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Seroepidemiology of Strongyloides stercoralis in Dhaka, Bangladesh

Published online by Cambridge University Press:  20 July 2012

YASMIN SULTANA ,
GWENDOLYN L. GILBERT ,
BE-NAZIR AHMED  and
ROGAN LEE
YASMIN SULTANA*
Affiliation:
Centre for Infectious Diseases and Microbiology Laboratory Services, ICPMR, Westmead Hospital, Westmead, NSW, Australia Discipline of Medicine, Sydney Medical School, University of Sydney, Camperdown, NSW, Australia
GWENDOLYN L. GILBERT
Affiliation:
Centre for Infectious Diseases and Microbiology Laboratory Services, ICPMR, Westmead Hospital, Westmead, NSW, Australia Discipline of Medicine, Sydney Medical School, University of Sydney, Camperdown, NSW, Australia
BE-NAZIR AHMED
Affiliation:
Institute of Epidemiology Disease Control and Research, Mohakhali, Dhaka, Bangladesh
ROGAN LEE
Affiliation:
Centre for Infectious Diseases and Microbiology Laboratory Services, ICPMR, Westmead Hospital, Westmead, NSW, Australia Discipline of Medicine, Sydney Medical School, University of Sydney, Camperdown, NSW, Australia
*
*Corresponding author: Centre for Infectious Diseases and Microbiology Laboratory Services, ICPMR, Westmead Hospital, Westmead, NSW 2145, Australia. Tel: +61 2 98457662. Fax: +61 2 98938659. E-mail: [email protected]
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Summary

Human strongyloidiasis is a neglected tropical disease with global distribution and this infection is caused by the parasitic nematode Strongyloides stercoralis. The aim of this study was to determine the prevalence of strongyloidiasis in Dhaka, Bangladesh. Sera from 1004 residents from a slum (group A) and 299 from city dwellers (group B) were tested for total IgG and IgG subclasses to Strongyloides antigen. There was a significant difference (P < 0·001) in IgG seroprevalence between group A (22%) and group B (5%). Reactive IgG subclasses (IgG1 and IgG4) were also higher in group A (P < 0·05). The seroprevalence of strongyloidiasis in group A increased with age but was unrelated to sex. The presence of reactive IgG to Strongyloides antigen had no correlation with either socio-economic or personal hygiene factors. However, a history of diarrhoea in a family member, in the past 6 months, but not in the respondents was associated with detection of antibodies to S. stercoralis (P < 0·01). None of the sera from either group had an HTLV-I reaction. This study demonstrates that strongyloidiasis is prevalent in Dhaka, especially among slum dwellers, but concurrent infection with HTLV-I was not found. Future epidemiological studies should identify individual risk factors and other communities at risk so that appropriate interventions can be planned.

Keywords

Strongyloides stercoralisslumprevalenceHTLV-IseroepidemiologyBangladesh
Type
Research Article
Information
Parasitology , Volume 139 , Issue 11 , September 2012 , pp. 1513 - 1520
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Adedayo, O., Grell, G. and Bellot, P. (2002). Hyperinfective strongyloidiasis in the medical ward: review of 27 cases in 5 years. Southern Medical Journal 95, 711–716.CrossRefGoogle Scholar
Agrawal, V., Agarwal, T. and Ghoshal, U. C. (2009). Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 242–246.CrossRefGoogle ScholarPubMed
Arakaki, T., Kohakura, M., Asato, R., Ikeshiro, T., Nakamura, S. and Iwanaga, M. (1992). Epidemiological aspects of Strongyloides stercoralis infection in Okinawa, Japan. Journal of Tropical Medicine and Hygiene 95, 210–213.Google ScholarPubMed
Atkins, N. S., Lindo, J. F., Lee, M. G., Conway, D. J., Bailey, J. W., Robinson, R. D. and Bundy, D. A. P. (1997). Humoral responses in human strongyloidiasis: correlations with infection chronicity. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 609–613.CrossRefGoogle ScholarPubMed
Baaten, G. G., Sonder, G. J., van Gool, T., Kint, J. A. and van den Hoek, A. (2011). Travel-related schistosomiasis, strongyloidiasis, filariasis, and toxocariasis: the risk of infection and the diagnostic relevance of blood eosinophilia. BMC Infectious Diseases 11, 84.CrossRefGoogle ScholarPubMed
Becker, S. L., Sieto, B., Silué, K. D., Adjossan, L., Koné, S., Hatz, C., Kern, W. V., N'Goran, E. K. and Utzinger, J. (2011). Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Neglected Tropical Diseases 5, e1292.CrossRefGoogle Scholar
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 1521–1532.CrossRefGoogle ScholarPubMed
Borda, C. E., Rea, M. J., Rosa, J. R. and Maidana, C. (1996). Intestinal parasitism in San Cayetano, Corrientes, Argentina. Bulletin of the Pan American Health Organization 30, 227–233.Google Scholar
Carvalho, E. M. and Da Fonseca Porto, A. (2004). Epidemiological and clinical interaction between HTLV-1 and Strongyloides stercoralis. Parasite Immunology 26, 487–497.CrossRefGoogle ScholarPubMed
Chieffi, P. P., Chiattone, C. S., Feltrim, E. N., Alves, R. C. and Paschoalotti, M. A. (2000). Coinfection by Strongyloides stercoralis in blood donors infected with human T-cell leukemia/lymphoma virus type 1 in Sao Paulo City, Brazil. Memorias do Instituto Oswaldo Cruz 95, 711–712.CrossRefGoogle Scholar
Conway, D. J., Bailey, J. W., Lindo, J. F., Robinson, R. D., Bundy, D. A. P. and Bianco, A. E. (1993). Serum IgG reactivity with 41-, 31-, and 28-kDa larval proteins of Strongyloides stercoralis in individuals with strongyloidiasis. Journal of Infectious Diseases 168, 784–787.CrossRefGoogle ScholarPubMed
Conway, D. J., Hall, A., Anwar, K. S., Rahman, M. L. and Bundy, D. A. P. (1995). Household aggregation of Strongyloides stercoralis infection in Bangladesh. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 258–261.CrossRefGoogle ScholarPubMed
Conway, D. J., Lindo, J. F., Robinson, R. D., Bundy, D. A. P. and Bianco, A. E. (1994). Strongyloides stercoralis: characterization of immunodiagnostic larval antigens. Experimental Parasitology 79, 99–105.CrossRefGoogle ScholarPubMed
Douce, R. W., Brown, A. E., Khamboonruang, C., Walzer, P. D. and Genta, R. M. (1987). Seroepidemiology of strongyloidiasis in a Thai village. International Journal for Parasitology 17, 1343–1348.CrossRefGoogle Scholar
Dreyer, G., Fernandes-Silva, E., Alves, S., Rocha, A., Albuquerque, R. and Addiss, D. (1996). Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. Journal of Clinical Microbiology 34, 2569–2571.CrossRefGoogle ScholarPubMed
Einsiedel, L. and Fernandes, L. (2008). Strongyloides stercoralis: a cause of morbidity and mortality for indigenous people in Central Australia. Internal Medicine Journal 38, 697–703.CrossRefGoogle ScholarPubMed
Faust, E. C. and Giraldo, L. E. (1960). Parasitological surveys in Cali, Departamento del Valle, Colombia. 6. Strongyloidiasis in Barrio Siloe, Cali, Colombia. Transactions of the Royal Society of Tropical Medicine and Hygiene 54, 556–563.CrossRefGoogle Scholar
Gam, A. A., Neva, F. A. and Krotoski, W. A. (1987). Comparative sensitivity and specificity of ELISA and IHA for serodiagnosis of strongyloidiasis with larval antigens. American Journal of Tropical Medicine and Hygiene 37, 157–161.CrossRefGoogle ScholarPubMed
Gamboa, M. I., Kozubsky, L. E., Costas, M. E., Garraza, M., Cardozo, M. I., Susevich, M. L., Magistrello, P. N. and Navone, G. T. (2009). Associations between geohelminths and socioenvironmental conditions among different human populations in Argentina. Pan American Journal of Public Health 26, 1–8.Google ScholarPubMed
Ganesh, S. and Cruz, R. J. Jr. (2011). Strongyloidiasis: a multifaceted disease. Gastroenterology and Hepatology (NY) 7, 194–196.Google ScholarPubMed
Genta, R. M., Weesner, R., Douce, R. W., Huitger-O'Connor, T. and Walzer, P. D. (1987). Strongyloidiasis in US veterans of the Vietnam and other wars. JAMA 258, 49–52.CrossRefGoogle ScholarPubMed
Gill, G. V. and Bell, D. R. (1979). Strongyloides stercoralis infection in former Far East prisoners of war. British Medical Journal 2, 572–574.CrossRefGoogle ScholarPubMed
Glinz, D., N'Guessan, N. A., Utzinger, J. and N'Goran, E. K. (2010). High prevalence of Strongyloides stercoralis among school children in rural Côte d'Ivoire. Journal of Parasitology 96, 431–433.CrossRefGoogle ScholarPubMed
Gonzaga, H. T., Ribeiro, V. S., Feliciano, N. D., Manhani, M. N., Silva, D. A., Ueta, M. T. and Costa-Cruz, J. M. (2011). IgG avidity in differential serodiagnosis of human strongyloidiasis active infection. Immunology Letters 139, 87–92.CrossRefGoogle ScholarPubMed
Gonzalez, A., Gallo, M., Valls, M. E., Munoz, J., Puyol, L., Pinazo, M. J., Mas, J. and Gascon, J. (2010). Clinical and epidemiological features of 33 imported Strongyloides stercoralis infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 613–616.CrossRefGoogle ScholarPubMed
Gotuzzo, E., Terashima, A., Alvarez, H., Tello, R., Infante, R., Watts, D. M. and Freedman, D. O. (1999). Strongyloides stercoralis hyperinfection associated with human T cell lymphotropic virus type-1 infection in Peru. American Journal of Tropical Medicine and Hygiene 60, 146–149.CrossRefGoogle ScholarPubMed
Grove, D. I. (1989). Diagnosis. In Strongyloidiasis: A Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 175–197. Taylor and Francis Ltd., Basingstoke, Hants, UK.Google Scholar
Gyorkos, T. W., Genta, R. M., Viens, P. and MacLean, J. D. (1990). Seroepidemiology of Strongyloides infection in the Southeast Asian refugee population in Canada. American Journal of Epidemiology 132, 257–264.CrossRefGoogle ScholarPubMed
Hakim, S. Z. and Genta, R. M. (1986). Fatal disseminated strongyloidiasis in a Vietnam War veteran. Archives of Pathology and Laboratory Medicine 110, 809–812.Google Scholar
Hall, A., Conway, D. J., Anwar, K. S. and Rahman, M. L. (1994). Strongyloides stercoralis in an urban slum community in Bangladesh: factors independently associated with infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 527–530.CrossRefGoogle Scholar
Hirata, T., Uchima, N., Kishimoto, K., Zaha, O., Kinjo, N., Hokama, A., Sakugawa, H., Kinjo, F. and Fujita, J. (2006). Impairment of host immune response against Strongyloides stercoralis by human T cell lymphotropic virus type 1 infection. American Journal of Tropical Medicine and Hygiene 74, 246–249.CrossRefGoogle ScholarPubMed
Igra-Siegman, Y., Kapila, R., Sen, P., Kaminski, Z. C. and Louria, D. B. (1981). Syndrome of hyperinfection with Strongyloides stercoralis. Reviews of Infectious Diseases 3, 397–407.CrossRefGoogle ScholarPubMed
Knopp, S., Mohammed, K. A., Rollinson, D., Stothard, J. R., Khamis, I. S., Utzinger, J. and Marti, H. (2009). Changing patterns of soil-transmitted helminthiases in Zanzibar in the context of national helminth control programs. American Journal of Tropical Medicine and Hygiene 81, 1071–1078.CrossRefGoogle ScholarPubMed
Lammie, P. J., Weil, G., Noordin, R., Kaliraj, P., Steel, C., Goodman, D., Lakshmikanthan, V. B. and Ottesen, E. (2004). Recombinant antigen-based antibody assays for the diagnosis and surveillance of lymphatic filariasis – a multicenter trial. Filaria Journal 3, 9.CrossRefGoogle ScholarPubMed
Lindo, J. F., Conway, D. J., Atkins, N. S., Bianco, A. E., Robinson, R. D. and Bundy, D. A. P. (1994). Prospective evaluation of enzyme-linked immunosorbent assay and immunoblot methods for the diagnosis of endemic Strongyloides stercoralis infection. American Journal of Tropical Medicine and Hygiene 51, 175–179.CrossRefGoogle ScholarPubMed
Lindo, J. F., Robinson, R. D., Terry, S. I., Vogel, P., Gam, A. A., Neva, F. A. and Bundy, D. A. P. (1995). Age-prevalence and household clustering of Strongyloides stercoralis infection in Jamaica. Parasitology 110, 97–102.CrossRefGoogle ScholarPubMed
Marcos, L. A., Terashima, A., Dupont, H. L. and Gotuzzo, E. (2008). Strongyloides hyperinfection syndrome: an emerging global infectious disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 314–318.CrossRefGoogle ScholarPubMed
Marnell, F., Guillet, A. and Holland, C. (1992). A survey of the intestinal helminths of refugees in Juba, Sudan. Annals of Tropical Medicine and Parasitology 86, 387–393.CrossRefGoogle ScholarPubMed
Menezes, A. L., Lima, V. M., Freitas, M. T., Rocha, M. O., Silva, E. F. and Dolabella, S. S. (2008). Prevalence of intestinal parasites in children from public daycare centers in the city of Belo Horizonte, Minas Gerais, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 50, 57–59.CrossRefGoogle ScholarPubMed
Nakada, K., Kohakura, M., Komoda, H. and Hinuma, Y. (1984). High incidence of HTLV antibody in carriers of Strongyloides stercoralis. Lancet 323, 633.CrossRefGoogle Scholar
Newton, R. C., Limpuangthip, P., Greenberg, S., Gam, A. and Neva, F. A. (1992). Strongyloides stercoralis hyperinfection in a carrier of HTLV-I virus with evidence of selective immunosuppression. American Journal of Medicine 92, 202–208.CrossRefGoogle Scholar
Olsen, A., van Lieshout, L., Marti, H., Polderman, T., Polman, K., Steinmann, P., Stothard, R., Thybo, S., Verweij, J. J. and Magnussen, P. (2009). Strongyloidiasis–the most neglected of the neglected tropical diseases? Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 967–972.CrossRefGoogle ScholarPubMed
Pawlowski, Z. S. (1989). Epidemiology, prevention and control. In Strongyloidiasis: A Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 233–249. Taylor and Francis Ltd. , Basingstoke, Hants, UK.Google Scholar
Pelletier, L. L. Jr. (1984). Chronic strongyloidiasis in World War II Far East ex-prisoners of war. American Journal of Tropical Medicine and Hygiene 33, 55–61.CrossRefGoogle Scholar
Porto, M. A., Alcantara, L. M., Leal, M., Castro, N. and Carvalho, E. M. (2005). Atypical clinical presentation of strongyloidiasis in a patient co-infected with human T cell lymphotrophic virus type I. American Journal of Tropical Medicine and Hygiene 72, 124–125.CrossRefGoogle Scholar
Repetto, S. A., Duran, P. A., Lasala, M. B. and Gonzalez-Cappa, S. M. (2010). High rate of strongyloidosis infection, out of endemic area, in patients with eosinophilia and without risk of exogenous reinfections. American Journal of Tropical Medicine and Hygiene 82, 1088–1093.CrossRefGoogle ScholarPubMed
Robinson, R. D., Lindo, J. F., Neva, F. A., Gam, A. A., Vogel, P., Terry, S. I. and Cooper, E. S. (1994). Immunoepidemiologic studies of Strongyloides stercoralis and human T lymphotropic virus type I infections in Jamaica. Journal of Infectious Diseases 169, 692–696.CrossRefGoogle ScholarPubMed
Rodrigues, R. M., de Oliveira, M. C., Sopelete, M. C., Silva, D. A., Campos, D. M., Taketomi, E. A. and Costa-Cruz, J. M. (2007). IgG1, IgG4, and IgE antibody responses in human strongyloidiasis by ELISA using Strongyloides ratti saline extract as heterologous antigen. Parasitology Research 101, 1209–1214.CrossRefGoogle ScholarPubMed
Sato, Y., Shiroma, Y., Kiyuna, S., Toma, H. and Kobayashi, J. (1994). Reduced efficacy of chemotherapy might accumulate concurrent HTLV-1 infection among strongyloidiasis patients in Okinawa, Japan. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 59.CrossRefGoogle ScholarPubMed
Satoh, M., Kiyuna, S., Shiroma, Y., Toma, H., Kokaze, A. and Sato, Y. (2003). Predictive markers for development of strongyloidiasis in patients infected with both Strongyloides stercoralis and HTLV-1. Clinical and Experimental Immunology 133, 391–396.CrossRefGoogle ScholarPubMed
Satoh, M., Toma, H., Sato, Y., Kikuchi, M., Takara, M., Shiroma, Y., Kiyuna, S. and Hirayama, K. (1999). Production of a high level of specific IgG4 antibody associated with resistance to albendazole treatment in HLA-DRB1*0901-positive patients with strongyloidiasis. American Journal of Tropical Medicine and Hygiene 61, 668–671.CrossRefGoogle ScholarPubMed
Satoh, M., Toma, H., Sato, Y., Takara, M., Shiroma, Y., Kiyuna, S. and Hirayama, K. (2002). Reduced efficacy of treatment of strongyloidiasis in HTLV-I carriers related to enhanced expression of IFN-gamma and TGF-beta1. Clinical and Experimental Immunology 127, 354–359.CrossRefGoogle ScholarPubMed
Siddiqui, A. A. and Berk, S. L. (2001). Diagnosis of Strongyloides stercoralis infection. Clinical Infectious Diseases 33, 1040–1047.CrossRefGoogle ScholarPubMed
Sornmani, S., Vivatanasesth, P., Bunnag, T., Intarakhao, C. and Harinasuta, C. (1973). A study on the pattern of socioeconomic and health status in relation to parasitic diseases in the inhabitants around Ubolratana Dam in northeast Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 4, 421–434.Google Scholar
Steinmann, P., Zhou, X. N., Du, Z. W., Jiang, J. Y., Wang, L. B., Wang, X. Z., Li, L. H., Marti, H. and Utzinger, J. (2007). Occurrence of Strongyloides stercoralis in Yunnan province, China, and comparison of diagnostic methods. PLoS Neglected Tropical Diseases 1, e75.CrossRefGoogle ScholarPubMed
Stothard, J. R., Pleasant, J., Oguttu, D., Adriko, M., Galimaka, R., Ruggiana, A., Kazibwe, F. and Kabatereine, N. B. (2008). Strongyloides stercoralis: a field-based survey of mothers and their preschool children using ELISA, Baermann and Koga plate methods reveals low endemicity in western Uganda. Journal of Helminthology 82, 263–269.CrossRefGoogle ScholarPubMed
Terashima, A., Alvarez, H., Tello, R., Infante, R., Freedman, D. O. and Gotuzzo, E. (2002). Treatment failure in intestinal strongyloidiasis: an indicator of HTLV-I infection. International Journal of Infectious Diseases 6, 28–30.CrossRefGoogle ScholarPubMed
Uparanukraw, P., Phongsri, S. and Morakote, N. (1999). Fluctuations of larval excretion in Strongyloides stercoralis infection. American Journal of Tropical Medicine and Hygiene 60, 967–973.CrossRefGoogle ScholarPubMed
Vadlamudi, R. S., Chi, D. S. and Krishnaswamy, G. (2006). Intestinal strongyloidiasis and hyperinfection syndrome. Clinical and Molecular Allergy 4, 8.CrossRefGoogle ScholarPubMed
van Doorn, H. R., Koelewijn, R., Hofwegen, H., Gilis, H., Wetsteyn, J. C., Wismans, P. J., Sarfati, C., Vervoort, T. and van Gool, T. (2007). Use of enzyme-linked immunosorbent assay and dipstick assay for detection of Strongyloides stercoralis infection in humans. Journal of Clinical Microbiology 45, 438–442.CrossRefGoogle ScholarPubMed
Yelifari, L., Bloch, P., Magnussen, P., van Lieshout, L., Dery, G., Anemana, S., Agongo, E. and Polderman, A. M. (2005). Distribution of human Oesophagostomum bifurcum, hookworm and Strongyloides stercoralis infections in northern Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 32–38.CrossRefGoogle ScholarPubMed
Yori, P. P., Kosek, M., Gilman, R. H., Cordova, J., Bern, C., Chavez, C. B., Olortegui, M. P., Montalvan, C., Sanchez, G. M., Worthen, B., Worthen, J., Leung, F. and Ore, C. V. (2006). Seroepidemiology of strongyloidiasis in the Peruvian Amazon. American Journal of Tropical Medicine and Hygiene 74, 97–102.CrossRefGoogle ScholarPubMed
Zaha, O., Hirata, T., Uchima, N., Kinjo, F. and Saito, A. (2004). Comparison of anthelmintic effects of two doses of ivermectin on intestinal strongyloidiasis in patients negative or positive for anti-HTLV-1 antibody. Journal of Infection and Chemotherapy 10, 348–351.CrossRefGoogle ScholarPubMed