. 2005;13(3):100–22. 51. Martin K. Giving birth like a girl. Gend Soc. 2003;17(1):54–72. 52. Hodnett ED, Gates S, Hofmeyr GJ, Sakala C, Weston J. Continu- ous support for women during childbirth. Cochrane Database Syst Rev. 2012 Feb 16;2:CD003766. PMID:21328263 53. Davari M, Maracy M, Ghorashi Z, Mokhtari M. The relationship between socioeconomic status and the prevalence of elective cesarean section in nulliparous women in Niknafs Teaching Cen- tre, Rafsanjan, Iran. Womens Health Bull. 2014 Jul;1(2):e20044 (https://www.google.co.uk/url?sa=t&rct=j&q=&esrc=s&sour ce=web&cd=1&cad=rja&uact=8&ved=0ahUKEwjTseqsvY3TA hVJBMAKHeUrAVYQFgghMAA&url=http%3A%2F%2Fwome nshealthbulletin.com%2F28880.pdf&usg=AFQjCNHXV_Xo- o6DRw73ZXqZ7GWUFN-Mng&bvm=bv.151426398,d.d24). 54. Barley K, Aylin P, Bottle A, Jarman B. Social class and elective Cae- sareans in the English NHS". BMJ. 2004 Jun 12;328(7453):1399. PMID:15191977 55. Zohreh F. Reza SG, Zahra F, Fatemeh P. Frequency of cesar- ean section and its related factors in Khomeinyshahr–Isfahan province 2005. 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Payesh. 2003;2(2):133–9 (in Persian). 61. Wax J, Cartin A, Pinette M, Blackstone J. Patient choice ce- sarean – the Maine experience. Birth. 2005 Sep;32(3):203–6. PMID:16128974 62. Gonen R, Tamir A, Degani S. Obstetricians’ opinions regarding patient choice in cesarean delivery. Obstet Gynecol. 2002 Apr;99(4):577–80. PMID:12039114 63. Mayberry L. Nursing implications of the 2006 NIH State of the Science Conference Statement: cesarean delivery on maternal request. MCN Am J Matern Child Nurs . 2006 Sep- Oct;31(5):286–9. 64. Habiba M, Kaminski M, Da Frè M, Marsal K, Bleker O, Librero J, et al. Caesarean section on request: a comparison of obste- tricians’ attitudes in eight European countries. BJOG. 2006 Jun;113(6):647–56. PMID:16709207 65. Lo J. Patients’ attitudes vs. physicians’ determination: Implica- tions for cesarean sections. Soc Sci Med. 2003 Jul;57(1):91. PMID:12753818 66. Brown HS 3rd. Physician demand for leisure: Implications for cesarean section rates. J Health Econ. 1996 Apr;15(2):233. PMID:10159111 67. Penna L, Arulkumaran S. Cesarean section for non-medical reasons. Int J Gynaecol Obstet. 2003 Sep;82(3):399–409. Book 23-06.indb 448 8/16/2017 1:24:19 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 449 1Institute of Hygiene, Catholic University of Sacred Heart, Rome, Italy (Correspondence to: A. Santoro: alessio.santoro@lshtm.ac.uk); 2Faculty of Public Health and Policy, European Centre on Health of Societies in Transition, London School of Hygiene and Tropical Medicine, London, United Kingdom. Received: 18/05/15; accepted: 3/11/16 Short communication Governing the Lebanese health system: strengthening the national response to the burden of Syrian refugees Alessio Santoro 1 and Martin McKee 2 Gouvernance du système de santé libanais : renforcer la réponse nationale pour faire face au fardeau des réfugiés syriens RÉSUMÉ Le Liban offre l’asile à 1,5 million de réfugiés syriens, selon les estimations, ce qui implique de potentielles conséquences sur le système de santé du pays. Dans la présente étude, nous analysons la façon dont le pays répond à ce défi, identifions les domaines sensibles dans lesquels un système de gouvernance national fort est requis, et réfléchissons aux moyens de le mettre en œuvre. Pour une réponse efficace à la crise des réfugiés syriens, une action internationale concertée est nécessaire. Néanmoins, la géographie impose au système de santé libanais de jouer un rôle central. Nous avons identifié les domaines où un renforcement du rôle de direction du ministère de la Santé publique est requis de toute urgence. Nous affirmons que le ministère de la Santé publique est bien placé pour assumer un rôle de direction, du fait de sa connaissance approfondie du système de santé libanais et de sa légitimité à mettre au point des interventions sanitaires à l’échelle nationale. Enfin, nous suggérons que cette crise peut être un catalyseur pour le renforcement du système de santé libanais, sur la base de politiques reposant sur des données factuelles qui pourraient bénéficier aux réfugiés ainsi qu’à la population libanaise. ينيروسلا ينئجلالا ءبعل ةينطولا ةباجتسلاا زيزعت :نيانبللا يحصلا ماظنلا مكح يكام نترام ،وروتناس ويسيلأ هذـه فيو .داـبلا في يـحصلا ماـظنلا ىـع ةيبلـس ًاراـثآ كترـي نأ نـكمي اـمم ،يروـس ئـجلا نوـيلم 1.5 هـعوممج اـلم ًاذاـم ناـنبل رـفوي :ةـصلالخا يوـق ةرادإ ماـظن لىإ جاـتتح يـتلا ةـساسلحا تلااـجلما دـيدحتب موـقنو ،يدـحتلا اذـله نياـنبللا يـحصلا ماـظنلا ىدـصت ةـيفيك لـّلحن ،ةـساردلا لاإ .ةـيلودلا دوـهلجا رـفاضت لاـعف وـحن ىـع نيروـسلا نـئجالا ةـمزأ ةـهجاوم بـلطتتو .هذـيفنت ةـيفيك فاـشكتساو يـنطولا ىوتـسلما ىـع رودلا زـيزعت اـهيف مزـلي يـتلا تلااـجلما ضـعب دـيدتح لىإ دـمعنف .يروـمح رودـب عـلطضي نأ نياـنبللا يـحصلا ماـظنلا ىـع ضرـفت اـيفارغلجا نأ اـهتفرعم ءوـض في ،ةرـسلما ةداـيقب اـله حمـسي عـضو في ةـماعلا ةـحصلا ةرازو نأ دـقتعنف .لـجاع وـحن ىـع ةـماعلا ةـحصلا ةرازوـل يداـيقلا مدختـسُت نأ حترـقن ،ًارـخأو .يـنطولا ىوتـسلما ىـع ةـيحص ةباجتـسا غوـصل ةـيعشرلا ةـهلجا اـنهوكو نياـنبللا يـحصلا ماـظنلاب ةـيليصفتلا ىـع عـفنلاب دوـعي نأ هنأـش نـم اـم وـهو ،ةـلدلأاب ةـموعدلما تاـسايسلا لىإ ًادانتـسا ،نياـنبللا يـحصلا ماـظنلا زـيزعتل زـفاحك ةـمزلأا هذـه .ءاوـس دـح ىـع نـينانبللا ناكـسلاو نـئجالا ABSTRACT Lebanon is providing sanctuary to an estimated 1.5 million Syrian refugees, with potential consequences for its health system. Here, we analyse how it has responded to this challenge, identify sensitive areas where a strong national governance system is needed and explore how it might be implemented. An effective response to the Syrian refugee crisis requires concerted international action. Nonetheless, geography dictates that the Lebanese health system must play a central role. We identify some areas where a strengthened stewardship role of the Ministry of Public Health is urgently required. We argue that the Ministry is well placed to take a lead, with its detailed knowledge of the Lebanese health system and its legitimacy to formulate a national health response. Finally, we suggest that this crisis could be a catalyst for the strengthening of the Lebanese health system, based on evidence-informed policies that would benefit refugees and the Lebanese population alike. Book 23-06.indb 449 8/16/2017 1:24:19 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 450 Introduction The Syrian conflict has caused an enormous number of refugees to seek sanctuary in neighbouring countries (1). This massive displacement of men, women and children has largely been absorbed by three countries: Lebanon, Jordan and Turkey, placing huge strain on their national health systems (2). Lebanon is a small country that hosts the largest density of refugees per capita in the world, and took informal steps to limit new arrivals in October 2014 (3). However, an estimated 1.5 million refugees have crossed the borders since the beginning of the conflict (1), placing severe pressure on the existing health system (4). The United Nations High Commission for Refugees (UNHCR) has called for the integration of refugees into the health system of the host coun- try (5). Yet, such integration requires that the host country has strong mecha- nisms of governance in place. Here, we examine the Lebanese experience, with a focus on health system governance, and suggest measures that could benefit both the Lebanese health system and the refugees. An analytical framework The World Health Organization (WHO) (Figure 1) health systems framework defines governance as the key pillar, or building block, to ensure optimal delivery of services, effective design of financing mechanisms, effi- cient allocation of health workforce, appropriate development of an inclu- sive health information system, and eventually, adoption of adequate drugs procurement policies (6). The Lebanese health system Historically, the Lebanese health system has been highly fragmented (7). It relies heavily on regressive private funding, with widespread user fees. Public health services are mainly delivered through primary healthcare centres, run by non- governmental organizations (NGOs) under contract. Secondary and tertiary care is mostly provided by the private sector (7). Within this context, the need for a strengthened MoPH was already acknowledged and led to the adoption of the “Ministry Action Plan 2003–2006”, aimed at strengthening its regulative capacity, providing uni- versal access for basic health needs, and improving financial coverage for health services (7). Governance during the crisis: an assessment Any health system would have been challenged to respond to such a hu- manitarian crisis, with a 30% increase in population in < 4 years (8). The health response is currently being jointly led by the MoPH, WHO and UNHCR (9). However, as the organ of national government, the MoPH must provide leadership (9). This view was reaffirmed at a policy dialogue held at the Gefinor Rotana Hotel in Beirut on 4th June 2014 that highlighted the need to strengthen the stewardship function of governmental departments (9). The MoPH has scaled up its commit- ments to respond to the health needs of the growing number of refugees, by in- creasing the capacity of primary health- care centres, launching immunization campaigns, and ensuring that Syrian refugees are covered for emergency care (9). Its unique understanding of the Lebanese context makes the MoPH the most appropriate institution to gov- ern the health response. The Ministry possesses a thorough knowledge of the Lebanese health system and its build- ing blocks, including the distribution of facilities, information systems, and financial and human resources. Thus, its institutional legitimacy should place the MoPH in the forefront of the design and implementation of a renewed Na- tional Health Response Plan. However, this has not yet been adopted (9). A national plan offers several op- portunities. First, it offers the possibility of matching existing assets efficiently to the needs of refugees; something that is particularly important in the absence of dedicated camps for Syrian refugees (10). There may have been good politi- cal reasons for not establishing refugee camps, although they would have made it easier to focus the health response within those settings, allowing a gradual integration of refugees within the Leba- nese health system. Second, a national plan could facilitate the definition of a basic package of essential health services for Syrian refugees and the Lebanese people, which would allow the provi- sion of services for refugees to be aligned with the health benefits provided for the host population (9). Third, by specify- ing precise roles and responsibilities for all the key actors, a national health plan could advance the long-advocated move to Lebanese ownership of the health system (9), allowing the MoPH to orchestrate the myriad of national and international actors involved while taking full advantage of the ability of the UN agencies in capacity building (11). Implications for health system building blocks The beneficial effects of strengthened governance led by the MoPH could have positive implications for the whole health system, which is severely overstretched by the rapidly increased demand for healthcare (4). Turning first to service delivery, in 2013, less than half of all refugees in need of care obtained it and, of those, > 50% did so privately (12). The health system could not meet the antenatal healthcare needs of Syrian women (13) and access to services for noncommunicable diseases was impeded by high costs of care (8). Book 23-06.indb 450 8/16/2017 1:24:19 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلا و ثلاثلا دلجلما سداسلا ددعلا 451 Financial barriers, many due to delays in registration with the UNHCR (the only means they had to obtain financial sup- port for healthcare), led many refugees to make desperate attempt to return to the Syrian Arab Republic to seek treatment (8). The gap in the provision of health assistance is exacerbated by the fact that most Syrian refugees are living in locations where 67% of the host population is already living below the poverty line (14). Weaknesses in the information system restrict the ability of the authorities to ascertain the health needs of the Syrian refugees. Drug sup- plies are rapidly depleted and increased demand undermines the capacity of health workers to provide high-quality services (15). The MoPH also provides a mechanism to ensure accountability and to facilitate cross-government co- ordination. Experiences from other countries Previous experience from other coun- tries suggests that there is huge scope for a strengthened national health re- sponse, with strong leadership by the MoPH. First, a particularly valuable les- son comes from Jordan; a country with a public healthcare system in which the Ministry of Health took the lead and worked with international organizations to implement a response that sought to provide full access to preventative and curative services by refugees (16). The result was the adoption of the Jordan Response Plan 2015 for the Syrian crisis (17). This sought to strengthen the national health system and to enable it to respond better to the Syrian crisis, by mobilizing additional human and financial resources, strengthening data collection systems, and redesigning drug procurement policies (17). Second, the Lebanese Government has the legitimacy to formulate a na- tional health response, which can take account of both the needs of the refugee population and the available resources and assets. In Afghanistan, the MoPH assumed leadership of the health system after removal of the Taliban Regime in 2001. The system it inherited was highly fragmented and, recognizing its initially limited capacity, the MoPH stepped back from the direct provision of ser- vices, defined a basic package of health services, and contracted the healthcare delivery function to NGOs. This, in turn, optimized the contribution of in- ternational donors, who directly funded such contracts (18). Additionally, the national data collection mechanisms were strengthened by ensuring that NGOs directly provided health data to the government’s Health Management Information System. Furthermore, the involvement of a third party consortium – including Johns Hopkins University – in the evaluation of the performance of the NGOs, increased the potential to ensure delivery of high-quality services (18). Third, Lebanon itself offers compel- ling evidence of what can be done to implement a data-driven package of basic health services, with alignment of donors’ efforts within a National Health Plan that directs resources to where they are most needed. In 1992, follow- ing the Lebanese Civil War, a weak MoPH was able to develop a health sec- tor strategy that emphasized its govern- ance and stewardship roles (19). The MoPH strengthened its managerial and administrative capacity and developed a comprehensive package of curative and preventive services at all primary healthcare facilities. The lessons learnt highlighting the need for the MoPH to be the central player in a pluralistic system (19). The way forward The scale of the challenges fac- ing the Lebanese health system is Figure 1 WHO Health System Framework (2007). Service delivery Health workforce Information Medical products Financing Leadership Improved health Responsiveness Risk protection Improved efficiency Access Coverage Quality Safety Book 23-06.indb 451 8/16/2017 1:24:19 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 452 enormous, and with no end in sight to the Syrian crisis, it is likely to get worse. Already, the UN Special Envoy to Syria, Staffan De Mistura, has said that the Syrian conflict has led to the largest humanitarian crisis since the Second World War (20). If the consequences in neighbouring countries are to be tackled effectively, there is a need to scale up the international response. The challenges brought by the Syrian refugees crisis should encourage the MoPH to take a lead, develop a national plan that will clarify roles and responsibilities of na- tional and international actors and define basic packages for essential services that can provide a basis for harmonization of service provision. This should build upon the WHO’s health system pillars. Despite the many challenges, this offers a means to begin the process of integrating the care of refugees within the Lebanese health system, with the definition of basic packages providing access to healthcare to refugees and host populations. The resulting strengthened Lebanese health system could bring benefits to the entire population. Funding: None. Competing interests: None declared. References 1. Coutts A, Fouad FM. Response to Syria’s health crisis–poor and uncoordinated. Lancet. 2013 Jun 29;381(9885):2242–3. PMID:23819155 2. 3RP Regional Refugee and Resilience Plan 2015-2016 in Re- sponse to the Syrian Crisis. 2015 Annual Report (data.unhcr. org/syrianrefugees/download.php?id=11002, accessed 26 April 2017). 3. Syrian refugees seeking help. Lancet. 2015 Jan 17;385(9964):202. PMID:25706695 4. Refaat MM, Mohanna K. Syrian refugees in Lebanon: facts and solutions. Lancet. 2013 Aug 31;382(9894):763–4. PMID:23870816 5. Zarocostas J. Integrate health services for refugees into na- tional healthcare, says UN report. BMJ. 2011 Aug 19;343:d5244. PMID:21856764 6. Everybody’s business. Strengthening health systems to im- prove health outcomes. WHO’s framework for action. Gene- va: World Health Organization; 2007 (http://www.who.int/ healthsystems/strategy/everybodys_business.pdf, accessed 21 March 2017). 7. Health System Profile Lebanon. Cairo: World Health Organi- zation. Regional Office for the Eastern Mediterranean; 2006 (http://apps.who.int/medicinedocs/documents/s17301e/ s17301e.pdf, accessed 21 March 2017). 8. Lebanon: agonizing choices: Syrian refugees in need of health care in Lebanon. London: Amnesty International; 2014 (htt- ps://www.amnesty.org/en/documents/MDE18/001/2014/ en/, accessed 21 March 2017). 9. Hammoud R, El-Jardali F. K2P dialogue summary: promoting access to essential health care services for Syrian refugees in Lebanon. Beirut: American University of Beirut; 2014 (https:// www.aub.edu.lb/k2p/products/Documents/Policy%20Dia- logue%20Summary_%20Syrian%20Refugees.pdf, accessed 21 March 2017). 10. American University in Beirut Knowledge to Policy. (K2P). Promoting access to essential health care services for Syrian refugees in Lebanon. Beirut, Lebanon: American University in Beirut, Knowledge to Policy (K2P)2014. 11. Salama P, Spiegel P, Talley L, Waldman R. Lessons learned from complex emergencies over past decade. Lancet. 2004 Nov 13-19;364(9447):1801–13. PMID:15541455 12. Rapid needs assesment: Haret Hreik. Amel Association Inter- national; 2013 (https://data.unhcr.org/syrianrefugees/down- load.php?id=2693, accessed 21 March 2017). 13. Benage M, Greenough PG, Vinck P, Omeira N, Pham P. An as- sessment of antenatal care among Syrian refugees in Lebanon. Confl Health. 2015;9:8. PMID:25741381 14. Improving health care services in Lebanon in the context of the Syrian crisis: the EU/IfS programme. Cairo: World Health Organization. Regional Office for the Eastern Mediterranean; 2017 (http://www.emro.who.int/lbn/lebanon-news/improv- ing-health-care-services-in-lebanon-in-the-context-of-the- syrian-crisis.html, accessed 21 March 2017). 15. Lebanon: economic and social impact assessment of the Syrian conflict. Washington: World Bank; 2013 (https://open- knowledge.worldbank.org/handle/10986/16790, accessed 21 March 2017). 16. His E, Murshidi MM, Hijjawi MQ, Jeriesat S, Eltom A. Syr- ian refugees and Jordan’s health sector. Lancet. 2013 Jul 20;382(9888):206–7. PMID:23830357 17. Jordan Responce Plan 2015 for the Syria Crisis, final draft. Hash- emite Kingdom of Jordan. Ministry of Planning and Interna- tional Cooperation; 2014 (http://www.jo.undp.org/content/ dam/jordan/docs/Publications/JRP+Final+Draft+2014.12.17. pdf, accessed 21 March 2017). 18. Balabanova D, Oliveira-Cruz V, Hanson K. Health sector governance and implications for the private sector. New York: Rockefeller Foundation; 2008 (Technical partner pa- per 9; http://www.resultsfordevelopment.org/sites/results- fordevelopment.org/files/resources/Health%20Sector%20 Governance%20and%20Implications%20for%20the%20Pri- vate%20Sector.pdf, accessed 21 March 2017). 19. Kronfol NM. Rebuilding of the Lebanese health care system: health sector reforms. East Mediterr Health J. 2006 May- Jul;12(3-4):459–73. PMID:17037717 20. UN News Centre. UN envoy says Syria set back 40 years by war, calls for renewed push towards solution (http:// www.un.org/apps/news/story.asp?NewsID=49806#.WNEr- rLSzD0c, accessed 21 March 2017). Book 23-06.indb 452 8/16/2017 1:24:19 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلاو ثلاثلا دلجلما سداسلا ددعلا 453 WHO events addressing public health priorities Bioethics may be defined as the application of ethics to the field of medicine and healthcare, as a joint and reflective inspection in health science, healthcare policy and delivery, based on established ethical standards within each profession (1). Bioethics is multidisciplinary and pluralistically draws on science, life technology, laws, traditions, and human values (2), and thus has a significant impact on standards for disease management and conduct of research (3). On 9 May 2016, the United Nations Education, Scientific and Cultural Organization (UNESCO) and World Health Organization (WHO) Regional Directors, met at the WHO Regional Office for the Eastern Mediterranean (EMRO) in Cairo to pursue and enhance collaboration between the two organizations in the field of bioethics in the Region (4). Dur- ing the meeting, the Directors acknowledged fruitful collabo- ration in the past. This included jointly organizing regional meetings; for example in 2007 the “First Regional Meeting on National Bioethics Committees”, and the international seminar “Dilemma of Stem Cell: Research, Future and Ethi- cal Challenges”; and during 2008 the “First meeting for the Eastern Mediterranean Region (EMR) and Arab Forum on Bioethics in Research”, and the “Expert Meeting on Ethical and Legal Issues in Human Embryo Research”. Recently, a Memorandum of Understanding (MoU) was signed be- tween the Directors General of UNESCO and WHO on 26 April 2017, fostering bilateral cooperation in bioethics and related fields between both agencies at the global level. The Global Health Ethics Unit at WHO hosts the perma- nent secretariat for the Global Summit of National Ethics/ Bioethics Committees, which held its latest biennial meet- ing in February 2016, and recommended holding regional bioethics summits. As a result, WHO/EMRO in collabora- tion with UNESCO/Arab States and the Omani National Bioethics Committee organized the first “Eastern Mediter- ranean/Arab States Regional Summit of National Ethics and Bioethics Committees” in Muscat, Oman, 5–6 April 2017, hosted at the Sultan Qaboos University. The main goal of the Regional Summit was to foster development of national ethics committees (NECs) and establish effective mechanisms of regional harmonization and cooperation to address emerging issues related to bio- ethics. The objectives were to explore methods of regional collaboration (with special focus on development and work of national ethics/bioethics committees), develop strategies to strengthen linkages between the bioethics committees and policy-makers, and share experiences and deliberate on rel- evant bioethics-related issues such as ethics during disasters and emergencies. Meeting developments and deliberations The Regional Summit was inaugurated by Prof Ali Al-Bemani, President of the Omani National Bioethics Committee, and Vice-Chancellor Sultan Qaboos University, as well as WHO and UNESCO representatives who emphasized the impor- tance of the Summit as a platform for sharing experiences and lessons learnt to forward bioethics in the countries of the Region. The first day of the Summit was dedicated to discussion of development, activities, and networking between national bioethics committees (NBCs), as well as challenges facing them from international, regional and national perspectives. On an international level, the participants were acquainted with the Global Summit of National Ethics/Bioethics Com- mittees, which acts as an international forum for exchange of views and debates on bioethics, contributes to common un- derstanding and consensus building between nations, as well as assisting in developing national bioethical frameworks and guidelines (5). The latest Global Summit was held in Berlin, Germany, during March 2016, and preparations for the next Global Summit – planned to convene in Dakar, Senegal, in 2018 – were discussed, including its overall theme (bioethics, sustainable development and societies) and sub-themes (bioethics in electronic data era; bioethics, social justice and civil society; bioethics, health emergencies and resilience and bioethics and vulnerable populations). In addition, UNESCO representatives presented a gen- eral overview on NBCs in the Region, Universal Declaration on Bioethics and Human Rights (6), and UNESCO Assist- ing Bioethics Committees Project (ABC) (7). UNESCO also reflected on recent surveys, including the 2014 NEC survey, and the 2009 UNESCO regional Legal survey, which covered 10 issues related to medical and genetic research in the Arab States, as follows: Fostering national bioethics committees: first regional summit in the Eastern Mediterranean Region/Arab States Region1 1 This report was prepared by Ahmed Mandil and Samar El-Feky, WHO Regional Office for the Eastern Mediterranean, Cairo, Egypt; and Seiko Sugita, UNESCO Regional Office for Education in the Arab States, Beirut, Lebanon. Book 23-06.indb 453 8/16/2017 1:24:19 PM EMHJ • Vol. 23 No. 6 • 2017 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale 454 • human reproductive and therapeutic cloning; • embryonic stem cell research; • genetic testing; • human genome and gene analysis; • research involving human subjects; • organ transplantation; • assisted reproductive technologies; • pharmaceutical research; • medical practice; and • abortion in the Arab States. The survey illustrated gaps in legal provision across the Region on advanced technologies, treatments and research. In addition, WHO representatives shared the methodology and main outcomes of the 2015 WHO Regional Bioethics Survey, which identified the main challenges facing NECs in the Region including: resources, transparency and autonomy, noncompliance, limited control over institutional ethical committees, gaps between policies and practice, reporting mechanisms and coordination between different ethical bod- ies, bioethics education and lack of legal stipulations govern- ing sensitive topics of public health importance. The experiences of NBCs were presented as case stud- ies from representatives of Jordan, Oman and Pakistan. In addition, specific topical experiences were presented by representatives of Bahrain (premarital genetic screening and women's social rights); Oman (Ministry of Health guide- lines for responsible conduct of clinical studies and trials); Lebanon (end of life care), and the Islamic Republic of Iran (integration of bioethics in health sciences curricula). UNESCO, WHO, and NBC presentations were fol- lowed by important discussions that emphasized the role of UNESCO and WHO in facilitating regional collaboration, multidisciplinary cooperation between members NBCs, the need for a “bottom up” approach in setting priorities, apply- ing strengths, weaknesses, opportunities, threats (SWOT) analysis to NECs to identify advantages and challenges, and establishing WHO collaborating centres on bioethics in the EMR. In addition, discussion covered the possible replication of Lebanon’s experience in terminal / palliative care and the integration of palliative care into graduate health sciences curricula. The second day of the meeting was dedicated to bioeth- ics during emergency and disaster situations, covering the process of generating evidence in humanitarian emergencies, and how the following questions should be addressed when planning for research in such circumstances, namely: what priority should research and other knowledge generation ac- tivities be given in humanitarian emergencies? What are the distinctive ethical features / challenges? How should these be accounted for? What constitutes effective and high-quality ethics review of protocols conducted in humanitarian crises? And what attributes characterize a research ethics commit- tee that is well suited to review crisis research? Discussion also took place about creating an ethical infrastructure for humanitarian organizations from a socio-political perspective in relation to organizational climate (formal and informal systems for communication, surveillance and sanctioning), ethics and justice. In addition, the International Bioethics Committee re- port on bioethical response to the situation of refugees, with special focus on Article 23 which provides for equality of treatment between refugees and citizens, was presented and discussed (8). The International Bioethics Committee was created in 1993 as a body of 36 independent experts to follow progress in the life sciences, and cooperate with international governmental and non-governmental organizations working in the field of bioethics. WHO’s guidance on ethical issues in infectious diseases (9) and ethics in emergencies and disasters (10) was exam- ined in detail in order to create a conceptual framework for enhancing the role of NBCs during emergencies and disas- ters. There also followed discussions on the specific principles for research during emergencies; possible political influence on such research; importance of distinguishing research ethics from general medical ethics during crises; importance of neutrality of data; and the need to share experiences and lessons learnt from inside and outside the Region. The second day of the meeting ended with two panel discussions: “legal regional harmonization” (challenges and priorities), and “national and regional cooperation among national ethics and bioethics committees” (challenges and support). The first panel discussion emphasized the adop- tion of the experience of the Gulf Cooperation Council (GCC) countries in premarital genetic counselling; firstly by making it voluntarily for one year followed by developing/ applying polices based on the year’s assessment; developing and ethically using data and biobanks; exploiting the role of WHO and UNESCO in developing frameworks for legal implementation; and the sharing of regional experiences. The second panel discussion on “national and regional cooperation among National Ethics and Bioethics Commit- tees” emphasized the need for networking among bioethics/ ethics bodies in the Region through similar fora or webinars; importance of priority-setting for rational use of resources; building capacity of policy-makers to take informed decisions that rely on a bottom-up approach; developing communica- tion skills among NBCs involving civil society and media to raise awareness of the relevant issues and create public demand; revisiting legal stipulations every 4 to 5 years; and expanding the UNESCO ABC project into other countries of the Region. Book 23-06.indb 454 8/16/2017 1:24:20 PM طسوتلما قشرل ةيحصلا ةلجلمانوشرعلاو ثلاثلا دلجلما سداسلا ددعلا 455 References 1. What is bioethics? Kansas City, MO: Center for Practical Bioethics; 2017 (https://www.practicalbioethics.org/what-is- bioethics, accessed 5 July 2017). 2. Hottois G. Defining bioethics: back to the sources. In: Mea- cham D, editor. Medicine and society, new perspectives in continental philosophy vol 120. Dordrecht: Springer Nether- lands; 2015. DOI 10.1007/978-94-017-9870-9_2. 3. Center for Ethics and Humanities in the Life Sciences. What is bioethics? East Lansing, MI: Michigan State University; 2017. (http://www.bioethics.msu.edu/what-is-bioethics, accessed 5 July 2017). 4. World Health Organization Regional Office for the Eastern Mediterranean (EMRO). UNESCO/WHO regional directors meet in support of bioethics. Cairo: EMRO; 2016 (http:// www.emro.who.int/rpc/rpc-news/unescowho-meeting-in- support-of-bioethics.html, accessed 5 July 2017). 5. World Health Organization. The global summit of national bioethics committees. Geneva: World Health Organization; 2016 (http://www.who.int/ethics/partnerships/globalsum- mit/en/, accessed 5 July 2017). 6. Ten Have H, Jean MS. The UNESCO universal declaration on bioethics and human rights. Paris: United Nations Educational Scientific and Cultural Organization (UNESCO); 2009 (http:// unesdoc.unesco.org/images/0017/001798/179844e.pdf, ac- cessed 5 July 2017). 7. Ten Have H, Dikenou C, Feinholz D. Assisting countries in establishing national bioethics committees: UNESCO’s as- sisting bioethics committees project. Camb Q Healthc Ethics. 2011;20(3):380-8. 8. United Nations Educational Scientific and Cultural Or- ganization (UNESCO). Preliminary draft report of the IBC on the bioethical response to the situation of refu- gees. Paris: UNESCO; 2016 (http://unesdoc.unesco.org/ images/0024/002452/245255E.pdf, accessed 5 July 2017). 9. World Health Organization. Guidance for managing ethi- cal issues in infectious disease outbreaks. Geneva: World Health Oranization; 2016; (http://apps.who.int/iris/bitstr eam/10665/250580/1/9789241549837-eng.pdf?ua=1, ac- cessed 5 July 2017). 10. World Health Organization. Ethics in epidemics, emergencies and disasters: research, surveillance and patient care. Geneva: World Health Organization; 2015 (http://apps.who.int/iris/ bitstream/10665/196326/1/9789241549349_eng.pdf, ac- cessed 5 July 2017). Conclusion and way forward The following recommendations resulted from the meeting in order to progress bioethics in the Region: I. Strengthening NBC/NECs through establishing/ enhancing work and roles of national ethics/bioethics com- mittees in the Region, in coordination with UNESCO/ WHO, and linking with the International Bioethics Commit- tee (IBC) and World Commission on the Ethics of Scientific Knowledge and Technology (COMEST), as needed. This would involve multi-sectoral involvement within NEC/ NBC work (including the role of media/civil society as key stakeholders to ensure compliance of concerned bodies) and allocating sufficient resources for bioethics-related com- munity protection/interventions. 2. Enhancing the role of NBC/NECs in promoting bio- ethics, health and research ethics through developing/enforc- ing legal stipulations for common ethical issues and ethical issues with significant impact on the society (e.g., premarital genetic testing, organ donation/trafficking, end-of-life care, assisted reproductive technologies); promoting consistency between regulations and practices within different institutions working on bioethical issues; raising public awareness includ- ing patients, vulnerable populations, women and youth, on bioethics related matters (e.g., informed consent process and the importance of bioethics in health care, collection, usage and storage of genetic data, etc.); promoting collaboration on education on bioethics and health ethics; fostering bioethics principles within the scientific community and other disci- plines such as laws and journalism, health sciences curricula of academic institutions and in-service training of healthcare providers (using regional/international expertise); building capacity of healthcare providers on medical/research ethics; and priority setting, impact assessment, ethics/research/ oversight during humanitarian emergencies and outbreaks (using the “Council for International Organizations of Medi- cal Sciences” [CIOMS], UNESCO, WHO guidelines, etc.) 3. Coordination and cooperation among NBC/NECs by establishing a follow-up committee of recommendations to identify priority actions, and organizing regional consulta- tion/coordination meetings during and between the bian- nual Global Summits (Dakar 2018 and beyond). Acknowledgements The authors wish to extend their thanks and gratitude to Sultan Qaboos University and members of the Omani National Bioethics Committee for hosting the Regional Summit, including Dr Ali Al-Bemani, Dr Ahmad Khitamy, Dr Muna Sadoon, Dr Ahmed Al Busaidy, Dr Ahmed Al Shukaily, Dr Taher Ba Omar, Ms Amna Al Balushi and Ms Ridha al- Hinai; as well as major support from UNESCO/HQ (Dr Dafna Feinholz, Dr Orio Ikebe) and WHO/HQ (Dr Abha Saxena, Dr Adreas Reis) offices. In addition, appreciation goes to all distinguished speakers and participants, including Dr Mariam Dashti (Bahrain), Dr Matthew Hunt (Canada), Dr Mary Medhat (Egypt), Dr Bagher Larijani (Islamic Republic of Iran), Dr Thikra Abdul-Wahab Mustafa (Iraq), Dr Mohammad Hamdan (Jordan), Dr Manal Bouhaimed (Kuwait), Dr Adnan Mroueh, Dr Michel Daher, Dr Roland Tomb (Lebanon), Dr Adhra Al-Mawali (Oman), Dr Aasim Ahmed (Pakistan), Dr Khalid Al Ali (Qatar), Dr Hasan Al Jabah (Syrian Arab Republic), Mr Mohammed Saeed Alghamdi (Saudi Arabia), Dr Aissatou Toure (Senegal), Dr Mohamed El Sheikh (Sudan), Dr Mohamed Ben Ammar, Dr Hend Bouacha (Tunisia) and Dr Ali Assabri (Yemen). Book 23-06.indb 455 8/16/2017 1:24:20 PM EASTERN MEDITERRANEAN HEALTH JOURNAL IS the official health journal published by the Eastern Mediterranean Regional Office of the World Health Organization. It is a forum for the presentation and promotion of new policies and initiatives in health services; and for the exchange of ideas, con‑ cepts, epidemiological data, research findings and other information, with special reference to the Eastern Mediterranean Region. It addresses all members of the health profession, medical and other health educational institutes, interested NGOs, WHO Col‑ laborating Centres and individuals within and outside the Region. LA REVUE DE SANTÉ DE LA MÉDITERRANÉE ORIENTALE EST une revue de santé officielle publiée par le Bureau régional de l’Organisation mondiale de la Santé pour la Méditerranée orientale. Elle offre une tribune pour la présentation et la promotion de nouvelles politiques et initiatives dans le domaine des ser‑vices de santé ainsi qu’à l’échange d’idées, de concepts, de données épidémiologiques, de résultats de recherches et d’autres informations, se rapportant plus particulièrement à la Région de la Méditerranée orientale. Elle s’adresse à tous les professionnels de la santé, aux membres des instituts médicaux et autres instituts de formation médico‑sanitaire, aux ONG, Centres collabora‑ teurs de l’OMS et personnes concernés au sein et hors de la Région. EMHJ is a trilingual, peer reviewed, open access journal and the full contents are freely available at its website: http://www/emro.who.int/emhj.htm EMHJ information for authors is available at its website: http://www.emro.who.int/emh-journal/authors/ EMHJ is abstracted/indexed in the Index Medicus and MEDLINE (Medical Literature Analysis and Retrieval Systems on Line), ISI Web of knowledge, the Cumulative Index to Nursing and Allied Health Literature (CINAHL), Embase, Lexis Nexis, Scopus and the Index Medicus for the WHO Eastern Mediterranean Region (IMEMR). © World Health Organization (WHO) 2017. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO licence (https://creativecommons.org/licenses/by-nc-sa/3.0/igo). Disclaimer. The designations employed and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of WHO concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted and dashed lines on maps represent approximate border lines for which there may not yet be full agreement. The mention of specific companies or of certain manufacturers’ products does not imply that they are endorsed or recommended by WHO in preference to others of a similar nature that are not mentioned. Errors and omissions excepted, the names of proprietary products are distinguished by initial capital letters. All reasonable precautions have been taken by WHO to verify the information contained in this publication. However, the published material is being distributed without warranty of any kind, either expressed or implied. The responsibility for the interpretation and use of the material lies with the reader. In no event shall WHO be liable for damages arising from its use. The authors alone are responsible for the views expressed in this publication and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated. If authors are staff members of the World Health Organization, the authors alone are responsible for the views expressed in this publication and do not necessarily represent the decisions, policy or views of the World Health Organization. ISSN 1020‑3397 تاسايسلا ميدقتل برنم ىهو .ةيلماعلا ةحصلا ةمظنمب طسوتلما قشرل ىميلقلإا بتكلما نع ردصت ىتلا ةيمسرلا ةلجلما ىه يرغو ثاحبلأا جئاتنو ةيئابولا تايطعلماو ميهافلماو ءارلآا لدابتلو ،اله جيوترلاو ةيحصلا تامدلخا فى ةديدلجا تاردابلماو تايلكلاو ،ةيحصلا نهلما ءاضعأ لك لىإ ةهجوم ىهو .طسوتلما قشر ميلقإب اهنم قلعتي ام ةصاخو ،تامولعلما نم كلذ دارفلأاو ةيلماعلا ةحصلا ةمظنم عم ةنواعتلما زكارلماو ،ةينعلما ةيموكلحا يرغ تماظنلما اذكو ،ةيميلعتلا دهاعلما رئاسو ةيبطلا .هجراخو ميلقلإا فى ةحصلاب ينمتهلما طسوتلما قشرل ةيحصلا ةلجلما Correspondence Editor-in-chief Eastern Mediterranean Health Journal WHO Regional Office for the Eastern Mediterranean P.O. 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Cover 23-06 (2).indd 8-10 8/16/2017 1:23:32 PM Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale Volume 23 / No. 6 June/Juin 6 ددع / نوشرعلاو ثلاثلا دلجلما ناريزح/وينوي2017 Contents V o lu m e 2 3 N u m b er 6 Ju n e 2 0 1 7 In 2015, tuberculosis still remained one of the top 10 causes of death worldwide. However, significant progress has been made in the Region over the last two decades, achieving the STOP TB Strategy target of halving the TB mortality rate since 1990. In November 2017, WHO is organizing the first global ministerial conference to support a multisectoral approach to End TB, which will take place in Moscow, Russian Federation. Editorial What would it take to eliminate tuberculosis in the Eastern Mediterranean Region? .........................................393 Research articles Surveillance of communicable diseases for decision-making in Egypt: 2006–2013 ............................................395 The relation between pica and iron deficiency in children in Zanjan, Islamic Republic of Iran: a case–control study ................................................................................................................................................ 404 Disease and treatment-related factors associated with tuberculosis treatment default in Khartoum State, Sudan: a case–control study ........................................................................................................ 408 Health labour market requirements of health professional education in Yemen .................................................415 Delays in diagnosis and treatment among children with cancer: Egyptian perspective ......................................422 Reviews The impact of antimicrobial stewardship strategies on antibiotic appropriateness and prescribing behaviours in selected countries in the Middle East: a systematic review ............................................................430 Determinants of caesarean birth on maternal demand in the Islamic Republic of Iran: a review ....................... 441 Short communication Governing the Lebanese health system: strengthening the national response to the burden of Syrian refugees ..........................................................................................................................................................449 WHO events addressing public health priorities Fostering national bioethics committees: first regional summit in the Eastern Mediterranean Region/Arab States Region ...................................................................................................................................... 453 Cover 23-06 (2).indd 5-7 8/16/2017 1:23:32 PM