In recent years there have been major socio-economic changes within Afghanistan such that the present public health burden of soil-transmitted helminths (STH), especially that within school-aged children, remains to be determined. A baseline parasitological survey was therefore carried out in four defined areas of Afghanistan to better assess the distribution, prevalence and intensity of STH infections prior to a nationwide de-worming campaign beginning within World Food Programme assisted schools. A cross-sectional examination of 1001 children aged between 8 and 15 years old revealed that approximately half (47.2%) were infected with at least one STH. Infections with Ascaris lumbricoides were most widespread (40.9%) and elevated prevalences were detected in urban environments; for example, schoolchildren in Kabul were more likely to be infected (OR=2.2, 95% CI 1.6-3.0) than elsewhere and these infections were often of higher intensity (OR=7.6, 95% CI 4.9-11.8). Trichuris trichiura (9.9%) and hookworms (0.7%), previously unknown from Afghanistan, were encountered. The blood haemoglobin concentration of surveyed children was also assessed: 4% resulted to be anaemic (Hb<11 g dl−1), and 0.4% to be severely anaemic (Hb<7 g dl−1

Bojang, B.

Connolly, M.

Gabrielli, A.F.

Khoshal, M.H.

Montresor, A.

Naumann, C.

Ramsan, M.

Savioli, L.

Stothard, J.R.

Tsogzolmaa, D.

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Research NoteSoil-transmitted helminths andhaemoglobin status among Afghan childrenin World Food Programme assisted schoolsA.F. Gabrielli1*, M. Ramsan2, C. Naumann3, D. Tsogzolmaa4,B. Bojang3, M.H. Khoshal5, M. Connolly1, J.R. Stothard6,A. Montresor7 and L. Savioli71Programme for Communicable Diseases in Complex Emergencies, WorldHealth Organization (WHO), 1211 Geneva, Switzerland: 2Public HealthLaboratory ‘Ivo de Carneri’, Pemba Island, Zanzibar, Tanzania: 3WorldFood Programme Country Office, Kabul, Afghanistan: 4Office of the WHORepresentative, Kabul, Afghanistan: 5Ministry of Health, Kabul,Afghanistan: 6The Natural History Museum, London SW7 5BD, UK:7Strategy Development and Monitoring for Parasitic Diseases and VectorControl, WHO, 1211 Geneva, SwitzerlandAbstractIn recent years there have been major socio-economic changes withinAfghanistan such that the present public health burden of soil-transmittedhelminths (STH), especially that within school-aged children, remains to bedetermined. A baseline parasitological survey was therefore carried out in fourdefined areas of Afghanistan to better assess the distribution, prevalence andintensity of STH infections prior to a nationwide de-worming campaignbeginning within World Food Programme assisted schools. A cross-sectionalexamination of 1001 children aged between 8 and 15 years old revealed thatapproximately half (47.2%) were infected with at least one STH. Infections withAscaris lumbricoides were most widespread (40.9%) and elevated prevalenceswere detected in urban environments; for example, schoolchildren in Kabul weremore likely to be infected (OR ¼ 2.2, 95% CI 1.6–3.0) than elsewhere and theseinfections were often of higher intensity (OR ¼ 7.6, 95% CI 4.9–11.8). Trichuristrichiura (9.9%) and hookworms (0.7%), previously unknown from Afghanistan,were encountered. The blood haemoglobin concentration of surveyed childrenwas also assessed: 4% resulted to be anaemic (Hb , 11 g dl21), and 0.4% to beseverely anaemic (Hb , 7 g dl21).Soil-transmitted helminths (STH) continue to be amajor public health burden throughout many countriesof the world where both sanitation and hygiene arepoor and access to anthelmintics is limited (Savioli et al.2002). Soil-transmitted helminth infections cause aspectrum of pathologies (Awasthi et al., 2003) andtheir detrimental effects are often most keenly feltwithin school-aged children where anaemia, retardedgrowth and impairment of cognitive developmentoccur (Crompton, 1992, 1999; Oberhelman et al., 1998;Crompton & Nesheim, 2002). At the public healthlevel, regular administration of single-dose chemother-apy (albendazole 400 mg or mebendazole 500 mg) hasproven to be a cost-effective method of control (Savioli*Present address: Schistosomiasis Control Initiative, ImperialCollege, London, W2 1PG, UKFax: 020 7262 8140E-mail: a.gabrielli@imperial.ac.ukJournal of Helminthology (2005) 79, 381–384 DOI: 10.1079/JOH2005316https:/www.cambridge.org/core/terms. https://doi.org/10.1079/JOH2005316Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 08:15:13, subject to the Cambridge Core terms of use, available atet al., 2002; Urbani & Albonico, 2003) and remainsa foundation of control in conjunction with thedesirable improvements of sanitation and hygiene(WHO, 2002).After decades of civil disruption and recent conflict, thehealth sector status within The Islamic Republic ofAfghanistan is only now beginning to improve. The totalpopulation of this landlocked country is close to 29 millionwith only a minority having access to suitable sanitationand safe water. There are approximately 4 million peoplesurrounding the urbanized areas of Kabul (World FoodProgramme (WFP) estimates, July 2004). The presentstatus and public health burden of STH within school-children remains poorly known with previous literaturenow out of date, for example, conducted nearly 30 yearsago (Buck et al., 1978). At that time onlyAscaris lumbricoideswas reported and was then assumed to be widespread. Aspart of a school health initiative, an inter-sectorialcollaboration between the Afghan Ministries of Healthand Education, the WFP and World Health Organization(WHO), established a platform to implement a de-worming campaign in Afghanistan. Prior to this generalintervention we report on a parasitological survey atintervention baseline to estimate the distribution andextent of STHs in schools assisted by the WFP.The survey was carried out in February and March 2003in each of the four ecologically homogeneous areas (eco-zones) in which the country can be divided (fig. 1). Theeco-zones are: (i) urban: inclusive of the capital Kabul andthe main cities, namely, Herat, Kandahar, Mazar-e-Sharifand Ghazni; (ii) central highlands: covering the centralregion being an extension of the Himalayan mountainchain, and including the Hindu-Kush; (iii) north-westernplains: the major agricultural area extending along theAfghan north-western border from Iran in the west toTajikistan in the east; and (iv) south-western plateau:desert and semi-desert landscape covering the southernthird of the country, including the Rı¯gestan desert.In each of the four eco-zones, one province wasrandomly selected: Kabul (urban); Nangarhar (centralhighlands); Farah (north-western plains); Kandahar(south-western plateau) and for each one of the identifiedfour provinces, one district was randomly chosen amongthose officially declared accessible for United Nationsstaff. Five primary schools were randomly selected withineach district for a total of 20 schools across the four eco-zones. Approximately 50 children per school wererandomly selected and enrolled in the survey followingWHO guidelines (WHO, 2002). Parasitological examin-ation was performed on a single, thick Kato-Katz(41.7 mg) smear from the stool of each child and viewedmicroscopically at £ 100 magnification for helminth eggs(WHO, 1991). Informed consent was obtained, todetermine the prevalence of haemoglobin concentrationassessed upon examination of fingerprick blood using adigital haemoglobinometer (HemoCue AB, Angelholm,Sweden). Following the WHO ethical guidelines of ‘nosurvey without service’, all children enrolled in thesurvey received one tablet of albendazole 400 mg(anthelmintic drug).A total of 1001 children were enrolled in the survey(55.3% male sex): 239 in Kabul, 256 in Nangarhar, 249 inFarah and 257 in Kandahar. The age range of the childrenwas between 8 and 15 years, the bulk of the sampleconsisting of 9- to 12-year-olds. Prevalence and intensityof STH infections in each of the provinces included in thesurvey are shown in table 1. About half (47.2%) of theschoolchildren population under study were infectedwith at least one STH. Ascaris lumbricoides was the mostwidespread, affecting 40.9% of the population understudy, followed by Trichuris trichiura (9.9%). Hookworminfection was detected in Nangarhar province only, whereits prevalence of infection was low (2.7%). Neither of thelatter two infections was reported in the 1978 survey(Buck et al., 1978). 9.7% of the sample presented infectionwith moderate-to-heavy intensity, the major determinantof severity of morbidity (Awasthi et al., 2003). Among thesubjects with any moderate-to-heavy intensity infection,97% were infected with A. lumbricoides, while only 5%were infected with T. trichiura. No moderate-to-heavyintensity infection due to hookworms was recorded.Overall, Kabul province appears to possess the mostsevere STH burden, both in terms of prevalence andintensity of infection (cumulative prevalence of STHinfection ¼ 61.9%; cumulative prevalence of moderate-to-heavy intensity STH infection ¼ 26.4%). In the three otherprovinces, cumulative prevalence of STH infectionranged from 34.8% in Nangarhar to 42.8% in Kandaharto 50.2% in Farah, and cumulative prevalence ofmoderate-to-heavy intensity STH infection was wellbelow the 10% threshold (Nangarhar: 3.1%; Kandahar:3.1%; Farah: 7.2%). The overall prevalence of poly-parasitism (co-occurrence of more than one STH infectionin the same individual) was 4.3%. All poly-parasiticinfections were double infections due to A. lumbricoides–T. trichiura co-infection, except a single A. lumbricoides–hookworm co-infection. Only 0.2% of the samplepresented with moderate-to-heavy intensity poly-TurkmenistanTajikistanAfghanistanIranPakistan100 km1 243Kabul (urban)Central highlandsNorth-western plainsSouth-western plateauFig. 1. Schematic map of Afghanistan showing eco-zonessuveyed. Numbers refer to provinces where the survey wascarried out: (1) Kabul; (2) Nangarhar; (3) Farah and (4) Kandahar.382 A.F. Gabrielli et al.https:/www.cambridge.org/core/terms. https://doi.org/10.1079/JOH2005316Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 08:15:13, subject to the Cambridge Core terms of use, available atparasitic STH infections. In both cases they were due toA. lumbricoides and T. trichiura, in which onlyA. lumbricoides intensity was moderate-to-heavy.Only 40 children (4%) were found to be anaemic(haemoglobin concentration ,11 g dl21); of these fourchildren (0.4%) all boys, were severely anaemic(haemoglobin concentration ,7 g dl21). However, itshould be noted that an iron-fortified bread/biscuitdistribution system targeting schoolchildren was startedin Kabul and Kandahar provinces during 2002, and wasin place at the time of the survey. On the contrary, noiron supplementation programmes were ongoing inFarah and Nangarhar at the time of the survey or in theperiod preceding it. The average altitude of the schoolswhere the survey was carried out was 1790 m (Kabul),600 m (Nangarhar), 730 m (Farah), and 1010 m(Kandahar). Within this altitudinal range, it may wellbe that a small additional confounding effect upon thechild’s haemoglobin level could have occurred and inthe absence of appropriate local standardization, asses-sing its relative contribution(s) on general haemoglobinlevels remains elusive.Since the last documented survey of STH in Afghani-stan (Buck et al., 1978), clearly A. lumbricoides still appearsto be widespread and T. trichiura and hookworminfections are now documented for the first time. Nodoubt as a result of overcrowding and poor sanitation andhygiene, the urban environment appears to offer aparticularly conducive environment for STH trans-mission. Schoolchildren surveyed in Kabul were morelikely than the others to be infected with at least one STH(OR ¼ 2.2; 95% CI 1.6–3.0) and to have a moderate-to-heavy intensity STH infection (OR ¼ 7.6; 95% CI4.9–11.8) in line with the observations of Phiri et al.(2000) for STHs in Malawi. Poly-parasitism in Afghani-stan appears to be less common than observed in othercountries (Booth et al., 1998; Tchuem Tchuente et al., 2003)and the levels of presently observable anaemia associatedwith infection were not particularly severe. Mass drugadministration of anthelmintics would therefore be bestfocused upon schools within a predominantly urbansetting.AcknowledgementsWe are very grateful to Dr Riadh Ben-Ismail ofWHO/EMRO; to Dr Said Salah Youssouf, Dr YonFleerackers, and Mr Ahmad Khalid Janbaz, ofWHO/Afghanistan; and to Mr Mujeeb Haidery, ofWFP/Afghanistan. Special thanks are due to Mr AbdulSaboor, Mr Mohamed Mussa and Mr Naqibullah for theirhelp and commitment. We also would like to express ourgratitude to all the schoolmasters and teachers involvedin this survey. Ethical approval for this study was grantedby the Ministry of Health, The Islamic Republic ofAfghanistan.ReferencesAwasthi, S., Bundy, D.A.P. & Savioli, L. (2003)Helminthic infections. Clinical review. British MedicalJournal 327, 431–433.Booth, M., Bundy, D.A.P., Albonico, M., Chwaya, H.M.,Alawi, K.S. & Savioli, L. (1998) Associations amongmultiple geohelminth species in schoolchildren fromPemba Island. Parasitology 116, 85–93.Buck, A.A., Anderson, R.I. & Mac Rae, A.A. (1978)Epidemiology of poly-parasitism. I. Occurrence, fre-quency and distribution of multiple infections in ruralcommunities in Chad, Peru, Afghanistan, and Zaire.Tropenmedizin und Parasitologie 29, 61–70.Crompton, D.W.T. (1992) Ascaris and childhood malnu-trition. Transactions of the Royal Society of TropicalMedicine and Hygiene 86, 577–579.Crompton, D.W.T. (1999) How much human helminthia-sis is there in the world? Journal of Parasitology 85,397–403.Crompton, D.W.T. & Nesheim, M.C. (2002) Nutritionalimpact of intestinal helminthiasis during the humanlife cycle. Annual Review of Nutrition 22, 35–59.Oberhelman, R.A., Guerrero, E.S., Fernandez, M.L.,Silio, M., Mercado, D., Comiskey, N., Ihenacho, G. &Mera, R. (1998) Correlations between intestinalparasitosis, physical growth, and psychomotor devel-opment among infants and children from ruralTable 1. Prevalence (%) and intensity category of soil-transmitted helminth (STH) infections across eco-zones in Afghanistan.ProvinceKabul Nangarhar Farah Kandahar TotalAscaris lumbricoidesPrevalence of infection 57.3 27 43 37.4 40.9Prevalence of moderate-to-heavy intensity infection 25.9 3.1 6.4 3.1 9.4Trichuris trichiuraPrevalence of infection 13 6.3 12.9 7.8 9.9Prevalence of moderate-to-heavy intensity infection 0.8 0.4 0.8 0 0.5HookwormsPrevalence of infection 0 2.7 0 0 0.7Prevalence of moderate-to-heavy intensity infection 0 0 0 0 0Any STHPrevalence of infection 61.9 34.8 50.2 42.8 47.2Prevalence of moderate-to-heavy intensity infection 26.4 3.1 7.2 3.1 9.7Prevalence of poly-parasitic infection 8.4 1.2 5.6 2.3 4.3Prevalence of moderate-to-heavy intensity poly-parasitic infection 0.4 0.4 0 0 0.2Soil-transmitted helminths in Afghanistan 383https:/www.cambridge.org/core/terms. https://doi.org/10.1079/JOH2005316Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 08:15:13, subject to the Cambridge Core terms of use, available atNicaragua. American Journal of Tropical Medicine andHygiene 58, 470–475.Phiri, K., Whitty, C.J.M., Graham, S.M. & Ssembatya-Lule, G. (2000) Urban/rural differences in prevalenceand risk factors for intestinal helminth infection insouthern Malawi. Annals of Tropical Medicine andParasitology 94, 381–387.Savioli, L., Stansfield, S., Bundy, D.A.P., Mitchell, A.,Bhatia, R., Engels, D., Montresor, A., Neira, M. &Shein, A.M. (2002) Schistosomiasis and soil-trans-mitted helminth infections: forging control efforts.Transactions of the Royal Society of Tropical Medicine andHygiene 96, 577–579 (Erratum in: 97, 90).Tchuem Tchuente, L.-A., Behnke, J.M., Gilbert, F.S.,Southgate, V.R. & Vercruysse, J. (2003) Polyparasitismwith Schistosoma haematobium and soil-transmittedhelminth infections among school children in Loum,Cameroon. Tropical Medicine and International Health 8,975–986.Urbani, C. & Albonico, M. (2003) Anthelminthic drugsafety and drug administration in the control of soil-transmitted helminthiasis in community campaigns.Acta Tropica 86, 215–221.World Health Organization (1991) Faecal specimens. pp.25–27 in Basic laboratory methods in medical parasitology,Geneva, World Health Organization.World Health Organization (2002) Prevention and controlof schistosomiasis and soil-transmitted helminths, 56 pp.Geneva, World Health Organization.(Accepted 14 June 2005)q CAB International, 2005384 A.F. Gabrielli et al.https:/www.cambridge.org/core/terms. https://doi.org/10.1079/JOH2005316Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 08:15:13, subject to the Cambridge Core terms of use, available at

Soil-transmitted helminths and haemoglobin status among Afghan children in World Food Programme assisted schools

Soil-transmitted helminths and haemoglobin status among Afghan children in World Food Programme assisted schools

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