Evolution of operational research studies and development of a national control strategy against intestinal helminths in Pemba Island, 1988-92.

Evolution of operational research studies and development of a national control strategy against intestinal helminths in Pemba Island, 1988-92 E. Renganathan,1 E. Ercole,2 M. Albonico,3 G. De Gregorio,2 K.S. Alawi,4 U.M. Kisumku,5 & L. Savioli3 Intestinal helminthic infections in Pemba Island, United Republic of Tanzania, have been perceived as a public health problem for many decades. School surveys in 1988 and 1992 and a community survey in 1991 were carried out to assess the distribution of prevalence and the intensity of these infections and to define the most effective strategy for control. The prevalence of helminthic infections exceeded 85% in all the surveys, and intensity was moderate. These studies identified the high-risk age groups, high transmission areas for different parasites, and the most cost-effective anthelminthic drug. This work is an example of how existing health systems and simple analytical tools may be used to generate useful data which, in turn, are used to define suitable intervention strategies. As a result, the Ministry of Health of Zanzibar has developed a national plan for the integrated control of intestinal helminths. This plan envisages periodic mass treatment of school-age children with mebendazole (500 mg, single dose, every four months) for the control of morbidity due to Ascaris, Trichuris, and hookworms. Introduction Infection with intestinal parasites is a widespread problem in the developing world (1, 2). The preva- lence and severity of infection is especially high in many developing countries where health and sanita- tion facilities are unable to cope with the needs of an increasing population (3). The main burden of these infections is borne by young children, with adverse effects on their physical and mental development which may be long-lasting (4-6). In Zanzibar, intestinal parasitoses are recognized as a major health problem.a A schistosomiasis con- trol programme was initiated in 1986, on the island I Scientific Consultant, Italian-Egyptian Cooperation Project, Medical Research Institute, Alexandria, Egypt. 2 Former Medical Officer, Helminth Control Programme, Pemba Island, United Republic of Tanzania. 3 Programme of Intestinal Parasitic Infections, Division of Com- municable Diseases, World Health Organization, 1211 Geneva 27, Switzerland. Requests for reprints should be sent to this address. 4 Public Health Officer, Helminth Control Programme, Pemba Island, United Republic of Tanzania. 5 Deputy Principal Secretary, Ministry of Health, Zanzibar, United Republic of Tanzania. a Zanzibar. Priority plan for health services 1991/2-1995/6. Min- istry of Health of Zanzibar, 1991. Reprint No. 5585 of Pemba, by the Ministry of Health of Zanzibar, with support from WHO, the Italian Ministry of For- eign Affairs, and the German Pharma Health Fund to deal with the high prevalence of infection with Schistosoma haematobium (7-13). As an extension to this programme, studies have been performed since 1988 to determine the extent of infection with soil-transmitted helminths such as hookworms, Ascaris and Trichuris, and to test the efficacy of low-cost anthelminthic drugs. In this paper we present the results and conclu- sions from operational research studies carried out between 1988 and 1992. This work has led to the initiation of a national plan of action for the control of helminths by the Ministry of Health of Zanzibar in 1992. Materials and methods The health administration of the island of Pemba is under the Ministry of Health of Zanzibar. Other rel- evant features of the island have been described elsewhere (7, 8). School surveys. Three school surveys were conduct- ed between 1988 and 1992. In the initial survey of 1988, about 10% of the total school population were studied. The study population (3436 children from all classes; age range, 4-20 years) was from eight Bulletin of the World Health Organization, 1995, 73 (2): 183-190 © World Health Organization 1995 183 E. Renganathan et al. schools selected randomly from various regions of the island. The second school survey was initiated in early 1992 to evaluate the impact of periodical anthelmin- thic chemotherapy on parasitological indicators (prevalence and intensity rates) and growth in schoolchildren. To this end, a random sample of about 1120 students (age range, 9-17 years) was selected from the standard 5 classes of 35 schools in the island. The latest survey was conducted in late 1992 on 3202 students (age range, 6-12 years) from 10 schools in the island. This was a pre-treatment sur- vey carried out within a drug-efficacy trial (albenda- zole 400 mg vs mebendazole 500 mg); all children testing positive were treated with either mebendazole or albendazole. Community survey. One community survey was per- formed in 1991. Faecal samples were collected from randomly sampled households of two towns (Wete and Chake Chake) and six villages (Makangale, Kiuyu, Shungi, Pujini, Ngwachani, Mzingani). A total of 2247 individuals in all age groups (age range, 1-85 years) were examined and subsequently treated with a single dose of mebendazole 500 mg (children aged <2 years received 250 mg). The geographical distribution of the schools, towns and villages studied, together with year of sur- vey, are shown in Fig. 1. Laboratory methods. Laboratory examination of stool samples were performed at the programme headquarters laboratory in Chake Chake. The Kato- Katz cellophane, thick-smear technique was used for faecal examination of helminth eggs following WHO recommendations, using a template delivering about 41.7 mg of faeces (14). A single microscopic stool examination was performed by trained health work- ers and quality control was maintained through re- examination of 10% of the slides by three supervis- ing medical officers (G.DG., E.R. and M.A.). Slides were examined within one hour of preparation to avoid over-clarification of hookworm eggs. Infec- tions were classified according to individual egg counts per gram of faeces (epg) as heavy, moderate, or light following WHO recommendations (15). Statistical analysis. Data from surveys were enter- ed into a microcomputer using the Epilnfo data- base package and the same programme was used to analyse the results from each survey. Data were ana- lysed both at local level and at WHO headquarters, Geneva. Intensity of infection was expressed as the geometric mean of egg counts, estimated as exp [(X log(c+l))/n]-1, where c is the count (epg) for each individual. Intensity is reported as the geo- Fig. 1. Geographical distribution of school and commu- nity surveys for intestinal heiminths in Pemba island, 1988-92. metric mean on the whole study population (positive and negative subjects) as described above. Preval- ences and intensities were compared with X2 tests and with Student's t-tests, respectively. Results In the first school survey (1988) Trichuris trichiura was the most common intestinal helminth, with an overall mean prevalence of 78.8% (the highest (96.7%) was recorded in Makombeni and the lowest (66.1%) in Kojani) and a geometric mean epg of 257. The overall prevalence of Ascaris was 58.7% (ranging from 93.5% in Makombeni to 28.9% in Kojani), and the mean for hookworms was 58.9% (from 92.2% in Makombeni to 10.9% in Chake nur- WHO Bulletin OMS. Vol 73 1995184 Studies to control intestinal helminths in Pemba sery). The geometric mean epg was 136 for Ascaris and 74 for hookworm infection. Summary results from this study are presented in Table 1. In the community survey in August 1991, 2247 individuals of all age groups from two towns (1109) and six villages (1138) were examined. Overall, 86.7% of the samples tested positive for helminth eggs (town population, 87.6%; villagers, 86.2%) (Table 2). As in the previous study, T. trichiura was the most prevalent infection at 76.0% (78.1% in towns and 74.4% in villages). The next most com- mon infection was with hookworms; 60.8% of stools examined were positive for hookworm eggs (urban sample, 53.0%; rural sample, 68.0%). Interestingly there was a marked focality in the distribution of infections with this parasite. Ascaris infection was present in 48.2% of individuals examined (preva- lence in the towns, 50.2%; villages, 46.7%). Fig. 2 shows prevalence and intensity of infection in rela- tion to age. The age/intensity relationship is quite typical, showing that the main burden of the infec- tion with Ascaris and Trichuris is borne by the school age group. The community survey was followed, in early 1992, by a second school study. Data from 1120 children from the standard 5 classes of 35 schools showed that 1117 (99.7%) were infected with either one of the three helminths studied. Mean prevalence rates were 88.7% for Trichuris, 84.8% for hook- worms, and 71.2% for Ascaris with mean epg values of 482, 463 and 218, respectively. Subsequently, almost all students (99.9%) tested in the late 1992 school survey were infected with at least one parasite and overall prevalence rates of 97.4% for Trichuris, 90.4% for hookworms and 68.3% for Ascaris were recorded. Geometric mean epg values were 678, 427 and 203 for Trichuris, hookworm and Ascaris infections, respectively (Table 3). In this third survey a drug-efficacy trial was also conducted, the details of which are reported elsewhere (16). Discussion The high prevalence of intestinal helminths in many parts of East Africa is well documented (17-19). In Pemba, for example, an earlier study has suggested a high prevalence rate of helminth infections in a cohort representing 0.2% of the population, although this was only a qualitative study (20). In addition, in the island which is endemic for S. haematobium, a regular testing and treatment campaign has been suc- cessfully conducted in schools since 1986. These campaigns involved testing for haematuria using reagent strips and selective treatment of positive individuals with a single dose of praziquantel (40 mg/ kg body weight) (7-13). This existing structure Table 1: School survey, Pemba, 1988 (age range, 4-20 years) Ascaris Trichuris Hookworms Total No. Prevalence Intensitya Prevalence Intensitya Prevalence lntensitya prevalenceb School examined (%) (epg) (%) (epg) (%) (epg) (%) Uondwe 603 60.0 139 85.2 478 27.1 6 94.7 Chake (nursery) 101 47.5 40 68.3 132 10.9 1 80.2 Kojani 180 28.9 6 66.1 63 35.0 8 81.1 Pujini 296 66.8 213 72.6 234 74.7 379 99.3 Makombeni 153 93.5 5 652 96.7 1 700 92.2 1071 100.0 Shumba 543 31.3 9 72.6 84 71.3 126 89.8 Michakaini (Chake) 719 60.2 134 79.1 308 51.5 40 96.1 Kiwani 841 72.7 672 81.0 308 79.4 382 97.6 Total 3 436 58.7 136 78.8 257 58.9 74 94.4 Classification:c Heavy 5.7% 6.2% 7.3% Moderate 19.6% 36.1% 7.9% Light 33.4% 36.6% 43.7% a The intensities (geometric means of epg) shown are for all the subjects examined. b Children with at least one of the parasites. c In Tables 1 to 3, heavy, moderate and light infections were classified as follows: Heavy Ascaris .50 000 epg Heavy Trichuris .10 000 epg\ Heavy hookworms 2 10 000 epg Moderate Ascaris 5 000-49 999 epg Moderate Trichuris 1 000-9 999 epg Moderate hookworms 3 000-9 999 epg Light Ascaris 1-4 999 epg Light Trichuris 1-999 epg Light hookworms 1-2 999 epg WHO Bulletin OMS. Vol 73 1995 185 E. Renganathan et al. Table 2: Community survey, Pemba, 1991 (age range, 1-85 years) Ascaris Trichuris Hookworms Total No. Prevalence Intensitya Prevalence Intensitya Prevalence Intensitya prevalenceb Area examined (%) (epg) (%) (epg) (%) (epg) (%) Town Chake Chake 614 55.9 53 76.5 94 41.0 11 86.6 Wete 495 43.3 23 80.0 162 67.9 87 88.7 Subtotal 1 109 50.2 37 78.1 119 53.0 29 87.6 Village Makangale 215 52.8 36 68.4 87 78.1 229 92.1 Kiuyu 197 36.0 13 69.0 73 70.6 108 78.2 Shungi 290 50.7 38 69.4 69 46.6 18 81.9 Pujini 152 45.4 36 89.5 278 80.3 224 93.4 Ngwachani 152 52.0 55 80.3 182 72.2 123 86.8 Mzingani 132 39.4 31 80.3 220 76.5 214 87.9 Subtotal 1 138 46.7 31 74.4 115 68.0 97 86.2 Total 2 247 48.2 33 76.0 115 60.8 54 86.7 Classification:c Heavy 0.0% 0.4% 0.4% Moderate 6.6% 20.0% 5.5% Light 41.6% 55.6% 54.8% a The intensities (geometric means of epg) shown are for all the subjects examined. b Children with at least one of the parasites. c For classification, see footnote c in Table 1. provided a good base for studying the situation with intestinal helminths in the island between 1988 and 1992. All activities in the schools were performed in collaboration with the health team from the nearest primary health care unit (dispensary), with the full involvement of school teachers and community leaders. This was an opportunity to strengthen the existing health care system and to promote a more comprehensive and integrated approach. The results of this research has led to the evolution of the con- trol strategy discussed below. In the initial survey of 1988, a very high cumu- lative prevalence of helminthic infections was found (94.4%, representing the number infected with any one parasite), thus confirming earlier reports (20) and our suspicion that intestinal helminths were indeed a major public health problem among school- children in Pemba. In particular, the school at Makombeni had the highest prevalence and intensity values recorded in this study. This may be explained by the high population density and lack of sanitation, resulting in heavy faecal contamination of the envi- ronment. In contrast, the lower rates seen in the island of Kojani are probably due to the local habit of defecating on the shores during low tide. Our second survey in 1991 was planned to clari- fy two important issues for the implementation of future control strategies. There was a need to obtain good epidemiological data related to the community, representing all age groups and preferably incorpo- rating communities from different parts of the island, and to identify an effective, safe and cheap single- dose anthelminthic that could be included in the con- trol programme. To this end, 446 individuals in the population that received therapy with 500 mg mebendazole were followed up, one and four months after treatment. The results showed that this single- dose regimen was effective, leading to both good cure rates (especially in Ascaris infection) and a marked decrease in intensity of infection with all three parasites (21). Although marked differences (P <0.001) were found in the distribution of the three nematodes by place (villages or towns), no signifi- cant variation was noticed between urban and rural areas. This latest finding, confirmed by a subsequent study (22), suggests that the same interval between treatments for control of morbidity might be adopted for children in urban and rural schools. The third survey in late 1992 was planned as an extension of the previous one, being a drug-efficacy trial comparing the single-dose regimens of 500 mg mebendazole and 400 mg albendazole. The outcome of the drug efficacy study is reported elsewhere (16), with the results showing that generic mebendazole was as effective as albendazole against Ascaris and slightly more effective against Trichuris. Against WHO Bulletin OMS. Vol 73 1995186 Studies to control intestinal helminths In Pemba Fig. 2. Distribution of prevalence and intensity of hel- minthic infections, by age, In the community survey, Pemba, 1991. Intensity is reported as the geometric mean of the whole population group (positive and negative sub- jects). 100 80 --_ a)0- - +---* 3W- ~~@X* 20 *Ascaris - +-Trichuris Hookworm ol 0-4 5-9 10-14 15-19 20-24 25-44 2!45 Age group (years) 100 - *-o Ascaris -+-Trichuris +Hookworm a 80 / 1 /60 40 . 20 0 0-4 5-9 10-14 15-19 20-24 25-44 .45 Age group (years) hookworm, generic mebendazole had lower cure rates than albendazole, but it decreased the intensity of infection by more than 80%. This finding has major implications for sustaining the large-scale con- trol programme in Zanzibar, because generic meben- dazole can be obtained at about US$ 0.02 per dose. During this series of research studies, there were continuing discussions and constant reassessment of our strategy by a joint working group made up of responsible staff from the Zanzibar Ministry of Health and Ministry of Education and WHO staff. As a result, we believe that we have achieved our initial objectives to determine disease prevalence, intensity, and distribution as accurately as possible and to define appropriate intervention. The most important achievement has been the definition of control strategies included in the Zanzi- bar Ministry of Health's National Action Plan for Control of Helminths. This plan envisages an inte- grated approach for the control of both schistosomia- sis and soil-transmitted helminths based on WHO recommendations (23).b For schistosomiasis the objective is to maintain the low levels of morbidity already reached on the island through selective popu- lation chemotherapy with the aid of reagent strips for haematuria and treatment with praziquantel targeted at schoolchildren (23). Owing to the significant reduction in morbidity achieved by the original six months retreatment schedules, schoolchildren are now retreated at one-year intervals. For the soil- transmitted helminths the specific target is to obtain, within two years, a reduction in intensity of infection of 60% for Ascaris, 30% for hookworms, and 20% for Trichuris in schoolchildren. To achieve this out- come, periodical mass treatment of schoolchildren with a single dose of mebendazole 500 mg was adopted as the most cost-effective strategy for the control of morbidity, as recommended by WHO for endemic areas.b It was agreed to treat the children every four months because of the very high reinfec- tion rate (21). Although repeated mass chemotherapy on a target group might have an impact in reducing the contamination of the environment, the control of transmission of helminthic infection cannot be achieved and sustained without intensive health edu- cation, particularly of children, through the school system together with promotion of environmental health through community involvement in building, maintaining and using latrines. WHO's Rural Envi- ronmental Health Unit is planning to undertake oper- ational research in Pemba within the helminth con- trol programme to promote affordable and acceptable sanitation in schools. The evaluation of the programme impact on morbidity due to intestinal helminths will be moni- tored once a year in samples of the standard 5 class- es. A specific evaluation of the impact of the school- based deworming programme on nutritional status, by measuring micronutrients and through anthropo- metric indices in the school-aged population, has been implemented in early 1994.c b Health of schoolchildren: treatment of intestinal helminths and schistosomiasis. Unpublished document WHO/CDS/IPI/CTD/ 92.1, 1992. c Stoltzfus RJ et al. Evaluation of the nutritional impact of a school-based deworming program in Zanzibar. Unpublished, 1994. WHO Bulletin OMS. Vol 73 1995 187 E. Renganathan et al. Table 3: School survey, Pemba, 1992 (age range, 6-12 years) Ascaris Trichuris Hookworms Total No. Prevalence Intensitya Prevalence Intensitya Prevalence Intensitya prevalenceb School examined (%) (epg) (%) (epg) (%) (epg) (%) Wingwi 106 50.0 37 96.2 433 99.1 1 223 100.0 Mchambandogo 345 72.5 249 97.4 577 95.1 624 100.0 Minungwini 201 76.1 445 96.0 594 97.0 646 99.5 Ole 566 56.9 59 95.4 424 94.0 515 100.0 Ziwani 417 70.7 207 97.8 637 89.9 346 99.8 Wawi 697 78.3 433 99.0 978 93.1 569 100.0 Pujini 91 58.2 114 98.9 764 51.6 24 100.0 Ngwachani 194 67.0 395 99.0 1 222 82.0 275 99.5 Kiwani 299 64.5 243 98.0 837 82.3 225 100.0 Kengeja 286 66.8 201 96.2 644 90.9 432 99.3 Total 3 202 68.3 203 97.4 678 90.4 427 99.9 Classification:c Heavy 1.0% 0.7% 0.9% Moderate 22.5% 43.6% 10.4% Light 44.8% 53.1% 79.1% a The intensities (geometric means of epg) shown are for all the subjects examined. b Children with at least one of the parasites. c For classification, see footnote c in Table 1. The decision to concentrate our monitoring and intervention efforts on school-age children is based on generally accepted findings showing that these individuals harbour the most intense infections, a fact which is reconfirmed in our study, and that intervention in this group achieves the maximum return per treatment in terms of morbidity reduction (4).d More importantly, schoolchildren are among the most accessible groups for monitoring and treat- ment of both schistosomiasis and intestinal hel- minths.b Indeed, school health programmes including parasite control were identified in the World Bank's 1993 Report (2) as one of the most cost-effective of public health interventions, and were included in a short list of five global public health priorities. Simi- lar considerations led WHO and UNDP, in collabo- ration with the Rockefeller and Edna McConnel Clark Foundations, to initiate the Partnership for Child Development programme in 1992. This inter- national programme seeks to evaluate the use of school-based services, including anthelminthic deliv- ery, as a means of improving the health and the edu- cation of school-age children. d Informal consultation on intestinal helminths infections. Unpub- lished document WHO/CDS/IPI/90.1, 1990. Another population group at high risk for helminth-associated morbidity are women of child- bearing age who are particularly prone to iron- deficiency anaemia associated with hookworm infec- tion. The govemment of Zanzibar, in collaboration with WHO, is currently planning further studies on the impact of helminth control on matemal and child health. In conclusion, the work described in this paper is an example of how existing health systems and simple analytical tools may be used to generate use- ful data which, in tum, are used to define suitable intervention strategies. Although planning, manage- ment and programme operation will be different from one country to another, most health care struc- tures are capable of introducing and sustaining the very simple technology involved.e e See footnote b on p. 187. Acknowledgements We thank the dedicated staff of the Helminth Control Team, the teachers, and the population of Pemba Island whose enthusiastic collaboration and participation made this study possible. We are also grateful to Dr A. Gabrielli, Dr L. Di Matteo and the late Professor 1. de Carneri for 188 WHO Bulletin OMS. Vol 73 1995 Studies to control intestinal helminths in Pemba their contribution in training the local health staff; Dr K.E. Mott, Dr A. Davis, Dr D. Cioli and Dr H. Nieve for their encouragement and support; Dr D.A.P. Bundy for his most useful comments and Professor P.G. Smith and Mr H. Dixon for their advice on data entry and analysis. Special thanks to SmithKline Beecham Pharmaceuticals Ltd, Jans- sen Pharmaceutica Ltd and Pharmamed Ltd for the gener- ous gift of anthelminthics used in the surveys. This study was initiated and financially supported by WHO (Division of Communicable Diseases and Division of Control of Tropical Diseases), the German Pharma Health Fund, and the Direzione Generale per la Cooperazione allo Sviluppo in the Italian Ministry of Foreign Affairs. Resume Evolution des travaux de recherche op6rationnelle et 6laboration d'une strat6gie nationale de lutte contre les helminthes intestinaux dans l'lIe de Pemba, 1988-1992 Dans I'lle de Pemba, en R6publique-Unie de Tan- zanie, les helminthiases intestinales sont depuis longtemps reconnues comme probleme de sante publique. Des enquetes ont ete r6alis6es, dans les 6coles en 1988 et 1992 et dans 1'ensemble de la communaut6 en 1991, pour 6valuer la distri- bution de la pr6valence et de l'intensit6 de ces infestations et definir la strat6gie de lutte la plus efficace. La pr6valence des infestations 6tait sup6rieu- re a 85% dans toutes les enquetes, avec une intensit6 mod6r6e. Ces enquetes ont permis d'identifier les groupes d'age a haut risque, les zones de forte transmission pour les diff6rents parasites, et l'anthelminthique ayant le meilleur rapport cout-efficacit6. Ce travail illustre la fa9on dont les systemes de sant6 existants et des outils analytiques simples peuvent etre employes pour fournir des donnees utiles, qui a leur tour serviront a definir des strat6gies d'intervention appropriees. A la suite de cette etude, le Ministere de la Sant6 de Zanzibar a 6labore un plan national de lutte int6gr6e contre les helminthes intestinaux. Ce plan pr6voit le traitement periodique de 1'ensemble des enfants d'age scolaire par le m6bendazole (500 mg en prise unique une fois tous les 4 mois), afin de combattre la morbidite due a Ascaris, a Trichuris et aux ankylostomes. References 1. Global health situation and projection estimates. Geneva, World Health Organization, 1992: 46-47. 2. World Bank. Appendix B. The global burden of dis- ease. In: World development report 1993. New York, Oxford University Press, 1993: 222. 3. Crompton DWT, Savioli L. Intestinal parasitic infections and urbanization. Bulletin of the World Health Organization, 1993, 71: 1-7. 4. Savioli L et al. Intestinal parasitic infections: a solu- ble public health problem. Transactions of the Royal Society of Tropical Medicine and Hygiene, 1992, 86: 353-354. 5. Nokes C et al. Parasitic helminth infection and cog- nitive function in school children. Proceedings of the Royal Society of London, 1992, 247: 77-81. 6. Stephenson LS et al. 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Parassitologia, 1987, 29: 27-35 (in Italian). 21. Albonico M et al. Efficacy of a single dose of mebendazole on prevalence and intensity of soil- transmitted nematodes in Zanzibar. Tropical and geographical medicine, 1994, 46: 142-146. 22. Albonico M et al. Intestinal parasitic infections in urban and rural children on Pemba Island: implica- tions for control. Annals of tropical medicine and parasitology, 1993, 87: 579-583. 23. The control of schistosomiasis. Second report of a WHO Expert Committee. Geneva, World Health Organization, 1993 (WHO Technical Report Series, No. 830): 67. 190 WHO Bulletin OMS. Vol 73 1995