An evaluation of infant immunization in Africa: is a transformation in progress?

449Bulletin of the World Health Organization | June 2007, 85 (6) Objective To assess the progress made towards meeting the goals of the African Regional Strategic Plan of the Expanded Programme on Immunization between 2001 and 2005. Methods We reviewed data from national infant immunization programmes in the 46 countries of WHO’s African Region, reviewed the literature and analysed existing data sources. We carried out face-to-face and telephone interviews with relevant staff members at regional and subregional levels. Findings The African Region fell short of the target for 80% of countries to achieve at least 80% immunization coverage by 2005. However, diphtheria–tetanus–pertussis-3 coverage increased by 15%, from 54% in 2000 to 69% in 2004. As a result, we estimate that the number of nonimmunized children declined from 1.4 million in 2002 to 900 000 in 2004. In 2004, four of seven countries with endemic or re-established wild polio virus had coverage of 50% or less, and some neighbouring countries at high risk of importation did not meet the 80% vaccination target. Reported measles cases dropped from 520 000 in 2000 to 316 000 in 2005, and mortality was reduced by approximately 60% when compared to 1999 baseline levels. A network of measles and yellow fever laboratories had been established in 29 countries by July 2005. Conclusions Rates of immunization coverage are improving dramatically in the WHO African Region. The huge increases in spending on immunization and the related improvements in programme performance are linked predominantly to increases in donor funding. Bulletin of the World Health Organization 2007;85:449–457. Une traduction en français de ce résumé figure à la fin de l’article. Al final del artículo se facilita una traducción al español. Introduction Every year more than 10 million chil- dren in low- and middle-income coun- tries die before they reach their fifth birthdays. Most die because they do not access effective interventions that would combat common and preventable child- hood illnesses.1 Infant immunization is considered essential for improving infant and child survival. Although global im- munization coverage has increased dur- ing the past decade to levels of around 78% for diphtheria–tetanus–pertussis-3 (DTP-3),2 WHO’s African Region has consistently fallen behind, reaching only 69% DTP-3 coverage by 2004 (Fig. 1). In response to challenges in global immunization, WHO and the United Nations Children’s Fund (UNICEF) set up the Global Immunization Vision and Strategy (GIVS) in 2003.3 The chief goal of GIVS is to reduce illness and death An evaluation of infant immunization in Africa: is a transformation in progress? L Arevshatian,a CJ Clements,b SK Lwanga,c AO Misore,d P Ndumbe,e JF Seward f & P Taylor g .ةلاقلما هذهل لماكلا صنلا ةياهن في ةصلاخلا هذهل ةيبرعلا ةمجترلا a PO Box 1447 MP, Harare, Zimbabwe. b Centre for International Health, Macfarlane Burnet Institute for Medical Research and Public Health, GPO Box 2284, Commercial Rd, Melbourne, Victoria 3004, Australia. Correspondence to CJ Clements (e-mail: john@clem.com.au). c PO Box 70471, Kampala, Uganda. d Department of Preventive & Promotive Health Services, Ministry of Health, Nairobi, Kenya. e Faculty of Medicine and Biomedical Sciences, University of Yaoundé, Yaoundé, Cameroon. f Centers for Disease Control and Prevention, Atlanta, GA, USA. g IMMUNIZATIONbasics, Arlington, VA, USA. doi: 10.2471/BLT.06.031526 (Submitted: 8 March 2006 – Final revised version received: 31 October 2006 – Accepted: 14 November 2006) due to vaccine-preventable diseases by at least two-thirds by 2015 or earlier. The Task Force on Immunization in Africa (TFI) recognized from the outset the need for high vaccination coverage to counter the disproportionate burden from vaccine-preventable diseases in the African Region, and therefore set chal- lenging goals for 2001–2005. These goals aimed to ensure that the immu- nization performance of the African Region caught up with other regions’ performance. The findings of a 1998 review of the Expanded Programme on Immuni- zation (EPI) 4 formed the basis for of the first EPI Regional Strategic Plan (2001–2005).5 This plan set five key objectives to be met by 2005: circulation of wild polio virus to be interrupted in all countries; maternal and neonatal tetanus to be eliminated in all high-risk districts; • • hepatitis B vaccine to be introduced into all countries, yellow fever vac- cines to be introduced in all coun- tries at risk, and Haemophilus influ- enza type b vaccine to be introduced in at least half of the countries offer- ing hepatitis B vaccine; measles to be controlled in all epide- miological blocks and eliminated in southern Africa; and 80% of the countries of the African Region to have reached at least 80% DTP-3 coverage in all districts. This paper explores the progress made on these objectives. Methods We reviewed national infant immuniza- tion programmes in the 46 countries of WHO’s African Region. (The WHO African Region does not include every • • • 450 Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in Africa L Arevshatian et al. country on the continent. Most Arabic- speaking African countries are Member States of WHO’s Eastern Mediterranean Region.) We carried out a literature review of official documents produced by minis- tries of health, WHO, UNICEF and nongovernmental organizations that related to immunization. WHO staff members subsequently were questioned about their programme areas. We carried out structured interviews with WHO staff members and partners at regional, country and intercountry levels, and conducted face-to-face and telephone interviews with subregional teams. We then analysed the data collected in light of the 25 separate immuniza- tion goals and five key objectives of the EPI Regional Strategic Plan. We com- pared the data and information gathered through the interviews and literature review with these strategic goals in order to determine whether the key objectives had been met; 2000 was considered the baseline year for measurement of performance. Finally, we collated all routine im- munization coverage estimates from the WHO/UNICEF Joint Reporting Forms submitted annually by each country. These reports outline the country’s of- ficial estimates of vaccination coverage, which are derived in most cases from administrative data collected during vaccination sessions. Coverage was estimated by clustering countries with similar target disease control dynamics weighted by population. One strategy WHO used to improve coverage was to divide countries within the African Region into five epidemiological blocks. The first block, the “Big Four”, includes Angola, the Democratic Republic of Congo, Ethiopia and Nigeria. These four countries incorporate 40% of the African Region’s population. The region is further divided into the central block (seven countries), eastern block (six countries), western block (16 countries) and southern block (13 countries). Findings In Table 1 (available at: http://www.who. int/bulletin) we summarize the progress made towards achieving the strategic goals. We found that although more infants had been immunized by 2005, most of the targets had been missed by at least half of the region’s countries. We identified eleven target areas, the find- ings from which are outlined below. Fig. 1. Diphtheria–tetanus–pertussis-3 (DTP-3) percentage coverage by WHO Region, 1999–2004 100 D TP -3 p er ce nt ag e co ve ra ge 1999 0 Year 90 80 70 60 50 2000 2001 2002 2003 2004 Eastern Mediterranean Region Western Pacific Region Africa Region European Region Region of the Americas South-East Asia Region Source: WHO database 2005. Routine immunization Between 2000 and 2004, the African Re- gion made progress in increasing routine immunization coverage (Table 2, avail- able at: http://www.who.int/bulletin). Although the region fell well short of the target of 80% of countries achieving at least 80% coverage nationwide, cover- age increased in a majority of countries. DTP-3 coverage is widely recognized as a good indicator of the strength of routine immunization services, and this coverage increased from 54% in 2000 to 69% in 2004 across the African Region; 22 (48%) of the countries reported achieving at least 80% DTP-3 coverage in 2004, an increase from 11 countries in 2000. The same number of countries, although not the same list of countries, also reported that 50% or more of their districts achieved DTP-3 coverage of 80% or higher in 2004. As a result, we estimate that the number of nonim- munized children, defined as children who had not received the third dose of DTP-3 by their first birthday, declined dramatically across the region from 1.4 million in 2002 to less than 900 000 in 2004. Despite these gains, more than one- third of African Region districts did not acquire 50% DTP-3 coverage by the end of 2004. Coverage levels of other routine vaccines, including measles, oral polio, bacillus Calmette Guerin (BCG) and tetanus toxoid also lagged in many of the same areas. Factors holding back routine immunization services in the African Region included civil unrest, lack of human resources within health ministries, limited funding for routine immunization services, and competi- tion for staff time among individuals involved in polio and measles supple- mentary immunization activities. Table 3 (available at: http://www. who.int/bulletin) summarizes the achievements made within these areas between 2001 and 2005. During this period, various strategies were imple- mented to help the Big Four and other low-performing countries increase rou- tine immunization coverage. The Reach- ing Every District initiative, for example, was implemented in 22 countries be- tween 2002 and 2004.6 This strategy involves prioritizing low-performing districts by strengthening five important immunization functions at the district level. These functions are planning and management of resources; capacity- building through training and support- ive supervision; sustainable outreach; links between communities and health facilities; and active monitoring and use of data for decision-making. A recent 451Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in AfricaL Arevshatian et al. Fig. 2. Estimated measles mortality in the African Region, 1999–2004 Source: WHO database 2005. 600 N um be r of c as es (t ho us an ds ) 1999 0 Year 500 400 300 200 100 2000 2001 2002 2003 2004 assessment carried out in five of these early implementation countries shows significant improvements in DTP-3 cov- erage.7 Other strategies included imple- menting an ambitious capacity-building programme to improve the management and vaccine logistics of national immuni- zation programmes; integrating routine immunization functions alongside polio and measles activities; building on new vaccine introduction to update routine immunization skills and systems; and streamlining communication and social mobilization activities. Although a relatively small amount of regional funding is available for routine immunization programmes, resources available to control polio and measles and to introduce new vaccines have been used to support their critical functions. GAVI Alliance (formerly known as the Global Alliance for Vac- cines and Immunisation) funding for immunization services became avail- able to many countries after 2001 and has contributed to the positive trend in routine coverage.8 Polio eradication The Polio Eradication Initiative faced a global crisis between 2001 and 2005, when a resurgence of polio cases oc- curred across Africa and Asia following the cessation of immunization activities in Nigeria.9 Nigeria became a major exporter of wild polio virus to many coun- tries, threatening the gains that had so painstakingly been achieved. However, in 2004 WHO brokered an alliance between the government and religious leaders that led to resumed immuniza- tion activities in the country’s northern area. This was followed by increased investment in the purchasing of vac- cines, national immunization days and improved surveillance across countries in the African Region. Although there has been extraordinary progress, it is not yet known when the wild polio virus will be eliminated from the African Region (Table 4, available at: http://www.who. int/bulletin). Between 2000 and 2002, the num- ber of polio-endemic countries de- clined from 11 in 2000 to 2 in 2002, and reported incidence of polio declined by 89%, from 1863 cases in 2000 to 208 cases in 2002. Polio was endemic in Nigeria and Niger, and possibly in Chad. In September 2003, amid speculation in northern Nigeria that the polio vaccine was contaminated with contraceptive and infectious agents, immunization activities in endemic states were sus- pended. Coverage significantly declined in almost all northern Nigerian states, resulting in a resurgence of polio cases with transmission to epidemic levels. Previously polio-free states in southern Nigeria saw the disease’s resurgence, and by the end of 2003 transmission had spread to eight African Region coun- tries (Benin, Burkina Faso, Cameroon, Central African Republic, Chad, Côte d’Ivoire, Ghana and Togo) and to others outside the region. By mid-2005, 18 countries in three WHO regions had reported wild polio virus cases: Angola, Benin, Botswana, Burkina Faso, Camer- oon, Chad, Côte d’Ivoire, Eritrea, Ethio- pia, Ghana, Guinea, Mali, Niger and Togo (African Region); Saudi Arabia, Sudan and Yemen (Eastern Mediterra- nean Region); and Indonesia (South- East Asian Region). In addition, five countries had re-established endemic transmission: Burkina Faso, Central African Republic, Chad, Côte d’Ivoire and Mali. The Nigerian states that had sus- pended immunization activities sub- sequently resumed campaigns in July 200410 in conjunction with other cam- paigns across west and central Africa. As a result, surveillance data from the first half of 2005 suggest that polio cases were decreasing in Nigeria, and that previously polio-free countries were no longer being directly infected by the Nigeria-derived virus. Despite some progress towards improving routine polio vaccine cover- age in the African Region, low coverage in several countries was a significant contributory factor to the 2003–2004 regional resurgence of wild polio virus transmission. In 2004, four of seven countries with endemic or re-established wild polio virus had vaccine coverage of 50% or less, and some neighbouring countries at high risk of importation still had routine immunization coverage levels well below the 80% target. Measles According to WHO estimates in 2000, measles accounted for approximately 777 000 deaths worldwide, of which around 60% occurred in sub-Saharan Africa. The number of cases reported to WHO/UNICEF dropped from 520 000 in 2000 to 316 000 in 2005. These data suggest that considerable progress has been made in reducing regional mor- tality from this disease, although the regional objectives have not yet been achieved. The joint WHO/UNICEF 2001 measles mortality reduction plan focuses on 45 priority countries that ac- count for almost 95% of global measles deaths. With support from the Measles Partnership, a consortium of nongov- ernmental and UN-based organizations, African Region countries have made outstanding progress towards the World Health Assembly goal of a 50% reduc- tion in measles mortality worldwide. By 2004, there was an estimated reduc- tion in measles mortality of 60% in the African Region from 1999 baseline levels (Fig. 2). Between 2000 and 2004, significant progress was made in improving routine measles coverage, one of the major strate- gies for mortality reduction. During this 452 Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in Africa L Arevshatian et al. time period, routine measles vaccine cov- erage increased 14%. In 2004, 17 coun- tries and 30% of districts in the African Region had measles vaccine coverage of 80% or more, and 20% of districts had coverage of 90% or more. However, in 2004 coverage remained low in some countries, with Côte d’Ivoire, Gabon, Liberia and Nigeria achieving coverage of less than 50%. Across the region, available data indicate that more than a third of all districts, most in the Big Four countries, reported routine measles coverage below this level (Fig. 3). Another successful strategy for mea- sles mortality reduction and control has been to use catch-up and follow-up im- munization campaigns. Between 2001 and 2004, country-wide measles catch- up campaigns targeting children aged between 9 months and 14 years were completed in 26 countries and follow-up campaigns in five countries. These strat- egies resulted in the immunization of 127 million children. During 2005, five additional countries planned to conduct catch-up campaigns, and nine planned to conduct follow-up campaigns target- ing children aged between 9 months and 5 years. By the end of 2005, the projected number of children vaccinated as a result of these campaigns was over 200 million. Coverage above 90% was achieved in most campaigns, and has in most of these countries resulted in a dramatic decrease in measles incidence. Between 2000 and 2003, 82.1 mil- lion children were targeted for vaccina- tion during initial campaigns in 12 Afri- can countries and follow-up campaigns in seven countries.11 The average decline in the number of reported measles cases was 91%. In 17 of the 19 countries, measles case-based surveillance con- firmed that transmission of measles virus and measles deaths were reduced to low rates. The estimated number of deaths averted in the year 2003 was 90 000. Between 2000 and 2003, there was a 20% decline in annual African Region measles deaths.11 Measles campaigns proved to be an important vehicle for the integrated delivery of other essential child health services, including insecticide-treated bednets, oral polio vaccine, vitamin A supplementation and treatment for para- sitic infections. Throughout 2004, suc- cessful integrated bednet and measles campaigns were carried out in Ghana, Togo and Zambia. Measles outbreaks, some large (for example, 2946 cases in Fig. 3. Measles coverage by district in the African Region, 2004 Source: WHO database, 2005. < 10% coverage 10—29% coverage ‡ 30% coverage No information Eastern Mediterranean Region countries Burkina Faso in 2003) occurred after the catch-up campaigns. These out- breaks provide some important lessons regarding gaps in coverage and the role of unpredictable events. For example, lessons learned from the large and ongo- ing population movements from Côte d’Ivoire to Burkina Faso and their impact on subsequent vaccination campaigns can be used to improve future regional measles elimination efforts. Communication Effective communication and social mo- bilization involve a variety of tasks, such as advocacy campaigns among political, traditional and religious leaders, as well as creating community demand for ser- vices and encouraging the community to use services. Almost every disease- control initiative we reviewed required increased advocacy of some sort, as well as counselling of family members and sustained community involvement. Many countries that we reviewed had successful communication campaigns because they received support from WHO and UNICEF country offices and a range of local organizations. We found that only a small number of staff mem- bers were dedicated to communication- related issues and that this limited their effectiveness. Since the introduction of the Reaching Every District initiative, however, resources for communication and social mobilization have increased at district and community levels. Surveillance and laboratories Between 2001 and 2005, 30% of dis- tricts within the African Region did not report data to WHO and UNICEF. During the period under review, the Polio Eradication Initiative generated 453Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in AfricaL Arevshatian et al. unprecedented regional interest and support for improving surveillance. The quality of regional surveillance for acute flaccid paralysis improved steadily between 2001 and 2005, with a consis- tent increase in the number of countries attaining and sustaining the two key performance indicator targets. The first indicator is the annual reporting rate; the target set for 2005 was for countries to achieve a reporting rate of non-polio acute flaccid paralysis of at least 1 case per 100 000 among children younger than 15 years old. The second indicator relates to the completeness of speci- men collection; the target set for 2005 was to ensure that two adequate stool specimens were collected from at least 80% of children with acute flaccid pa- ralysis. In 2000, only five countries had achieved both these minimum targets; by July 2005, 35 countries had achieved them. In 2004, 38 countries carrying out acute flaccid paralysis surveillance had achieved surveillance rates greater than 1 case per 100 000, and the regional rate was 3 per 100 000. This improve- ment was largely a result of increased recruitment of surveillance officers to undertake active case-finding. By July 2005, case-based measles surveillance and laboratory confirmation had been initiated in 26 countries. Routine moni- toring showed that the quality of measles surveillance improved steadily between 2002 and 2004 (Table 5, available at: http://www.who.int/bulletin). In 2004, the annual reported rate of suspected measles cases confirmed with serum specimens was 3.6 per 100 000 popula- tion, well above the recommended level of 1 per 100 000. For diseases such as maternal and neonatal tetanus and yellow fever, sig- nificant surveillance gaps remain in most countries. Case-based yellow fever surveillance has been implemented but performance remains poor throughout the region. However, newly created sur- veillance networks offer opportunities to better understand the health burden of particular diseases, and to monitor the impact of new vaccines for Haemophilus influenzae type b, rotavirus and pneumo- coccal pneumonia. We found that laboratories initially dedicated to surveillance of acute flaccid paralysis also took on other surveillance roles between 2001 and 2005. Expand- ing on the polio laboratory network, a network of measles and yellow fever lab- oratories was established in 29 countries by July 2005. Training was undertaken and laboratories received accreditation if they met required standards. These laboratories all had initiated testing for measles by 2005, and all had the capac- ity to confirm and test measles-negative cases for rubella. These laboratories may be able to test for other diseases in the future. By 2005, these laboratories’ ca- pacity was expanded to enable outbreak investigations for measles and meningi- tis. Significant progress was also made in implementing integrated disease surveil- lance and response. Lost emphasis on target diseases Funded activities for two other target diseases, yellow fever and maternal/ neonatal tetanus, in many cases did not receive much-needed in-country atten- tion. Unprecedented financing from donors such as UNICEF occurred be- tween 2001 and 2005 for these diseases. National programmes, however, were focused on the vaccination of diseases considered to be essential, and govern- ments received less donor pressure to vaccinate for yellow fever and tetanus. In addition, there was a worldwide short- age of vaccines for these two diseases. As a result, only half the regional surveil- lance objectives were achieved for ma- ternal and neonatal tetanus, and tetanus elimination goals were not met. Only 15 (32.5%) of 46 countries achieved a neonatal tetanus incidence rate of less than 1 case per 1000 live births. Only one country achieved coverage of 80% among pregnant women in every district for two or more doses of tetanus toxoid vaccine (TT2+); TT2+ coverage of 50–79% in every district was reported by only three of 46 countries. The remain- ing 42 countries reported TT2+ coverage of less than 50% in every district. Despite impressive additional sup- port from the Children’s Vaccine Initia- tive and the GAVI Alliance, yellow fever goals were not met by 2005. Only 22 of 31 at-risk countries had incorporated yellow fever vaccination into their na- tional immunization programmes by the end of 2004, and only four had achieved 80% vaccine coverage by 2004. Surveillance of the disease was also poor, and targets for district-level reporting of suspected cases were not met. Many at- risk countries did not prioritize yellow fever control or were unable to afford the vaccine. Renewed GAVI Alliance support is expected to improve vaccine availability. Vitamin A While vitamin A deficiency remains a health issue in 44 of 46 African Region countries, the integration of programme delivery with immunization services dramatically improved the situation between 2001 and 2005. Prior to 1998, distribution had been limited to nutri- tional and maternal and child health clinics. Subsequently, vitamin A began to be administered through routine and supplementary immunization activities in an increasing number of countries.12 We found that by 2005, only 22 of the 44 at-risk countries had established a policy for integrating vitamin A supple- mentation with vaccine delivery; 12 of the 22 countries reported the integra- tion of vitamin A distribution with routine immunization services. Between 2000 and 2004, 36 countries in the re- gion reported administering vitamin A during polio campaigns or subnational measles immunization days. New vaccine introduction The region’s disease burden of hepatitis B virus infection is considered to be moderate to high. With support from the GAVI Alliance, substantial progress has been made in introducing new and under-used vaccines since 2000, including hepatitis B (HepB) vaccine. However, the key objective of the EPI Regional Strategic Plan 2001–2005 to in- troduce HepB vaccination programmes in every country was not achieved. In 2000, the vaccine’s introduction was limited to Botswana, Gambia, Mauritius, Seychelles, South Africa, Swaziland and Zimbabwe. The reasons for delayed in- troduction included high vaccine cost, weak infrastructure and low financing priority among donors. By 2005, 28 (61%) countries had reported using the HepB vaccine (Table 6, available at: http://www.who.int/bulletin). Coverage ranged from 8% in Nigeria to 100% in Sao Tome, indicating a highly variable degree of implementation. However, most countries that introduced the HepB vaccine had achieved coverage of 60% or higher. Of 28 countries that introduced the vaccine, 17 achieved coverage levels equal to DTP-3 coverage, largely because a combination diphtheria–tetanus– pertussis-HepB vaccine was used. WHO estimates that between 100 000 and 160 000 children die each 454 Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in Africa L Arevshatian et al. year from Haemophilous influenzae type b (Hib) infection in Africa, which remains by far the highest rate in the world. The annual incidence of this infection ranges from 25 to 60 cases per 100 000 among children younger than 5 years old.13 Data for 1999–2004 from a newly established national laboratory-based surveillance system in South Africa showed a decrease in disease burden among children fol- lowing conjugate vaccine introduction in 1999.14 The absolute number of cases in the study among children younger than 1 year decreased by 65%, from 55 cases in 1999–2000 to 19 cases in 2003–2004. The Hib vaccine remains regionally un- derused because of a lack of awareness of disease burden, high vaccine cost and concern about financial sustainability. The Paediatric Bacterial Meningitis labo- ratory surveillance network has helped countries to document disease burden; however, by the end of 2004 only ten countries had introduced Hib vaccines. This outcome fell short of the regional objective to introduce Hib vaccination into the programmes of half of the African Region countries. We highlight coverage levels in Table 7 (available at: http://www.who.int/bulletin). Financial sustainability and waste disposal The huge increase in spending on im- munization and the related improve- ments in programme performance can be tracked predominantly to donor funding increases, as 38 of 46 countries in the African Region established line items for immunization in their national budgets, 12 countries bought all of their own vaccines and 19 countries that re- ceived support from the GAVI Alliance developed financial sustainability plans. Unfortunately, more than a third of the countries that established budget line items did not fund them, and most of the countries with financial plans did not use them to the degree expected. The GAVI Alliance is now developing comprehensive multi-year plans that must be both costed and incorporated into national budgets. Lastly, we found that countries have not yet paid sufficient attention to the proper disposal of used injection equip- ment. With the advent of the injection- based measles campaigns, as oppose to the oral vaccines used in the polio cam- paigns, this has become an important issue. We found that 41 countries dis- tributed safety boxes for the collection of used syringes and 33 countries re- ported using some kind of incineration. However, most of the incinerators are single-chamber burners that burn at low temperatures. Many countries adopted the method of open burning of syringes, although environmentalists consider this practice unacceptable. Conclusions Immunization coverage is improving dramatically in the African Region. The huge increases in spending on immu- nization and the related improvements in programme performance are linked predominantly to increased donor fund- ing. The African Region has witnessed unprecedented successes in its immuni- zation campaigns, in developing surveil- lance infrastructure, and in its ability to purchase vaccines through external support. Campaigns have enabled phe- nomenal advances in the control of polio and measles. However, polio’s resurgence in Nigeria underlines the need for eradi- cation to be pursued rapidly to ensure that the huge investments made to date are not lost. Failure to achieve this goal will harm immunization programmes across the continent. Although the analysis of the data presented in our review is accurate, there is less certainty about the valid- ity of the data that we analysed. Some of the analysis of coverage and disease incidence trends was carried out with data submitted by countries through the WHO/UNICEF Joint Reporting Form and was not independently validated or cross-checked. The absolute numbers of deaths averted, infants immunized or cases reported are therefore subject to under- or over-reporting. However, we consider the overall trends more reliable and these consistently point towards dramatic performance improvements by the majority of African Region coun- tries. Although regional surveillance infrastructure has definitely improved tremendously, doubts remain about the quality of data generated. An assessment of the accuracy or validity of official cov- erage rates was not part of this review. The official country estimates have several limitations. Although the quality and completeness of the administrative data used to calculate these estimates have improved in recent years, no coun- tries reported on 100% of their districts in any given year. In 2004, for example, Liberia and Nigeria both failed to report on 30% or more of their districts. In addition, although coverage estimates derived from administrative data are considered to reflect trends in immuni- zation coverage, they are often higher or lower than the actual coverage rates. A recent study of official DTP-3 coverage rates in 45 countries, which included countries in Africa, found higher DTP- 3 coverage levels being reported than those reported from household cover- age surveys.15 The size of the difference increased with higher levels of reported coverage. As a result, there are several countries in Africa in which official cov- erage estimates are considered to be low because populations have been over- estimated. Although this may mean that the regional goals are less likely to be reached, reporting problems have been present in all years and we therefore consider trends in coverage over time to be valid. The GAVI Alliance and the Mil- lennium Development Goals have es- tablished ambitious objectives for strengthening national immunization programmes during 2006–2015, provid- ing a road map for the African Region to follow. Although the region has made progress in recent years, there is still much to be done to achieve these new goals. The gains documented in our review show substantial progress, yet these achievements are modest, despite massive investment. The cost of immu- nization has increased and will continue to increase with the addition of new and more expensive vaccines and technolo- gies, and funding is not yet secured for the coming years. During the past 5 years the GAVI Alliance, the Polio Eradication Initiative, the Measles Partnership and others have increased resources available for immu- nization; however, the ways in which countries access and use donor support have changed. The changing donor environment highlights fundamental differences between donors in the way they interact with countries and with each other. There is a real danger that donors with different agendas could bias the immunization agenda, resulting in national health ministries diverting their attention away from their man- date. In addition, coverage rates could fall if donor fatigue again sets in, as it did in the 1990s. Acquiring long-term funding, from both government sources and external partners, will be crucial in 455Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in AfricaL Arevshatian et al. improving immunization coverage. In Table 8 we outline the key issues and future priorities for the African Region during the next 5 years. Although campaigns have greatly contributed to increased immunization coverage, lasting success will depend on development of robust routine ser- vices. The African Region is beginning the transition to a time without polio eradication funds, and creative thinking is urgently needed to maintain the gains previously made. Efforts are needed to build strong and sustainable routine immunization services and improve sur- veillance capacity before polio-focused resources are withdrawn. Measles con- trol in Africa has the potential to be the successor to polio eradication, and holds the promise of continuing as a major primary health-care intervention and as a magnet for external investment in the coming decade. We hope this initiative will galvanize partner support for im- munization and be an important vehicle for other public health initiatives. Improvements in routine immuni- zation have not kept up with regional advances in other areas of immuniza- tion. Many countries in which coverage remains below 50% put initiatives such as polio eradication and measles control at risk. Considerable work is needed to consolidate past gains and effectively address pockets of low vaccination cov- erage. The Reaching Every District ini- tiative shows potential for invigorating routine services, particularly outreach activities. However, low routine coverage is particularly alarming in the countries like Nigeria where 25% of sub-Saharan Africa’s children reside. Here, low rou- tine coverage and the implementation of polio national immunization days have failed to interrupt polio transmission. Other countries where recent outbreaks have occurred may also require extra attention to ensure that routine services are not neglected. The Measles Partner- ship has agreed to set aside up to 10% of its funding in each country to increase routine measles vaccination and, where appropriate, to help countries introduce a second dose of measles vaccination within the routine programme. National programmes need to maintain and improve routine immu- nization services, yet new vaccines and new technologies are waiting to be in- troduced. Can both be done effectively? Will governments take ownership of running and financing routine services? Instead of being pressured to accept a new vaccine, or being encouraged to introduce a new vaccine because it is politically expedient, countries must base their decisions and applications for new vaccines on solid epidemiological data and on evidence that supports the cost-effectiveness of any new approach. Encouragingly, post-introduction as- sessments carried out to date in six countries show that the introduction of new vaccines does not cause disruption, but instead stimulates improvements in routine services.8 The WHO African Region is at a crucial point in immunization history. Table 8. Key issues and future priorities in the African Region Strategic goals Key issues Funding Secure long-term funding sources. Increase government commitment to budget for immunization programmes and to fund them. Routine coverage Raise coverage to uniformly high levels, particularly in the Big Four countries. Surveillance Integrate and expand surveillance for other vaccine- preventable diseases in conjunction with existing surveillance programmes for acute flaccid paralysis. Work towards incorporating all surveillance programmes into one system. Polio eradication Meet targets to eliminate polio, focusing particularly on Nigeria. Transfer the skills and resources developed through the polio programme to other control programmes. Measles control Ensure that measles control is at the centre of immunization programmes in the next 10 years. Vitamin A supplementation Fully integrate vitamin A distribution with immunization services and focus on reaching wider age groups through new strategies: for example, pre-school programmes. Immunization strategies Test strategies that could raise routine coverage and expand these campaigns to improve coverage. Waste disposal Find better solutions for the disposal of injection equipment. These solutions must be environmentally acceptable, practical and low-cost. Staff Incorporate polio staff into the regular work force before their funding dries up. New vaccines Take advantage of new funds to support the introduction of new vaccines and new technologies. We have already begun to see consider- able improvements, and in the next de- cade we anticipate further progress. We must aim for higher vaccination coverage rates, fewer deaths and cases of vaccine- preventable diseases, a wider range of age groups targeted for immunization and the introduction of new vaccines and new technologies. Immunization donors and regional governments have been instrumental in initiating change, yet continued donor support will be needed if greater improvements are to be made. The enthusiasm, expertise and resources mobilized through the Polio Eradication Initiative, the Measles Partnership, the GAVI Alliance and other initiatives have transformed the immunization scene in Africa, but a more robust and long-term approach to funding is needed to sustain these improvements. O Competing interests: None declared. 456 Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in Africa L Arevshatian et al. Résumé Vaccination des nourissons : évaluation des progrès réalisés en Afrique Objectif Evaluer les progrès enregistrés entre 2001 et 2005 dans la réalisation des objectifs du Plan régional stratégique pour l’Afrique du Programme élargi de vaccination. Méthodes Nous avons analysé les informations provenant des programmes de vaccination des nourissons de 46 pays de la Région africaine de l’OMS et celles tirées de la littérature et des sources de données existantes à ce sujet. Nous avons procédé à des entretiens en face-à-face ou par téléphone avec des responsables au niveau régional ou infrarégional de ces programmes, pouvant être utiles à l’étude. Résultats En 2005, 80 % des pays de la Région africaine de l’OMS n’avaient pas réussi à atteindre l’objectif en termes de couverture vaccinale fixé pour cette année, à savoir 80 % au moins. Néanmoins, le taux de couverture par le vaccin antidiphtérique- antitétanique-anticoquelucheux 3 (DTC3) est passé de 54 % en 2000 à 69 % en 2004, soit une augmentation de 15 %. Nous estimons par conséquent que le nombre d’enfants non vaccinés a baissé de 1,4 million en 2002 à 900 000 en 2004. Au cours de cette dernière année, on a relevé un taux de couverture par le DTC ne dépassant pas 50 % dans quatre des sept pays d’endémie ou de résurgence du poliovirus sauvage et un taux de couverture n’atteignant pas l’objectif de 80 % dans certains pays voisins exposés à un risque élevé d’importation de ce virus. Le nombre des cas notifiés de rougeole est tombé de 520 000 en 2000 à 316 000 en 2005 et la mortalité due à cette maladie a diminué de 60 % par rapport aux niveaux de référence de 1999. Un réseau de laboratoires a été mis en place dans 29 pays pour la surveillance de la rougeole et de la fièvre jaune. Conclusion Les taux de couverture vaccinale augmentent considérablement dans la Région africaine de l’OMS. La très forte hausse des dépenses consacrées à la vaccination et à l’amélioration des résultats programmatiques connexes est liée principalement à l’augmentation du financement par les donateurs. Resumen Evaluación de la inmunización de los lactantes en África: ¿está cambiando la situación? Objetivo Evaluar los progresos realizados para alcanzar las metas del Plan Estratégico de la Región de África del Programa Ampliado de Inmunización entre 2001 y 2005. Métodos Estudiamos los datos de los programas nacionales de inmunización de lactantes de los 46 países de la Región de África de la OMS, y analizamos la bibliografía y las fuentes de datos existentes al respecto. Además, llevamos a cabo entrevistas personales y telefónicas con los funcionarios oportunos a nivel regional y subregional. Resultados La Región de África no alcanzó la meta de que un 80% de los países garantizara una cobertura de inmunización de al menos un 80% para 2005. Sin embargo, la cobertura con la vacuna contra la difteria, el tétanos y la tos ferina (DTP3) aumentó en un 15%, del 54% en 2000 al 69% en 2004. En consecuencia, estimamos que el número de niños no inmunizados disminuyó de 1,4 millones en 2002 a 900 000 en 2004. En ese último año, cuatro de siete países con poliovirus salvaje endémico o reintroducido presentaban una cobertura del 50% o menos, y algunos países vecinos con alto riesgo de importación no lograron la meta de vacunación del 80%. Los casos de sarampión notificados cayeron de 520 000 en 2000 a 316 000 en 2005, y la mortalidad por esa causa se redujo aproximadamente en un 60% en comparación con los niveles basales de 1999. En julio de 2005 se había establecido una red de laboratorios para el sarampión y la fiebre amarilla en 29 países. Conclusión Las tasas de cobertura inmunitaria están mejorando extraordinariamente en la Región de África de la OMS. Los enormes incrementos del gasto en inmunización y las mejoras resultantes en la ejecución de los programas se deben sobre todo al aumento de los fondos de donantes. صخلم زرْحُمـلا م ُّدقتلا في لُّوحت ثدح له :ايقيرفأ في ع َّضرلا عينتم ةطشنأ ميـيقت فادهأ قيقحت هاجت زرْحُمـلا م ُّدقتلا ميـيقت ةساردلا هذه تفدهتسا :ضرغلا ع َّسولما جمانبرلا راطإ في ةذ َّفنلما ،ةيقيرفلأا ةيميلقلإا ةيجيتارـتسلاا ةطخلا .2005 ماع لىإ 2001 ماع نم ةدلما في كلذو ،عينمتلل عينمتل ةينطولا جمابرلا نم ةدمتْسُمـلا تايطعلما ةعجارم تتم :ةقيرطلا 46 اهددع غلابلا ،ةيلماعلا ةحصلا ةمظنلم يقيرفلأا ميلقلإا نادلب في ع َّضرلا تايطعلما رداصم ليلحتو ،ةلصلا تاذ تاساردلا ةعجارم تتم ماك ،ًادلب عم ،فتاهلا قيرط نع تلاباقمو ةيصخش تلاباقم تيرجأ دقو .ةيلاحلا .يميلقلإا نودو يميلقلإا ىوتسلما لىع ينّـِ ينعلما ينلماعلا ةيعينتم ةيطغت قيقحت في لِّثمتلما فدهلا يقيرفلأا ميلقلإا ققحي لم :جئاتنلا ،كلذ عمو .2005 ماع لولحب نادلبلا نم %80 في لقلأا لىع %80 ةبسنب ،%15 ةبسنب قوهاشلاو زازكلاو قانخلل ثيلاثلا حاقللاب ةيطغتلا تعفترا نأ اننكيم .2004 ماع في %69 لىإ 2000 ماع في %54 نم تعفترا ثيح لفط نويلم 1.4 نم ضفخنا ينعَّنملما يرغ لافطلأا ددع نأ كلذ نم صلختسن ق َّقح ًاضيأ 2004 ماع فيو .2004 ماع في لفط 900000 لىإ 2002 ماع في وأ ،يبرلا لافطلأا للش سويرف اهيف شرتني نادلب ةعبس لصأ نم نادلب ةعبرأ ةرواجلما نادلبلا ضعب نأ ماك .لقأ وأ %50 ةبسنب ةيطغت ،اهيف روهظلا دواع نم %80 ميعطت فده ق ِّقحت لم سويرفلا ةدافو رطخل ةدشب ةضَّرعلما ماع في 520000 نم ،ةغلبلما ةبصحلا تلااح ددع ضافخنا ظحولو .ناكسلا %60 وحنب تايفولا لدعم ضفخنا ماك ،2005 ماع في 316000 لىإ 2000 ،2005 ويلوي/زوتم لولحبو .1999 ماع في ةيساسلأا اهتايوتسم عم ةنراقلماب .ًادلب 29 في ءارفصلا ىمحلاو ةبصحلا صيخشت تابرتخم نم ةكبش ْتَئِشْنُأ ميلقلإا في سوملم لكشب عينمتلاب ةيطغتلا تلادعم ن َّسحتـت :جاتنتسلاا ،عينمتلا لىع قافنلإا في ةيربكلا ةدايزلا امأ .ةيلماعلا ةحصلا ةمظنلم يقيرفلأا نم م َّدقلما ليومتلا في ةدايزلا لىإ ًاساسأ ىزعُتف ،جمانبرلا ءادأ في ن ُّسحتلاو .ةحنالما تاهجلا 457Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in AfricaL Arevshatian et al. References 1. Lee JW. Child survival: a global health challenge. Lancet 2003;362:262. 2. Global Immunization Vision and Strategy (GIVS). Facts and figures April 2005. Geneva: WHO; 2005. Available at: http://www.who.int/immunization/ newsroom/Global_imm_data_October2006.pdf 3. Global immunization vision and strategy 2006-2015. Geneva: WHO; 2005. Available at: http://www.who.int/vaccines-documents/DocsPDF05/GIVS_ Final_EN.pdf 4. A review of the Expanded Programme on Immunization (EPI) in the African Region 1998. Harare: WHO; 1998. 5. Expanded Programme on Immunization (EPI) in the African Region: strategic plan of action 2001-2005. Harare: WHO; 2001. 6. Reaching Every District Strategy implementation in the African Region. evaluation report. Geneva: WHO; 2005. 7. Implementation of the strategy “Reaching Every District” and improvement of the vaccination coverage in the African Region: World Health Organization (AFRO). Vaccine Preventable Diseases Bulletin 2005;056:1-2. 8. Chee G, Fields R, Hsi N, Schott W. Evaluation of GAVI immunization services support funding. 13 th GAVI Board Meeting, Washington, 6-7 July 2004. Available at: www.gavialliance.org/Governance/Board_Reports/13_board_ ISS findings.php 9. Ahmad K. Kano to recommence vaccination against poliomyelitis. Lancet Neurol 2004;3:388. 10. Progress towards poliomyelitis eradication in Nigeria; January 2004-July 2005. Wkly Epidemiol Rec 2005;80:305-10. 11. Otten M, Kezaala R, Fall A, Masresha B, Martin R, Cairns L, et al. Public- health impact of accelerated measles control in the WHO African Region 2000–03. Lancet 2005;366:832-39. 12. Integration of vitamin A supplementation with immunization: policy and programme implications: report of a meeting (WHO/EPI/GEN/98.07). UNICEF, New York, 12-13 January 1998. Available at: http://www.who.int/vaccines- documents/DocsPDF/www9837.pdf 13. Haemophilus influenzae type b (Hib) meningitis in the pre-vaccine era: a global review of incidence, age distributions, and case-fatality rates. Geneva: WHO; 2002 (WHO/V&B/02.18). 14. von Gottberg A, de Gouveia L, Madhi SA, du Plessis M, Quan V, Soma K, et al. Respiratory and meningeal disease surveillance in South Africa: impact of conjugate Haemophilus influenzae type b (Hib) vaccine introduction in South Africa. Bull World Health Organ 2006;84:811-18. 15. Murray CJ, Shengelia B, Gupta N, Moussavi S, Tandon A, Thieren M. Validity of reported vaccination coverage in 45 countries. Lancet 2003;362:1022-27. ABulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in AfricaL Arevshatian et al. Table 1. Level of achievement of strategic goals defined in the EPI Regional Strategic Plan, 2001–2005 Strategic goals Level of attainment by mid-2005a Strengthen immunization systems At least 80% of the countries to attain at least 80% DTP-3 coverage in all districts 22 countries (48%) All countries to attain 100% safety of immunization injections 14 countries exclusively use auto-disposable syringes All countries to assure sustainable funding for EPI Regional Strategic Plan 38 countries have budget lines; 20 have their budgets funded at some level Polio eradication No cases of acute flaccid paralysis associated with wild polio virus 408 laboratory-confirmed cases of wild polio virus reported as of 26 August 2005 No wild polio virus in the African Region, assessed through virological sampling of patients with acute flaccid paralysis and their contacts Seven countries reporting wild polio virus (Burkino Faso, Central African Republic, Chad, Côte d’Ivoire, Mali, Niger and Nigeria) The process of independent certification of polio-free status will lead to full regional certification 15 countries were invited to present polio-free certification documentationa Measles control/elimination Countries with low immunization coverage (< 50%) and high mortality (case fatality rate > 4%) to reduce measles morbidity by 90% and measles mortality by 95% in comparison with pre-vaccine figures None of the four identified countries (Côte d’Ivoire, Gabon, Liberia, Nigeria) achieved this objective Countries with moderate measles routine coverage (50–75%) and low/medium mortality to reach and maintain near-zero measles mortality Data not available Countries with high routine measles coverage (> 75%) and low mortality to eliminate indigenous transmission of measles virus Seven countries eliminated indigenous transmission of measles virus Maternal and neonatal tetanus At least 80% of countries to achieve neonatal tetanus incidence rate of less than 1 case per 1000 live births in every district 14 countries (33%) At least 80% of countries to attain a minimum of 80% TT2+ coverage among pregnant women in every district One country (2%) Yellow fever control in countries at risk Increase routine immunization coverage to at least 80% 4 of 33 countries (13%) At least 80% of districts to report at least one case of suspected yellow fever per year 1 of 33 countries (3%) Ability to conduct emergency response for all confirmed cases of yellow fever within 3 days of laboratory confirmation 0 of 33 countries Vitamin A supplementation in countries at risk 80% of countries at risk for vitamin A deficiency to integrate vitamin A supplementation with routine immunization services 12 of 44 countries (27%) Introduction of new vaccines All countries to include Hepatitis B vaccine into their national immunization programmes 28 countries (61%) All countries using Hepatitis B vaccine to achieve HepB-3 vaccine coverage equal to coverage for DTP-3 17 of 28 countries (60%) Half of all countries to include Haemophilus influenzae type b vaccine 10 (22%) countries implemented; 14 (33%) countries approved by the GAVI Alliance Introduction of injection technologies All countries to adopt auto-disable-syringes and/or equally safe injection technologies for all immunization injections 14 countries using auto-disable syringes exclusively; 18 countries using them for some immunizations Vaccine management policy and waste disposal All countries to adopt the multidose vial policy and vaccine vial monitors and to introduce monitoring methods 46 (100%) countries All countries to adopt and implement technologies and management systems for safe disposal and destruction of injection materials and other sharps Safe waste disposal remains suboptimal  Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in Africa L Arevshatian et al. Strategic goals Level of attainment by mid-2005a Disease surveillance To achieve certified levels of non-polio acute flaccid paralysis in all countriesb 15 countries invited to present certification papers To establish case-based surveillance of EPI diseases 26 countries (56%) To improve the quality of data on routine coverage using simple administrative and reliable assessment methods Improved Laboratory systems To establish and/or strengthen laboratory services within the EPI Disease Surveillance System National laboratories in 29 countries have expanded polio functions to cover other diseases DTP-3, diphtheria–tetanus–pertussis-3; EPI, Expanded Programme on Immunization; HepB-3, third dose of hepatitus B vaccine; TT2+, tetanus toxoid vaccine. a Data are for all 46 countries unless stated otherwise. b Global Polio Eradication Initiative standards state that individual countries cannot be certified as polio-free, only regions. (Table 1, cont.) Table 2. Diphtheria–tetanus–pertussis-3 (DTP-3) coverage in the African Region, 2000–2004 Measurement Year 2000 2002 2004 % regional DTP-3 coverage 54% 55% 69% N (%) countries achieving national DTP-3 coverage of 80% or higher 11 (24%) of 46 16 (37%) of 46 22 (48%) of 46 N (%) countries that reported DTP-3 coverage of 80% or higher in all districts. NA 2 (4%) of 46 5 (11%) of 46 N (%) countries in which 50% or more of all districts achieved at least 80% DTP-3 coverage NA 12 (26%) of 46 22 (48%) of 46 Estimated number of non-immunized childrena NA 1.4 million 0.9 million NA, data not available. a Children aged < 1 year who were not immunized with DTP-3. Source: WHO/AFRO information database 2005. Table 3. Immunization coverage in the five epidemiological blocks of the African Region African Region Immunization coverage “ig Four” countries Each country faced a different set of obstacles to improving and sustaining routine immunization coverage. Angola, Democratic Republic of Congo and Ethiopia made good progress in improving routine immunization coverage. Nigeria started and ended the period with diphtheria–tetanus–pertussis-3 (DTP-3) coverage of approximately 38%. During the 2001 to 2003 time-period, DTP-3 coverage was between 25% and 26% in Nigeria. Central block Between 2000 and 2004 coverage of DTP-3 increased by an average of 21% (from 40% to 61%). However, DTP-3 rates remained the same in most central-block countries in 2004. In Gabon, the government failed to purchase vaccines in 2004 and subsequently DTP-3 coverage decreased by 26% (from 63% in 2003 to 37%). Weak health systems and a lack of basic infrastructure were obstacles to improving immunization coverage. As a result, despite the improvements, only three of seven countries had achieved DTP-3 coverage of 50% or more by the end of 2004. Eastern block An increase in coverage of 26% was noted across all countries in this block (from 63% to 89%), and four of six countries achieved DTP-3 coverage of 80% or more by the end of 2004. Eritrea reported the lowest DTP-3 coverage (68%) in 2004, and the United Republic of Tanzania reported the highest (95%). Western block Three of the 16 countries had civil unrest, making the delivery of routine immunization services difficult in certain areas. Six countries achieved DTP-3 coverage of 80% or more in 2004. Coverage varied dramatically across the countries in this block, ranging from 93% in the Gambia to 31% in Liberia. Countries showing the greatest improvements in coverage were Burkina Faso, Guinea Bissau, Mali, Mauritania, Niger, Senegal and Sierra Leone. All of these countries achieved increases in coverage of more than 30% between 2000 and 2004. Southern block Performance by the countries in this block was relatively high in 2001 (75%). All but two countries showed improvements in their DTP-3 coverage. Madagascar, the country with the lowest DTP-3 coverage in the block at the start of the period (40%), reported 87% coverage by 2003. Unfortunately, coverage fell to 75% in 2004. CBulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in AfricaL Arevshatian et al. Table 4. Selected polio eradication indicators Key indicators Year 2000 2001 2002 2003 2004 2005a Number of regional cases of acute flaccid paralysis associated with wild polio virus 1863 68 208 443 944 408 Number of countries reporting wild polio virus 11 6 3 10 12 7 Number of polio-endemic countries in the African Region 11 4 2 2 7b 7b Number of countries with no cases of acute flaccid paralysis associated with wild polio virus 35 40 43 36 34 39 Number of countries with no polio cases in the past 3 years 28 33 37 31 31 30 Number of countries achieving certification-level surveillance indicators for acute flaccid paralysis 5 19 25 31 34 35 Number of countries with an established national Task Force for containment of wild polio virus 0 0 0 31 31 32 a Data as of 2 August 2005. b This number includes two endemic countries (Niger, Nigeria) plus five with re-established transmission (Burkina Faso, Central African Republic, Chad, Côte d’Ivoire and Mali). Source: WHO/African Region information database 2005. Table 5. Indicators for measles surveillance in the African Region, 2002–2004 Indicator Year 2002 2003 2004 Number of countries under case-based surveillance 15 24 26 Number of suspected measles cases reported 4836 21 199 17 100 % of reported cases in which specimens were collected 77% 72% 85% % of districts reporting at least one case with a blood specimen 31% 54% 69% Number (%) of measles cases confirmed by laboratory and epidemiological linkage 1346 (28%) 3851 (18%) 2505 (15%) Annual rate (per 100 000 population) of suspected measles cases reported with blood specimen 1.8 4.9 3.6 Annual rate (per 100 000 population) of confirmed laboratory and epidemic linkage measles cases 0.64 1.2 0.63 Source: WHO/African Region information database 2005. D Bulletin of the World Health Organization | June 2007, 85 (6) Research Infant immunization in Africa L Arevshatian et al. Table 6. Vaccination coverage for the third dose of hepatitis  vaccine (HV-3) by country, 2000–2004 Country Coverage (%) by year 2000 2001 2002 2003 2004 Algeria NA NA NA NA 81 Benin NA NA 15 15 97 Botswana 73 64 46 46 79 Burundi a NA NA NA NA 83 Cape Verde NA NA NA 48 68 Comorosa NA NA NA NA 77 Côte d’Ivoirea NA 10 48 40 50 Eritreaa NA NA 61 61 68 Gambia 89 84 40 83 90 Ghanaa NA NA 83 80 80 Guinea NA NA 100 NA NA Kenya NA NA NA 65 65 Lesotho NA NA NA NA 51 Madagascara NA NA 62 62 74 Malawi a NA NA 64 64 89 Mali a NA NA NA NA 73 Mauritiusa 88 93 88 88 90 Mozambiquea NA NA 84 84 91 Nigeria NA NA NA NA 8 Rwandaa NA NA 88 88 89 Sao Tomea NA NA NA NA 117 Senegal NA NA NA NA 54 Seychellesa NA 89 100 100 100 South Africaa 78 80 77 93 92 Swaziland NA 78 63 63 78 United Republic of Tanzaniaa NA NA 89 95 95 Ugandaa NA NA 42 42 87 Zimbabwe a 77 36 55 55 85 NA, data not available. a Countries that reached HBV-3 coverage equal to that of DTP-3. Source: WHO/African Region information database 2005. Table 7. Hib vaccine percentage coverage among reporting African Region countriesa Country Coverage (%) Burundi 83 Gambia 93 Ghana 80 Kenya 65 Madagascar 50 Malawi 89 Rwanda 89 South Africa 93 Uganda 87 Zambia 94 a Data collected up to December 2004. Source: WHO/African Region information database 2005.