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The association between multiple intestinal helminth infections and blood group, anaemia and nutritional status in human populations from Dore Bafeno, southern Ethiopia

  • A. Degarege (a1), A. Animut (a1), G. Medhin (a1), M. Legesse (a1) and B. Erko (a1)...


In this cross-sectional study, the associations between helminth infections and ABO blood group, anaemia and undernutrition were investigated in 480 febrile outpatients who visited Dore Bafeno Health Centre, southern Ethiopia, in December 2010. Stool specimens were processed using the Kato–Katz method and examined for intestinal helminth infections. Haemoglobin level was measured using a HemoCue machine and blood group was determined using an antisera haemagglutination test. Nutritional status of the study participants was assessed using height and weight measurements. Among the study participants, 50.2% were infected with intestinal helminths. Ascaris lumbricoides (32.7%), Trichuris trichiura (12.7%), Schistosoma mansoni (11.9%) and hookworm (11.0%) were the most frequently diagnosed helminths. The odds of infection and mean eggs per gram of different intestinal helminth species were comparable between the various blood groups. Among individuals who were infected with intestinal helminth(s), the mean haemoglobin level was significantly lower in individuals harbouring three or more helminth species and blood type AB compared to cases with double or single helminth infection and blood type O, respectively. The odds of being underweight was significantly higher in A. lumbricoides and T. trichiura infected individuals of age ≤ 5 and ≥ 20 years, respectively, when compared to individuals of the matching age group without intestinal helminths. In conclusion, infection with multiple intestinal helminths was associated with lower haemoglobin level, which was more severe in individuals with blood type AB. Future studies should focus on mechanisms by which blood group AB exacerbates the helminth-related reduction in mean haemoglobin level.


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Assis, A.M., Prado, M.S., Barreto, M.L., Reis, M.G., Conceicao Pinheiro, S.M., Rraga, I.M. & Blanton, R.E. (2004) Childhood stunting in Northeast Brazil: the role of Schistosoma mansoni infection and in adequate dietary intake. European Journal of Clinical Nutrition 58, 10221029.
Brito, L.L., Barreto, M.L., Silva Rde, C., Assis, A.M., Reis, M.G., Parraga, I.M. & 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, 939944.
Brooker, S., Peshu, N., Warn, P.A., Mosobo, M., Guyatt, H.L., Marsh, K. & Snow, R.W. (1999) The epidemiology of hookworm infection and its contribution to anaemia among pre-school children on the Kenyan coast. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 240246.
Brooker, S., Akhwale, W.S., Pullan, R., Estambale, B., Clarke, S., Snow, R.W. & Hotez, P.J. (2007) Epidemiology of Plasmodium–helminth co-infeciton in Africa: potential impact on anaemia and prospects for combining control. American Journal of Tropical Medicine and Hygiene 77, 8898.
Camus, D., Bina, J.C., Carlier, Y. & Santoro, F. (1977) ABO blood groups and clinical forms schistosomiasis mansoni (letter). Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 182.
Cooper, P.J., Guevara, A. & Guderian, R.H. (1993) Intestinal helminthiases in Ecuador: the relationship between prevalence, genetic, and socioeconomic factors. Revista da Sociedade Brasileira de Medicina Tropical 26, 175180.
Curtale, F., Abdel-Fattah, M., el-Shazly, M., Shamy, M.Y. & el-Sahn, F. (2000) Anaemia among young male workers in Alexandria, Egypt. East Mediterranean Health Journal 6, 10051016.
Dean, D. (1974) Schistosoma mansoni: adsorption of human blood group A and B antigens by schistosomula. Journal of Parasitology 60, 260263.
Degarege, A., Animut, A., Legesse, M. & Erko, B. (2009) Malaria severity status in patients with soil-transmitted helminth infections. Acta Tropica 112, 811.
Degarege, A., Animut, A., Legesse, M. & Erko, B. (2010) Malaria and helminth co-infections in outpatients of Alaba Kulito Health Center, southern Ethiopia: a cross sectional study. BMC Research Notes 3, 143149.
Degarege, A., Girmay, M., Animut, A., Legesse, M.A. & Erko, B. (2012) Association of ABO blood group and malaria related outcomes: a cross-sectional study in Ethiopia. Acta Tropica 123, 164169.
Deleon, P.P. & Valverdeh, J. (2003) P System antigenic determiners expression in Ascaris lumbricoides. Revista do Instituto de Medicina Tropical de Sao Paulo 45, 5354.
Deleon, P.P., Foresto, P., Zdero, M. & Valverdeh, J. (2000) Preliminary studies on antigenic mimicry of Ascaris lumbricoides. Revista do Instituto de Medicina Tropical de Sao Paulo 42, 295296.
El Masri, S.H. & Sharfi, A.R.M. (1982) ABO blood groups in hepatosplenic schistosomiasis. Journal of Tropical Medicine and Hygiene 85, 223224.
Ezeamama, A.E., Friedman, J.F., Olveda, R.M., Acosta, L.P., Kurtis, J.D., Mor, V. & McGarvey, S.T. (2005) Functional significance of low-intensity polyparasite helminth infections in anemia. Journal of Infectious Diseases 192, 21602170.
Ezeamama, A.E., McGarvey, S.T., Acosta, L.P., Zierler, S., Manalo, D.L., Wu, H.W., Kurtis, J.D., Mor, V., Olveda, R.M. & Friedman, J.F. (2008) The synergistic effect of concomitant schistosomiasis, hookworm, and Trichuris infections on children's anemia burden. PLoS Neglected Tropical Diseases 2, 245253.
Faulkner, H., Turner, J., Behnke, J., Kamgno, J., Rowlinson, M.C., Bradley, J.E. & Boussinesq, M. (2005) Associations between filarial and gastrointestinal nematodes. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 301312.
Friedman, J.F., Kanzaria, H.K. & McGarvey, S.T. (2005) Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology 21, 386392.
Gabr, N.S. & Mandour, A.M. (1991) Relation of parasitic infection to blood group in El Minia Governorate, Egypt. Journal of Egyptian Society of Parasitology 21, 679683.
Haseeb, M.A., Thors, C., Linder, E. & Eveland, L.K. (2008) Schistosoma mansoni: Chemoreception through N-acetyl-d-galactosamine-containing receptors in females offers insight into increased severity of schistosomiasis in individuals with blood group A. Experimental Parasitology 119, 6773.
Jardim-Botelho, A., Brooker, S., Geiger, S.M., Fleming, F., Lopes, A.C.S., Diemert, D.J., Correa-Oliveira, R. & Bothony, J.M. (2008) Age-patterns in undernutrition and helminth infection in a rural area of Brazil: associations with Ascaris and hookworm. Tropical Medicine and International Health 13, 458467.
Katz, N., Tavares, J. & Abrantes, W.L. (1976) ABO and Rh blood groups from patients with hepatosplenic schistosomiasis mansoni. Journal of Parasitology 53, 99.
Khattab, M., El-Gengehy, M.T. & Sharaf, M. (1968) ABO blood groups in bilharzial hepatic fibrosis. Journal of the Egyptian Medical Association 208, 11451148.
Knopp, S., Mgeni, A.F., Khamis, I.S., Steinmann, P., Stothard, J.R. & Rollinson, D. (2008) Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Neglected Tropical Disease 2, 331334.
Koukounari, A., Fenwick, A., Whawell, S., Kabatereine, N.B., Kazibwe, F., Tukahebwa, E.M., Stothard, J.R., Donnelly, C.A. & Webster, J.P. (2006) Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. American Journal of Tropical Medicine and Hygiene 75, 278286.
Marini, E., Maldonado-Contreras, A.L., Cabras, S., Hidalgo, G., Buffa, R., Marin, A. & Floris, G. (2007) Helicobacter pylori and intestinal parasites are not detrimental to the nutrition status of Amerindians. American Journal of Tropical Medicine and Hygiene 76, 534540.
May, R.M. & Anderson, R.M. (1979) Population biology of infectious diseases: part II. Nature 280, 455461.
Mupfasoni, D., Karibushi, B., Koukounari, A., Ruberanziza, E., Kaberuka, T., Kramer, M.H., Mukabayire, O., Kabera, M., Nizeyimana, V., Deville, M.A., Ruxin, J., Webster, J.P. & Fenwick, A. (2009) Polyparasite helminth infections and their association to anaemia and undernutrition in Northern Rwanda. PLoS Neglected Tropical Diseases 3, 517526.
Ndamba, J., Gomo, J.E., Nyazema, N., Makaza, N. & Kaondera, K.C. (1997) Schistosomiasis infection in relation to the ABO blood groups among school children in Zimbabwe. Acta Tropica 65, 181190.
Oliver-gonzalez, J. & Gonzalez, L.M. (1949) Release of the A2 isoagglutinogen-like substance of infectious organisms into human blood serum. Journal of Infectious Diseases 85, 66.
Pareira, F.E., Bostolini, E.R., Carneiro, J.L., da Silva, C.R. & Neves, R.C. (1979) ABO blood groups and hepatosplenic form of schistosomiasis mansoni (Symmers fibrosis). Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 238.
Pullan, A. & Brooker, S. (2008) The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology 135, 783794.
Quinnell, R.J. (2003) Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33, 12191231.
Roche, M. & Layrisse, M. (1966) The nature and causes of hookworm anemia. American Journal of Tropical Medicine and Hygiene 15, 10311100.
Stephenson, L.S., Latham, M.C. & Ottesen, E.A. (2000) Malnutrition and parasitic helminth infections. Parasitology 121, 2338.
Stoltzfus, R.J., Chwaya, H.M., Tielsch, J.M., Schulze, K.J., Albonico, M. & Savioli, L. (1997) Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. American Journal of Clinical Nutrition 65, 153159.
Thein-Hlaing, , Thane-Toe, , Than-Saw, , Myat-Lay-Kyin, & Myint-Lwin, (1991) A controlled chemotherapeutic intervention trial on the relationship between Ascaris lumbricoides infection and malnutrition in children. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 523528.
T> , K.L., Goluska, M.J., O'Leary, M.J. & Douglas, S.D. (1979) Distribution of blood groups and secretor status in schistosomiasis. Parasite Immunology 1, 133140.
Ulukanligil, M. & Seyrek, A. (2004) Anthropometric status, anaemia and intestinal helminthic infections in shantytown and apartment schoolchildren in the Sanliurfa province of Turkey. European Journal of Clinical Nutrition 58, 10561061.
World Health Organization (1991) Basic laboratory methods in medical parasitology. Geneva, WHO.
World Health Organization (1995) Physical status: the use and interpretation of anthropometry. Expert Committee Report. WHO Technical Report Series 854. Geneva, WHO.
World Health Organization (2001) Iron deficiency anaemia: assessment, prevention and control, a guide for programme managers. Geneva, WHO.
World Health Organization (2005) Deworming for health and development: Report of the third global meeting of the partners for parasite control. Geneva, WHO.
World Health Organization (2006) Child Growth Standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age. Methods and development. Geneva, WHO.
World Health Organization (2009) AnthroPlus for personal computers Manual: Software for assessing growth of the world's children and adolescents. Geneva, WHO.
World Health Organization (2010) Anthro for personal computers, version 3.1, 2010: Software for assessing growth and development of the world's children. Geneva, WHO.
Zerihun, T., Degarege, A. & Erko, B. (2011) Association of ABO blood group and Plasmodium falciparum malaria in Dore Baafeno Area, Southern Ethiopia. Asian Pacific Journal of Tropical Biomedicine 1, 289294.

The association between multiple intestinal helminth infections and blood group, anaemia and nutritional status in human populations from Dore Bafeno, southern Ethiopia

  • A. Degarege (a1), A. Animut (a1), G. Medhin (a1), M. Legesse (a1) and B. Erko (a1)...


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