Prevalence and correlates of helminth co-infection in Kenyan HIV-1 infected adults
Judd L Walson, Barclay T Stewart, Laura Sangaré, Loice W Mbogo, Phelgona A Otieno, Benjamin K S Piper, Barbra A Richardson, Grace John-Stewart, Judd L Walson, Barclay T Stewart, Laura Sangaré, Loice W Mbogo, Phelgona A Otieno, Benjamin K S Piper, Barbra A Richardson, Grace John-Stewart
Abstract
Background: Deworming HIV-1 infected individuals may delay HIV-1 disease progression. It is important to determine the prevalence and correlates of HIV-1/helminth co-infection in helminth-endemic areas.
Methods: HIV-1 infected individuals (CD4>250 cells/ul) were screened for helminth infection at ten sites in Kenya. Prevalence and correlates of helminth infection were determined. A subset of individuals with soil-transmitted helminth infection was re-evaluated 12 weeks following albendazole therapy.
Results: Of 1,541 HIV-1 seropositive individuals screened, 298 (19.3%) had detectable helminth infections. Among individuals with helminth infection, hookworm species were the most prevalent (56.3%), followed by Ascaris lumbricoides (17.1%), Trichuris trichiura (8.7%), Schistosoma mansoni (7.1%), and Strongyloides stercoralis (1.3%). Infection with multiple species occurred in 9.4% of infections. After CD4 count was controlled for, rural residence (RR 1.40, 95% CI: 1.08-1.81), having no education (RR 1.57, 95% CI: 1.07-2.30), and higher CD4 count (RR 1.36, 95% CI: 1.07-1.73) remained independently associated with risk of helminth infection. Twelve weeks following treatment with albendazole, 32% of helminth-infected individuals had detectable helminths on examination. Residence, education, and CD4 count were not associated with persistent helminth infection.
Conclusions: Among HIV-1 seropositive adults with CD4 counts above 250 cells/mm(3) in Kenya, traditional risk factors for helminth infection, including rural residence and lack of education, were associated with co-infection, while lower CD4 counts were not.
Trial registration: ClinicalTrials.gov NCT00130910.
Conflict of interest statement
The authors have declared that no competing interests exist.
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References
- de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, et al. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol. 2003;19:547–551.
- Fincham JE, Markus MB, Adams VJ. Could control of soil-transmitted helminthic infection influence the HIV/AIDS pandemic. Acta Trop. 2003;86:315–333.
- Walson JL, Otieno PA, Mbuchi M, Richardson BA, Lohman-Payne B, et al. Albendazole treatment of HIV-1 and helminth co-infection: a randomized, double-blind, placebo-controlled trial. AIDS. 2008;22:1601–1609.
- Wolday D, Mayaan S, Mariam ZG, Berhe N, Seboxa T, et al. Treatment of intestinal worms is associated with decreased HIV plasma viral load. J Acquir Immune Defic Syndr. 2002;31:56–62.
- Walson JL, Herrin BR, John-Stewart G. Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database Syst Rev: CD006419 2009
- Kallestrup P, Zinyama R, Gomo E, Butterworth AE, van Dam GJ, et al. Schistosomiasis and HIV in rural Zimbabwe: efficacy of treatment of schistosomiasis in individuals with HIV coinfection. Clin Infect Dis. 2006;42:1781–1789.
- Gupta SB, Jacobson LP, Margolick JB, Rinaldo CR, Phair JP, et al. Estimating the benefit of an HIV-1 vaccine that reduces viral load set point. J Infect Dis. 2007;195:546–550.
- Modjarrad K, Chamot E, Vermund SH. Impact of small reductions in plasma HIV RNA levels on the risk of heterosexual transmission and disease progression. AIDS. 2008;22:2179–2185.
- Brooker S, Rowlands M, Haller L, Savioli L, Bundy DA. Towards an atlas of human helminth infection in sub-Saharan Africa: the use of geographical information systems (GIS). Parasitol Today. 2000;16:303–307.
- Montresor A, DC, Hall A, Bundy D, Savioli L. World Health Organization; 2000. Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level.
- Emery S, Bodrug S, Richardson BA, Giachetti C, Bott MA, et al. Evaluation of performance of the Gen-Probe human immunodeficiency virus type 1 viral load assay using primary subtype A, C, and D isolates from Kenya. J Clin Microbiol. 2000;38:2688–2695.
- Khan MM, Kraemer A. Socio-economic factors explain differences in public health-related variables among women in Bangladesh: a cross-sectional study. BMC Public Health. 2008;8:254.
- Filmer D, Pritchett LH. Estimating wealth effects without expenditure data–or tears: an application to educational enrollments in states of India. Demography. 2001;38:115–132.
- Van de Poel E, Hosseinpoor AR, Speybroeck N, Van Ourti T, Vega J. Socioeconomic inequality in malnutrition in developing countries. Bull World Health Organ. 2008;86:282–291.
- Barros AJ, Hirakata VN. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol. 2003;3:21.
- Lumley T, KR, Ma S. Relative Risk Regression in Medical Research: Models, Contrasts, Estimators, and Algorithms. UW Biostatistics Working Paper Series. 2006:293 p.
- Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–1532.
- Borkow G, Bentwich Z. Chronic immune activation associated with chronic helminthic and human immunodeficiency virus infections: role of hyporesponsiveness and anergy. Clin Microbiol Rev. 2004;17:1012–1030, table of contents.
- Hotez PJ, Kamath A. Neglected tropical diseases in sub-Saharan Africa: Review of their prevalence, distribution and disease burden. PLoS Negl Trop Dis. 2009;3:e412. doi: .
- Riesel JN, Ochieng FO, Wright P, Vermund SH, Davidson M. High Prevalence of Soil-transmitted Helminths in Western Kenya: Failure to Implement Deworming Guidelines in Rural Nyanza Province. J Trop Pediatr. 2009;56:60–62.
- Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, et al. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis. 2008;2:e331. doi: .
- Hailemariam G, Kassu A, Abebe G, Abate E, Damte D, et al. Intestinal parasitic infections in HIV/AIDS and HIV seronegative individuals in a teaching hospital, Ethiopia. Jpn J Infect Dis. 2004;57:41–43.
- Tarimo DS, Killewo JZ, Minjas JN, Msamanga GI. Prevalence of intestinal parasites in adult patients with enteropathic AIDS in north-eastern Tanzania. East Afr Med J. 1996;73:397–399.
- Gomez Morales MA, Atzori C, Ludovisi A, Rossi P, Scaglia M, et al. Opportunistic and non-opportunistic parasites in HIV-positive and negative patients with diarrhoea in Tanzania. Trop Med Parasitol. 1995;46:109–114.
- Gassama A, Sow PS, Fall F, Camara P, Gueye-N'diaye A, et al. Ordinary and opportunistic enteropathogens associated with diarrhea in Senegalese adults in relation to human immunodeficiency virus serostatus. Int J Infect Dis. 2001;5:192–198.
- Bethony J, Williams JT, Brooker S, Gazzinelli A, Gazzinelli MF, et al. Exposure to Schistosoma mansoni infection in a rural area in Brazil. Part III: household aggregation of water-contact behaviour. Trop Med Int Health. 2004;9:381–389.
- Bethony J, Williams JT, Kloos H, Blangero J, Alves-Fraga L, et al. Exposure to Schistosoma mansoni infection in a rural area in Brazil. II: household risk factors. Trop Med Int Health. 2001;6:136–145.
- Dumba R, Kaddu JB, Wabwire Mangen F. Intestinal helminths in Luweero district, Uganda. Afr Health Sci. 2008;8:90–96.
- Olsen A, Samuelsen H, Onyango-Ouma W. A study of risk factors for intestinal helminth infections using epidemiological and anthropological approaches. J Biosoc Sci. 2001;33:569–584.
- Modjarrad K, Zulu I, Redden DT, Njobvu L, Freedman DO, et al. Prevalence and predictors of intestinal helminth infections among human immunodeficiency virus type 1-infected adults in an urban African setting. Am J Trop Med Hyg. 2005;73:777–782.
- Wiwanitkit V. Intestinal parasite infestation in HIV infected patients. Curr HIV Res. 2006;4:87–96.
- Woodburn PW, Muhangi L, Hillier S, Ndibazza J, Namujju PB, et al. Risk Factors for Helminth, Malaria, and HIV Infection in Pregnancy in Entebbe, Uganda. PLoS Negl Trop Dis. 2009;3:e473. doi: .
- Sauca Subias G, Barrufet Barque P, Besa Beringues A, Rodriguez Ramos E. [Strongyloides stercoralis hyperinfection in a patient with acquired immunodeficiency syndrome]. An Med Interna. 2005;22:139–141.
- Kaushal Kumar Dwivedi GP, Saini Sanjeev, Mahajan Surbhi, Lal Shiv, Baveja Usha Krishan. Enteric Opportunistic Parasites among HIV Infected Individuals: Associated Risk Factors and Immune Status. Jpn J Infect Dis. 2007;60:76–81.
- Bachur TP, Vale JM, Coelho IC, Queiroz TR, Chaves Cde S. Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Braz J Infect Dis. 2008;12:115–122.
- Actor JK, Shirai M, Kullberg MC, Buller RM, Sher A, et al. Helminth infection results in decreased virus-specific CD8+ cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc Natl Acad Sci U S A. 1993;90:948–952.
- Chenine AL, Buckley KA, Li PL, Rasmussen RA, Ong H, et al. Schistosoma mansoni infection promotes SHIV clade C replication in rhesus macaques. AIDS. 2005;19:1793–1797.
- Sher A, Gazzinelli RT, Oswald IP, Clerici M, Kullberg M, et al. Role of T-cell derived cytokines in the downregulation of immune responses in parasitic and retroviral infection. Immunol Rev. 1992;127:183–204.
- Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, et al. Human immunodeficiency virus-driven expansion of CD4+CD25+ regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood. 2004;104:3249–3256.
- Viney ME, Brown M, Omoding NE, Bailey JW, Gardner MP, et al. Why does HIV infection not lead to disseminated strongyloidiasis? J Infect Dis. 2004;190:2175–2180.
- Brooker S, Kabatereine NB, Gyapong JO, Stothard JR, Utzinger J. Rapid mapping of schistosomiasis and other neglected tropical diseases in the context of integrated control programmes in Africa. Parasitology. 2009;136:1707–1718.
- Brown M, Mawa P, Kaleebu P, Elliott A. Helminths and HIV infection: epidemiological observations on immunological hypotheses. Parasite Immunol. 2006;28:613–623.
- Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, et al. Helminth infections: the great neglected tropical diseases. J Clin Invest. 2008;118:1311–1321.
- Bundy DA, editor. London: Chapman & Hall Medical; 1995. Epidemiology and Transmission of Intestinal Helminths. pp. 5–24.
- Thiong'o FW, Luoba A, Ouma JH. Intestinal helminths and schistosomiasis among school children in a rural district in Kenya. East Afr Med J. 2001;78:279–282.
- van Eijk AM, Lindblade KA, Odhiambo F, Peterson E, Rosen DH, et al. Geohelminth Infections among Pregnant Women in Rural Western Kenya; a Cross-Sectional Study. PLoS Negl Trop Dis. 2009;3:e370. doi: .
- Handzel T, Karanja DM, Addiss DG, Hightower AW, Rosen DH, et al. Geographic distribution of schistosomiasis and soil-transmitted helminths in Western Kenya: implications for anthelminthic mass treatment. Am J Trop Med Hyg. 2003;69:318–323.
- Brown M, Bukusuba J, Hughes P, Nakiyingi J, Watera C, et al. Screening for intestinal helminth infestation in a semi-urban cohort of HIV-infected people in Uganda: a combination of techniques may enhance diagnostic yield in the absence of multiple stool samples. Trop Doct. 2003;33:72–76.
Source: PubMed