Empiric Deworming and CD4 Count Recovery in HIV-Infected Ugandans Initiating Antiretroviral Therapy

PLoS Neglected Tropical Diseases

Volumn 8, Issue 8, 2014, Pages

  Lankowski, Alexander J ^a,b,c   Tsai, Alexander C ^c   Kanyesigye, Michael ^d   Bwana, Mwebesa ^d   Haberer, Jessica E ^c   Wenger, Megan ^e   Martin, Jeffrey N ^e   Bangsberg, David R ^c,d,f   Hunt, Peter W ^e   Siedner, Mark J ^c  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d MBARARA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Uganda)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBENDAZOLE; ANTHELMINTIC AGENT; HEMOGLOBIN; MEBENDAZOLE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; SOIL;

ADOLESCENT; ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; DISEASE COURSE; FEMALE; HELMINTHIASIS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MAJOR CLINICAL STUDY; MALE; MIXED INFECTION; OBSERVATIONAL STUDY; RETROSPECTIVE STUDY; SENSITIVITY ANALYSIS; TREATMENT OUTCOME; UGANDAN; WORM EXPULSION; HIV INFECTIONS; IMMUNOLOGY; PARASITOLOGY; SOIL; UGANDA;

ADULT; ANTI-HIV AGENTS; CD4 LYMPHOCYTE COUNT; COINFECTION; FEMALE; HELMINTHIASIS; HIV INFECTIONS; HUMANS; MALE; RETROSPECTIVE STUDIES; SOIL; UGANDA;

EID: 84923278235     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003036     Document Type: Article

References (64)

1. Joint United Nations Programme on HIV/AIDS (2013) Global report: UNAIDS report on the global AIDS epidemic 2013.
2. Braitstein P, Brinkhof MW, Dabis F, Schechter M, Boulle A, et al. (2006) Mortality of HIV-1-infected patients in the first year of antiretroviral therapy: comparison between low-income and high-income countries. Lancet 367: 817–824.
3. Bentwich Z, Kalinkovich A, Weisman Z, (1995) Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunol Today 16: 187–191.
4. Borkow G, Bentwich Z, (2006) HIV and helminth co-infection: is deworming necessary? Parasite Immunol 28: 605–612.
5. Brown M, Mawa PA, Kaleebu P, Elliott AM, (2006) Helminths and HIV infection: epidemiological observations on immunological hypotheses. Parasite Immunol 28: 613–623.
6. Blish CA, Sangare L, Herrin BR, Richardson BA, John-Stewart G, et al. (2010) Changes in plasma cytokines after treatment of ascaris lumbricoides infection in individuals with HIV-1 infection. J Infect Dis 201: 1816–1821.
7. Kalinkovich A, Borkow G, Weisman Z, Tsimanis A, Stein M, et al. (2001) Increased CCR5 and CXCR4 expression in Ethiopians living in Israel: environmental and constitutive factors. Clin Immunol 100: 107–117.
8. Lawn SD, Butera ST, Folks TM, (2001) Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin Microbiol Rev 14: 753–777.
9. Chachage M, Podola L, Clowes P, Nsojo A, Bauer A, et al. (2014) Helminth-associated systemic immune activation and HIV co-receptor expression: response to albendazole/praziquantel treatment. PLoS Negl Trop Dis 8: e2755.
10. El-Sadr WM, Lundgren J, Neaton JD, Gordin F, Abrams D, et al. (2006) CD4+ count-guided interruption of antiretroviral treatment. N Engl J Med 355: 2283–2296.
11. Hunt PW, Cao HL, Muzoora C, Ssewanyana I, Bennett J, et al. (2011) Impact of CD8+ T-cell activation on CD4+ T-cell recovery and mortality in HIV-infected Ugandans initiating antiretroviral therapy. AIDS 25: 2123–2131.
12. Hunt PW, (2012) HIV and inflammation: mechanisms and consequences. Curr HIV/AIDS Rep 9: 139–147.
13. Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE, et al. (2007) Control of neglected tropical diseases. N Engl J Med 357: 1018–1027.
14. Molyneux DH, Hotez PJ, Fenwick A, (2005) “Rapid-impact interventions”: how a policy of integrated control for Africa's neglected tropical diseases could benefit the poor. PLoS Med 2: e336.
15. Hotez PJ, Bundy DAP, Beegle K, et al. (2006) Helminth Infections: Soil-transmitted Helminth Infections and Schistosomiasis. In: Jamison DT, Breman JG, Measham AR, et al., editors. Disease Control Priorities in Developing Countries. 2nd edition. Washington D.C.: World Bank. Chapter 24. Available: http://www.ncbi.nlm.nih.gov/books/NBK11748/. Accessed 15 July 2014.
16. Santos FL, Cerqueira EJ, Soares NM, (2005) Comparison of the thick smear and Kato-Katz techniques for diagnosis of intestinal helminth infections. Rev Soc Bras Med Trop 38: 196–198.
17. Bergquist R, Johansen MV, Utzinger J, (2009) Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 25: 151–156.
18. Arndt MB, John-Stewart G, Richardson BA, Singa B, van Lieshout L, et al. (2013) Impact of helminth diagnostic test performance on estimation of risk factors and outcomes in HIV-positive adults. PLoS One 8: e81915.
19. Ojha SC, Jaide C, Jinawath N, Rotjanapan P, Baral P, (2014) Geohelminths: public health significance. J Infect Dev Ctries 8: 5–16.
20. Petti CA, Polage CR, Quinn TC, Ronald AR, Sande MA, (2006) Laboratory medicine in Africa: a barrier to effective health care. Clin Infect Dis 42: 377–382.
21. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, et al. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521–1532.
22. Walson JL, John-Stewart G, (2007) Treatment of helminth co-infection in individuals with HIV-1: A systematic review of the literature. PLoS Negl Trop Dis 1: e102.
23. Gerns HL, Sangare LR, Walson JL, (2012) Integration of deworming into HIV care and treatment: a neglected opportunity. PLoS Negl Trop Dis 6: e1738.
24. Walson JL, Otieno PA, Mbuchi M, Richardson BA, Lohman-Payne B, et al. (2008) Albendazole treatment of HIV-1 and helminth co-infection: a randomized, double-blind, placebo-controlled trial. AIDS 22: 1601–1609.
25. Modjarrad K, Zulu I, Redden DT, Njobvu L, Lane HC, et al. (2005) Treatment of intestinal helminths does not reduce plasma concentrations of HIV-1 RNA in coinfected Zambian adults. J Infect Dis 192: 1277–1283.
26. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, Mudenge B, et al. (2005) Schistosomiasis and HIV-1 infection in rural Zimbabwe: effect of treatment of schistosomiasis on CD4 cell count and plasma HIV-1 RNA load. J Infect Dis 192: 1956–1961.
27. Nielsen NO, Simonsen PE, Dalgaard P, Krarup H, Magnussen P, et al. (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. Am J Trop Med Hyg 77: 507–513.
28. Walson JL, Herrin BR, John-Stewart G, (2009) Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database Syst Rev CD006419.
29. Walson J, Singa B, Sangare L, Naulikha J, Piper B, et al. (2012) Empiric deworming to delay HIV disease progression in adults with HIV who are ineligible for initiation of antiretroviral treatment (the HEAT study): a multi-site, randomised trial. Lancet Infect Dis 12: 925–932.
30. World Health Organization (2013) Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection. Available: http://apps.who.int/iris/bitstream/10665/85321/1/9789241505727_eng.pdf. Accessed 9 November 2013.
31. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365–1371.
32. Estes JD, Harris LD, Klatt NR, Tabb B, Pittaluga S, et al. (2010) Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog 6: e1001052.
33. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, et al. (2011) Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 204: 1217–1226.
34. Tien PC, Choi AI, Zolopa AR, Benson C, Tracy R, et al. (2010) Inflammation and mortality in HIV-infected adults: analysis of the FRAM study cohort. J Acquir Immune Defic Syndr 55: 316–322.
35. Kuller LH, Tracy R, Belloso W, De Wit S, Drummond F, et al. (2008) Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 5: e203.
36. Kalayjian RC, Machekano RN, Rizk N, Robbins GK, Gandhi RT, et al. (2010) Pretreatment levels of soluble cellular receptors and interleukin-6 are associated with HIV disease progression in subjects treated with highly active antiretroviral therapy. J Infect Dis 201: 1796–1805.
37. Boulware DR, Hullsiek KH, Puronen CE, Rupert A, Baker JV, et al. (2011) Higher levels of CRP, D-dimer, IL-6, and hyaluronic acid before initiation of antiretroviral therapy (ART) are associated with increased risk of AIDS or death. J Infect Dis 203: 1637–1646.
38. Sandler NG, Wand H, Roque A, Law M, Nason MC, et al. (2011) Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 203: 780–790.
39. Hatano H, (2013) Immune activation and HIV persistence: considerations for novel therapeutic interventions. Curr Opin HIV AIDS 8: 211–216.
40. Brooker S, Kabatereine NB, Tukahebwa EM, Kazibwe F, (2004) Spatial analysis of the distribution of intestinal nematode infections in Uganda. Epidemiol Infect 132: 1065–1071.
41. Kabatereine NB, Tukahebwa EM, Kazibwe F, Twa-Twa JM, Barenzi JF, et al. (2005) Soil-transmitted helminthiasis in Uganda: epidemiology and cost of control. Trop Med Int Health 10: 1187–1189.
42. Shapiro AE, Tukahebwa EM, Kasten J, Clarke SE, Magnussen P, et al. (2005) Epidemiology of helminth infections and their relationship to clinical malaria in southwest Uganda. Trans R Soc Trop Med Hyg 99: 18–24.
43. Clements AC, Deville MA, Ndayishimiye O, Brooker S, Fenwick A, (2010) Spatial co-distribution of neglected tropical diseases in the east African great lakes region: revisiting the justification for integrated control. Trop Med Int Health 15: 198–207.
44. Global Atlas of Helminth Infections. Available: http://www.thiswormyworld.org/maps/2013/distribution-of-soil-transmitted-helminth-survey-data-in-uganda. Accessed 22 April 2014.
45. Global Atlas of Helminth Infections. Available: http://www.thiswormyworld.org/sites/www.thiswormyworld.org/files/images/maps/Uganda_Schisto.png. Accessed 22 April 2014.
46. Kabatereine NB, Brooker S, Tukahebwa EM, Kazibwe F, Onapa AW, (2004) Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control. Trop Med Int Health 9: 372–380.
47. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, et al. (2004) Hookworm infection. N Engl J Med 351: 799–807.
48. Jia TW, Melville S, Utzinger J, King CH, Zhou XN, (2012) Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis 6: e1621.
49. Huber PJ, (1967) The behavior of maximum likelihood estimates under nonstandard conditions. Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability 1: 221–233.
50. White H, (1980) A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. Econometrica 48: 817–830.
51. Walson JL, Stewart BT, Sangare L, Mbogo LW, Otieno PA, et al. (2010) Prevalence and correlates of helminth co-infection in Kenyan HIV-1 infected adults. PLoS Negl Trop Dis 4: e644.
52. Cingolani A, Cozzi Lepri A, Castagna A, Goletti D, De Luca A, et al. (2012) Impaired CD4 T-cell count response to combined antiretroviral therapy in antiretroviral-naive HIV-infected patients presenting with tuberculosis as AIDS-defining condition. Clin Infect Dis 54: 853–861.
53. Kaufmann GR, Bloch M, Finlayson R, Zaunders J, Smith D, et al. (2002) The extent of HIV-1-related immunodeficiency and age predict the long-term CD4 T lymphocyte response to potent antiretroviral therapy. AIDS 16: 359–367.
54. Elliott AM, Mawa PA, Joseph S, Namujju PB, Kizza M, et al. (2003) Associations between helminth infection and CD4+ T cell count, viral load and cytokine responses in HIV-1-infected Ugandan adults. Trans R Soc Trop Med Hyg 97: 103–108.
55. Brown M, Kizza M, Watera C, Quigley MA, Rowland S, et al. (2004) Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. J Infect Dis 190: 1869–1879.
56. Modjarrad K, Zulu I, Redden DT, Njobvu L, Freedman DO, et al. (2005) 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 73: 777–782.
57. Knopp S, Mohammed KA, Stothard JR, Khamis IS, Rollinson D, et al. (2010) Patterns and risk factors of helminthiasis and anemia in a rural and a peri-urban community in Zanzibar, in the context of helminth control programs. PLoS Negl Trop Dis 4: e681.
58. Keiser J, Utzinger J, (2008) Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 299: 1937–1948.
59. Yazdanbakhsh M, Kremsner PG, van Ree R, (2002) Allergy, parasites, and the hygiene hypothesis. Science 296: 490–494.
60. Fallon PG, Mangan NE, (2007) Suppression of TH2-type allergic reactions by helminth infection. Nat Rev Immunol 7: 220–230.
61. Mkhize-Kwitshana ZL, Taylor M, Jooste P, Mabaso ML, Walzl G, (2011) The influence of different helminth infection phenotypes on immune responses against HIV in co-infected adults in South Africa. BMC Infect Dis 11: 273.
62. Chachage M, Podola L, Clowes P, Nsojo A, Bauer A, et al. (2014) Helminth-associated systemic immune activation and HIV co-receptor expression: response to albendazole/praziquantel treatment. PLoS Negl Trop Dis 8: e2755.
63. Boyett D, Hsieh MH, (2014) Wormholes in host defense: how helminths manipulate host tissues to survive and reproduce. PLoS Pathog 10: e1004014.
64. Wolday D, Mayaan S, Mariam ZG, Berhe N, Seboxa T, et al. (2002) Treatment of intestinal worms is associated with decreased HIV plasma viral load. J Acquir Immune Defic Syndr 31: 56–62.