Evaluation of two years of mass chemotherapy against ascariasis in Hamadan, Islamic Republic of Iran.

Evaluation of two years ofmass chemotherapy against ascariasis in Hamadan, Islamic Republic of Iran Mohammad Fallah,1 Akbar Mirarab,2 Farzad Jamalian,3 & Ahmad Ghaderi3 Objective To evaluate the mass treatment of ascariasis in rural areas of Hamadan Province, Islamic Republic of Iran. Methods A control programme in rural areas of Hamadan Province, which began in November 1997, involved giving all persons a single dose of 400 mg albendazole at intervals of three months. The efficacy of the treatment was evaluated by the formalin–ether concentration technique for stool examination and by the Stoll quantitative method. Findings The average rate of infection with Ascaris before treatment was 53.3%, ranging from 40% in Hamadan district to 75% in Toysercan. Two areas, Malayer and Nahavand, were excluded from the programme because the infection rates were only 13% and 4%, respectively. After two years of mass treatment the infection rate had decreased to 6%. The proportion of positive cases excreting only unfertilized eggs increased to 32%. No side-effects of mass treatment were observed. Conclusion Systematic mass treatment giving high coverage proved to be very effective in the control of ascariasis, notwithstanding a lack of other preventive measures. Keywords Ascariasis/drug therapy; Albendazole/therapeutic use; Ascaris lumbricoides/pathogenicity; Trichuris/pathogenicity; Giardia lamblia/pathogenicity; Hymenolepis/pathogenicity; Treatment outcome; Iran (source: MeSH, NLM ). Mots cle´s Ascaridiase larvaire/chimiothe´rapie; Albendazole/usage the´rapeutique; Ascaris lumbricoı¨des/pathoge´nicite´; Trichuris/ pathoge´nicite´; Giardia lamblia/pathoge´nicite´; Hymenolepis/pathoge´nicite´; Evaluation re´sultats traitement; Iran (source: MeSH, INSERM ). Palabras clave Ascariasis/quimioterapia; Albendazol/uso terape´utico; Ascaris lumbricoides/patogenicidad; Trichuris/patogenicidad; Giardia lamblia/patogenicidad; Hymenolepis/patogenicidad; Resultado del tratamiento; Ira´n (fuente: DeCS, BIREME ). Bulletin of the World Health Organization 2002;80:399-402. Voir page 401 le re´sume´ en franc¸ais. En la pa´gina 401 figura un resumen en espan˜ol. Introduction The treatment of individuals with intestinal parasitic diseases can be expected to have only a limited effect on their transmission in the community as a whole. Consequently, community-oriented projects have an essential role in the prevention and control of such diseases (1). Ascaris lumbricoides infection reflects socioeconomic status, environmental sanitary practices, health awareness and health education (2). Mass treatment againstAscaris spp. in developing countries, particularly those where ascariasis is highly endemic, has been reported to be highly effective in controlling this soil-transmitted helminth (2). This is especially true in communities where other interventions, e.g. health education, the improvement of environmental sanitation, and the provision of clean water and nutritional supplements, are not immediately feasible (3). In addition to certain sociological factors, parasitological factors have a great impact on such control. In tropical regions the rate of reinfection with Ascaris spp. after mass treatment is often remarkably high (4). The efficacy of control is clearly influenced by the drug used, its dosage rate, the intervals between successive doses, and the number of times the dose is repeated. The suggestion has been made that infections of soil-borne helminthic parasites might be controlled by intensively repeating the administration of highly effective drugs (5, 6). A. lumbricoides is the commonest intestinal parasite in Hamadan Province, Islamic Republic of Iran (7, 8). Its prevalence ranges from 40.4% in Hamadan district to 75.6% in the Toysercan area (9). A review of 56 cases of surgical complications caused by Ascaris infection indicated an incidence of nearly 3 cases per 1000 children under 10 years of age (Motahhari N., unpublished thesis, School of Medicine, Hamadan University of Medical Sciences, Hama- dan, Islamic Republic of Iran).A. lumbricoides eggs were found in 79% of 259 samples of soil (100 g each) collected in 12 consecutive months from 19 public parks (M. Fallah, unpublished data, 1998). Children who spontaneously eliminate worms by vomiting are not rare, even among inhabitants of urban areas. Cold conditions prevail in Hamadan Province in winter, the minimum temperature being –28 oC and the mean 9 oC. Farming is the principal occupation, and until recently most farmers used night soil as fertilizer because of its ready availability. Untreated sewage flowed into the rivers or was widely used in vegetable gardens. Such conditions provide a favourable environment for the development ofA. lumbricoides infection. 1 Associate Professor, Department of Parasitology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Islamic Republic of Iran (email: keshawarz@yahoo.com). Correspondence should be addressed to this author. 2 Assistant Professor, Provincial Public Health Centre, Hamadan University of Medical Sciences, Hamadan, Islamic Republic of Iran. 3 Public Health Officer, Provincial Public Health Centre, Hamadan University of Medical Sciences, Hamadan, Islamic Republic of Iran. Ref. No. 00-0883 399Bulletin of the World Health Organization 2002, 80 (5) # World Health Organization 2002 Materials and methods The formalin–ether sedimentation method was used for pretreatment stool examinations of 10 750 individuals in order to determine the initial prevalence; the modified Stoll technique was employed for baseline egg counting (10). After the stool survey a mass chemotherapy programme was conducted in all rural areas of the province except for the towns of Malayer and Nahavand, where the infection rates were only 13% and 4%, respectively. A single dose of 400 mg albendazole was given to every person except children under 2 years of age and pregnant women. These groups were excluded in order to avoid possible side-effects (11, 12). The first treatment was given in November 1997 and further treatments were given at intervals of three months for two years. The programme was evaluated in December 1999, by which time eight treatments had been administered. Results The overall prevalence of intestinal helminths in the target localities before treatment was 56.5%, with the principal helminth parasites beingA. lumbricoides (53.3%), Trichuris trichiura (4.5 %), andHymenolepsis nana (2.2%) (see Table 1 and Table 2). The age group 2–5 years had a lower infection rate than other age groups. After two years the overall prevalence of ascariasis had fallen from 53.3% to 6%. The proportion of all positive individuals excreting only unfertilized A. lumbricoides eggs reached about 32%. A steep decline occurred in all rural areas, including the centre of the province (Table 3). Coverage ranged from 93% to 97% in different villages. The meanA. lumbricoides egg count per g of faeces was 9361 (range, 450–60 300). The mean, mode and median egg counts in different localities are indicated in Table 4. Among the positive cases, 57.1% had egg counts below 10 000 per g, 23.8% had counts from 10 001 to 30 000 per g, and 19.1% had counts above 30 000 per g. No reduction in the prevalence of intestinal protozoan parasites such as Giardia lamblia or in that of H. nana was observed. Discussion Evaluation of programmes during their execution is essential in order to determine whether satisfactory progress is beingmade and whether any adjustments are required (13, 14). The existence of a source of A. lumbricoides is a significant factor leading to high incidence of infection in an area of endemicity. Poor personal hygiene and environmental sanitation, which can occur as a consequence of indiscriminate defecation by young children and the use of human excreta as fertilizer on farms and vegetable gardens, may result in infection (15). Periodic treatment for the control of intestinal parasitic infections is highly effective and inexpensive (16). Never- theless, it is desirable to make a careful study of the epidemiology of soil-transmitted helminths before under- taking large-scale control activities, especially with regard to periodic treatment schedules (17). The most effective approach has involved universal treatment at intervals of two months. However, excessively frequent drug administration should be avoided, while the high cost per individual and the very substantial manpower requirement for mass campaigns need to be taken into consideration. Ascariasis has been successfully controlled by treating at intervals of four or six months (12, 18, 19). We found that the prevalence of Ascaris spp. varied geographically in the study area: it was highest in the southern town of Toysercan and lowest, surprisingly, in the nearby towns of Malayer and Nahavand. In this region, especially in the Hamadan city area, people use all available open spaces for private vegetable gardens, and raw sewage is used for irrigation and sometimes as fertilizer. There is an efficient and comprehensive network of health centres in the rural areas of the Islamic Republic of Iran. Table 1. Pre- and post-treatment prevalence of major intestinal parasites in the rural areas of Hamadan Province, Islamic Republic of Iran % of samples positive Parasite Pre-treatment Post-treatment (n = 3098) (n = 2667) Ascaris lumbricoides 53.3 6 Trichuris trichiura 19.6 0.84 Hymenolepsis nana 2.23 1.84 Giardia lamblia 6.42 6.45 Table 2. Pre-treatment prevalence of major intestinal parasites in different localities of Hamadan Province, Islamic Republic of Iran Ascaris Trichuris Hymenolepsis Giardia lumbricoides trichiura nana lamblia Locality na % +ve % +ve % +ve % +ve Hamadan city 325 40.9 0.3 3.38 8 Asadabad 1161 46.5 0.17 3.45 8.8 Bahar 220 56.3 0 1.8 5.45 Kabootar Ahang 378 40.4 0 1.3 3.7 Razan 317 55.2 0 0.6 1.58 Toysercan 97 75.6 19.6 1 5.74 Total 3098 53.3 4.51 2.23 6.42 a No. of samples examined. Table 3. Post-treatment prevalence of major intestinal parasites in different localities of Hamadan Province, Islamic Republic of Iran Ascaris Trichuris Hymenolepsis Giardia lumbricoides trichiura nana lamblia Cities na % +ve % +ve % +ve % +ve Hamadan 345 8.7 0 1.7 5.5 Asadabad 1053 5.4 0 2 3.45 Bahar 165 8.48 0 2.42 2.42 Kabootar Ahang 254 4.7 0 1.57 5.9 Razan 257 2.72 0 1.17 3.9 Toyserkan 593 6.75 0.84 1.85 8.09 Total 2667 6 0.18 1.84 6.45 a No. of samples examined. 400 Bulletin of the World Health Organization 2002, 80 (5) Research This played a key role in the success of the programme, and district health officers were focal points for the community- oriented project. Requests for anthelmintics, especially mebendazole, the main such drug on the local market, diminished dramatically after the implementation of the mass treatment programme. Primary care workers have a basic role in ascariasis control because of their close links with communities. Their initiatives, educational work and efforts to improve commu- nity sanitation and hygiene contribute significantly to the effectiveness of control activities (20). In order to evaluate the improvement of public health in depth and the impact at community level it is necessary to conduct nutritional assessment in some target age groups. The interruption of mass treatment can be expected allow a rapid increase in egg- positive rates because of rapid reinfection with Ascaris spp. (5). It is considered that the present mass control pro- gramme should continue for at least three more years with six- monthly intervals between treatments and that further changes in the intensity of infection attributable to a decrease in the egg prevalence should be taken into account. It is worth noting that, although there were no significant reductions in Giardia spp. or H. nana, albendazole has been reported to be effective against these parasites (21–23). The present study indicated that systematic mass treatment provided effective control of ascariasis even in the absence of other preventive measures. n Acknowledgement We thank Dr Y. Pireh of the Ministry of Health and Medical Education of the Islamic Republic of Iran for constructive comments on the evaluation of the programme and for helping to design the study. Conflicts of interest: none declared. Re´sume´ Evaluation de deux anne´es de chimiothe´rapie de masse contre l’ascaridiase dans la province de Hamadan (Re´publique islamique d’Iran) Objectif Evaluer le traitement de masse de l’ascaridiase dans les zones rurales de la province de Hamadan (Re´publique islamique d’Iran). Me´thodes Un programme de lutte, commence´ en novembre 1997 dans les zones rurales de la province de Hamadan, consistait a` administrer a` chaque habitant une dose unique de 400 mg d’albendazole tous les 3 mois. L’efficacite´ du traitement a e´te´ e´value´e par examen des selles apre`s concentration (me´thode formol-e´ther) et par la me´thode quantitative de Stoll. Re´sultats Le taux moyen d’infection par Ascaris e´tait de 53,3 % avant traitement, avec des valeurs allant de 40 % dans le district de Hamadan a` 75 % a` Toysercan. Deux zones, Malayer et Nahavand, ont e´te´ exclues du programme en raison de leur faible taux d’infection (13 % et 4 % respectivement). Apre`s deux anne´es de traitement de masse, le taux d’infection est tombe´ a` 6 % et la proportion de cas positifs n’excre´tant que des œufs non fe´conde´s est passe´e a` 32 %. Aucun effet secondaire n’a e´te´ observe´. Conclusion Un traitement de masse syste´matique avec un fort taux de couverture s’est re´ve´le´ tre`s efficace pour lutter contre l’ascaridiase, malgre´ l’absence d’autres mesures pre´ventives. Resumen Evaluacio´n de dos an˜os de quimioterapiamasiva contra la ascariasis en Hamadan, Repu´blica Isla´mica del Ira´n Objetivo Evaluar el tratamiento masivo de la ascariasis en zonas rurales de la provincia de Hamadan, en la Repu´blica Isla´mica del Ira´n. Me´todos En noviembre de 1997 dio comienzo en zonas rurales de la mencionada provincia un programa de lucha en virtud del cual se administro´ a todas las personas una dosis u´nica de 400 mg de albendazol a intervalos de tres meses. La eficacia del tratamiento se evaluo´ empleando la te´cnica de concentracio´n con formalina-e´ter para examinar las heces y mediante el me´todo cuantitativo de Stoll. Resultados La tasa media de infeccio´n por Ascaris antes del tratamiento fue del 53,3%, entre el 40% del distrito de Hamadan y el 75% de Toysercan. Dos zonas — Malayer y Nahavand — quedaron excluidas del programa debido a que sus tasas de infeccio´n fueron so´lo del 13% y el 4%, respectivamente. Al cabo de dos an˜os de tratamiento masivo la tasa de infeccio´n habı´a disminuido al 6%. La proporcio´n de casos positivos que excretaban so´lo huevos no fecundados aumento´ al 32%. No se observaron efectos secundarios asociados al tratamiento masivo. Conclusio´n El tratamiento masivo sistema´tico con alta cobertura fue una alternativa muy eficaz para combatir la ascariasis, pese a la falta de otras medidas preventivas. Table 4. Post-treatment intensity of infection of Ascaris lumbricoides in different localities of Hamadan Province, Islamic Republic of Iran Eggs per g stool (epg) Location Mean Median Mode Hamadan city 18 493 15 800 35 850 Asadabad – – – Bahar 6459 4350 4400 Kabootar Ahang 19 877 16 600 16 200 Razan 7070 6900 6900 Toyserkan 8835 3025 1400 Total 9361 8550 2400 401Bulletin of the World Health Organization 2002, 80 (5) Mass chemotherapy against ascariasis in Hamadan, Islamic Republic of Iran References 1. Prevention and control of intestinal parasitic infections. Report of a WHO Expert Committee. Geneva: World Health Organization; 1987. WHO Technical Report Series, No. 749. 2. Intestinal protozoan and helminthic infections. Report of a WHO Scientific Group. Geneva: World Health Organization;1981. WHO Technical Report Series, No. 666. 3. Hayashi S. Standardization of the methods for evaluation of the effect of intestinal parasite control. In: Yokogawa M, Hayashi S, Kobayashi A, Kagei N, Suzuki N, Kunii C, editors. Collected papers on the soil-transmitted helminthiases, Vol. I. Tokyo: Asian Parasite Control Organization; 1981. p. 13-6. 4. Upatham ES, Viyanant V, Brockelman WY, Kurathong S, Ardsungnoen P, Chindaphol U. Predisposition to reinfection by intestinal helminths after chemotherapy in south Thailand. International Journal for Parasitology 1992;22:801-6. 5. Hall A, Anwar KS, Tompkins AM. Intensity of reinfection with Ascaris lumbricoides and its implications for parasite control. Lancet 1992;339: 1253-7. 6. Intestinal helminths. Weekly Epidemiological Record 1995;70(4):25-8. 7. Ahmadi NA. [Epidemiological study of intestinal parasites in the Asadabad area, Hamadan Province in the west of Iran] [dissertation].Teheran: School of Public Health, Teheran University of Medical Sciences; 1989 (in Persian). 8. Taherkhani H. [Epidemiological study of intestinal parasites in the suburb of Hamadan, west of Iran] [dissertation]. Teheran: School of Public Health, Teheran University of Medical Sciences; 1990 (in Persian). 9. [Epidemiological study of intestinal parasites in the rural areas of Iran: a countrywide study ]. Teheran: Ministry of Health and Medical Education;1992. Unpublished document (in Persian). 10. Garcia LS, Bruckner DA. Diagnostic medical parasitology. 3rd ed. Washington (DC): ASM Press; 1997. p. 661-3. 11. Albonico M, Smith PG, Hall A, Chwaya HM, Alawi KS, Savioli L. A randomized controlled trial comparing mebendazole and albendazole against Ascaris, Trichuris and hookworm infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 1994;88:585-9. 12. Seo BS, Lee SH, Chai J. An evaluation on the student-directed mass control program against ascariasis in Korea (1969–81). In: Yokogawa M, Hayashi S, Kobayashi A, Kagei N, Suzuki N, Kunii C, editors. Collected papers on the control of soil-transmitted helminthiases. Vol. 2. Tokyo: Asian Parasite Control Organization; 1981. 13. de Sliva R, Chan MS, Bundy DA. Morbidity and mortality due to ascariasis: re-estimation and sensitivity analysis of global numbers at risk. Tropical Medicine and International Health 1997;2:519-28. 14. Crompton DWT, Savioli L. Intestinal parasitic infections and urbanization. Bulletin of the World Health Organization 1993;71:1-7. 15. Savioli L. Personal communication. 16. Bundy DAP, Hall A, Medley GF, Savioli L. Evaluating measures to control intestinal parasitic infections. World Health Statistics Quarterly 1992;45: 168-79. 17. Booth M, Bundy DAP. Comparative prevalence of Ascaris lumbricoides, Trichuris trichiura and hookworm infections and the prospects for combined control. Parasitology 1992;105:151-7. 18. Crompton DWT. How much human helminthiasis is there in the world? Journal of Parasitology 1999;85:397-402. 19. Savioli L, Bundy DAP, Tomkins A. Intestinal parasitic infection: a soluble public health problem. Transactions of the Royal Society of Tropical Medicine and Hygiene 1992;86:353-4 20. Bundy DAP. This wormy world — then and now. Parasitology Today 1997; 13:407-8. 21. Reynoldson JA, Thompson RCA, Horton RJ. Albendazole as a future antigiardial agent. Parasitology Today 1992;8:412-3. 22. Pengsaa K, Sirivichayakul C, Pojjaroen-anant C, Nimnual S, Wisetsing P. Albendazole treatment for Giardia intestinalis infections in school children. South-East Asian Journal of Tropical Medicine and Public Health 1999; 30: 78-83. 23. Horton J. Albendazole: a review of anthelminthic efficacy and safety in humans. Parasitology 2000;121 (Suppl):S113-32. 402 Bulletin of the World Health Organization 2002, 80 (5) Research