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Species-specific treatment effects of helminth/HIV-1 co-infection: a systematic review and meta-analysis

Published online by Cambridge University Press:  18 May 2011

LAURA R. SANGARÉ ,
BRADELY R. HERRIN ,
GRACE JOHN-STEWART  and
JUDD L. WALSON
LAURA R. SANGARÉ
Affiliation:
University of Washington, Department of Global Health, Box 359909, 325 Ninth Avenue Seattle, WA 98104, USA
BRADELY R. HERRIN
Affiliation:
University of Washington, Department of Global Health, Box 359909, 325 Ninth Avenue Seattle, WA 98104, USA
GRACE JOHN-STEWART
Affiliation:
University of Washington, Department of Global Health, Box 359909, 325 Ninth Avenue Seattle, WA 98104, USA
JUDD L. WALSON*
Affiliation:
University of Washington, Department of Global Health, Box 359909, 325 Ninth Avenue Seattle, WA 98104, USA
*
Corresponding author: Judd L. Walson, MD, MPH Departments of Global Health, Medicine, Pediatrics and Epidemiology, University of Washington, Box 359909, 325 Ninth Avenue Seattle, WA 98104 Tel: (206) 744-3695 Fax: (206) 543-4818 E-mail: [email protected]
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Summary

In sub-Saharan Africa, over 22 million people are estimated to be co-infected with both helminths and HIV-1. Several studies have suggested that de-worming individuals with HIV-1 may delay HIV-1 disease progression, and that the benefit of de-worming may vary by individual helminth species. We conducted a systematic review and meta-analysis of the published literature to determine the effect of treatment of individual helminth infections on markers of HIV-1 progression (CD4 count and HIV viral load). There was a trend towards an association between treatment for Schistosoma mansoni and a decrease in HIV viral load (Weighted mean difference (WMD)=−0·10; 95% Confidence interval (CI): −0·24, 0·03), although this association was not seen for Ascaris lumbricoides, hookworm or Trichuris trichiura. Treatment of A. lumbricoides, S. mansoni, hookworm or T. trichiura was not associated with a change in CD4 count. While pooled data from randomized trials suggested clinical benefit of de-worming for individual helminth species, these effects decreased when observational data were included in the pooled analysis. While further trials are needed to confirm the role of anthelmintic treatment in HIV-1 co-infected individuals, providing anthelmintics to individuals with HIV-1 may be a safe, inexpensive and practical intervention to slow progression of HIV-1.

Keywords

HelminthHIV-1co-infectionmeta-analysisKenya
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 12: Symposia of the British Society for Parasitology Volume 47 , October 2011 , pp. 1546 - 1558
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Anonymous (2007). Drugs for parasitic infections. Medical Letter on Drugs and Therapeutics 5 (Suppl), e1–e15.Google Scholar
Anthony, R. M., Rutitzky, L. I., Urban, J. F. Jr., Stadecker, M. J. and Gause, W. C. (2007). Protective immune mechanisms in helminth infection. Nature Reviews. Immunology 7, 975–987. doi: nri2199 [pii] 10.1038/nri2199.CrossRefGoogle ScholarPubMed
Baggaley, R. F., Griffin, J. T., Chapman, R., Hollingsworth, T. D., Nagot, N., Delany, S., Mayaud, P., de Wolf, F., Fraser, C., Ghani, A. C. and Weiss, H. A. (2009). Estimating the public health impact of the effect of herpes simplex virus suppressive therapy on plasma HIV-1 viral load. AIDS 23, 1005–1013. doi: 10.1097/QAD.0b013e32832aadf2.CrossRefGoogle Scholar
Bennett, A. and Guyatt, H. (2000). Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitology Today 16, 71–74. doi: S0169-4758(99)01544-6 [pii].CrossRefGoogle ScholarPubMed
Blish, C. A., Sangaré, L., Herrin, B. R., Richardson, B. A., John-Stewart, G. and Walson, J. L. (2010). Changes in plasma cytokines after treatment of Ascaris lumbricoides infection in individuals with HIV-1 infection. Journal of Infectious Diseases 201, 1816–1821. doi: 10.1086/652784.CrossRefGoogle ScholarPubMed
Bourke, C. D., Maizels, R. M. and Mutapi, F. (2010). Acquired immune heterogeneity and its sources in human helminth infection. Parasitology, 1–21. doi: S0031182010001216 [pii] 10.1017/S0031182010001216.Google ScholarPubMed
Bradley, J. E. and Jackson, J. A. (2004). Immunity, immunoregulation and the ecology of trichuriasis and ascariasis. Parasite Immunology 26, 429–441. doi: PIM730 [pii] 10.1111/j.0141-9838.2004.00730.x.CrossRefGoogle ScholarPubMed
Brooker, S., Akhwale, W., Pullan, R., Estambale, B., Clarke, S. E., Snow, R. W. and Hotez, P. J. (2007). Epidemiology of plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. American Journal of Tropical Medicine and Hygiene 77, 88–98. doi: 77/6_Suppl/88 [pii].CrossRefGoogle ScholarPubMed
Brooker, S., Kabatereine, N. B., Smith, J. L., Mupfasoni, D., Mwanje, M. T., Ndayishimiye, O., Lwambo, N. J., Mbotha, D., Karanja, P., Mwandawiro, C., Muchiri, E., Clements, A. C., Bundy, D. A. and Snow, R. W. (2009). An updated atlas of human helminth infections: the example of East Africa. International Journal of Health Geographics 8, 42. doi: 1476-072X-8-42 [pii] 10.1186/1476-072X-8-42.CrossRefGoogle ScholarPubMed
Brooker, S., Rowlands, M., Haller, L., Savioli, L. and Bundy, D. A. (2000). Towards an atlas of human helminth infection in sub-Saharan Africa: the use of geographical information systems (GIS). Parasitology Today 16, 303–307. doi: S0169-4758(00)01687-2 [pii].CrossRefGoogle ScholarPubMed
Brown, M., Kizza, M., Watera, C., Quigley, M. A., Rowland, S., Hughes, P., Whitworth, J. A. and Elliott, A. M. (2004). Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. Journal of Infectious Diseases 190, 1869–1879. doi: JID32687 [pii] 10.1086/425042.CrossRefGoogle Scholar
Burke, M. L., Jones, M. K., Gobert, G. N., Li, Y. S., Ellis, M. K. and McManus, D. P. (2009). Immunopathogenesis of human schistosomiasis. Parasite Immunology 31, 163–176. doi: PIM1098 [pii] 10.1111/j.1365-3024.2009.01098.x.CrossRefGoogle ScholarPubMed
Cooper, P. J., Chico, M. E., Sandoval, C., Espinel, I., Guevara, A., Kennedy, M. W., Urban, J. F. Jr., Griffin, G. E. and Nutman, T. B. (2000). Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. Journal of Infectious Diseases 182, 1207–1213. doi: JID000478 [pii] 10.1086/315830.CrossRefGoogle ScholarPubMed
de Silva, N. R., Brooker, S., Hotez, P. J., Montresor, A., Engels, D. and Savioli, L. (2003). Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19, 547–551. doi: S1471492203002757 [pii].CrossRefGoogle ScholarPubMed
Elias, D., Britton, S., Aseffa, A., Engers, H. and Akuffo, H. (2008). Poor immunogenicity of BCG in helminth infected population is associated with increased in vitro TGF-beta production. Vaccine 26, 3897–3902. doi: S0264-410X(08)00540-9 [pii] 10.1016/j.vaccine.2008.04.083 [doi].CrossRefGoogle ScholarPubMed
Elias, D., Britton, S., Kassu, A. and Akuffo, H. (2007). Chronic helminth infections may negatively influence immunity against tuberculosis and other diseases of public health importance. Expert Review of Anti-Infective Therapy 5, 475–484. doi: 10.1586/14787210.5.3.475 [doi].CrossRefGoogle ScholarPubMed
Elliott, A. M., Mawa, P. A., Joseph, S., Namujju, P. B., Kizza, M., Nakiyingi, J. S., Watera, C., Dunne, D. W. and Whitworth, J. A. (2003). Associations between helminth infection and CD4+ T cell count, viral load and cytokine responses in HIV-1-infected Ugandan adults. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 103–108.CrossRefGoogle ScholarPubMed
Ferrari, M. L., Coelho, P. M., Antunes, C. M., Tavares, C. A. and da Cunha, A. S. (2003). Efficacy of oxamniquine and praziquantel in the treatment of Schistosoma mansoni infection: a controlled trial. Bulletin of the World Health Organization 81, 190–196. doi: S0042-96862003000300009 [pii].Google ScholarPubMed
Fincham, J. E., Markus, M. B. and Adams, V. J. (2003). Could control of soil-transmitted helminthic infection influence the HIV/AIDS pandemic. Acta Tropica 86, 315–333. doi: S0001706X03000639 [pii].CrossRefGoogle ScholarPubMed
Geiger, S. M., Caldas, I. R., McGlone, B. E., Campi-Azevedo, A. C., De Oliveira, L. M., Brooker, S., Diemert, D., Correa-Oliveira, R. and Bethony, J. M. (2007). Stage-specific immune responses in human Necator americanus infection. Parasite Immunology 29, 347–358. doi: PIM950 [pii] 10.1111/j.1365-3024.2007.00950.x.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Grainger, J. R. and Maizels, R. M. (2009). Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 1–11. doi: S0166-6851(09)00122-4 [pii] 10.1016/j.molbiopara.2009.04.008.CrossRefGoogle ScholarPubMed
Higgins, J. and Green, S. (2009) (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2 [updated September 2009]. The Cochrane Collaboration, 2009. Available from www.cochrane-handbook.org.Google Scholar
Horton, J. (2000). Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology 121 (Suppl.) S113–S132.CrossRefGoogle ScholarPubMed
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. M., Bethony, J., Correa–Oliveira, R., Shu–Hua, X., Fenwick, A. and Savioli, L. (2006). Helminth Infections: Soil–Transmitted Helminth Infections and Schistosomiasis. Disease Control Priorities in Developing Countries 2nd Edition, (ed. Dean, T. Jamison, Joel, G. Breman, Anthony, R. Measham, George, Alleyne, Mariam, Claeson, David, B. Evans, Prabhat, Jha, Anne, Mills and Philip, Musgrove), 467–482. New York: Oxford University Press. doi: 10.1596/978-0-821-36179-5/Chpt-24.Google Scholar
Jackson, J. A., Turner, J. D., Rentoul, L., Faulkner, H., Behnke, J. M., Hoyle, M., Grencis, R. K., Else, K. J., Kamgno, J., Bradley, J. E. and Boussinesq, M. (2004). Cytokine response profiles predict species-specific infection patterns in human GI nematodes. International Journal for Parasitology 34, 1237–1244. doi: S0020-7519(04)00166-3 [pii] 10.1016/j.ijpara.2004.07.009.CrossRefGoogle ScholarPubMed
Kallestrup, P., Zinyama, R., Gomo, E., Butterworth, A. E., Mudenge, B., van Dam, G. J., Gerstoft, J., Erikstrup, C. and Ullum, H. (2005). Schistosomiasis and HIV-1 infection in rural Zimbabwe: effect of treatment of schistosomiasis on CD4 cell count and plasma HIV-1 RNA load. Journal of Infectious Diseases 192, 1956–1961. doi: JID34637 [pii] 10.1086/497696.CrossRefGoogle ScholarPubMed
Keiser, J. and Utzinger, J. (2008). Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. Journal of the American Medical Association 299, 1937–1948. doi: 299/16/1937 [pii] 10.1001/jama.299.16.1937.Google ScholarPubMed
Labeaud, A. D., Malhotra, I., King, M. J., King, C. L. and King, C. H. (2009). Do antenatal parasite infections devalue childhood vaccination? PLoS Neglected Tropical Diseases 3, e442.CrossRefGoogle ScholarPubMed
Malla, N., Fomda, B. A. and Thokar, M. A. (2006). Serum cytokine levels in human ascariasis and toxocariasis. Parasitology Research 98, 345–348. doi: 10.1007/s00436-005-0081-z.CrossRefGoogle ScholarPubMed
Marti, H., Haji, H. J., Savioli, L., Chwaya, H. M., Mgeni, A. F., Ameir, J. S. and Hatz, C. (1996). A comparative trial of a single-dose ivermectin versus three days of albendazole for treatment of Strongyloides stercoralis and other soil-transmitted helminth infections in children. American Journal of Tropical Medicine and Hygiene 55, 477–481.CrossRefGoogle ScholarPubMed
Modjarrad, K., Chamot, E. and Vermund, S. H. (2008). Impact of small reductions in plasma HIV RNA levels on the risk of heterosexual transmission and disease progression. AIDS 22, 2179–2185. doi: 10.1097/QAD.0b013e328312c756 00002030-200810180-00015 [pii].CrossRefGoogle ScholarPubMed
Modjarrad, K., Zulu, I., Redden, D. T., Njobvu, L., Lane, H. C., Bentwich, Z. and Vermund, S. H. (2005). Treatment of intestinal helminths does not reduce plasma concentrations of HIV-1 RNA in coinfected Zambian adults. Journal of Infectious Diseases 192, 1277–1283. doi: JID33853 [pii] 10.1086/444543.CrossRefGoogle Scholar
Moreau, E. and Chauvin, A. (2010). Immunity against helminths: interactions with the host and the intercurrent infections. Journal of Biomedicine & Biotechnology 2010, 428593. doi: 10.1155/2010/428593 [doi].CrossRefGoogle ScholarPubMed
Mutapi, F. (2001). Heterogeneities in anti-schistosome humoral responses following chemotherapy. Trends in Parasitology 17, 518–524. doi: S1471-4922(01)02118-3 [pii].CrossRefGoogle ScholarPubMed
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. doi: 10.1179/136485906X118468.CrossRefGoogle ScholarPubMed
Nielsen, N. O., Simonsen, P. E., Dalgaard, P., Krarup, H., Magnussen, P., Magesa, S. and Friis, H. (2007). Effect of diethylcarbamazine on HIV load, CD4%, and CD4/CD8 ratio in HIV-infected adult Tanzanians with or without lymphatic filariasis: randomized double-blind and placebo-controlled cross-over trial. American Journal of Tropical Medicine and Hygiene 77, 507–513. doi: 77/3/507 [pii].CrossRefGoogle ScholarPubMed
Pit, D. S., Polderman, A. M., Baeta, S., Schulz-Key, H. and Soboslay, P. T. (2001). Parasite-specific antibody and cellular immune responses in human infected with Necator americanus and Oesophagostomum bifurcum. Parasitology Research 87, 722–729.Google ScholarPubMed
Roussilhon, C., Brasseur, P., Agnamey, P., Perignon, J. L. and Druilhe, P. (2010). Understanding human-Plasmodium falciparum immune interactions uncovers the immunological role of worms. PLoS One 5, e9309.CrossRefGoogle ScholarPubMed
Taylor, J. J., Krawczyk, C. M., Mohrs, M. and Pearce, E. J. (2009). Th2 cell hyporesponsiveness during chronic murine schistosomiasis is cell intrinsic and linked to GRAIL expression. Journal of Clinical Investigation 119, 1019–1028. doi: 36534 [pii] 10.1172/JCI36534.CrossRefGoogle ScholarPubMed
Troye-Blomberg, M. and Berzins, K. (2008). Immune interactions in malaria co-infections with other endemic infectious diseases: implications for the development of improved disease interventions. Microbes and Infection 10, 948–952. doi: S1286-4579(08)00191-3 [pii] 10.1016/j.micinf.2008.07.014.CrossRefGoogle ScholarPubMed
UNAIDS (2007). AIDS Epidemic Update. UNAIDS 2007.Google Scholar
Walson, J. L., Otieno, P. A., Mbuchi, M., Richardson, B. A., Lohman-Payne, B., Macharia, S. W., Overbaugh, J., Berkley, J., Sanders, E. J., Chung, M. H. and John-Stewart, G. C. (2008). Albendazole treatment of HIV-1 and helminth co-infection: a randomized, double-blind, placebo-controlled trial. AIDS 22, 1601–1609. doi: 10.1097/QAD.0b013e32830a502e 00002030-200808200-00009 [pii].CrossRefGoogle ScholarPubMed
Walson, J. L. and John-Stewart, G. (2008). Treatment of helminth co-infection in HIV-1 infected individuals in resource-limited settings. Cochrane Database of Systematic Reviews (1), CD006419. doi: 10.1002/14651858.CD006419.pub2.CrossRefGoogle ScholarPubMed
Walson, J. L., Herrin, B. R. and John-Stewart, G. (2009). Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database of Systematic Reviews (3), CD006419. doi: 10.1002/14651858.CD006419.pub3.CrossRefGoogle ScholarPubMed
WHO (2010). First WHO Report on Neglected Tropical Diseases 2010: Working to Overcome the Global Impact of Neglected Tropical Diseases. WHO/HTM/NTD/2010.1.Google Scholar
Wolday, D., Mayaan, S., Mariam, Z. G., Berhe, N., Seboxa, T., Britton, S., Galai, N., Landay, A. and Bentwich, Z. (2002). Treatment of intestinal worms is associated with decreased HIV plasma viral load. Journal of Acquired Immune Deficiency Syndromes 31, 56–62.CrossRefGoogle ScholarPubMed