Epidemiology of coinfection with soil transmitted helminths and Plasmodium falciparum among school children in Bumula District in western Kenya

Particle and Fibre Toxicology

Simon J Brooker¹  Charles S. Mwandawiro²  Sammy M. Njenga²  Elizabeth Allen⁴  Tansy Edwards⁴  Paul Gichuki²  Birgit Nikolay⁴  Fred Nuwaha³  Stella Kepha² 

[1] KEMRI-Wellcome Trust Research Programme, Nairobi, Kenya;Eastern and Southern Africa Centre of International Parasite Control, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya;College of Health Sciences, Makerere University, Kampala, Uganda;London School of Hygiene & Tropical Medicine, London, UK

关键词: Coinfection;    Plasmodium falciparum;    Ascaris lumbricoides;    Hookworm;    Soil transmitted helminths;   

Others  :  1224207
DOI  :  10.1186/s13071-015-0891-5

 received in 2015-03-30, accepted in 2015-05-07,  发布年份 2015

【 摘 要 】

Background

Many school children living in Africa are infected with plasmodia and helminth species and are consequently at risk of coinfection. However, the epidemiology of such coinfection and the implications of coinfection for children’s health remain poorly understood. This study describes the epidemiology of Ascaris lumbricoides-Plasmodium and hookworm-Plasmodium coinfection among school children living in western Kenya and investigates the associated risk factors.

Methods

As part of a randomized trial, a baseline cross-sectional survey was conducted among school children aged 5–18 years in 23 schools in Bumula District. Single stool samples were collected to screen for helminth infections using the Kato-Katz technique and malaria parasitaemia was determined from a finger prick blood sample. Demographic and anthropometric data were also collected.

Results

Overall, 46.4 % of the children were infected with Plasmodium falciparum while 27.6 % of the children were infected with at least one soil transmitted helminth (STH) species, with hookworm being the most common (16.8 %) followed by A. lumbricoides (15.3 %). Overall 14.3 % of the children had STH-Plasmodium coinfection, with hookworm-Plasmodium (9.0 %) coinfection being the most common. Geographical variation in the prevalence of coinfection occurred between schools. In multivariable logistic regression analysis, hookworm was positively associated with P. falciparum infection. In stratified analysis, hookworm infection was associated with increased odds of P. falciparum infection among both boys (P < 0.001) and girls (P = 0.01), whereas there was no association between A. lumbricoides and P. falciparum.

Conclusion

These findings demonstrate STH infections are still prevalent, despite the ongoing national deworming programme in Kenya, and that malaria parasitaemia is widespread, such that coinfection occurs among a proportion of children. A subsequent trial will allow us to investigate the implications of coinfection for the risk of clinical malaria.

【 授权许可】

   
2015 Kepha et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

【 参考文献 】

• [1]Salim N, Knopp S, Lweno O, Abdul U, Mohamed A, Schindler T, Rothen J, Masimba J, Kwaba D, Mohammed AS et al.. Distribution and Risk Factors for Plasmodium and Helminth Co-infections: A Cross-Sectional Survey among Children in Bagamoyo District, Coastal Region of Tanzania. PLoS Negl Trop Dis. 2015; 9(4):e0003660.
• [2]Mazigo HD, Waihenya R, Lwambo NJ, Mnyone LL, Mahande AM, Seni J, Zinga M, Kapesa A, Kweka EJ, Mshana SE et al.. Co-infections with Plasmodium falciparum Schistosoma mansoni and intestinal helminths among schoolchildren in endemic areas of northwestern Tanzania. Parasit Vectors. 2010; 3:44. BioMed Central Full Text
• [3]Bisanzio D, Mutuku F, Bustinduy AL, Mungai PL, Muchiri EM, King CH, Kitron U. Cross-sectional study of the burden of vector-borne and soil-transmitted polyparasitism in rural communities of Coast Province Kenya. PLoS Negl Trop Dis. 2014; 8(7):e2992.
• [4]Brooker SJ, Pullan RL, Gitonga CW, Ashton RA, Kolaczinski JH, Kabatereine NB, Snow RW. Plasmodium-helminth coinfection and its sources of heterogeneity across East Africa. J Infect Dis. 2012; 205(5):841-52.
• [5]Kinung’hi SM, Magnussen P, Kaatano GM, Kishamawe C, Vennervald BJ. Malaria and helminth co-infections in school and preschool children: a cross-sectional study in Magu district, north-western Tanzania. PLoS One. 2014; 9(1):e86510.
• [6]Mboera LE, Senkoro KP, Rumisha SF, Mayala BK, Shayo EH, Mlozi MR. Plasmodium falciparum and helminth coinfections among schoolchildren in relation to agro-ecosystems in Mvomero District Tanzania. Acta Trop. 2011; 120(1–2):95-102.
• [7]Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KK, Sumbele I. Malaria and helminth co-infection in children living in a malaria endemic setting of mount Cameroon and predictors of anemia. J Parasitol. 2006; 92(6):1191-5.
• [8]Pullan RL, Kabatereine NB, Bukirwa H, Staedke SG, Brooker S. Heterogeneities and consequences of Plasmodium species and hookworm coinfection: a population based study in Uganda. J Infect Dis. 2011; 203(3):406-17.
• [9]Righetti AA, Glinz D, Adiossan LG, Koua AY, Niamke S, Hurrell RF, Wegmuller R, N’Goran EK, Utzinger J. Interactions and potential implications of Plasmodium falciparum-hookworm coinfection in different age groups in south-central Cote d’Ivoire. PLoS Negl Trop Dis. 2012; 6(11):e1889.
• [10]Tshikuka JG, Scott ME, Gray-Donald K, Kalumba ON. Multiple infection with Plasmodium and helminths in communities of low and relatively high socio-economic status. Ann Trop Med Parasit. 1996; 90(3):277-93.
• [11]Yapi RB, Hurlimann E, Houngbedji CA, Ndri PB, Silue KD, Soro G, Kouame FN, Vounatsou P, Furst T, N’Goran EK et al.. Infection and co-infection with helminths and Plasmodium among school children in Cote d’Ivoire: results from a National Cross-Sectional Survey. PLoS Negl Trop Dis. 2014; 8(6):e2913.
• [12]Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites–masters of regulation. Immunol Rev. 2004; 201:89-116.
• [13]Adegnika AA, Kremsner PG. Epidemiology of malaria and helminth interaction: a review from 2001 to 2011. Curr Opin HIV AIDS. 2012; 7(3):221-4.
• [14]Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ. 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. 2007; 77(6 Suppl):88-98.
• [15]Mwandawiro C, Nikolay B, Kihara JH, Ozier O, Mukoko DA, Mwanje MT, Hakobyan A, Pullan RL, Brooker SJ, Njenga SM. Monitoring and evaluating the impact of national school-based deworming in Kenya: study design and baseline results. Parasit Vectors. 2013; 6:198. BioMed Central Full Text
• [16]Gitonga CW, Karanja PN, Kihara J, Mwanje M, Juma E, Snow RW, Noor AM, Brooker S. Implementing school malaria surveys in Kenya: towards a national surveillance system. Malar J. 2010; 9:306. BioMed Central Full Text
• [17]Brooker S, Kabatereine NB, Smith JL, Mupfasoni D, Mwanje MT, Ndayishimiye O, Lwambo NJ, Mbotha D, Karanja P, Mwandawiro C et al.. An updated atlas of human helminth infections: the example of East Africa. Int J Health Geogr. 2009; 8:42. BioMed Central Full Text
• [18]Pullan RL, Gething PW, Smith JL, Mwandawiro CS, Sturrock HJ, Gitonga CW, Hay SI, Brooker S. Spatial modelling of soil-transmitted helminth infections in Kenya: a disease control planning tool. PLoS Negl Trop Dis. 2011; 5(2):e958.
• [19]Anthroplus: growth reference 5–19 years. WHO, Geneva; 2007.
• [20]WHO Expert Committe: Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser. 2002; 912:1-57.
• [21]Accelerating work to overcome the global impact of neglected tropical diseases – A roadmap for implementation. World Health Organization, Geneva; 2012.
• [22]Handzel T, Karanja DM, Addiss DG, Hightower AW, Rosen DH, Colley DG, Andove J, Slutsker L, Secor WE. Geographic distribution of schistosomiasis and soil-transmitted helminths in Western Kenya: implications for anthelminthic mass treatment. Am J Trop Med Hyg. 2003; 69(3):318-23.
• [23]Brooker S, Miguel EA, Moulin S, Luoba AI, Bundy DA, Kremer M. Epidemiology of single and multiple species of helminth infections among school children in Busia District Kenya. East Afr Med J. 2000; 77(3):157-61.
• [24]Sang HC, Muchiri G, Ombok M, Odiere MR, Mwinzi PN. Schistosoma haematobium hotspots in south Nyanza, western Kenya: prevalence, distribution and co-endemicity with Schistosoma mansoni and soil-transmitted helminths. Parasit Vectors. 2014; 7:125. BioMed Central Full Text
• [25]Odiere MR, Opisa S, Odhiambo G, Jura WG, Ayisi JM, Karanja DM, Mwinzi PN. Geographical distribution of schistosomiasis and soil-transmitted helminths among school children in informal settlements in Kisumu City Western Kenya. J Parasitol. 2011; 138(12):1569-77.
• [26]Humphries D, Mosites E, Otchere J, Twum WA, Woo L, Jones-Sanpei H, Harrison LM, Bungiro RD, Benham-Pyle B, Bimi L et al.. Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. Am J Trop Med Hyg. 2011; 84(5):792-800.
• [27]Brutus L, Watier L, Hanitrasoamampionona V, Razanatsoarilala H, Cot M. Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. Am J Trop Med Hyg. 2007; 77(6):1091-5.
• [28]Brutus L, Watier L, Briand V, Hanitrasoamampionona V, Razanatsoarilala H, Cot M. Parasitic co-infections: does Ascaris lumbricoides protect against Plasmodium falciparum infection? Am J Trop Med Hyg. 2006; 75(2):194-8.
• [29]Nacher M. Interactions between worms and malaria: good worms or bad worms? Malar J. 2011; 10:259. BioMed Central Full Text
• [30]Le Hesran JY, Akiana J, el Ndiaye HM, Dia M, Senghor P, Konate L. Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Trans R Soc Trop Med Hyg. 2004; 98(7):397-9.
• [31]Banoo S, Bell D, Bossuyt P, Herring A, Mabey D, Poole F, Smith PG, Sriram N, Wongsrichanalai C, Linke R et al.. Evaluation of diagnostic tests for infectious diseases: general principles. Nat Rev Microbiol. 2006; 4(12 Suppl):S20-32.
• [32]Krauth SJ, Coulibaly JT, Knopp S, Traore M, N’Goran EK, Utzinger J. An in-depth analysis of a piece of shit: distribution of Schistosoma mansoni and hookworm eggs in human stool. PLoS Negl Trop Dis. 2012; 6(12):e1969.