Infection and Co-infection with Helminths and Plasmodium among School Children in Côte d'Ivoire: Results from a National Cross-Sectional Survey

PLoS Neglected Tropical Diseases

Volumn 8, Issue 6, 2014, Pages

  Yapi, Richard B ^a,b,c,d   Hürlimann, Eveline ^b,c,d   Houngbedji, Clarisse A ^b,e   Ndri, Prisca B ^b,e   Silué, Kigbafori D ^a,b   Soro, Gotianwa ^f   Kouamé, Ferdinand N ^f   Vounatsou, Penelope ^c,d   Fürst, Thomas ^c,d,g   N'Goran, Eliézer K ^a,b   Utzinger, Jürg ^c,d   Raso, Giovanna ^b,c,d  

^a UNIVERSITÉ FÉLIX HOUPHOUËT BOIGNY   (Côte d’Ivoire)

^b CENTRE SUISSE DE RECHERCHES SCIENTIFIQUES EN CÔTE D'IVOIRE   (Côte d’Ivoire)

^c SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

^e UNIVERSITÉ NANGUI ABROGOUA   (Côte d’Ivoire)

^f Programme National de Santé Scolaire et Universitaire   (Côte d’Ivoire)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALBENDAZOLE; ARTEMISININ; DRINKING WATER; PRAZIQUANTEL; WELL WATER;

ADOLESCENT; ARTICLE; ASCARIASIS; CHILD; CROSS-SECTIONAL STUDY; FEMALE; HAND WASHING; HELMINTHIASIS; HEMATURIA; HOOKWORM INFECTION; HUMAN; INFORMED CONSENT; MALARIA; MALARIA FALCIPARUM; MALE; MIXED INFECTION; PARASITE PREVALENCE; PLASMODIUM; PLASMODIUM MALARIAE INFECTION; PLASMODIUM OVALE MALARIA; PRESCHOOL CHILD; QUESTIONNAIRE; RISK; SANITATION; SCHISTOSOMIASIS; SCHISTOSOMIASIS HAEMATOBIA; SCHISTOSOMIASIS MANSONI; SCHOOL CHILD; SINGLE DRUG DOSE; SOCIAL STATUS; TRICHURIASIS; URBAN POPULATION; WATER CONTAMINATION; ANIMAL; BLOOD; COINFECTION; COTE D'IVOIRE; EPIDEMIOLOGY; FECES; PARASITOLOGY; PREVALENCE; RISK FACTOR; SCHOOL; STUDENT; URINE;

ADOLESCENT; ANIMALS; BLOOD; CHILD; CHILD, PRESCHOOL; COINFECTION; COTE D'IVOIRE; CROSS-SECTIONAL STUDIES; FECES; FEMALE; HUMANS; MALARIA; MALE; PREVALENCE; QUESTIONNAIRES; RISK FACTORS; SCHISTOSOMIASIS MANSONI; SCHOOLS; STUDENTS; URINE;

EID: 84903466285     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002913     Document Type: Article

References (68)

1. Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, et al. (2012) Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413-431.
2. Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, et al. (2012) Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380: 2163-2196.
3. Fürst T, Raso G, Acka CA, Tschannen AB, N'Goran EK, et al. (2009) Dynamics of socioeconomic risk factors for neglected tropical diseases and malaria in an armed conflict. PLoS Negl Trop Dis 3: e513.
4. Krefis AC, Schwarz NG, Nkrumah B, Acquah S, Loag W, et al. (2010) Principal component analysis of socioeconomic factors and their association with malaria in children from the Ashanti region, Ghana. Malar J 9: 201.
5. WHO (2012) World malaria report 2012. Geneva: World Health Organization.
6. WHO (2006) Preventive chemotherapy in human helminthiasis: coordinated use of anthelmintic drugs in control interventions: a manual for health professionals and programme managers. Geneva: World Health Organization.
7. Bartram J, Cairncross S, (2010) Hygiene, sanitation, and water: forgotten foundations of health. PLoS Med 7: e1000367.
8. Cairncross S, Bartram J, Cumming O, Brocklehurst C, (2010) Hygiene, sanitation, and water: what needs to be done? PLoS Med 7: e1000365.
9. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, et al. (2012) Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med 9: e1001162.
10. Brooker S, Akhwale W, Pullan RL, Estambale B, Clarke SE, et al. (2007) Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77 (6 Suppl) (): 88-98.
11. Baragatti M, Fournet F, Henry MC, Assi S, Ouedraogo H, et al. (2009) Social and environmental malaria risk factors in urban areas of Ouagadougou, Burkina Faso. Malar J 8: 13.
12. Pages F, Orlandi-Pradines E, Corbel V, (2007) Vecteurs du paludisme: biologie, diversité, contrôle et protection individuelle. Médecine Mal Infect 37: 153-161.
13. Utzinger J, N'Goran EK, Caffrey CR, Keiser J, (2011) From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Trop 120(Supp 1): S121-S137.
14. Mboera LEG, Senkoro KP, Rumisha SF, Mayala BK, Shayo EH, et al. (2011) Plasmodium falciparum and helminth coinfections among schoolchildren in relation to agro-ecosystems in Mvomero district, Tanzania. Acta Trop 120: 95-102.
15. Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KKJ, Sumbele I, (2006) Malaria and helminth co-infection in children living in a malaria endemic setting of Mount Cameroon and predictors of anemia. J Parasitol 92: 1191-1195.
16. Betsi NA, Koudou BG, Cissé G, Tschannen AB, Pignol AM, et al. (2006) Effect of an armed conflict on human resources and health systems in Côte d'Ivoire: prevention of and care for people with HIV/AIDS. AIDS Care 18: 356-365.
17. Bonfoh B, Raso G, Koné I, Dao D, Girardin O, et al. (2011) Research in a war zone. Nature 474: 569-571.
18. Raso G, Schur N, Utzinger J, Koudou BG, Tchicaya ES, et al. (2012) Mapping malaria risk among children in Côte d'Ivoire using Bayesian geo-statistical models. Malar J 11: 160.
19. Diggle P, Lophaven S, (2006) Bayesian geostatistical design. Scand J Stat 33: 53-64.
20. Montresor A, Crompton DWT, Gyorkos TW, Savioli L (2002) Helminth control in school-age children: a guide for managers of control programmes in planning. Geneva: World Health Organization.
21. Lwambo NJ, Savioli L, Kisumku UM, Alawi KS, Bundy DA, (1997) Control of Schistosoma haematobium morbidity on Pemba Island: validity and efficiency of indirect screening tests. Bull World Health Organ 75: 247-252.
22. Raso G, Utzinger J, Silué KD, Ouattara M, Yapi A, et al. (2005) Disparities in parasitic infections, perceived ill health and access to health care among poorer and less poor schoolchildren of rural Côte d'Ivoire. Trop Med Int Health 10: 42-57.
23. WHO (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Tech Rep Ser 912: 1-57.
24. Raso G, Luginbühl A, Acka CA, Tian-Bi NT, Silué KD, et al. (2004) Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d'Ivoire. Int J Epidemiol 33: 1092-1102.
25. O'Donnell O, Doorsslaer EV, Wagstaff A, Lindelow M (2008) Analyzing health equity using household survey data: a guide to techniques and their implementation. Washington DC: World Bank.
26. Utzinger J, N'Goran EK, Ossey YA, Booth M, Traoré M, et al. (2000) Rapid screening for Schistosoma mansoni in western Côte d'Ivoire using a simple school questionnaire. Bull World Health Organ 78: 389-398.
27. Raso G, Matthys B, N'Goran EK, Tanner M, Vounatsou P, et al. (2005) Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Côte d'Ivoire. Parasitology 131: 97-108.
28. Silué KD, Raso G, Yapi A, Vounatsou P, Tanner M, et al. (2008) Spatially-explicit risk profiling of Plasmodium falciparum infections at a small scale: a geostatistical modelling approach. Malar J 7: 111.
29. Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, et al. (2010) Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis 4: e754.
30. Righetti AA, Koua AYG, Adiossan LG, Glinz D, Hurrell RF, et al. (2012) Etiology of anemia among infants, school-aged children, and young non-pregnant women in different settings of south-central Côte d'Ivoire. Am J Trop Med Hyg 87: 425-434.
31. Fürst T, Silué KD, Ouattara M, N'Goran DN, Adiossan LG, et al. (2012) Schistosomiasis, soil-transmitted helminthiasis, and sociodemographic factors influence quality of life of adults in Côte d'Ivoire. PLoS Negl Trop Dis 6: e1855.
32. Righetti AA, Glinz D, Adiossan LG, Koua AYG, Niamké S, et al. (2012) Interactions and potential implications of Plasmodium falciparum-hookworm coinfection in different age groups in south-central Côte d'Ivoire. PLoS Negl Trop Dis 6: e1889.
33. Kouadio MKD, Righetti AA, Abé NN, Wegmüller R, Weiss MG, et al. (2013) Local concepts of anemia-related illnesses and public health implications in the Taabo health demographic surveillance system, Côte d'Ivoire. BMC Hematol 13: 5.
34. Schmidlin T, Hürlimann E, Silué KD, Yapi RB, Houngbedji C, et al. (2013) Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Côte d'Ivoire. PLoS One 8: e65722.
35. Raso G, Vounatsou P, Gosoniu L, Tanner M, N'Goran EK, et al. (2006) Risk factors and spatial patterns of hookworm infection among schoolchildren in a rural area of western Côte d'Ivoire. Int J Parasitol 36: 201-210.
36. Gemperli A, Vounatsou P, Kleinschmidt I, Bagayoko M, Lengeler C, et al. (2004) Spatial patterns of infant mortality in Mali: the effect of malaria endemicity. Am J Epidemiol 159: 64-72.
37. Halliday KE, Karanja P, Turner EL, Okello G, Njagi K, et al. (2012) Plasmodium falciparum, anaemia and cognitive and educational performance among school children in an area of moderate malaria transmission: baseline results of a cluster randomized trial on the coast of Kenya. Trop Med Int Health 17: 532-549.
38. Hviid L, (2005) Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop 95: 270-275.
39. Felger I, Maire M, Bretscher MT, Falk N, Tiaden A, et al. (2012) The dynamics of natural Plasmodium falciparum infections. PLoS One 7: e45542.
40. Proietti C, Verra F, Bretscher MT, Stone W, Kanoi BN, et al. (2013) Influence of infection on malaria-specific antibody dynamics in a cohort exposed to intense malaria transmission in northern Uganda. Parasite Immunol 35: 164-173.
41. Boutlis CS, Gowda DC, Naik RS, Maguire GP, Mgone CS, et al. (2002) Antibodies to Plasmodium falciparum glycosylphosphatidylinositols: inverse association with tolerance of parasitemia in Papua New Guinean children and adults. Infect Immun 70: 5052-5057.
42. Müller I, Coulibaly JT, Fürst T, Knopp S, Hattendorf J, et al. (2011) Effect of schistosomiasis and soil-transmitted helminth infections on physical fitness of school children in Côte d'Ivoire. PLoS Negl Trop Dis 5: e1239.
43. Coulibaly JT, Fürst T, Silué KD, Knopp S, Hauri D, et al. (2012) Intestinal parasitic infections in schoolchildren in different settings of Côte d'Ivoire: effect of diagnostic approach and implications for control. Parasit Vectors 5: 135.
44. N'Goran EK, Diabate S, Utzinger J, Sellin B, (1997) Changes in human schistosomiasis levels after the construction of two large hydroelectric dams in central Côte d'Ivoire. Bull World Health Organ75: 541-545.
45. Booth M, Vounatsou P, N'Goran EK, Tanner M, Utzinger J, (2003) The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d'Ivoire. Parasitology 127: 525-531.
46. Utzinger J, Müller I, Vounatsou P, Singer BH, N'Goran EK, et al. (2003) Random spatial distribution of Schistosoma mansoni and hookworm infections among school children within a single village. J Parasitol 89: 686-692.
47. Vounatsou P, Raso Tanner, N'Goran EK, Utzinger J, (2009) Bayesian geostatistical modelling for mapping schistosomiasis transmission. Parasitology 136: 1695-1705.
48. Acka CA, Raso G, N'Goran EK, Tschannen AB, Bogoch II, et al. (2010) Parasitic worms: knowledge, attitudes, and practices in western Côte d'Ivoire with implications for integrated control. PLoS Negl Trop Dis 4: e910.
49. Hotez P, (2008) Hookworm and poverty. Ann N Y Acad Sci 1136: 38-44.
50. Mazigo HD, Waihenya R, Lwambo NJS, Mnyone LL, Mahande AM, et al. (2010) Co-infections with Plasmodium falciparum, Schistosoma mansoni and intestinal helminths among schoolchildren in endemic areas of northwestern Tanzania. Parasit Vectors 3: 44.
51. Pullan RL, Kabatereine NB, Bukirwa H, Staedke SG, Brooker S, (2011) Heterogeneities and consequences of Plasmodium species and hookworm coinfection: a population based study in Uganda. J Infect Dis 203: 406-417.
52. Abanyie FA, McCracken C, Kirwan P, Molloy SF, Asaolu SO, et al. (2013) Ascaris co-infection does not alter malaria-induced anaemia in a cohort of Nigerian preschool children. Malar J 12: 1.
53. Kirwan P, Jackson AL, Asaolu SO, Molloy SF, Abiona TC, et al. (2010) Impact of repeated four-monthly anthelmintic treatment on Plasmodium infection in preschool children: a double-blind placebo-controlled randomized trial. BMC Infect Dis 10: 277.
54. Rudge JW, Stothard JR, Basáñez MG, Mgeni AF, Khamis IS, et al. (2008) Micro-epidemiology of urinary schistosomiasis in Zanzibar: Local risk factors associated with distribution of infections among schoolchildren and relevance for control. Acta Trop 105: 45-54.
55. Brooker SJ, Pullan RL, Gitonga CW, Ashton RA, Kolaczinski JH, et al. (2012) Plasmodium-helminth coinfection and its sources of heterogeneity across East Africa. J Infect Dis 205: 841-852.
56. Brooker S, Clements ACA, Bundy DAP, (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62: 221-261.
57. Bayoh MN, Lindsay SW, (2007) Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bull Entomol Res 93: 375-381.
58. Briët OJT, Vounatsou P, Amerasinghe PH, (2008) Malaria seasonality and rainfall seasonality in Sri Lanka are correlated in space. Geospat Health 2: 183-190.
59. Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, et al. (2008) The synergistic effect of concomitant schistosomiasis, hookworm, and Trichuris infections on children's anemia burden. PLoS Negl Trop Dis 2: e245.
60. Utzinger J, N'Goran EK, Esse E, Acka CA, Lohourignon KL, et al. (1998) Schistosoma mansoni, intestinal parasites and perceived morbidity indicators in schoolchildren in a rural endemic area of western Côte d'Ivoire. Trop Med Int Health 3: 711-720.
61. Utzinger J, Booth M, N'Goran EK, Müller I, Tanner M, et al. (2001) Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 122: 537-544.
62. Tarafder M, Carabin H, Joseph L, Balolong E, Olveda R, et al. (2010) Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a 'gold standard'. Int J Parasitol 40: 399-404.
63. Houmsou R, Kela S, Suleiman M, (2011) Performance of microhaematuria and proteinuria as measured by urine reagent strips in estimating intensity and prevalence of Schistosoma haematobium infection in Nigeria. Asian Pac J Trop Med 4: 997-1000.
64. Bogoch II, Andrews JR, Dadzie Ephraim RK, Utzinger J, (2012) Simple questionnaire and urine reagent strips compared to microscopy for the diagnosis of Schistosoma haematobium in a community in northern Ghana. Trop Med Int Health 17: 1217-1221.
65. Odiere MR, Opisa S, Odhiambo G, Jura WGZO, Ayisi JM, et al. (2011) Geographical distribution of schistosomiasis and soil-transmitted helminths among school children in informal settlements in Kisumu City, western Kenya. Parasitology 138: 1569-1577.
66. Ohrt C, Purnomo, Sutamihardja MA, Tang D, Kain KC, (2002) Impact of microscopy error on estimates of protective efficacy in malaria-prevention trials. J Infect Dis 186: 540-546.
67. O'Meara W, Hall BF, McKenzie FE, (2007) Malaria vaccine efficacy: the difficulty of detecting and diagnosing malaria. Malar J 6: 36.
68. Hotez PJ, Brindley PJ, Bethony MJ, King CH, Pearce EJ, et al. (2008) Helminth infections: the great neglected tropical diseases. J Clin. Invest 118: 1311-1321.