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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

Published online by Cambridge University Press:  03 January 2013

A. Degarege ,
A. Animut ,
G. Medhin ,
M. Legesse  and
B. Erko
A. Degarege*
Affiliation:
Aklilu Lemma Institute of Pathobiology, Addis Ababa University, PO Box 1176, Addis Ababa, Ethiopia
A. Animut
Affiliation:
Aklilu Lemma Institute of Pathobiology, Addis Ababa University, PO Box 1176, Addis Ababa, Ethiopia
G. Medhin
Affiliation:
Aklilu Lemma Institute of Pathobiology, Addis Ababa University, PO Box 1176, Addis Ababa, Ethiopia
M. Legesse
Affiliation:
Aklilu Lemma Institute of Pathobiology, Addis Ababa University, PO Box 1176, Addis Ababa, Ethiopia
B. Erko
Affiliation:
Aklilu Lemma Institute of Pathobiology, Addis Ababa University, PO Box 1176, Addis Ababa, Ethiopia
*
*Fax: +251 112755296 E-mail: abrahamdegarege@yahoo.com
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Abstract

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.

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 2 , June 2014 , pp. 152 - 159
Copyright
Copyright © Cambridge University Press 2013 

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References

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, 1022–1029.CrossRefGoogle Scholar
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, 939–944.CrossRefGoogle ScholarPubMed
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, 240–246.Google Scholar
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, 88–98.Google Scholar
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.CrossRefGoogle Scholar
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, 175–180.CrossRefGoogle ScholarPubMed
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, 1005–1016.CrossRefGoogle ScholarPubMed
Dean, D. (1974) Schistosoma mansoni: adsorption of human blood group A and B antigens by schistosomula. Journal of Parasitology 60, 260–263.CrossRefGoogle Scholar
Degarege, A., Animut, A., Legesse, M. & Erko, B. (2009) Malaria severity status in patients with soil-transmitted helminth infections. Acta Tropica 112, 8–11.CrossRefGoogle ScholarPubMed
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, 143–149.CrossRefGoogle Scholar
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, 164–169.Google Scholar
Deleon, P.P. & Valverdeh, J. (2003) P System antigenic determiners expression in Ascaris lumbricoides. Revista do Instituto de Medicina Tropical de Sao Paulo 45, 53–54.Google Scholar
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, 295–296.Google Scholar
El Masri, S.H. & Sharfi, A.R.M. (1982) ABO blood groups in hepatosplenic schistosomiasis. Journal of Tropical Medicine and Hygiene 85, 223–224.Google Scholar
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, 2160–2170.CrossRefGoogle ScholarPubMed
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, 245–253.CrossRefGoogle ScholarPubMed
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, 301–312.CrossRefGoogle ScholarPubMed
Friedman, J.F., Kanzaria, H.K. & McGarvey, S.T. (2005) Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology 21, 386–392.CrossRefGoogle ScholarPubMed
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, 679–683.Google Scholar
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, 67–73.Google Scholar
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, 458–467.Google Scholar
Katz, N., Tavares, J. & Abrantes, W.L. (1976) ABO and Rh blood groups from patients with hepatosplenic schistosomiasis mansoni. Journal of Parasitology 53, 99.Google Scholar
Khattab, M., El-Gengehy, M.T. & Sharaf, M. (1968) ABO blood groups in bilharzial hepatic fibrosis. Journal of the Egyptian Medical Association 208, 1145–1148.Google Scholar
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, 331–334.CrossRefGoogle ScholarPubMed
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, 278–286.CrossRefGoogle ScholarPubMed
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, 534–540.Google Scholar
May, R.M. & Anderson, R.M. (1979) Population biology of infectious diseases: part II. Nature 280, 455–461.Google Scholar
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, 517–526.Google Scholar
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, 181–190.Google Scholar
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.Google Scholar
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.Google Scholar
Pullan, A. & Brooker, S. (2008) The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology 135, 783–794.CrossRefGoogle ScholarPubMed
Quinnell, R.J. (2003) Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33, 1219–1231.Google Scholar
Roche, M. & Layrisse, M. (1966) The nature and causes of hookworm anemia. American Journal of Tropical Medicine and Hygiene 15, 1031–1100.Google Scholar
Stephenson, L.S., Latham, M.C. & Ottesen, E.A. (2000) Malnutrition and parasitic helminth infections. Parasitology 121, 23–38.Google Scholar
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, 153–159.CrossRefGoogle ScholarPubMed
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, 523–528.Google Scholar
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, 133–140.Google Scholar
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, 1056–1061.CrossRefGoogle ScholarPubMed
World Health Organization (1991) Basic laboratory methods in medical parasitology. Geneva, WHO.Google Scholar
World Health Organization (1995) Physical status: the use and interpretation of anthropometry. Expert Committee Report. WHO Technical Report Series 854. Geneva, WHO.Google Scholar
World Health Organization (2001) Iron deficiency anaemia: assessment, prevention and control, a guide for programme managers. Geneva, WHO.Google Scholar
World Health Organization (2005) Deworming for health and development: Report of the third global meeting of the partners for parasite control. Geneva, WHO.Google Scholar
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.Google Scholar
World Health Organization (2009) AnthroPlus for personal computers Manual: Software for assessing growth of the world's children and adolescents. Geneva, WHO.Google Scholar
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.Google Scholar
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, 289–294.CrossRefGoogle ScholarPubMed