Plasmodium-helminth coinfection and its sources of heterogeneity across East Africa

Journal of Infectious Diseases

Volumn 205, Issue 5, 2012, Pages 841-852

  Brooker, Simon J ^a,b   Pullan, Rachel L ^b   Gitonga, Caroline W ^a,b   Ashton, Ruth A ^a,b,c,d   Kolaczinski, Jan H ^a,d   Kabatereine, Narcis B ^d   Snow, Robert W ^a,e  

^a KEMRI WELLCOME TRUST RESEARCH PROGRAMME   (Kenya)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c Malaria Consortium Ethiopia Office   (Ethiopia)

^d MINISTRY OF HEALTH   (Uganda)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BAYSESIAN MODELLING FRAMEWORK; CHILD; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; ETHIOPIA; FEMALE; GENETIC HETEROGENEITY; GEOGRAPHIC DISTRIBUTION; HOOKWORM INFECTION; HOST PATHOGEN INTERACTION; HOUSEHOLD; HUMAN; INDIVIDUALIZATION; INFECTION RISK; KENYA; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; MULTIVARIATE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMIASIS HAEMATOBIA; SCHISTOSOMIASIS MANSONI; SCHOOL; SPECIES DISTRIBUTION; UGANDA;

ADOLESCENT; BAYES THEOREM; CHILD; COINFECTION; ETHIOPIA; FEMALE; HOOKWORM INFECTIONS; HUMANS; KENYA; LOGISTIC MODELS; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; RISK FACTORS; SCHISTOSOMIASIS HAEMATOBIA; SCHISTOSOMIASIS MANSONI; UGANDA;

EID: 84856882266     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jir844     Document Type: Article

References (45)

1. Petney TN, Andrews RH. Muliparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 1998; 28:377-93. (Pubitemid 28156768)
2. Brooker S, Akhwale W, Pullan R, et al. Epidemiology of plasmodiumhelminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 2007; 77:88-98.
3. Brooker S, Clements AC. Spatial heterogeneity of parasite co-infection: determinants and geostatistical prediction at regional scales. Int J Parasitol 2009; 39:591-7.
4. Telfer S, Lambin X, Birtles R, et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science 2010; 330:243-6.
5. Pedersen AB, Fenton A. Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 2007; 22:133-9. (Pubitemid 46273826)
6. Graham AL. Ecological rules governing helminth-microparasite coinfection. Proc Natl Acad Sci USA 2008; 105:566-70. (Pubitemid 351171748)
7. Lello J, Boag B, Fenton A, Stevenson IR, Hudson PJ. Competition and mutualism among the gut helminths of a mammalian host. Nature 2004; 428:840-4. (Pubitemid 38529495)
8. Brooker S, Clements AC, Hotez PJ, et al. The co-distribution of Plasmodium falciparum and hookworm among African schoolchildren. Malar J 2006; 5:99.
9. Diallo TO, Remoue F, Gaayeb L, et al. Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens. PLoS One 2010; 5:e12764.
10. Hartgers FC, Obeng BB, Kruize YC, et al. Responses to malarial antigens are altered in helminth-infected children. J Infect Dis 2009; 199: 1528-35.
11. Sangweme DT, Midzi N, Zinyowera-Mutapuri S, Mduluza T, Diener-West M, Kumar N. Impact of schistosome infection on Plasmodium falciparum malariometric indices and immune correlates in school age children in Burma Valley, Zimbabwe. PLoS Negl Trop Dis 2010; 4:e882.
12. 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; 77:1091-5. (Pubitemid 351837799)
13. Sokhna C, Le Hesran JY, Mbaye PA, et al. Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar J 2004; 3:43.
14. Spiegel A, Tall A, Raphenon G, Trape JF, Druilhe P. Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 2003; 97:198-9. (Pubitemid 37265633)
15. Wilson S, Vennervald BJ, Kadzo H, et al. Hepatosplenomegaly in Kenyan schoolchildren: exacerbation by concurrent chronic exposure to malaria and Schistosoma mansoni infection. Trop Med Int Health 2007; 12:1442-9. (Pubitemid 350212709)
16. 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; 203:406-17.
17. Ashton R, Kefyalew T, Tesfaye G, et al. School-based surveys of malaria in Oromia Regional State, Ethiopia: a rapid malaria surveillance approach for low transmission settings. Malar J 2011; 10:25.
18. Gitonga CW, Karanja PN, Kihara J, et al. Implementing school malaria surveys in Kenya: towards a national surveillance system. Malar J 2010; 9:306.
19. Abeku TA, van Oortmarssen GJ, Borsboom G, de Vlas SJ, Habbema JD. Spatial and temporal variations of malaria epidemic risk in Ethiopia: factors involved and implications. Acta Trop 2003; 87: 331-40. (Pubitemid 37271999)
20. Noor AM, Gething PW, Alegana VA, et al. The risks of malaria infection in Kenya in 2009. BMC Infect Dis 2009; 9:180.
21. Okello PE, Van Bortel W, Byaruhanga AM, et al. Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg 2006; 75:219-25. (Pubitemid 46941334)
22. Brooker S, Kabatereine NB, Smith JL, et al. An updated atlas of human helminth infections: the example of East Africa. Int J Health Geogr 2009; 8:42.
23. Chunge RN, Karumba PN, Andala EO. Hookworm species in patients from Kenyatta National Hospital Nairobi. Ann Trop Med Parasitol 1986; 80:147-8. (Pubitemid 16180526)
24. Filmer D, Pritchett LH. Estimating wealth effects without expenditure datador tears: an application to educational enrollments in states of India. Demography 2001; 38:115-32. (Pubitemid 33597463)
25. Museum of Vertebrate Zoology. WorldClim. 2005: University of California, Berkeley. http://www.worldclim.org. Accessed 7 June 2009.
26. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 2005; 25:1965-78. (Pubitemid 43013915)
27. Hay SI, Tatem AJ, Graham AJ, Goetz SJ, Rogers DJ. Global environmental data for mapping infectious disease distribution. Adv Parasitol 2006; 62:37-77.
28. Scharlemann JP, Benz D, Hay SI, et al. Global data for ecology and epidemiology: a novel algorithm for temporal Fourier processing MODIS data. PLoS ONE 2008; 3:e1408.
29. US Geological Survey. GTOPO30: global 30 arc second elevation data. Global http://eros.usgs.gov/#/Find-Data/Products-and-Data-Available/gtopo30- info. Accessed 1 September 2010.
30. Olson DM, Dinerstein E. The Global 200: priority ecoregions for global conservation. Ann Mo Bot Gard 2009; 89:125-6.
31. Diggle P, Moyeed R, Tawn J. Model-based geostatistics (with discussion). Appl Stat 1998; 47:299-350. (Pubitemid 128076703)
32. Rabe-Hesketh S, Skrondal A. Multilevel and longitudinal modelling using Stata. 2nd ed. College Station, TX: Stata Press, 2008.
33. Hillier SD, Booth M, Muhangi L, et al. Plasmodium falciparum and helminth coinfection in a semi urban population of pregnant women in Uganda. J Infect Dis 2008; 198:920-7.
34. Mazigo HD, Waihenya R, Lwambo NJ, et al. Co-infections with Plasmodium falciparum, Schistosoma mansoni and intestinal helminths among school children in endemic areas of northwestern Tanzania. Parasit Vectors 2010; 3:44.
35. Midzi N, Sangweme D, Zinyowera S, et al. The burden of polyparasitism among primary school children in rural and farming areas in Zimbabwe. Trans R Soc Trop Med Hyg 2008; 102: 1039-45.
36. 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; 92:1191-5.
37. Hay SI, Guerra CA, Gething PW, et al. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 2009; 6:e1000048.
38. Brooker S, Hotez PJ, Bundy DA. The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PLoS Negl Trop Dis 2010; 4:e779.
39. Pullan RL, Gething PW, Smith JL, et al. Spatial modelling of soiltransmitted helminths in Kenya: a disease control planning tool. PLoS Negl Trop Dis 2011; 5:e958.
40. Raso G, Vounatsou P, Singer BH, N'Goran EK, Tanner M, Utzinger J. An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm coinfection. Proc Natl Acad Sci USA 2006; 103:6934-9.
41. Schur N, Gosoniu L, Raso G, Utzinger J, Vounatsou P. Modelling the geographical distribution of co-infection risk from single-disease surveys. Stat Med 2011; 30:1761-76.
42. Yatich NJ, Yi J, Agbenyega T, et al. Malaria and intestinal helminth co-infection among pregnant women in Ghana: prevalence and risk factors. Am J Trop Med Hyg 2009; 80:896-901.
43. Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis 2009; 200:1509-17.
44. Booth M, Vounatsou P, N'Goran EK, Tanner M, Utzinger J. The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm coinfections in rural Cote d'Ivoire. Parasitology 2003; 127:525-31. (Pubitemid 38091103)
45. Taylor SM, Juliano JJ, Trottman PA, et al. High-throughput pooling and real-time PCR-based strategy for malaria detection. J Clin Microbiol 2010; 48:512-9.