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Tissue Parasites in HIV Infection

  • HIV/AIDS (C Yoon, Section Editor)
  • Published:
Current Infectious Disease Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The purpose of this review is to discuss the current knowledge of HIV and tissue parasite co-infection in the context of transmission enhancement, clinical characteristics, treatment, relapse, and clinical outcomes.

Recent Findings

The pathophysiology and clinical sequelae of tissue parasites in people living with HIV (PLWH) have been well described for only a handful of organisms, primarily protozoa such as malaria and leishmaniasis. Available published data indicate that the interactions between HIV and tissue parasites are highly variable depending on the infecting organism and the degree of host immunosuppression. Some tissue parasites, such as Schistosoma species, are known to facilitate the transmission of HIV. Conversely, uncontrolled HIV infection can lead to the earlier and more severe presentation of a variety of tissue parasites and can make treatment more challenging.

Summary

Although much investigation remains to be done to better understand the interactions between consequences of HIV and tissue parasite co-infection, it is important to disseminate the current knowledge on this topic to health care providers in order to prevent, treat, and control infections in PLWH.

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References

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

  1. World Malaria Report. World Health Organization. 2017. http://www.who.int/malaria/publications/world-malaria-report-2017/report/en/. 2018. Accessed May 2019.

  2. Molineaux L. Malaria and mortality: some epidemiological considerations. Ann Trop Med Parasitol. 1997;91(7):811–25. https://doi.org/10.1080/00034989760572.

    Article  CAS  PubMed  Google Scholar 

  3. French N, Nakiyingi J, Lugada E, Watera C, Whitworth JA, Gilks CF. Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults. AIDS. 2001;15(7):899–906.

    CAS  PubMed  Google Scholar 

  4. Jegede FE, Oyeyi TI, Abdulrahman SA, Mbah HA, Badru T, Agbakwuru C, et al. Effect of HIV and malaria parasites co-infection on immune-hematological profiles among patients attending anti-retroviral treatment (ART) clinic in Infectious Disease Hospital Kano, Nigeria. PLoS One. 2017;12(3):e0174233. https://doi.org/10.1371/journal.pone.0174233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hoffman IF, Jere CS, Taylor TE, Munthali P, Dyer JR, Wirima JJ, et al. The effect of plasmodium falciparum malaria on HIV-1 RNA blood plasma concentration. AIDS. 1999;13(4):487–94.

    CAS  PubMed  Google Scholar 

  6. Okonkwo I, Ibadin M, Sadoh W, Omoigberale A. A study of malaria parasite density in HIV-1 positive under-fives in Benin City, Nigeria. J Trop Pediatr. 2018;64(4):289–96. https://doi.org/10.1093/tropej/fmx065.

    Article  PubMed  Google Scholar 

  7. Abu-Raddad LJ, Patnaik P, Kublin JG. Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science. 2006;314(5805):1603–6. https://doi.org/10.1126/science.1132338.

    Article  CAS  PubMed  Google Scholar 

  8. Franke MF, Spiegelman D, Ezeamama A, Aboud S, Msamanga GI, Mehta S, et al. Malaria parasitemia and CD4 T cell count, viral load, and adverse HIV outcomes among HIV-infected pregnant women in Tanzania. Am J Trop Med Hyg. 2010;82(4):556–62. https://doi.org/10.4269/ajtmh.2010.09-0477.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Organization WH. Guidelines for the treatment of malaria. 3rd ed; 2015.

    Google Scholar 

  10. •• 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. https://doi.org/10.1016/S1473-3099(11)70031-7. A comprehensive review of malaria in HIV infection.

    PubMed  Google Scholar 

  11. Seden K, Gibbons S, Marzolini C, Schapiro JM, Burger DM, Back DJ, et al. Development of an evidence evaluation and synthesis system for drug-drug interactions, and its application to a systematic review of HIV and malaria co-infection. PLoS One. 2017;12(3):e0173509. https://doi.org/10.1371/journal.pone.0173509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. •• HIV Drug Interaction Checker. University of Liverpool. https://www.hiv-druginteractions.org/checker. Accessed July 26, 2019. The Liverpool HIV Drug Interaction Checker is an extremely up-to-date and useful tool for querying the interactions between any HIV drug and any other medication.

  13. • Ottichilo RK, Polyak CS, Guyah B, Singa B, Nyataya J, Yuhas K, et al. Malaria parasitemia and parasite density in antiretroviral-treated HIV-infected adults following discontinuation of cotrimoxazole prophylaxis. J Infect Dis. 2017;215(1):88–94. https://doi.org/10.1093/infdis/jiw495. This reference describes a carefully-designed study describing the consequences of cotrimazole prophylaxis in PLWH in malaria-endemic areas.

    PubMed  Google Scholar 

  14. Bloland PB, Wirima JJ, Steketee RW, Chilima B, Hightower A, Breman JG. Maternal HIV infection and infant mortality in Malawi: evidence for increased mortality due to placental malaria infection. AIDS. 1995;9(7):721–6.

    CAS  PubMed  Google Scholar 

  15. Verhoeff FH, Brabin BJ, Hart CA, Chimsuku L, Kazembe P, Broadhead RL. Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control. Tropical Med Int Health. 1999;4(1):5–12.

    CAS  Google Scholar 

  16. Eki-Udoko FE, Sadoh AE, Ibadin MO, Omoigberale AI. Prevalence of congenital malaria in newborns of mothers co-infected with HIV and malaria in Benin city. Infect Dis (Lond). 2017;49(8):609–16. https://doi.org/10.1080/23744235.2017.1312667.

    Article  CAS  Google Scholar 

  17. Brahmbhatt H, Kigozi G, Wabwire-Mangen F, Serwadda D, Sewankambo N, Lutalo T, et al. The effects of placental malaria on mother-to-child HIV transmission in Rakai, Uganda. AIDS. 2003;17(17):2539–41. https://doi.org/10.1097/01.aids.0000096868.36052.29.

    Article  PubMed  Google Scholar 

  18. Mwapasa V, Rogerson SJ, Molyneux ME, Abrams ET, Kamwendo DD, Lema VM, et al. The effect of plasmodium falciparum malaria on peripheral and placental HIV-1 RNA concentrations in pregnant Malawian women. AIDS. 2004;18(7):1051–9.

    PubMed  Google Scholar 

  19. Ayisi JG, van Eijk AM, ter Kuile FO, Kolczak MS, Otieno JA, Misore AO, et al. The effect of dual infection with HIV and malaria on pregnancy outcome in western Kenya. AIDS. 2003;17(4):585–94. https://doi.org/10.1097/01.aids.0000042977.95433.37.

    Article  PubMed  Google Scholar 

  20. Akinyotu O, Bello F, Abdus-Salam R, Arowojolu A. Comparative study of mefloquine and sulphadoxine-pyrimethamine for malaria prevention among pregnant women with HIV in Southwest Nigeria. Int J Gynaecol Obstet. 2018;142(2):194–200. https://doi.org/10.1002/ijgo.12516.

    Article  CAS  PubMed  Google Scholar 

  21. Gonzalez R, Desai M, Macete E, Ouma P, Kakolwa MA, Abdulla S, et al. Intermittent preventive treatment of malaria in pregnancy with mefloquine in HIV-infected women receiving cotrimoxazole prophylaxis: a multicenter randomized placebo-controlled trial. PLoS Med. 2014;11(9):e1001735. https://doi.org/10.1371/journal.pmed.1001735.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Piola P, Nabasumba C, Turyakira E, Dhorda M, Lindegardh N, Nyehangane D, et al. Efficacy and safety of artemether-lumefantrine compared with quinine in pregnant women with uncomplicated plasmodium falciparum malaria: an open-label, randomised, non-inferiority trial. Lancet Infect Dis. 2010;10(11):762–9. https://doi.org/10.1016/S1473-3099(10)70202-4.

    Article  CAS  PubMed  Google Scholar 

  23. Rijken MJ, McGready R, Boel ME, Barends M, Proux S, Pimanpanarak M, et al. Dihydroartemisinin-piperaquine rescue treatment of multidrug-resistant plasmodium falciparum malaria in pregnancy: a preliminary report. Am J Trop Med Hyg. 2008;78(4):543–5.

    CAS  PubMed  Google Scholar 

  24. White NJ. Intermittent presumptive treatment for malaria. PLoS Med. 2005;2(1):e3. https://doi.org/10.1371/journal.pmed.0020003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Desai M, Gutman J, L’Lanziva A, Otieno K, Juma E, Kariuki S, et al. Intermittent screening and treatment or intermittent preventive treatment with dihydroartemisinin-piperaquine versus intermittent preventive treatment with sulfadoxine-pyrimethamine for the control of malaria during pregnancy in western Kenya: an open-label, three-group, randomised controlled superiority trial. Lancet. 2015;386(10012):2507–19. https://doi.org/10.1016/S0140-6736(15)00310-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kakuru A, Jagannathan P, Muhindo MK, Natureeba P, Awori P, Nakalembe M, et al. Dihydroartemisinin-piperaquine for the prevention of malaria in pregnancy. N Engl J Med. 2016;374(10):928–39. https://doi.org/10.1056/NEJMoa1509150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. • Natureeba P, Kakuru A, Muhindo M, Ochieng T, Ategeka J, Koss CA, et al. Intermittent preventive treatment with dihydroartemisinin-piperaquine for the prevention of malaria among HIV-infected pregnant women. J Infect Dis. 2017;216(1):29–35. https://doi.org/10.1093/infdis/jix110. This reference describes the most recent data on intermittent preventive treatment with dihydroartemisinin-piperaquine for the prevention of malaria in pregnant PLWH.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Molina R, Gradoni L, Alvar J. HIV and the transmission of Leishmania. Ann Trop Med Parasitol. 2003;97(Suppl 1):29–45. https://doi.org/10.1179/000349803225002516.

    Article  PubMed  Google Scholar 

  29. Diro E, Lynen L, Ritmeijer K, Boelaert M, Hailu A, van Griensven J. Visceral Leishmaniasis and HIV coinfection in East Africa. PLoS Negl Trop Dis. 2014;8(6):e2869. https://doi.org/10.1371/journal.pntd.0002869.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Bernier R, Barbeau B, Tremblay MJ, Olivier M. The lipophosphoglycan of Leishmania donovani up-regulates HIV-1 transcription in T cells through the nuclear factor-kappaB elements. J Immunol. 1998;160(6):2881–8.

    CAS  PubMed  Google Scholar 

  31. Harms G, Feldmeier H. HIV infection and tropical parasitic diseases - deleterious interactions in both directions? Tropical Med Int Health. 2002;7(6):479–88.

    Google Scholar 

  32. Leishmania/HIV co-infection, south-western Europe, 1990–1998. Wkly Epidemiol Rec. 1999;74(44):365–75.

  33. Alvar J, Canavate C, Gutierrez-Solar B, Jimenez M, Laguna F, Lopez-Velez R, 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 

  34. Lopez-Velez R, Perez-Molina JA, Guerrero A, Baquero F, Villarrubia J, Escribano L, et al. Clinicoepidemiologic characteristics, prognostic factors, and survival analysis of patients coinfected with human immunodeficiency virus and Leishmania in an area of Madrid, Spain. Am J Trop Med Hyg. 1998;58(4):436–43.

    CAS  PubMed  Google Scholar 

  35. ter Horst R, Tefera T, Assefa G, Ebrahim AZ, Davidson RN, Ritmeijer K. Field evaluation of rK39 test and direct agglutination test for diagnosis of visceral leishmaniasis in a population with high prevalence of human immunodeficiency virus in Ethiopia. Am J Trop Med Hyg. 2009;80(6):929–34.

    PubMed  Google Scholar 

  36. Pintado V, Martin-Rabadan P, Rivera ML, Moreno S, Bouza E. Visceral leishmaniasis in human immunodeficiency virus (HIV)-infected and non-HIV-infected patients. A comparative study. Medicine (Baltimore). 2001;80(1):54–73.

    CAS  Google Scholar 

  37. Bossolasco S, Gaiera G, Olchini D, Gulletta M, Martello L, Bestetti A, et al. Real-time PCR assay for clinical management of human immunodeficiency virus-infected patients with visceral leishmaniasis. J Clin Microbiol. 2003;41(11):5080–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Pandey N, Siripattanapipong S, Leelayoova S, Manomat J, Mungthin M, Tan-Ariya P, et al. Detection of Leishmania DNA in saliva among patients with HIV/AIDS in Trang Province, southern Thailand. Acta Trop. 2018;185:294–300. https://doi.org/10.1016/j.actatropica.2018.06.006.

    Article  CAS  PubMed  Google Scholar 

  39. Vogt F, Mengesha B, Asmamaw H, Mekonnen T, Fikre H, Takele Y, et al. Antigen detection in urine for noninvasive diagnosis and treatment monitoring of visceral Leishmaniasis in human immunodeficiency virus coinfected patients: an exploratory analysis from Ethiopia. Am J Trop Med Hyg. 2018;99(4):957–66. https://doi.org/10.4269/ajtmh.18-0042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Laguna F, Videla S, Jimenez-Mejias ME, Sirera G, Torre-Cisneros J, Ribera E, et al. Amphotericin B lipid complex versus meglumine antimoniate in the treatment of visceral leishmaniasis in patients infected with HIV: a randomized pilot study. J Antimicrob Chemother. 2003;52(3):464–8. https://doi.org/10.1093/jac/dkg356.

    Article  CAS  PubMed  Google Scholar 

  41. Delgado J, Macias J, Pineda JA, Corzo JE, Gonzalez-Moreno MP, de la Rosa R, et al. High frequency of serious side effects from meglumine antimoniate given without an upper limit dose for the treatment of visceral leishmaniasis in human immunodeficiency virus type-1-infected patients. Am J Trop Med Hyg. 1999;61(5):766–9.

    CAS  PubMed  Google Scholar 

  42. •• Diro E, Blesson S, Edwards T, Ritmeijer K, Fikre H, Admassu H, et al. A randomized trial of AmBisome monotherapy and AmBisome and miltefosine combination to treat visceral leishmaniasis in HIV co-infected patients in Ethiopia. PLoS Negl Trop Dis. 2019;13(1):e0006988. https://doi.org/10.1371/journal.pntd.0006988. This trial describes using IV Ambisome and oral miltefosine combination to treat visceral leishmaniasis in HIV co-infected patients.

    PubMed  PubMed Central  Google Scholar 

  43. Tumbarello M, Tacconelli E, Bertagnolio S, Cauda R. Highly active antiretroviral therapy decreases the incidence of visceral leishmaniasis in HIV-infected individuals. AIDS. 2000;14(18):2948–9.

    CAS  PubMed  Google Scholar 

  44. Abongomera C, Diro E, Vogt F, Tsoumanis A, Mekonnen Z, Admassu H, et al. The risk and predictors of visceral Leishmaniasis relapse in human immunodeficiency virus-coinfected patients in Ethiopia: a retrospective cohort study. Clin Infect Dis. 2017;65(10):1703–10. https://doi.org/10.1093/cid/cix607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lopez-Velez R. The impact of highly active antiretroviral therapy (HAART) on visceral leishmaniasis in Spanish patients who are co-infected with HIV. Ann Trop Med Parasitol. 2003;97(Suppl 1):143–7. https://doi.org/10.1179/000349803225002615.

    Article  CAS  PubMed  Google Scholar 

  46. Villanueva JL, Alarcon A, Bernabeu-Wittel M, Cordero E, Prados D, Regordan C, et al. Prospective evaluation and follow-up of European patients with visceral leishmaniasis and HIV-1 coinfection in the era of highly active antiretroviral therapy. Eur J Clin Microbiol Infect Dis. 2000;19(10):798–801.

    CAS  PubMed  Google Scholar 

  47. Lopez-Velez R, Videla S, Marquez M, Boix V, Jimenez-Mejias ME, Gorgolas M, et al. Amphotericin B lipid complex versus no treatment in the secondary prophylaxis of visceral leishmaniasis in HIV-infected patients. J Antimicrob Chemother. 2004;53(3):540–3. https://doi.org/10.1093/jac/dkh084.

    Article  CAS  PubMed  Google Scholar 

  48. Diro E, Ritmeijer K, Boelaert M, Alves F, Mohammed R, Abongomera C, et al. Long-term clinical outcomes in visceral Leishmaniasis/human immunodeficiency virus-coinfected patients during and after pentamidine secondary prophylaxis in Ethiopia: a single-arm clinical trial. Clin Infect Dis. 2018;66(3):444–51. https://doi.org/10.1093/cid/cix807.

    Article  CAS  PubMed  Google Scholar 

  49. Noireau F, Brun-Vezinet F, Larouze B, Nzoukoudi MY, Gouteux JP. Absence of relationship between human immunodeficiency virus 1 and sleeping sickness. Trans R Soc Trop Med Hyg. 1987;81(6):1000.

    CAS  PubMed  Google Scholar 

  50. Louis JP, Moulia-Pelat JP, Jannin J, Asonganyi T, Hengy C, Trebucq A, et al. Absence of epidemiological inter-relations between HIV infection and African human trypanosomiasis in central Africa. Trop Med Parasitol. 1991;42(2):155.

    CAS  PubMed  Google Scholar 

  51. Meda HA, Doua F, Laveissiere C, Miezan TW, Gaens E, Brattegaard K, et al. Human immunodeficiency virus infection and human African trypanosomiasis: a case-control study in cote d’Ivoire. Trans R Soc Trop Med Hyg. 1995;89(6):639–43.

    CAS  PubMed  Google Scholar 

  52. •• Pelfrene E, Harvey Allchurch M, Ntamabyaliro N, Nambasa V, Ventura FV, Nagercoil N, et al. The European Medicines Agency’s scientific opinion on oral fexinidazole for human African trypanosomiasis. PLoS Negl Trop Dis. 2019;13(6):e0007381. https://doi.org/10.1371/journal.pntd.0007381. This reference describes a new and safer drug for the treatment of African trypanosomiasis, oral fexinidazole.

    PubMed  PubMed Central  Google Scholar 

  53. Pepin J, Ethier L, Kazadi C, Milord F, Ryder R. 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.

    CAS  PubMed  Google Scholar 

  54. Blum J, Nkunku S, Burri C. Clinical description of encephalopathic syndromes and risk factors for their occurrence and outcome during melarsoprol treatment of human African trypanosomiasis. Tropical Med Int Health. 2001;6(5):390–400.

    CAS  Google Scholar 

  55. Perez-Ramirez L, Barnabe C, Sartori AM, Ferreira MS, Tolezano JE, Nunes EV, et al. Clinical analysis and parasite genetic diversity in human immunodeficiency virus/Chagas’ disease coinfections in Brazil. Am J Trop Med Hyg. 1999;61(2):198–206.

    CAS  PubMed  Google Scholar 

  56. • Sartori AM, Neto JE, Nunes EV, Braz LM, Caiaffa-Filho HH, Oliveira Oda C Jr, 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. https://doi.org/10.1086/342510. A comparison of the differences between Trypanosoma cruzi parasitemia in PLWH and those without HIV

  57. Almeida EA, Ramos Junior AN, Correia D, Shikanai-Yasuda MA. Co-infection Trypanosoma cruzi/HIV: systematic review (1980-2010). Rev Soc Bras Med Trop. 2011;44(6):762–70.

    PubMed  Google Scholar 

  58. Nishioka Sde A, Ferreira MS, Rocha A, Burgarelli MK, Silva AM, Duarte MI, et al. Reactivation of Chagas’ disease successfully treated with benznidazole in a patient with acquired immunodeficiency syndrome. Mem Inst Oswaldo Cruz. 1993;88(3):493–6. https://doi.org/10.1590/s0074-02761993000300022.

    Article  PubMed  Google Scholar 

  59. • Ferreira MS, Nishioka Sde A, Silvestre MT, Borges AS, Nunes-Araujo FR, Rocha A. Reactivation of Chagas’ disease in patients with AIDS: report of three new cases and review of the literature. Clin Infect Dis. 1997;25(6):1397–400. This reference describes reactivation of Trypanosoma cruzi infection in PLWH with low CD4 counts.

    CAS  PubMed  Google Scholar 

  60. Pacheco RS, Ferreira MS, Machado MI, Brito CM, Pires MQ, Da-Cruz AM, et al. Chagas’ disease and HIV co-infection: genotypic characterization of the Trypanosoma cruzi strain. Mem Inst Oswaldo Cruz. 1998;93(2):165–9.

    CAS  PubMed  Google Scholar 

  61. Yasukawa K, Patel SM, Flash CA, Stager CE, Goodman JC, Woc-Colburn L. Trypanosoma cruzi meningoencephalitis in a patient with acquired immunodeficiency syndrome. Am J Trop Med Hyg. 2014;91(1):84–5. https://doi.org/10.4269/ajtmh.14-0058.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ferreira MS, Nishioka Sde A, Rocha A, Silva AM, Ferreira RG, Olivier W, et al. Acute fatal Trypanosoma cruzi meningoencephalitis in a human immunodeficiency virus-positive hemophiliac patient. Am J Trop Med Hyg. 1991;45(6):723–7.

    CAS  PubMed  Google Scholar 

  63. Cohen JE, Tsai EC, Ginsberg HJ, Godes J. Pseudotumoral chagasic meningoencephalitis as the first manifestation of acquired immunodeficiency syndrome. Surg Neurol. 1998;49(3):324–7.

    CAS  PubMed  Google Scholar 

  64. Di Lorenzo GA, Pagano MA, Taratuto AL, Garau ML, Meli FJ, Pomsztein MD. Chagasic granulomatous encephalitis in immunosuppressed patients. Computed tomography and magnetic resonance imaging findings. J Neuroimaging. 1996;6(2):94–7.

    PubMed  Google Scholar 

  65. Castro-Sesquen YE, Gilman RH, Mejia C, Clark DE, Choi J, Reimer-McAtee MJ, et al. Use of a Chagas urine nanoparticle test (Chunap) to correlate with parasitemia levels in T. cruzi/HIV co-infected patients. PLoS Negl Trop Dis. 2016;10(2):e0004407. https://doi.org/10.1371/journal.pntd.0004407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Sartori AM, Caiaffa-Filho HH, Bezerra RC, Do SGC, Lopes MH, Shikanai-Yasuda MA. Exacerbation of HIV viral load simultaneous with asymptomatic reactivation of chronic Chagas’ disease. Am J Trop Med Hyg. 2002;67(5):521–523.

    PubMed  Google Scholar 

  67. Sartori AM, Ibrahim KY, Nunes Westphalen EV, Braz LM, Oliveira OC Jr, Gakiya E, et al. Manifestations of Chagas disease (American trypanosomiasis) in patients with HIV/AIDS. Ann Trop Med Parasitol. 2007;101(1):31–50. https://doi.org/10.1179/136485907X154629.

    Article  CAS  PubMed  Google Scholar 

  68. Dolcini GL, Solana ME, Andreani G, Celentano AM, Parodi LM, Donato AM, et al. Trypanosoma cruzi (Chagas’ disease agent) reduces HIV-1 replication in human placenta. Retrovirology. 2008;5:53–13. https://doi.org/10.1186/1742-4690-5-53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Castro JA, de Mecca MM, Bartel LC. Toxic side effects of drugs used to treat Chagas’ disease (American trypanosomiasis). Hum Exp Toxicol. 2006;25(8):471–9. https://doi.org/10.1191/0960327106het653oa.

    Article  CAS  PubMed  Google Scholar 

  70. Fischer P, Kipp W, Kabwa P, Buttner DW. Onchocerciasis and human immunodeficiency virus in western Uganda: prevalences and treatment with ivermectin. Am J Trop Med Hyg. 1995;53(2):171–8.

    CAS  PubMed  Google Scholar 

  71. Tawill SA, Gallin M, Erttmann KD, Kipp W, Bamuhiiga J, Buttner DW. 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.

    CAS  PubMed  Google Scholar 

  72. Sentongo E, Rubaale T, Buttner DW, Brattig NW. T cell responses in coinfection with Onchocerca volvulus and the human immunodeficiency virus type 1. Parasite Immunol. 1998;20(9):431–9.

    CAS  PubMed  Google Scholar 

  73. 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. https://doi.org/10.1016/s0035-9203(03)90157-x.

    Article  PubMed  Google Scholar 

  74. Kipp W, Bamhuhiiga J, Rubaale T, Kabagambe G. Adverse reactions to the ivermectin treatment of onchocerciasis patients: does infection with the human immunodeficiency virus play a role? Ann Trop Med Parasitol. 2005;99(4):395–402. https://doi.org/10.1179/136485905X36262.

    Article  CAS  PubMed  Google Scholar 

  75. Njambe Priso GD, Lissom A, Ngu LN, Nji NN, Tchadji JC, Tchouangueu TF, et al. Filaria specific antibody response profiling in plasma from anti-retroviral naive Loa loa microfilaraemic HIV-1 infected people. BMC Infect Dis. 2018;18(1):160–11. https://doi.org/10.1186/s12879-018-3072-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Janssen S, Hermans S, Knap M, Moekotte A, Rossatanga EG, Adegnika AA, 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. https://doi.org/10.1371/journal.pntd.0003769.

    Article  CAS  PubMed  Google Scholar 

  77. Hunt NH, Grau GE. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 2003;24(9):491–9.

    CAS  PubMed  Google Scholar 

  78. • Gopinath R, Ostrowski M, Justement SJ, Fauci AS, Nutman TB. Filarial infections increase susceptibility to human immunodeficiency virus infection in peripheral blood mononuclear cells in vitro. J Infect Dis. 2000;182(6):1804–8. https://doi.org/10.1086/317623. This reference presents data that supports the increased susceptibility of individuals with filarial infections to acquisition of HIV.

    CAS  PubMed  Google Scholar 

  79. Nielsen NO, Friis H, Magnussen P, Krarup H, Magesa S, Simonsen PE. 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. https://doi.org/10.1016/j.trstmh.2007.02.009.

    Article  CAS  PubMed  Google Scholar 

  80. Talaat KR, Kumarasamy N, Swaminathan S, Gopinath R, Nutman TB. Filarial/human immunodeficiency virus coinfection in urban southern India. Am J Trop Med Hyg. 2008;79(4):558–60.

    PubMed  PubMed Central  Google Scholar 

  81. Tafatatha T, Taegtmeyer M, Ngwira B, Phiri A, Kondowe M, Piston W, 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. https://doi.org/10.1371/journal.pntd.0003825.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Kroidl I, Saathoff E, Maganga L, Makunde WH, Hoerauf A, Geldmacher C, et al. Effect of Wuchereria bancrofti infection on HIV incidence in Southwest Tanzania: a prospective cohort study. Lancet. 2016;388(10054):1912–20. https://doi.org/10.1016/S0140-6736(16)31252-1.

    Article  PubMed  Google Scholar 

  83. Kroidl I, Saathof E, Maganga L, Clowes P, Maboko L, Hoerauf A, et al. 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(4):e0004618. https://doi.org/10.1371/journal.pntd.0004618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Modi M, Mochan A, Modi G. Management of HIV-associated focal brain lesions in developing countries. QJM. 2004;97(7):413–21. https://doi.org/10.1093/qjmed/hch080.

    Article  CAS  PubMed  Google Scholar 

  85. Jessurun J, Barron-Rodriguez LP, Fernandez-Tinoco G, Hernandez-Avila M. The prevalence of invasive amebiasis is not increased in patients with AIDS. AIDS. 1992;6(3):307–9.

    CAS  PubMed  Google Scholar 

  86. Delobel P, Signate A, El Guedj M, Couppie P, Gueye M, Smadja D, et al. Unusual form of neurocysticercosis associated with HIV infection. Eur J Neurol. 2004;11(1):55–8.

    CAS  PubMed  Google Scholar 

  87. •• Prasad S, MacGregor RR, Tebas P, Rodriguez LB, Bustos JA, White AC Jr. Management of potential neurocysticercosis in patients with HIV infection. Clin Infect Dis. 2006;42(4):e30–4. https://doi.org/10.1086/499359. This reference describes the management of neurocysticercosis in PLWH.

    PubMed  Google Scholar 

  88. Foyaca-Sibat H, Cowan LD, Carabin H, Targonska I, Anwary MA, Serrano-Ocana G, et al. Accuracy of serological testing for the diagnosis of prevalent neurocysticercosis in outpatients with epilepsy, Eastern Cape Province. South Africa PLoS Negl Trop Dis. 2009;3(12):e562. https://doi.org/10.1371/journal.pntd.0000562.

    Article  PubMed  Google Scholar 

  89. •• White AC Jr, Coyle CM, Rajshekhar V, Singh G, Hauser WA, Mohanty A, et al. Diagnosis and treatment of Neurocysticercosis: 2017 clinical practice guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Am J Trop Med Hyg. 2018;98(4):945–66. https://doi.org/10.4269/ajtmh.18-88751. The recently updated clinical practice guidelines for the management of neurocysticercosis.

    PubMed  PubMed Central  Google Scholar 

  90. Serpa JA, Moran A, Goodman JC, Giordano TP, White AC Jr. 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 

  91. Secor WE. The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Curr Opin HIV AIDS. 2012;7(3):254–9. https://doi.org/10.1097/COH.0b013e328351b9e3.

    Article  CAS  PubMed  Google Scholar 

  92. Siddappa NB, Hemashettar G, Shanmuganathan V, Semenya AA, Sweeney ED, Paul KS, et al. Schistosoma mansoni enhances host susceptibility to mucosal but not intravenous challenge by R5 clade C SHIV. PLoS Negl Trop Dis. 2011;5(8):e1270. https://doi.org/10.1371/journal.pntd.0001270.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H, et al. Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg. 2011;84(3):364–9. https://doi.org/10.4269/ajtmh.2011.10-0585.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Downs JA, van Dam GJ, Changalucha JM, Corstjens PL, Peck RN, de Dood CJ, et al. Association of schistosomiasis and HIV infection in Tanzania. Am J Trop Med Hyg. 2012;87(5):868–73. https://doi.org/10.4269/ajtmh.2012.12-0395.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Downs JA, Dupnik KM, van Dam GJ, Urassa M, Lutonja P, Kornelis D, et al. Effects of schistosomiasis on susceptibility to HIV-1 infection and HIV-1 viral load at HIV-1 seroconversion: a nested case-control study. PLoS Negl Trop Dis. 2017;11(9):e0005968. https://doi.org/10.1371/journal.pntd.0005968.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Wall KM, Kilembe W, Vwalika B, Dinh C, Livingston P, Lee YM, et al. Schistosomiasis is associated with incident HIV transmission and death in Zambia. PLoS Negl Trop Dis. 2018;12(12):e0006902. https://doi.org/10.1371/journal.pntd.0006902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Leutscher P, Ramarokoto CE, Reimert C, Feldmeier H, Esterre P, Vennervald BJ. Community-based study of genital schistosomiasis in men from Madagascar. Lancet. 2000;355(9198):117–8. https://doi.org/10.1016/S0140-6736(99)04856-4.

    Article  CAS  PubMed  Google Scholar 

  98. Karanja DM, Hightower AW, Colley DG, Mwinzi PN, Galil K, Andove J, et al. Resistance to reinfection with Schistosoma mansoni in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet. 2002;360(9333):592–6. https://doi.org/10.1016/S0140-6736(02)09781-7.

    Article  PubMed  Google Scholar 

  99. • Colombe S, Lee MH, Masikini PJ, van Lieshout L, de Dood CJ, Hoekstra PT, et al. Decreased sensitivity of Schistosoma sp. egg microscopy in women and HIV-infected individuals. Am J Trop Med Hyg. 2018;98(4):1159–64. https://doi.org/10.4269/ajtmh.17-0790. This reference describes the difficulties in diagnosing schistosomiasis in PLWH.

    PubMed  PubMed Central  Google Scholar 

  100. Mwanakasale V, Vounatsou P, Sukwa TY, Ziba M, Ernest A, Tanner M. Interactions between Schistosoma haematobium and human immunodeficiency virus type 1: the effects of coinfection on treatment outcomes in rural Zambia. Am J Trop Med Hyg. 2003;69(4):420–8.

    PubMed  Google Scholar 

  101. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, Mudenge B, van Dam GJ, 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. https://doi.org/10.1086/497696.

    Article  CAS  PubMed  Google Scholar 

  102. Karanja DM, Boyer AE, Strand M, Colley DG, Nahlen BL, Ouma JH, et al. Studies on schistosomiasis in western Kenya: II. Efficacy of praziquantel for treatment of schistosomiasis in persons coinfected with human immunodeficiency virus-1. Am J Trop Med Hyg. 1998;59(2):307–11.

    CAS  PubMed  Google Scholar 

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Clark, E.H., Serpa, J.A. Tissue Parasites in HIV Infection. Curr Infect Dis Rep 21, 49 (2019). https://doi.org/10.1007/s11908-019-0703-8

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