Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-22T10:10:52.837Z Has data issue: false hasContentIssue false
  • English
  • Français

The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases?

Published online by Cambridge University Press:  27 March 2008

R. PULLAN  and
S. BROOKER
R. PULLAN*
Affiliation:
Department of Infectious and Tropical Disease, London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
S. BROOKER
Affiliation:
Malaria Public Health and Epidemiology Group, Centre for Geographic Medicine, KEMRI/Wellcome Trust Research Laboratories, Nairobi, Kenya
*
Corresponding author: Rachel Pullan, Department of Infectious and Tropical Disease, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK. Email: rachel.pullan@lshtm.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Parasitic infections are widespread throughout the tropics and sub-tropics, and infection with multiple parasite species is the norm rather than the exception. Despite the ubiquity of polyparasitism, its public health significance has been inadequately studied. Here we review available studies investigating the nutritional and pathological consequences of multiple infections with Plasmodium and helminth infection and, in doing so, encourage a reassessment of the disease burden caused by polyparasitism. The available evidence is conspicuously sparse but is suggestive that multiple human parasite species may have an additive and/or multiplicative impact on nutrition and organ pathology. Existing studies suffer from a number of methodological limitations and adequately designed studies are clearly necessary. Current methods of estimating the potential global morbidity due to parasitic diseases underestimate the health impact of polyparasitism, and possible reasons for this are presented. As international strategies to control multiple parasite species are rolled-out, there is a number of options to investigate the complexity of polyparasitism, and it is hoped that that the parasitological resarch community will grasp the opportunity to understand better the health of polyparasitism in humans.

Keywords

polyparasitismhelminthsmalariamorbidityundernutritionanaemiadisease burden
Type
Original Articles
Information
Parasitology , Volume 135 , Special Issue 7: Parasitic co-infections: challenges and solutions , June 2008 , pp. 783 - 794
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abdel-Salam, E., Abdel Khalik, A., Abdel-Meguid, A., Barakat, W. and Mahmoud, A. A. (1986). Association of HLA class I antigens (A1, B5, B8 and CW2) with disease manifestations and infection in human schistosomiasis mansoni in Egypt. Tissue Antigens 27, 142–146.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press, 374–429.CrossRefGoogle Scholar
Asobayire, F. S., Adou, P., Davidsson, L., Cook, J. D. and Hurrell, R. F. (2001). Prevalence of iron deficiency with and without concurrent anemia in population groups with high prevalences of malaria and other infections: a study in Cote d'Ivore. American Journal of Clinical Nutrition 74, 776–782.CrossRefGoogle Scholar
Beisel, W. R. (1996). Nutrition in pediatric HIV infection: Setting the research agenda. Nutrition and immune function: Overview. Journal of Nutrition 126, 2611–2615.Google Scholar
Bloem, M. W., Wedel, M., Van Agtmaal, E. J., Speek, A. J., Soawakontha, S. and Schreurs, W. H. P. (1990). Vitamin A intervention: short term effects of a single oral massive dose on iron metabolism. American Journal of Clinical Nutrition 51, 76–79.CrossRefGoogle ScholarPubMed
Boivin, M. J. and Giordani, B. (1993). Improvements in cognitive performance for schoolchildren in Zaire, Africa, following an iron supplement and treatment for intestinal parasites. Journal of Pediatric Psychology 18, 249–264.Google Scholar
Boivin, M. J., Giordani, B., Ndanga, K., Maky, M. M., Manzeki, K. M., Ngunu, N. and Muamba, K. (1993). Effects of treatment for intestinal parasites and malaria on the cognitive abilities of schoolchildren in Zaire, Africa. Health Psychology 12, 220–226.CrossRefGoogle ScholarPubMed
Booth, M. (1998). The application of attributable risk analysis in helminth epidemiology. Parasitology Today 14, 497–500.CrossRefGoogle ScholarPubMed
Booth, M. and Bundy, D. A. (1995). Estimating the number of multiple-species geohelminth infections in human communities. Parasitology 111, 645–653.CrossRefGoogle ScholarPubMed
Booth, M., Bundy, D. A., Albonico, M., Chwaya, H. M., Alawi, K. S. and Savioli, L. (1998 a). Associations among multiple geohelminth species infections in schoolchildren from Pemba Island. Parasitology 116, 85–93.Google Scholar
Booth, M., Mayombana, C. and Kilima, P. (1998 b). The population biology and epidemiology of schistosome and geohelminth infections among schoolchildren in Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 491–495.CrossRefGoogle ScholarPubMed
Booth, M., Vennervald, B. J., Butterworth, A. E., Kariuki, H. C., Amaganga, C., Kimani, G., Mwatha, J. K., Otedo, A., Ouma, J. H. and Dunne, D. W. (2004 a). Exposure to malaria affects the regression of hepatosplenomegaly after treatment for Schistosoma mansoni infection in Kenyan children. BMC Medicine 2, 36.CrossRefGoogle ScholarPubMed
Booth, M., Vennervald, B. J., Kenty, L., Butterworth, A. E., Kariuki, H. C., Kadzo, H., Ireri, E., Amaganga, C., Kimani, G., Mwatha, J. K., Otedo, A., Ouma, J. H., Muchiri, E. and Dunne, D. W. (2004 b). Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children. BMC Infectious Diseases 4, 13.CrossRefGoogle ScholarPubMed
Bradley-Moore, A. M., Greenwood, B. M., Bradley, A. K., Kirkwood, B. R. and Gilles, H. M. (1985). Malaria chemoprophylaxis with chloroquine in young Nigerian children. III. Its effect on nutrition. Annals of Tropical Medicine and Parasitology 79, 575–584.CrossRefGoogle ScholarPubMed
Brito, L. L., Barreto, M. L., Silva, R. D. E. C., Assis, A. M., Reis, M. G., Parraga, I. M. and Blanton, R. E. (2006). Moderate- and low-intensity co-infections by intestinal helminths and Schistosoma mansoni, Dietary iron intake, and anemia in Brazilian Children. American Journal of Tropical Medicine and Hygiene 75, 939–944.Google Scholar
Brooker, S., Akhwale, W. S., Pullan, R., Estambale, B., Clarke, S. and Hotez, P. J. (2007). Epidemiology of Plasmodium-Helminth coinfection in Africa: potential impact on anaemia and prospects for combining control. American Journal of Tropical Medicine and Hygiene 77, 88–98.Google Scholar
Brooker, S., Miguel, E. A., Moulin, S., Luoba, A. I., Bundy, D. A. and Kremer, M. (2000). Epidemiology of single and multiple species of helminth infections among school children in Busia District, Kenya. East African Medicine Journal 77, 157–161.Google ScholarPubMed
Buck, A. A., Anderson, R. I. and Macrae, A. A. (1978). Epidemiology of poly-parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities in Chad, Peru, Afghanistan, and Zaire. Tropenmedizin und Parasitologie 29, 61–70.Google ScholarPubMed
Bundy, D. A. (1995). Epidemiology and transmission of helminths. In Enteric Infections & Intestinal Helminths. London: Chapman and Hall Medical 5-24.Google Scholar
Bundy, D. A. and Guyatt, H. L. (1996). Schools for health: Focus on health, education and the school-age child. Parasitology Today 12, suppl 1–16.Google Scholar
Bundy, D. A. and Medley, G. F. (1992). Immuno-epidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden. Parasitology 104 (Suppl), S105–S119.Google Scholar
Bundy, D. A. P. (1988). Population ecology of intestinal helminth infections in human communities. Philosphical Transactions of the Royal Society (Series B) 321, 405–420.Google Scholar
Bundy, D. A. P. and Cooper, E. S. (1989). Trichuris and trichuriasis in humans. Advances in Parasitology 28, 107–173.Google Scholar
Chamone, M., Marques, C. A., Atuncar, G. S., Pereira, A. L. and Pereira, L. H. (1990). Are there interactions between schistosomes and intestinal nematodes Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 557–558.Google Scholar
Crompton, D. W. and Nesheim, M. C. (2002). Nutritional impact of intestinal helminthiasis during the human life cycle. Annual Review of Nutrition 22, 35–59.CrossRefGoogle ScholarPubMed
Das, B. S., Thurnham, D. I. and Das, D. B. (1997). Influence of malaria on markers of iron status in children: implications for interpreting iron status in malaria-endemic communities. British Journal of Nutrition 78, 751–760.CrossRefGoogle ScholarPubMed
Drake, L. J. and Bundy, D. A. (2001). Multiple helminth infections in children: impact and control. Parasitology 122 (Suppl), S73–S81.Google Scholar
Druilhe, P., Tall, A. and Sokhna, C. (2005). Worms can worsen malaria: towards a new means to roll back malaria Trends in Parasitology 21, 359–362.Google Scholar
Egwunyenga, A. O., Ajayi, J. A., Nmorsi, O. P. and Duhlinska-Popova, D. D. (2001). Plasmodium/intestinal helminth co-infections among pregnant Nigerian women. Memórias do Instituto Oswaldo Cruz 96, 1055–1059.Google Scholar
Engels, D. and Savioli, L. (2006). Reconsidering the underestimated burden caused by neglected tropical diseases. Trends in Parasitology 22, 363–366.CrossRefGoogle ScholarPubMed
Ezeamama, A. E., Friedman, J. F., Olveda, R. M., Acosta, L. P., Kurtis, J. D., Mor, V. and McGarvey, S. T. (2005). Functional significance of low-intensity polyparasite helminth infections in anemia. Journal of Infectious Diseases 192, 2160–2170.Google Scholar
Faulkner, H., Turner, J., Behnke, J., Kamgno, J., Rowlinson, M. C., Bradley, J. E. and Boussinesq, M. (2005). Associations between filarial and gastrointestinal nematodes. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 301–312.Google Scholar
Ferreira, C. S., Ferreira, M. U. and Nogueira, M. R. (1994). The prevalence of infection by intestinal parasites in an urban slum in Sao Paulo, Brazil. Journal of Tropical Medicine and Hygiene 97, 121–127.Google Scholar
Fleming, F. M., Brooker, S., Geiger, S. M., Caldas, I. R., Correa-Oliveira, R., Hotez, P. J. and Bethony, J. M. (2006). Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Tropical Medicine and International Health 11, 56–64.Google Scholar
Friedman, J. F., Kanzaria, H. K. and McGarvey, S. T. (2005). Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology 21, 386–392.CrossRefGoogle ScholarPubMed
Friedman, J. F., Phillips-Howard, P. A., Hawley, W. A., Terlouw, D. J., Kolczak, M. S., Barber, M., Okello, N., Vulule, J. M., Duggan, C., Nahlen, B. L. and Ter Kuile, F. O. (2003). Impact of permethrin-treated bed nets on growth, nutritional status, and body composition of primary school children in Western Kenya. American Journal of Tropical Medicine and Hygiene 68, 78–85.Google Scholar
Friis, H., El Karib, S. A., Sulaiman, S. M., Rahama, A., Magnussen, P. and Mascie-Taylor, C. G. (2000). Does Schistosoma haematobium co-infection reduce the risk of malaria-induced splenomegaly Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 535–536.CrossRefGoogle ScholarPubMed
Friis, H., Ndhlovu, I., Kaondera, K., Franke, D., Vennervald, B. J., Christensen, N. and Doehring, E. (1996). Ultrasonographic assessment of Schistosoma mansoni and S. haematobium morbidity in Zimbabwean schoolchildren. American Journal of Tropical Medicine and Hygiene 55, 290–294.Google Scholar
Fulford, A., Mbugua, G., Ouma, J. H., Kariuki, H. C., Sturrock, R. F. and Butterworth, A. E. (1991). Differences in the rate of hepatosplenomegaly due to Schistosoma mansoni infection between two areas in Machakos District, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 481–488.Google Scholar
Gibson, R. S. (2005). Assessment of iron status. In Principles of Nutritional Assessment. Oxford University Press, New York, 443–476.CrossRefGoogle Scholar
Gold, M. R., Stevenson, D. and Fryback, D. G. (2002). HALYS and QALYS and DALYS, Oh My: similarities and differences in summary measures of population Health. Annual Review of Public Health 23, 115–134.Google Scholar
Grobusch, M. P. and Kremsner, P. G. (2005). Uncomplicated malaria. Current Topics in Microbiology and Immunology 295, 83–104.Google Scholar
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. Lancet 368, 1106–1118.CrossRefGoogle ScholarPubMed
Guyatt, H. (2000). Do intestinal nematodes affect productivity in adulthood Parasitology Today 16, 153–158.CrossRefGoogle ScholarPubMed
Haas, J. D. and Brownlie, T. T. (2001). Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. Journal of Nutrition 131, 676S–690S.Google Scholar
Hartgers, F. C. and Yazdanbakhsh, M. (2006). Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunology 28, 497–506.CrossRefGoogle ScholarPubMed
Haswell-Elkins, M. R., Elkins, D. B. and Anderson, R. M. (1987). Evidence for predisposition in humans to infection with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community. Parasitology 95, 323–337.Google Scholar
Hlaing, T. (1993). Ascariasis and childhood malnutrition. Parasitology 107 (Suppl), S125–S136.Google Scholar
Hodges, R. E., Sauberlich, H. E. and Canham, J. E. E. A. (1978). Hematopoietic studies in Vitamin A deficiency. American Journal of Clinical Nutrition 31, 876–885.CrossRefGoogle ScholarPubMed
Holland, C. V., Asaolu, S. O., Crompton, D. W., Stoddart, R. C., MacDonald, R. and Torimiro, S. E. (1989). The epidemiology of Ascaris lumbricoides and other soil-transmitted helminths in primary school children from Ile-Ife, Nigeria. Parasitology 99, 275–285.Google Scholar
Hotez, P. J., Brooker, S., Bethony, J. M., Bottazzi, M. E., Loukas, A. and Xiao, S. (2004). Hookworm infection. New England Journal of Medicine 351, 799–807.Google Scholar
Hotez, P. J., Bundy, D. A. P., Beegle, K., Brooker, S., Drake, L., De Silva, N., Montresor, A., Engels, D., Jukes, M., Chitsulo, L., Chow, J., Laxminarayan, R., Michaud, C., Bethony, J., Oliveira, R., Xiao, S. H., Fenwick, A. and Savioli, L. (2006). Helminth Infections: soil-transmitted helminth infections and schistosomiasis. In Disease Control Priorities in Developing Countries (eds. Jamison, D. T., Breman, J. G., Measham, A. R., Alleyne, G., Claeson, M., Evans, D. B., Jha, P., Mills, A. and Musgrove, P.), pp. 467–497. Oxford University Press, New York.Google Scholar
Howard, S. C., Donnelly, C. A. and Chan, M. S. (2001). Methods for estimation of associations between multiple species parasite infections. Parasitology 122, 233–251.CrossRefGoogle ScholarPubMed
Howard, S. C., Donnelly, C. A., Kabatereine, N. B., Ratard, R. C. and Brooker, S. (2002). Spatial and intensity-dependent variations in associations between multiple species helminth infections. Acta Tropica 83, 141–149.Google Scholar
Ing, R., Su, Z., Scott, M. E. and Koski, K. G. (2000). Suppressed T helper 2 immunity and prolonged survival of a nematode parasite in protein-malnourished mice. Proceedings of the National Academy of Sciences, USA 97, 7078–7083.Google Scholar
Keiser, J., N'goran, E. K., Singer, B. H., Lengeler, C., Tanner, M. and Utzinger, J. (2002). Association between Schistosoma mansoni and hookworm infections among schoolchildren in Cote d'Ivoire. Acta Tropica 84, 31–41.CrossRefGoogle ScholarPubMed
Kightlinger, L. K., Seed, J. R. and Kightlinger, M. B. (1995). The epidemiology of Ascaris lumbricoides, Trichuris trichiura, and hookworm in children in the Ranomafana rainforest, Madagascar. Journal of Parasitology 81, 159–169.CrossRefGoogle ScholarPubMed
Kihara, M., Carter, J. A. and Newton, C. R. (2006). The effect of Plasmodium falciparum on cognition: a systematic review. Tropical Medicine and International Health 11, 386–397.Google Scholar
King, C. H., Dickman, K. and Tisch, D. J. (2005). Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561–1569.CrossRefGoogle ScholarPubMed
Kloos, H., Fulford, A. J., Butterworth, A. E., Sturrock, R. F., Ouma, J. H., Kariuki, H. C., Thiongo, F. W., Dalton, P. R. and Klumpp, R. K. (1997). Spatial patterns of human water contact and Schistosoma mansoni transmission and infection in four rural areas in Machakos District, Kenya. Social Science and Medicine 44, 949–968.CrossRefGoogle ScholarPubMed
Korenromp, E. L., Armstrong-Schellenberg, J. R., Williams, B. G., Nahlen, B. L. and Snow, R. W. (2004). Impact of malaria control on childhood anaemia in Africa – a quantitative review. Tropical Medicine and International Health 9, 1050–1065.Google Scholar
Koski, K. G. and Scott, M. E. (2001). Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annual Review of Nutrition 21, 297–321.Google Scholar
Koski, K. G., Su, Z. and Scott, M. E. (1999). Energy deficits suppress both systemic and gut immunity during infection. Biochemical and Biophysics Research Communications 264, 796–801.Google Scholar
Kurtzhals, J. A., Addae, M. M., Akanmori, B. D., Dunyo, S., Koram, K. A., Appawu, M. A., Nkrumah, F. K. and Hviid, L. (1999). Anaemia caused by asymptomatic Plasmodium falciparum infection in semi-immune African schoolchildren. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 623–627.CrossRefGoogle ScholarPubMed
Mahalanabis, D., Simpson, T. W., Chakraborty, M. L., Ganguli, C., Bhattacharjee, A. K. and Mukherjee, K. L. (1979). Malabsorption of water miscible vitamin A in children with giardiasis and ascariasis. American Journal of Clinical Nutrition 32, 313–318.Google Scholar
Mathers, C. D., Lopez, A. D. and Murray, C. J. L. (2006). Global Burden of Disease and Risk Factors. New York: Oxford University Press.Google Scholar
McDevitt, M. A., Xie, J., Gordeuk, V. and Bucala, R. (2004). The anemia of malaria infection: role of inflammatory cytokines. Current Hematology Reports 3, 97–106.Google ScholarPubMed
McGregor, I. A., Gilles, H. M., Walters, J. H., Davies, A. H. and Pearson, F. A. (1956). Effects of heavy and repleted malarial infections on Gambian infants and children. Effects of erythrocyte parasitization. British Medical Journal 2, 686–692.Google Scholar
Meakins, R. H., Harland, P. S. and Carswell, F. (1981). A preliminary survey of malnutrition and helminthiasis among schoolchildren in one mountain and one lowland ujamaa village in Northern Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 731–735.Google Scholar
Menendez, C., Fleming, A. F. and Alonso, P. L. (2000). Malaria-related anaemia. Parasitology Today 16, 469–476.Google Scholar
Menendez, C., Quinto, L. L., Kahigwa, E., Alvarez, L., Fernandez, R., Gimenez, N., Schellenberg, D., Aponte, J. J., Tanner, M. and Alonso, P. L. (2001). Effect of malaria on soluble transferrin receptor levels in Tanzanian infants. American Journal of Tropical Medicine and Hygiene 65, 138–142.Google Scholar
Mott, K. E. (2004). Schistosomaisis. In The Global Epidemiology of Infectious Diseases (eds. Murray, C. J. L., Lopez, A. D. and Mathers, C. D.), WHO: Geneva.Google Scholar
Murray, C. J. and Lopez, A. D. (1994). Quantifying disability: data, methods and results. Bulletin of the World Health Organisation 72, 481–494.Google Scholar
Murray, C. J. and Lopez, A. D. (1996). Evidence-based health policy – lessons from the Global Burden of Disease Study. Science 274, 740–743.Google Scholar
Mwangi, T. W., Bethony, J. M. and Brooker, S. (2006). Malaria and helminth interactions in humans: an epidemiological viewpoint. Annals of Tropical Medicine and Parasitology 100, 551–570.Google Scholar
Mwatha, J. K., Jones, F. M., Mohamed, G., Naus, C. W., Riley, E. M., Butterworth, A. E., Kimani, G., Kariuki, C. H., Ouma, J. H., Koech, D. and Dunne, D. W. (2003). Associations between anti-Schistosoma mansoni and anti-Plasmodium falciparum antibody responses and hepatosplenomegaly, in Kenyan schoolchildren. Journal of Infectious Disease 187, 1337–1341.Google Scholar
Nacher, M. (2004). Interactions between worm infections and malaria. Clinical Reviews in Allergy and Immunology 26, 85–92.Google Scholar
Needham, C., Kim, H. T., Hoa, N. V., Cong, L. D., Michael, E., Drake, L., Hall, A. and Bundy, D. A. (1998). Epidemiology of soil-transmitted nematode infections in Ha Nam Province, Vietnam. Tropical Medicine and International Health 3, 904–912.Google Scholar
Newman, R. D., Parise, M. E., Slutsker, L., Nahlen, B. and Steketee, R. W. (2003). Safety, efficacy and determinants of effectiveness of antimalarial drugs during pregnancy: implications for prevention programmes in Plasmodium falciparum-endemic sub-Saharan Africa. Tropical Medicine and International Health 8, 488–506.Google Scholar
Nkuo-Akenji, T. K., Chi, P. C., Cho, J. F., Ndamukong, K. K. J. and Sumbele, I. (2006). Malaria and helminth co-infection in children living in a malaria endemic setting of Mount Cameroon and predictors of anaemia. Journal of Parasitology 92, 1191–1195.Google Scholar
Nyakeriga, A. M., Troye-Blomberg, M., Chemtai, A. K., Marsh, K. and Williams, T. N. (2004). Malaria and nutritional status in children living on the coast of Kenya. American Journal of Clinical Nutrition 80, 1604–1610.Google Scholar
Odunukwe, N. N., Salako, L. A., Okany, C. and Ibrahim, M. M. (2000). Serum ferritin and other haematological measurements in apparently healthy adults with malaria parasitaemia in Lagos, Nigeria. Tropical Medicine and International Health 5, 582–586.CrossRefGoogle ScholarPubMed
Persson, V., Ahmed, F., Gebre-Medhin, M. and Greiner, T. (2000). Relationships between vitamin A, iron status and helminthiasis in Bangladeshi school children. Public Health Nutrition 3, 83–89.Google Scholar
Rogerson, S. J., Chaluluka, E., Kanjala, M., Mkundika, P., Mhango, C. and Molyneux, M. E. (2000). Intermittent sulfadoxine-pyrimethamine in pregnancy: effectiveness against malaria morbidity in Blantyre, Malawi, in 1997–99. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 549–553.CrossRefGoogle ScholarPubMed
Saldiva, S. R., Silveira, A. S., Philippi, S. T., Torres, D. M., Mangini, A. C., Dias, R. M., Da Silva, R. M., Buratini, M. N. and Massad, E. (1999). Ascaris-Trichuris association and malnutrition in Brazilian children. Paediatric and Perinatal Epidemiology 13, 89–98.Google Scholar
Schaible, U. E. and Kaufman, S. H. E. (2007). Malnutrition and infection: Complex mechanisms and global impacts. Public Library of Science Medicine 4, 806–812.Google Scholar
Shulman, C. E., Dorman, E. K., Cutts, F., Kawuondo, K., Bulmer, J. N., Peshu, N. and Marsh, K. (1999). Intermittent sulphadoxine-pyrimethamine to prevent severe anaemia secondary to malaria in pregnancy: a randomised placebo-controlled trial. Lancet 353, 632–636.Google Scholar
Snow, R. W., Molyneux, C. S., Njeru, E. K., Et Al Omumbo, J., Nevill, C. G., Muniu, E. and Marsh, K. (1997). The effects of malaria control on nutritional status in infancy. Acta Tropica 65, 1–10.Google Scholar
Sommer, A. and West, K. P. J. (1996). Vitamin A Deficiency: Health, Survival and Vision. New York: Oxford University Press.Google Scholar
Stephenson, L. S., Holland, C. V. and Cooper, E. S. (2000 a). The public health significance of Trichuris trichiura. Parasitology 121 (Suppl), S73–S95.Google Scholar
Stephenson, L. S., Latham, M. C., Kurz, K. M., Kinoti, S. N., Oduori, M. L. and Crompton, D. W. (1985). Relationships of Schistosoma hematobium, hookworm and malarial infections and metrifonate treatment to hemoglobin level in Kenyan school children. American Journal of Tropical Medicine and Hygiene 34, 519–528.Google Scholar
Stephenson, L. S., Latham, M. C. and Ottesen, E. A. (2000 b). Malnutrition and parasitic helminth infections. Parasitology 121 (Suppl), S23–S38.Google Scholar
Stoltzfus, R. J., Chwaya, H. M., Albonico, M., Schulze, K. J., Savioli, L. and Tielsch, J. M. (1997 a). Serum ferritin, erythrocyte protoporphyrin and hemoglobin are valid indicators of iron status of school children in a malaria-holoendemic population. Journal of Nutrition 127, 293–298.Google Scholar
Stoltzfus, R. J., Chwaya, H. M., Montresor, A., Albonico, M., Savioli, L. and Tielsch, J. M. (2000). Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age. Journal of Nutrition 130, 1724–1733.Google Scholar
Stoltzfus, R. J., Chwaya, H. M., Tielsch, J. M., Schulze, K. J., Albonico, M. and Savioli, L. (1997 b). Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. American Journal of Clinical Nutrition 65, 153–159.Google Scholar
Stoltzfus, R. J., Dreyfuss, M. L., Chwaya, H. M. and Albonico, M. (1997 c). Hookworm control as a strategy to prevent iron deficiency. Nutrition Reviews 55, 223–232.Google Scholar
Suharno, D., West, C. E., Muhilal Karyadi, D. and Hautvast, G. A. J. (1993). Supplementation with vitamin A and iron for nutritional anaemia in pregnant women in West Java, Indonesia. Lancet 342, 1325–1328.Google Scholar
Tchuem Tchuente, L. A., Behnke, J. M., Gilbert, F. S., Southgate, V. R. and Vercruysse, J. (2003). Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine and International Health 8, 975–986.Google Scholar
Ter Kuile, F., Terlouw, D. J. and Kariuki, S., et al. (2003). Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya. American Journal of Tropical Medicine and Hygiene 68, 68–77.Google Scholar
Tracey, K. J. and Cerami, A. (1992). Tumor necrosis factor in the malnutrition (cachexia) of infection and cancer. American Journal of Tropical Medicine and Hygiene 47, 2–7.Google Scholar
Tripathy, K., Duque, E., Bolanos, O., Lotero, H. and Mayoral, L. G. (1972). Malabsorption syndrome in ascariasis. American Journal of Clinical Nutrition 25, 1276–1281.Google Scholar
UNICEF (2004). The State of the World's Children 2005: childhood under threat. New York: UNICEF.Google Scholar
Vennervald, B. J. and Dunne, D. W. (2004). Morbidity in schistosomiasis: an update. Current Opinions in Infectious Disease 17, 439–447.Google Scholar
Verhoef, H., West, C. E., Ndeto, P., Burema, Y. and Kok, F. J. (2001). Serum transferrin receptor concentration indicates increased erythropoiesis in Kenyan children with asymptomatic malaria. American Journal of Clinical Nutrition 74, 767–775.Google Scholar
Walker, S. P., Wachs, T. D., Gardner, J. M., Lozoff, B., Wasserman, G. A., Pollitt, E. and Carter, J. A. (2006). Child development: risk factors for adverse outcomes in developing countries. Lancet 369, 145–157.Google Scholar
Whittle, H. C., Gelfand, M., Sampson, E., Purvis, A. and Weber, M. (1969). Enlarged livers and spleens in an area endemic for malaria and schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 353–361.Google Scholar
WHO (2002 a). Quantifying selected major risks to health. In The World Health Report 2002 – Reducing Risks, Promoting Healthy Life. World Health Organisation: Geneva.Google Scholar
WHO (2002 b). Report of the WHO informal consultation on the use of Praziquantel during pregnancy/lactation and albendazole/mebendazole in children under 24 months. World Health Organisation: Geneva.Google Scholar
WHO (2004). The Global Epidemiology of Infectious Diseases, World Health Organisation: Geneva.Google Scholar
Wilson, S., Vennervald, B. J., Kadzo, H., Ireri, E., Amaganga, C., Booth, M., Kariuki, C., Mwatha, J., Kimani, G., Ouma, J. H., Muchiri, E. and Dunne, D. W. (2007). Hepatosplenomegaly in Kenyan schoolchildren: exacerbation by concurrent chronic exposure to malaria and Schistosoma mansoni infection. Tropical Medicine and International Health 12, 1442–1449.Google Scholar