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Tropical Parasitic Infections in Individuals Infected With HIV

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Abstract

Purpose of Review

Neglected tropical diseases share both geographic and socio-behavioral epidemiological risk factors with HIV infection. In this literature review, we describe interactions between parasitic diseases and HIV infection, with a focus on the impact of parasitic infections on HIV infection risk and disease progression, and the impact of HIV infection on clinical characteristics of tropical parasitic infections. We limit our review to tropical parasitic infections of the greatest public health burden, and exclude discussion of classic HIV-associated opportunistic infections that have been well reviewed elsewhere.

Recent Findings

Tropical parasitic infections, HIV infection, and treatment with antiretroviral therapy alter host immunity, which can impact susceptibility, transmissibility, diagnosis, and severity of both HIV and parasitic infections. These relationships have a broad range of consequences, from putatively increasing susceptibility to HIV acquisition, as in the case of schistosomiasis, to decreasing risk of protozoal infections through pharmacokinetic interactions between antiretroviral therapy and antiparasitic agents, as in the case of malaria. However, despite this intimate interplay in pathophysiology and a broad overlap in epidemiology, there is a general paucity of data on the interactions between HIV and tropical parasitic infections, particularly in the era of widespread antiretroviral therapy availability.

Summary

Additional data are needed to motivate clinical recommendations for detection and management of parasitic infections in HIV-infected individuals, and to consider the implications of and potential opportunity granted by HIV treatment programs on parasitic disease control.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 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(8):e412.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Downs JA, et al. Renal dysfunction and schistosomiasis among HIV-infected patients starting antiretroviral therapy in Mwanza. Tanzania AIDS. 2015;29(18):2532–3.

  3. Mpondo BC, Neilson E. Renal dysfunction among HIV-infected patients starting antiretroviral therapy in Mwanza, Tanzania. AIDS. 2015;29(18):2531–2.

    Article  PubMed  Google Scholar 

  4. Otieno RO, et al. Increased severe anemia in HIV-1-exposed and HIV-1-positive infants and children during acute malaria. AIDS. 2006;20(2):275–80.

    Article  PubMed  Google Scholar 

  5. Dooley KE, Flexner C, Andrade AS. Drug interactions involving combination antiretroviral therapy and other anti-infective agents: repercussions for resource-limited countries. J Infect Dis. 2008;198(7):948–61.

    Article  CAS  PubMed  Google Scholar 

  6. Nissapatorn V, Sawangjaroen N. Parasitic infections in HIV infected individuals: diagnostic & therapeutic challenges. Indian J Med Res. 2011;134(6):878–97.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Karagiannis-Voules D-A, et al. Spatial and temporal distribution of soil-transmitted helminth infection in sub-Saharan Africa a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 15(1):74–84.

  8. Becker Y. The changes in the T helper 1 Th1 and T helper 2 Th2 cytokine balance during HIV-1 infection are indicative of an allergic response to viral proteins that may be reversed by Th2 cytokine inhibitors and immune response modifiers—a review and hypothesis. Virus Genes. 2004;28(1):5–18.

    Article  CAS  PubMed  Google Scholar 

  9. Range N, et al. HIV and parasitic co-infections in tuberculosis patients: a cross-sectional study in Mwanza. Tanzania Ann Trop Med Parasitol. 2007;101(4):343–51.

  10. Webb EL, et al. The effect of anthelmintic treatment during pregnancy on HIV plasma viral load: results from a randomized, double-blind, placebo-controlled trial in Uganda. J Acquir Immune Defic Syndr. 2012;60(3):307–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mulu A, Maier M, Liebert UG. Deworming of intestinal helminths reduces HIV-1 subtype C viremia in chronically co-infected individuals. Int J Infect Dis. 2013;17(10):e897–901.

    Article  PubMed  Google Scholar 

  12. Hosseinipour MC, et al. HIV and parasitic infection and the effect of treatment among adult outpatients in Malawi. J Infect Dis. 2007;195(9):1278–82.

    Article  PubMed  Google Scholar 

  13. •• Walson J, et al. 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. 2012;12(12):925–32. Empiric deworming with quarterly albendazole and annual praziquantel compared to no deworming did not delay progression of HIV disease in ART-ineligible adults in Kenya, regardless of the presence of helminth co-infection

    Article  PubMed  Google Scholar 

  14. Walson JL, et al. Albendazole treatment of HIV-1 and helminth co-infection a randomized, double-blind, placebo-controlled trial. AIDS. 2008;22(13):1601–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Modjarrad K, et al. Treatment of intestinal helminths does not reduce plasma concentrations of HIV-1 RNA in coinfected Zambian adults. J Infect Dis. 2005;192(7):1277–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lankowski AJ, et al. Empiric deworming and CD4 count recovery in HIV-infected Ugandans initiating antiretroviral therapy. PLoS Negl Trop Dis. 2014;8(8):e3036.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Sangare LR, et al. Species-specific treatment effects of helminth/HIV-1 co-infection a systematic review and meta-analysis. Parasitology. 2011;138(12):1546–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. • Means AR, et al. Antihelminthics in helminth-endemic areas: effects on HIV disease progression. Cochrane Database Syst Rev. 2016;4:CD006419. Means et al. performed a meta-analysis of 8 RCTs examining the effect of treating either empirically or confirmed parasitic infection with anthelmintic therapy on HIV disease and found that using empiric anthelmintic treatment provided no significant difference in HIV disease markers, however, treating confirmed parasitic infection resulted in modest CD4+ T cell expansion and HIV RNA viral load suppression at 12 weeks. The effect on viral load was influenced by the inclusion of a study of praziquantel for schistosomiasis. The use of ART in this meta-analysis was limited to two studies

    PubMed  Google Scholar 

  19. Corti N, et al. Effect of ritonavir on the pharmacokinetics of the benzimidazoles albendazole and mebendazole: an interaction study in healthy volunteers. Eur J Clin Pharmacol. 2009;65(10):999–1006.

    Article  CAS  PubMed  Google Scholar 

  20. Pawluk SA, et al. A review of pharmacokinetic drug-drug interactions with the anthelmintic medications albendazole and mebendazole. Clin Pharmacokinet. 2015;54(4):371–83.

    Article  CAS  PubMed  Google Scholar 

  21. Jongwutiwes U, et al. Prevalence and risk factors of acquiring Strongyloides stercoralis infection among patients attending a tertiary hospital in Thailand. Pathog Glob Health. 2014;108(3):137–40.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Chordia P, et al. Risk factors for acquiring Strongyloides stercoralis infection among patients attending a tertiary hospital in south India. Indian J Med Microbiol. 2011;29(2):147–51.

    Article  CAS  PubMed  Google Scholar 

  23. Adamu H, Wegayehu T, Petros B. High prevalence of diarrhoegenic intestinal parasite infections among non-ART HIV patients in Fitche Hospital. Ethiopia PLoS One. 2013;8(8):e72634.

  24. Walson JL, et al. Prevalence and correlates of helminth co-infection in Kenyan HIV-1 infected adults. PLoS Negl Trop Dis. 2010;4(3):e644.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Fontanet AL, et al. Epidemiology of infections with intestinal parasites and human immunodeficiency virus HIV among sugar-estate residents in Ethiopia. Ann Trop Med Parasitol. 2000;94(3):269–78.

    Article  CAS  PubMed  Google Scholar 

  26. Gassama 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(4):192–8.

    Article  CAS  PubMed  Google Scholar 

  27. Bachur TP, et al. Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Braz J Infect Dis. 2008;12(2):115–22.

    Article  PubMed  Google Scholar 

  28. Mkhize-Kwitshana ZL, Mabaso ML, Walzl G. Proliferative capacity and cytokine production by cells of HIV-infected and uninfected adults with different helminth infection phenotypes in South Africa. BMC Infect Dis. 2014;14:499.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Abossie A, Petros B. Deworming and the immune status of HIV positive pre-antiretroviral therapy individuals in Arba Minch, Chencha and Gidole hospitals, Southern Ethiopia. BMC Res Notes. 2015;8:483.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Kroidl I, et al. Correction: Prevalence of Lymphatic Filariasis and Treatment Effectiveness of Albendazole/ Ivermectin in Individuals with HIV Co-infection in Southwest-Tanzania. PLoS Negl Trop Dis. 2016;10(8):e0004967.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Tafatatha T, et al. Human immunodeficiency virus, antiretroviral therapy and markers of lymphatic filariasis infection: a cross-sectional study in rural northern Malawi. PLoS Negl Trop Dis. 2015;9(6):e0003825.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Talaat KR, et al. Treatment of W. bancrofti (Wb) in HIV/Wb coinfections in South India. PLoS Negl Trop Dis. 2015;9(3):e0003622.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Nielsen NO, et al. Cross-sectional relationship between HIV, lymphatic filariasis and other parasitic infections in adults in coastal northeastern Tanzania. Trans R Soc Trop Med Hyg. 2006;100(6):543–50.

    Article  CAS  PubMed  Google Scholar 

  34. •• Kroidl I, et al. Effect of Wuchereria bancrofti infection on HIV incidence in southwest Tanzania a prospective cohort study. Lancet. 2016; A prospective study in Tanzania enrolled HIV-negative adolescents and adults with and without lymphatic filariasis and found that over a 5-year period, there was a significantly higher incidence of HIV acquisition among those with lymphatic filariasis

  35. Petersen HH, et al. The effect of HIV on filarial-specific antibody response before and after treatment with diethylcarbamazine in Wuchereria bancrofti infected individuals. Parasitol Int. 2009;58(2):141–4.

    Article  CAS  PubMed  Google Scholar 

  36. Kipp W, Bamuhiiga J, Rubaale T. Simulium neavei-transmitted onchocerciasis: HIV infection increases severity of onchocercal skin disease in a small sample of patients. Trans R Soc Trop Med Hyg. 2003;97(3):310–1.

    Article  PubMed  Google Scholar 

  37. Tawill SA, et al. Impaired antibody responses and loss of reactivity to Onchocerca volvulus antigens by HIV-seropositive onchocerciasis patients. Trans R Soc Trop Med Hyg. 1996;90(1):85–9.

    Article  CAS  PubMed  Google Scholar 

  38. Sentongo E, et al. T cell responses in coinfection with Onchocerca volvulus and the human immunodeficiency virus type 1. Parasite Immunol. 1998;20(9):431–9.

    Article  CAS  PubMed  Google Scholar 

  39. Katawa G, et al. Hyperreactive onchocerciasis is characterized by a combination of Th17-Th2 immune responses and reduced regulatory T cells. PLoS Negl Trop Dis. 2015;9(1):e3414.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Hoerauf A, Brattig N. Resistance and susceptibility in human onchocerciasis beyond Th1 vs. Th2. Trends Parasitol. 2002;18(1):25–31.

    Article  CAS  PubMed  Google Scholar 

  41. Serpa JA, et al. Neurocysticercosis in the HIV era: a case report and review of the literature. Am J Trop Med Hyg. 2007;77(1):113–7.

    PubMed  Google Scholar 

  42. Anand KS, et al. HIV-Associated Neurocysticercosis. J Int Assoc Provid AIDS Care. 2015;14(2):120–2.

    Article  PubMed  Google Scholar 

  43. Tharmalingam J, et al. Host Th1/Th2 immune response to Taenia solium cyst antigens in relation to cyst burden of neurocysticercosis. Parasite Immunol. 2016;38(10):628–34.

    Article  CAS  PubMed  Google Scholar 

  44. Ran B, et al. Surgical treatment of hepatic cystic echinococcosis in patients co-infected with HIV/AIDS. J Helminthol. 2016;90(1):125–8.

    Article  CAS  PubMed  Google Scholar 

  45. Wahlers K, et al. Cystic echinococcosis in South Africa the worst yet to come? Acta Trop. 2013;128(1):1–6.

    Article  PubMed  Google Scholar 

  46. Shenoy VV, et al. Pulmonary hydatid cyst in HIV-1 disease. J Assoc Physicians India. 2005;53:1070–2.

    CAS  PubMed  Google Scholar 

  47. Erayman I, et al. Primary spinal hydatid cyst in a patient with acquired immunodeficiency syndrome. Eur Spine J. 2011;20(Suppl 2):S235–8.

    Article  PubMed  Google Scholar 

  48. Ozoilo KN, et al. Anterior abdominal wall hydatid cyst; an unusual presentation. Niger J Med. 2007;16(2):181–2.

    Article  CAS  PubMed  Google Scholar 

  49. Keskin F, Erdi F, Fatih M, Erdal K, Karatas Y. Recurrence of primary spinal cyst hydatid in a HIV (+) patient: a case report. J Neurol Sci. 2013;30(2):455–60.

    Google Scholar 

  50. Kjetland EF, et al. Genital schistosomiasis and its unacknowledged role on HIV transmission in the STD intervention studies. Int J STD AIDS. 2014;25(10):705–15.

    Article  PubMed  Google Scholar 

  51. Jourdan PM, et al. HIV target cells in Schistosoma haematobium-infected female genital mucosa. Am J Trop Med Hyg. 2011;85(6):1060–4.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Kjetland EF, et al. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS. 2006;20(4):593–600.

    Article  PubMed  Google Scholar 

  53. Secor WE. The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Curr Opin HIV AIDS. 2012;7(3):254–9.

    Article  CAS  PubMed  Google Scholar 

  54. Efraim L, et al. Schistosomiasis and impaired response to antiretroviral therapy among HIV-infected patients in Tanzania. J Acquir Immune Defic Syndr. 2013;62(5):e153–6.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Lawn SD, et al. The effect of treatment of schistosomiasis on blood plasma HIV-1 RNA concentration in coinfected individuals. AIDS. 2000;14(16):2437–43.

    Article  CAS  PubMed  Google Scholar 

  56. Kallestrup P, et al. 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. 2005;192(11):1956–61.

    Article  CAS  PubMed  Google Scholar 

  57. Brown M, et al. Treatment of Schistosoma mansoni infection increases helminth-specific type 2 cytokine responses and HIV-1 loads in coinfected Ugandan adults. J Infect Dis. 2005;191(10):1648–57.

    Article  CAS  PubMed  Google Scholar 

  58. Grimwade K, et al. HIV infection as a cofactor for severe falciparum malaria in adults living in a region of unstable malaria transmission in South Africa. AIDS. 2004;18(3):547–54.

    Article  PubMed  Google Scholar 

  59. Flateau C, Le Loup G, Pialoux G. Consequences of HIV infection on malaria and therapeutic implications: a systematic review. Lancet Infect Dis. 2011;11(7):541–56.

    Article  PubMed  Google Scholar 

  60. Alemu A, et al. Effect of malaria on HIV/AIDS transmission and progression. Parasit Vectors. 2013;6:18.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Hoffman IF, et al. The effect of Plasmodium falciparum malaria on HIV-1 RNA blood plasma concentration. AIDS. 1999;13(4):487–94.

    Article  CAS  PubMed  Google Scholar 

  62. Albrecht H. Leishmaniosis: new perspectives on an underappreciated opportunistic infection. AIDS. 1998;12(16):2225–6.

    Article  CAS  PubMed  Google Scholar 

  63. Albrecht H, et al. Visceral leishmaniasis emerging as an important opportunistic infection in HIV-infected persons living in areas nonendemic for Leishmania donovani. Arch Pathol Lab Med. 1996;120(2):189–98.

    CAS  PubMed  Google Scholar 

  64. Handler MZ, et al. Cutaneous and mucocutaneous leishmaniasis: differential diagnosis, diagnosis, histopathology, and management. J Am Acad Dermatol. 2015;73(6):911–26. 927-8

    Article  PubMed  Google Scholar 

  65. Couppie P, et al. Comparative study of cutaneous leishmaniasis in human immunodeficiency virus HIV-infected patients and non-HIV-infected patients in French Guiana. Br J Dermatol. 2004;151(6):1165–71.

    Article  CAS  PubMed  Google Scholar 

  66. Orsini M, et al. High frequency of asymptomatic Leishmania spp. infection among HIV-infected patients living in endemic areas for visceral leishmaniasis in Brazil. Trans R Soc Trop Med Hyg. 2012;106(5):283–8.

    Article  PubMed  Google Scholar 

  67. Lyons S, Veeken H, Long J. Visceral leishmaniasis and HIV in Tigray. Ethiopia Trop Med Int Health. 2003;8(8):733–9.

  68. Russo R, et al. Clinical survey of leishmania/HIV co-infection in Catania, Italy: the impact of highly active antiretroviral therapy (HAART). Ann Trop Med Parasitol. 2003;97(Suppl 1):149–55.

    Article  PubMed  Google Scholar 

  69. Sartori AM, et al. Trypanosoma cruzi parasitemia in chronic Chagas disease: comparison between human immunodeficiency virus (HIV)-positive and HIV-negative patients. J Infect Dis. 2002;186(6):872–5.

    Article  PubMed  Google Scholar 

  70. Martins-Melo FR, et al. Mortality related to Chagas Disease and HIV/AIDS coinfection in Brazil. J Trop Med. 2012;2012:534649.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Kuepfer I, et al. Clinical presentation of T.b. rhodesiense sleeping sickness in second stage patients from Tanzania and Uganda. PLoS Negl Trop Dis. 2011;5(3):e968.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Pepin J, et al. The impact of human immunodeficiency virus infection on the epidemiology and treatment of Trypanosoma brucei gambiense sleeping sickness in Nioki. Zaire Am J Trop Med Hyg. 1992;47(2):133–40.

  73. Meda HA, et al. Human immunodeficiency virus infection and human African trypanosomiasis a case-control study in Cote dIvoire. Trans R Soc Trop Med Hyg. 1995;89(6):639–43.

    Article  CAS  PubMed  Google Scholar 

  74. Matete GO, Kajejo OA. Human African trypanosomiasis and human immunodeficiency virus co-infection in Western Kenya. East Afr Med J. 2005;82(1):20–3.

    Article  CAS  PubMed  Google Scholar 

  75. Pearson MS, et al. Molecular mechanisms of hookworm disease stealth, virulence, and vaccines. J Allergy Clin Immunol. 2012;130(1):13–21.

    Article  CAS  PubMed  Google Scholar 

  76. Brooker S, Hotez PJ, Bundy DA. Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl Trop Dis. 2008;2(9):e291.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Brabin B, et al. Anaemia prevention for reduction of mortality in mothers and children. Trans R Soc Trop Med Hyg. 2003;97(1):36–8.

    Article  PubMed  Google Scholar 

  78. Finkelstein JL, et al. Predictors of anaemia and iron deficiency in HIV-infected pregnant women in Tanzania: a potential role for vitamin D and parasitic infections. Public Health Nutr. 2012;15(5):928–37.

    Article  PubMed  Google Scholar 

  79. Gyorkos TW, Gilbert NL. Blood drain: soil-transmitted helminths and anemia in pregnant women. PLoS Negl Trop Dis. 2014;8(7):e2912.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Hotez PJ, et al. Hookworm infection. N Engl J Med. 2004;351(8):799–807.

    Article  CAS  PubMed  Google Scholar 

  81. Kipyegen CK, Shivairo RS, Odhiambo RO. Prevalence of intestinal parasites among HIV patients in Baringo, Kenya. Pan Afr Med J. 2012;13:37.

    PubMed  PubMed Central  Google Scholar 

  82. Mwambete KD, Justin-Temu M, Peter S. Prevalence and management of intestinal helminthiasis among HIV-infected patients at Muhimbili National Hospital. J Int Assoc Physicians AIDS Care (Chic). 2010;9(3):150–6.

    Article  Google Scholar 

  83. Idindili B, et al. HIV and parasitic co-infections among patients seeking care at health facilities in Tanzania. Tanzan J Health Res. 2011;13(4):75–85.

    Article  PubMed  Google Scholar 

  84. Morawski BM, et al. Hookworm infection is associated with decreased CD4+ T cell counts in HIV-infected adult Ugandans. PLoS Negl Trop Dis. 2017;11(5):e0005634.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Brown M, et al. Helminths and HIV infection: epidemiological observations on immunological hypotheses. Parasite Immunol. 2006;28(11):613–23.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Stylianou E, et al. IL-10 in HIV infection: increasing serum IL-10 levels with disease progression—down-regulatory effect of potent anti-retroviral therapy. Clin Exp Immunol. 1999;116(1):115–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Kwon DS, Kaufmann DE. Protective and detrimental roles of IL-10 in HIV pathogenesis. Eur Cytokine Netw. 2010;21(3):208–14.

    CAS  PubMed  Google Scholar 

  88. Chachage M, Geldmacher C. Immune system modulation by helminth infections: potential impact on HIV transmission and disease progression. Adv Exp Med Biol. 2014;828:131–49.

    Article  PubMed  Google Scholar 

  89. Inoue MNS, Chadeka E, Mutung F, Osada-Oka M. Relationship between Mycobacterium tuberculosis and hookworm infections among school Children in Mbita, Kenya. Journal of Tropical Diseases & Public Health. 2013;1:120.

    Google Scholar 

  90. Thomas TA, et al. Malnutrition and helminth infection affect performance of an interferon gamma-release assay. Pediatrics. 2010;126(6):e1522–9.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Li XX, et al. Profiling B and T cell immune responses to co-infection of Mycobacterium tuberculosis and hookworm in humans. Infect Dis Poverty. 2015;4:20.

    Article  PubMed  PubMed Central  Google Scholar 

  92. George PJ, et al. Modulation of mycobacterial-specific Th1 and Th17 cells in latent tuberculosis by coincident hookworm infection. J Immunol. 2013;190(10):5161–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Hasanain AF, et al. Hookworm infection among patients with pulmonary tuberculosis: impact of co-infection on the therapeutic failure of pulmonary tuberculosis. Int J Mycobacteriol. 2015;4(4):318–22.

    Article  PubMed  Google Scholar 

  94. George PJ, et al. Evidence of microbial translocation associated with perturbations in T cell and antigen-presenting cell homeostasis in hookworm infections. PLoS Negl Trop Dis. 2012;6(10):e1830.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Micro. 2012;10(9):655–66.

    Article  CAS  Google Scholar 

  96. Brown M, et al. Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. J Infect Dis. 2004;190(10):1869–79.

    Article  PubMed  Google Scholar 

  97. Ivan E, et al. Effect of deworming on disease progression markers in HIV-1-infected pregnant women on antiretroviral therapy a longitudinal observational study from Rwanda. Clin Infect Dis. 2015;60(1):135–42.

    Article  CAS  PubMed  Google Scholar 

  98. Abate E, et al. Effects of albendazole on the clinical outcome and immunological responses in helminth co-infected tuberculosis patients: a double blind randomised clinical trial. Int J Parasitol. 2015;45(2–3):133–40.

    Article  CAS  PubMed  Google Scholar 

  99. Janssen S, et al. Impact of anti-retroviral treatment and cotrimoxazole prophylaxis on helminth infections in HIV-infected patients in Lambarene. Gabon PLoS Negl Trop Dis. 2015;9(5):e0003769.

  100. Riccardi N, et al. Antiretroviral and antiparasitic therapy management in an expatriate patient with loiasis and HIV: a case report. J Trop Dis. 2015;4(178):2.

    Google Scholar 

  101. Ashcroft MT, Milner PF, Wood CW. Haemoglobin concentration, eosinophilia and intestinal helminths in children in rural Jamaica. Trans R Soc Trop Med Hyg. 1969;63(6):811–20.

    Article  CAS  PubMed  Google Scholar 

  102. Simeon DT, et al. Treatment of Trichuris trichiura infections improves growth, spelling scores and school attendance in some children. J Nutr. 1995;125(7):1875–83.

    CAS  PubMed  Google Scholar 

  103. Akinbo FO, Okaka CE, Omoregie R. Prevalence of intestinal parasitic infections among HIV patients in Benin City. Nigeria Libyan J Med. 2010;5

  104. Lindo JF, et al. Intestinal parasitic infections in human immunodeficiency virus HIV-positive and HIV-negative individuals in San Pedro Sula, Honduras. Am J Trop Med Hyg. 1998;58(4):431–5.

    Article  CAS  PubMed  Google Scholar 

  105. Chachage M, et al. Helminth-associated systemic immune activation and HIV co-receptor expression: response to albendazole/praziquantel treatment. PLoS Negl Trop Dis. 2014;8(3):e2755.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Siegel MO, Simon GL. Is human immunodeficiency virus infection a risk factor for Strongyloides stercoralis hyperinfection and dissemination. PLoS Negl Trop Dis. 2012;6(7):e1581.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Viney ME, et al. Why does HIV infection not lead to disseminated strongyloidiasis? J Infect Dis. 2004;190(12):2175–80.

    Article  PubMed  Google Scholar 

  108. Bollela VR, et al. Fulminant gastrointestinal hemorrhage due to Strongyloides stercoralis hyperinfection in an AIDS patient. Rev Soc Bras Med Trop. 2013;46(1):111–3.

    Article  PubMed  Google Scholar 

  109. Feitosa G, et al. High prevalence of giardiasis and stronglyloidiasis among HIV-infected patients in Bahia, Brazil. Braz J Infect Dis. 2001;5(6):339–44.

    Article  CAS  PubMed  Google Scholar 

  110. Mohammed Awole SG-S, Kassa T, Kibru G. Prevalence of intestinal parasites in HIV-infected adult patients in Southwestern Ethiopia. Ethiop J Health Dev. 2003;17(1):71–8.

    Google Scholar 

  111. Cabral AC, et al. Clinical conditions associated with intestinal strongyloidiasis in Rio de Janeiro, Brazil. Rev Soc Bras Med Trop. 2015;48(3):321–5.

    Article  PubMed  Google Scholar 

  112. Getaneh A, Medhin G, Shimelis T. Cryptosporidium and Strongyloides stercoralis infections among people with and without HIV infection and efficiency of diagnostic methods for Strongyloides in Yirgalem Hospital, southern Ethiopia. BMC Res Notes. 2010;3:90.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Kaminsky RL, Reyes-Garcia SZ, Zambrano LI. Unsuspected Strongyloides stercoralis infection in hospital patients with comorbidity in need of proper management. BMC Infect Dis. 2016;16:98.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Ursini T, et al. Late diagnosis of central nervous system involvement associated with lethal dissemination of Strongyloides stercoralis in an advanced HIV patient from Nigeria. Int J Infect Dis. 2013;17(4):e280–2.

    Article  PubMed  Google Scholar 

  115. Jaka H, et al. Strongyloides stercoralis infection presenting as an unusual cause of massive upper gastrointestinal bleeding in an immunosuppressed patient: a case report. Trop Dr. 2013;43(1):46–8.

    Google Scholar 

  116. Teklemariam Z, et al. Prevalence of intestinal parasitic infection among HIV positive persons who are naive and on antiretroviral treatment in Hiwot Fana Specialized University Hospital, Eastern Ethiopia. ISRN AIDS. 2013;2013:324329.

    Article  PubMed  PubMed Central  Google Scholar 

  117. CDC Parasites-Strongyloides. Resources for Health Professionals, 2016.

  118. Karagiannis-Voules DA, et al. Geostatistical modelling of soil-transmitted helminth infection in Cambodia do socioeconomic factors improve predictions? Acta Trop. 2015;141(Pt B):204–12.

    Article  PubMed  Google Scholar 

  119. Wani I, et al. Intestinal ascariasis in children. World J Surg. 2010;34(5):963–8.

    Article  PubMed  Google Scholar 

  120. Cooper PJ, et al. Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis. 2000;182(4):1207–13.

    Article  CAS  PubMed  Google Scholar 

  121. Mkhize-Kwitshana ZL, et al. The influence of different helminth infection phenotypes on immune responses against HIV in co-infected adults in South Africa. BMC Infect Dis. 2011;11:273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. CDC, Parasites-Ascariasis: Resources for Health Professionals. 2013.

  123. WHO, Lymphatic Filariasis: Fact Sheet. 2016.

  124. UNAIDS, Global AIDS Update. 2016.

  125. Alvar J, et al. The relationship between leishmaniasis and AIDS: the second 10 years. Clin Microbiol Rev. 2008;21(2):334–59. table of contents

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Gopinath R, et al. Filarial infections increase susceptibility to human immunodeficiency virus infection in peripheral blood mononuclear cells in vitro. J Infect Dis. 2000;182(6):1804–8.

    Article  CAS  PubMed  Google Scholar 

  127. Babu S, Kumaraswami V, Nutman TB. Alternatively activated and immunoregulatory monocytes in human filarial infections. J Infect Dis. 2009;199(12):1827–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Nielsen NO, et al. Co-infection with subclinical HIV and Wuchereria bancrofti, and the role of malaria and hookworms, in adult Tanzanians: infection intensities, CD4/CD8 counts and cytokine responses. Trans R Soc Trop Med Hyg. 2007;101(6):602–12.

    Article  CAS  PubMed  Google Scholar 

  129. Dunyo SK, Nkrumah FK, Simonsen PE. Single-dose treatment of Wuchereria bancrofti infections with ivermectin and albendazole alone or in combination: evaluation of the potential for control at 12 months after treatment. Trans R Soc Trop Med Hyg. 2000;94(4):437–43.

    Article  CAS  PubMed  Google Scholar 

  130. Taylor MJ, et al. Macrofilaricidal activity after doxycycline treatment of Wuchereria bancroft a double-blind, randomised placebo-controlled trial. Lancet. 365(9477):2116–21.

  131. Foster A, Resnikoff S. The impact of Vision 2020 on global blindness. Eye (Lond). 2005;19(10):1133–5.

    Article  CAS  Google Scholar 

  132. Friedrich MJ. Mexico Says Adios to Onchocerciasis. JAMA. 2015;314(19):2014.

    Google Scholar 

  133. Pan American Health Organization, WHO verifies that Guatemala is the fourth country in the world to eliminate transmission of 'river blindness'. 2016.

  134. Schweitzer BI, Dicker AP, Bertino JR. Dihydrofolate reductase as a therapeutic target. FASEB J. 1990;4(8):2441–52.

    CAS  PubMed  Google Scholar 

  135. Hande S, et al. Targeting folate metabolism for therapeutic option: a bioinformatics approach. Indian J Exp Biol. 2015;53(11):762–6.

    PubMed  Google Scholar 

  136. Sharma RD, et al. Exploration of 2, 4-diaminopyrimidine and 2, 4-diamino-s-triazine derivatives as potential antifilarial agents. Parasitology. 2013;140(8):959–65.

    Article  CAS  PubMed  Google Scholar 

  137. Winkler AS. Neurocysticercosis in sub-Saharan Africa: a review of prevalence, clinical characteristics, diagnosis, and management. Pathog Glob Health. 2012;106(5):261–74.

    Article  PubMed  PubMed Central  Google Scholar 

  138. Rodriguez S, et al. Detection of Taenia solium antigens and anti-T. solium antibodies in paired serum and cerebrospinal fluid samples from patients with intraparenchymal or extraparenchymal neurocysticercosis. J Infect Dis. 2009;199(9):1345–52.

    Article  PubMed  PubMed Central  Google Scholar 

  139. Noormahomed EV, et al. A cross-sectional serological study of cysticercosis, schistosomiasis, toxocariasis and echinococcosis in HIV-1 infected people in Beira, Mozambique. PLoS Negl Trop Dis. 2014;8(9):e3121.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Baird RA, et al. Evidence-based guideline: treatment of parenchymal neurocysticercosis: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology. 2013;80(15):1424–9.

    Article  PubMed  PubMed Central  Google Scholar 

  141. Prasad S, et al. Management of potential neurocysticercosis in patients with HIV infection. Clin Infect Dis. 2006;42(4):e30–4.

    Article  PubMed  Google Scholar 

  142. Rigano R, et al. Echinococcus granulosus-specific T-cell lines derived from patients at various clinical stages of cystic echinococcosis. Parasite Immunol. 2004;26(1):45–52.

    Article  CAS  PubMed  Google Scholar 

  143. Wahlers K, et al. Human cystic echinococcosis in South Africa. Acta Trop. 2011;120(3):179–84.

    Article  PubMed  Google Scholar 

  144. WHO, What is schistosomiasis?

  145. •• Ssetaala A, et al. Schistosoma mansoni and HIV acquisition in fishing communities of Lake Victoria, Uganda: a nested case-control study. Tropical Med Int Health. 2015;20(9):1190–5. Ssetaala et al. performed a case-control study in a fishing community along Lake Victoria in Uganda with a high prevalence of schistosomiasis with 50 cases defined as people who HIV seroconverted and 150 controls who did not HIV seroconvert. They found no difference in prevalence of baseline schistosomiasis infection between the groups suggesting that infection with Schistosoma mansoni does not increase transmission of HIV

    Article  Google Scholar 

  146. Thigpen MC, et al. Associations between peripheral Plasmodium falciparum malaria parasitemia, human immunodeficiency virus, and concurrent helminthic infection among pregnant women in Malawi. Am J Trop Med Hyg. 2011;84(3):379–85.

    Article  PubMed  PubMed Central  Google Scholar 

  147. Secor WE. Interactions between schistosomiasis and infection with HIV-1. Parasite Immunol. 2006;28(11):597–603.

    CAS  PubMed  Google Scholar 

  148. Kayange NM, et al. The influence of HIV and schistosomiasis on renal function: a cross-sectional study among children at a hospital in Tanzania. PLoS Negl Trop Dis. 2015;9(1):e0003472.

    Article  PubMed  PubMed Central  Google Scholar 

  149. Mbabazi PS, et al. Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl Trop Dis. 2011;5(12):e1396.

    Article  PubMed  PubMed Central  Google Scholar 

  150. CDC, Parasites-Schistosomiasis; Resources for Health Professionals. 2012.

  151. Organization, W.H., World Malaria Report 2015. 2015.

  152. Cotter C, et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013;382(9895):900–11.

    Article  PubMed  Google Scholar 

  153. Homsy J, et al. Protective efficacy of prolonged co-trimoxazole prophylaxis in HIV-exposed children up to age 4 years for the prevention of malaria in Uganda: a randomised controlled open-label trial. Lancet Glob Health. 2014;2(12):e727–36.

    Article  PubMed  Google Scholar 

  154. Bwakura-Dangarembizi M, et al. A randomized trial of prolonged co-trimoxazole in HIV-infected children in Africa. N Engl J Med. 2014;370(1):41–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Campbell JD, et al. HIV-infected ugandan adults taking antiretroviral therapy with CD4 counts 200 cells/muL who discontinue cotrimoxazole prophylaxis have increased risk of malaria and diarrhea. Clin Infect Dis. 2012;54(8):1204–11.

    Article  CAS  PubMed  Google Scholar 

  156. Branquinha MH, et al. The Widespread Anti-Protozoal Action of HIV Aspartic Peptidase Inhibitors: Focus on Plasmodium spp., Leishmania spp. and Trypanosoma cruzi. Curr Top Med Chem. 2016;

  157. Andrews KT, et al. Potencies of human immunodeficiency virus protease inhibitors in vitro against Plasmodium falciparum and in vivo against murine malaria. Antimicrob Agents Chemother. 2006;50(2):639–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Kredo T, et al. The interaction between artemether-lumefantrine and lopinavir/ritonavir-based antiretroviral therapy in HIV-1 infected patients. BMC Infect Dis. 2016;16:30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Byakika-Kibwika P, et al. Cardiac conduction safety during coadministration of artemether-lumefantrine and lopinavir/ritonavir in HIV-infected Ugandan adults. Chemother Res Pract. 2011;2011:393976.

    PubMed  PubMed Central  Google Scholar 

  160. Kamya MR, et al. The effect of HIV on malaria in the context of the current standard of care for HIV-infected populations in Africa. Future Virol. 2012;7(7):699–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Byakika-Kibwika P, et al. Lopinavir/ritonavir significantly influences pharmacokinetic exposure of artemether/lumefantrine in HIV-infected Ugandan adults. J Antimicrob Chemother. 2012;67(5):1217–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Achan J, et al. Antiretroviral agents and prevention of malaria in HIV-infected Ugandan children. N Engl J Med. 2012;367(22):2110–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. WHO, Consolidated Guidelines on the Use of Antiretroviral Drugs for Treating and Preventing HIV Infection. 2016.

  164. van Griensven J, et al. HIV-1 protease inhibitors for treatment of visceral leishmaniasis in HIV-co-infected individuals. Lancet Infect Dis. 2013;13(3):251–9.

    Article  PubMed  CAS  Google Scholar 

  165. Molina R, Gradoni L, Alvar J. HIV and the transmission of Leishmania. Ann Trop Med Parasitol. 2003;97(Suppl 1):29–45.

    Article  PubMed  Google Scholar 

  166. Diro E, et al. Atypical manifestations of visceral leishmaniasis in patients with HIV in north Ethiopia: a gap in guidelines for the management of opportunistic infections in resource poor settings. Lancet Infect Dis. 2015;15(1):122–9.

    Article  PubMed  Google Scholar 

  167. Druzian AF, et al. Risk factors for death from visceral leishmaniasis in an urban area of Brazil. PLoS Negl Trop Dis. 2015;9(8):e0003982.

    Article  PubMed  PubMed Central  Google Scholar 

  168. Trudel N, et al. Intracellular survival of Leishmania species that cause visceral leishmaniasis is significantly reduced by HIV-1 protease inhibitors. J Infect Dis. 2008;198(9):1292–9.

    Article  CAS  PubMed  Google Scholar 

  169. • Diro, E., et al., Use of pentamidine as secondary prophylaxis to prevent visceral leishmaniasis relapse in HIV infected patients, the first twelve months of a prospective cohort study. PLoS Negl Trop Dis, 2015\. 9(10): p. e0004087. A single-arm open-label trial of monthly pentamidine infusions for prophylaxis in HIV-infected individuals with first-episode visceral leishmanisis demonstrated a relapse-free survival of 71% at 12 months compared to historical controls of 0–50%.

  170. Alvar J, et al. Leishmania and human immunodeficiency virus coinfection: the first 10 years. Clin Microbiol Rev. 1997;10(2):298–319.

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Alsina-Gibert M, et al. Cutaneous manifestations of visceral leishmaniasis resistant to liposomal amphotericin B in an HIV-positive patient. Arch Dermatol. 2006;142(6):787–9.

    Article  PubMed  Google Scholar 

  172. Bern C, et al. Liposomal amphotericin B for the treatment of visceral leishmaniasis. Clin Infect Dis. 2006;43(7):917–24.

    Article  CAS  PubMed  Google Scholar 

  173. Laguna F. Treatment of leishmaniasis in HIV-positive patients. Ann Trop Med Parasitol. 2003;97(Suppl 1):135–42.

    Article  CAS  PubMed  Google Scholar 

  174. Berenguer J, et al. Discontinuation of secondary anti-leishmania prophylaxis in HIV-infected patients who have responded to highly active antiretroviral therapy. AIDS. 2000;14(18):2946–8.

    Article  CAS  PubMed  Google Scholar 

  175. Nuno Marques RS, Coelho F, Oliveira J, Saraiva Da Cunha J, Melico-Silvestre A. Miltefosine for visceral leishmaniasis relapse treatment and secondary prophylaxis in HIV-infected patients. Scandinavian Journal of Infectious Diseases, 2009. 40(6–7)

  176. Rassi A Jr. A. Rassi, and J. Marcondes de Rezende, American trypanosomiasis (Chagas disease). Infect Dis Clin N Am. 2012;26(2):275–91.

    Article  Google Scholar 

  177. Vaidian AK, Weiss LM, Tanowitz HB. Chagas’ disease and AIDS. Kinetoplastid Biol Dis. 2004;3(1):2.

    Article  PubMed  PubMed Central  Google Scholar 

  178. Ramos AN Jr. Inclusion of Chagas’ disease reactivation as a condition for AIDS case definition to epidemiological surveillance in Brazil. Rev Soc Bras Med Trop. 2004;37(2):192–3.

    Article  PubMed  Google Scholar 

  179. Ministerio da Saude, Criterios de definicao de casos de AIDS em adultos y criancas. 2004.

  180. Sangenito LS, et al. HIV aspartic peptidase inhibitors are effective drugs against the trypomastigote form of the human pathogen Trypanosoma cruzi. Int J Antimicrob Agents. 2016;48(4):440–4.

    Article  CAS  PubMed  Google Scholar 

  181. CDC, Parasites- American Trypanosomiasis (also known as Chagas Disease); Antiparasitic Treatment. 2013.

  182. Viotti R, et al. Towards a paradigm shift in the treatment of chronic Chagas disease. Antimicrob Agents Chemother. 2014;58(2):635–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Morillo CA, et al. Randomized Trial of Benznidazole for Chronic Chagas’ Cardiomyopathy. N Engl J Med. 2015;373(14):1295–306.

    Article  CAS  PubMed  Google Scholar 

  184. Brun R, et al. Human African trypanosomiasis. Lancet. 2010;375(9709):148–59.

    Article  PubMed  Google Scholar 

  185. Lejon V, et al. Low specificities of HIV diagnostic tests caused by Trypanosoma brucei gambiense sleeping sickness. J Clin Microbiol. 2010;48(8):2836–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. CDC, Parasites-African Trypanosomiasis (also known as Sleeping Sickness); Resources for Health Professionals. 2016.

  187. Hotez PJ, et al. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis. 2014;8(7):e2865.

    Article  PubMed  PubMed Central  Google Scholar 

  188. Hotez PJ, et al. Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Med. 2006;3(5):e102.

    Article  PubMed  PubMed Central  Google Scholar 

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Mark Siedner receives research support from the National Institutes of Health (MH 099916).

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Evans, E.E., Siedner, M.J. Tropical Parasitic Infections in Individuals Infected With HIV. Curr Trop Med Rep 4, 268–280 (2017). https://doi.org/10.1007/s40475-017-0130-6

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