• 1.

    World Health Organization, 2016. chistosomiasis Fact Sheet No. 115. Available at: http://www.who.int/topics/schistosomiasis/en/. Accessed May 8, 2016.

    • Search Google Scholar
    • Export Citation
  • 2.

    Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H, Kalluvya SE, Changalucha JM, Johnson WD Jr, Fitzgerald DW, 2011. Urogenital schistosomiasis in women of reproductive age in Tanzania's Lake Victoria region. Am J Trop Med Hyg 84: 364–369.

    • Search Google Scholar
    • Export Citation
  • 3.

    Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L, Mason PR, Sandvik L, Friis H, Gundersen SG, 2006. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 20: 593–600.

    • Search Google Scholar
    • Export Citation
  • 4.

    Downs JA, van Dam GJ, Changalucha JM, Corstjens PL, Peck RN, de Dood CJ, Bang H, Andreasen A, Kalluvya SE, van Lieshout L, Johnson WD Jr, Fitzgerald DW, 2012. Association of schistosomiasis and HIV infection in Tanzania. Am J Trop Med Hyg 87: 868–873.

    • Search Google Scholar
    • Export Citation
  • 5.

    Mazigo HD, Dunne DW, Wilson S, Kinung'hi SM, Pinot de Moira A, Jones FM, Morona D, Nuwaha F, 2014. Co-infection with Schistosoma mansoni and human immunodeficiency virus-1 (HIV-1) among residents of fishing villages of north-western Tanzania. Parasit Vectors 7: 587.

    • Search Google Scholar
    • Export Citation
  • 6.

    Sanya RE, Muhangi L, Nampijja M, Nannozi V, Nakawungu PK, Abayo E, Webb EL, Elliott AM; LaVIISWA Study Team, 2015. Schistosoma mansoni and HIV infection in a Ugandan population with high HIV and helminth prevalence. Trop Med Int Health 20: 1201–1208.

    • Search Google Scholar
    • Export Citation
  • 7.

    Corstjens PLAM, Nyakundi RK, de Dood CJ, Kariuki TM, Ochola EA, Karanja DM, Mwinzi PN, van Dam GJ, 2015. Improved sensitivity of the urine CAA lateral-flow assay for diagnosing active Schistosoma infections by using larger sample volumes. Parasit Vectors 8: 241.

    • Search Google Scholar
    • Export Citation
  • 8.

    Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE, 1997. Studies on schistosomiasis in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 56: 515–521.

    • Search Google Scholar
    • Export Citation
  • 9.

    Fontanet AL, Woldemichael T, Sahlu T, van Dam GJ, Messele T, Rinke de Wit T, Masho W, Yeneneh H, Coutinho RA, van Lieshout L, 2000. Epidemiology of HIV and Schistosoma mansoni infections among sugar-estate residents in Ethiopia. Ann Trop Med Parasitol 94: 145–155.

    • Search Google Scholar
    • Export Citation
  • 10.

    Ssetaala A, Nakiyingi-Miiro J, Asiki G, Kyakuwa N, Mpendo J, Van Dam GJ, Corstjens PL, Pala P, Nielsen L, Bont J, Pantaleo G, Kiwanuka N, Kaleebu P, Kamali A, Elliott AM, 2015. Schistosoma mansoni and HIV acquisition in fishing communities of Lake Victoria, Uganda: a nested case-control study. Trop Med Int Health 20: 1190–1195.

    • Search Google Scholar
    • Export Citation
  • 11.

    Berhe N, Medhin G, Erko B, Smith T, Gedamu S, Bereded D, Moore R, Habte E, Redda A, Gebre-Michael T, Gundersen SG, 2004. Variations in helminth faecal egg counts in Kato–Katz thick smears and their implications in assessing infection status with Schistosoma mansoni. Acta Trop 92: 205–212.

    • Search Google Scholar
    • Export Citation
  • 12.

    WHO, 2006. Preventative Chemotherapy in Human Heminthiasis. Geneva, Switzerland: WHO Press.

  • 13.

    National Aids Control Programe and Reproductive and Child Health Services, 2007. National Guidelines for Management of Sexually Transmitted and Reproductive Tract Infections. Dar es Salaam, the United Republic of Tanzania: The United Republic of Tanzania, Ministry of Health and Social Welfare.

    • Search Google Scholar
    • Export Citation
  • 14.

    de Water R, Fransen JAM, Deelder AM, 1986. Ultrastructural localization of the circulating anodic antigen in the digestive tract of Schistosoma mansoni using monoclonal antibodies in an immunogold labeling procedure. Am J Trop Med 35: 549–558.

    • Search Google Scholar
    • Export Citation
  • 15.

    Kremsner PG, Enyong P, Krijger FW, De Jonge N, Zotter GM, Thalhammer F, Mühlschlegel F, Bienzle U, Feldmeier H, Deelder AM, 1994. Circulating anodic and cathodic antigen in serum and urine from Schistosoma haematobium-infected Cameroonian children receiving praziquantel: a longitudinal study. Clin Infect Dis 18: 408–413.

    • Search Google Scholar
    • Export Citation
  • 16.

    de Jonge N, De Caluwé P, Hilberath GW, Krijger FW, Polderman AM, Deelder AM, 1989. Circulating anodic antigen levels in serum before and after chemotherapy with praziquantel in schistosomiasis mansoni. Trans R Soc Trop Med Hyg 83: 368–372.

    • Search Google Scholar
    • Export Citation
  • 17.

    Corstjens PLAM, De Dood CJ, Kornelis D, Fat EM, Wilson RA, Kariuki TM, Nyakundi RK, Loverde PT, Abrams WR, Tanke HJ, Van Lieshout L, Deelder AM, Van Dam GJ, 2014. Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology 141: 1841–1855.

    • Search Google Scholar
    • Export Citation
  • 18.

    Corstjens PL, van Lieshout L, Zuiderwijk M, Kornelis D, Tanke HJ, Deelder AM, van Dam GJ, 2008. Up-converting phosphor technology-based lateral flow assay for detection of Schistosoma circulating anodic antigen in serum. J Clin Microbiol 46: 171–176.

    • Search Google Scholar
    • Export Citation
  • 19.

    Banoo S, Bell D, Bossuyt P, Herring A, Mabey D, Poole F, Smith PG, Sriram N, Wongsrichanalai C, Linke R, O'Brien R, Perkins M, Cunningham J, Matsoso P, Nathanson CM, Olliaro P, Peeling RW, Ramsay A, 2010. Evaluation of diagnostic tests for infectious diseases: general principles. Nat Rev Microbiol 8: S17–S29.

    • Search Google Scholar
    • Export Citation
  • 20.

    Obuku AE, Asiki G, Abaasa A, Ssonko I, Harari A, van Dam GJ, Corstjens PL, Joloba M, Ding S, Mpendo J, Nielsen L, Kamali A, Elliott AM, Pantaleo G, Kaleebu P, Pala P, 2016. Effect of Schistosoma mansoni infection on innate and HIV-1-specific T-cell immune responses in HIV-1-infected Ugandan fisher folk. AIDS Res Hum Retroviruses 32: 668–675.

    • Search Google Scholar
    • Export Citation
  • 21.

    Reese TA, Wakeman BS, Choi HS, Hufford MM, Huang SC, Zhang X, Buck MD, Jezewski A, Kambal A, Liu CY, Goel G, Murray PJ, Xavier RJ, Kaplan MH, Renne R, Speck SH, Artyomov MN, Pearce EJ, Virgin HW, 2014. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter. Science 345: 573–577.

    • Search Google Scholar
    • Export Citation
  • 22.

    Osborne LC, Monticelli LA, Nice TJ, Sutherland TE, Siracusa MC, Hepworth MR, Tomov VT, Kobuley D, Tran SV, Bittinger K, Bailey AG, Laughlin AL, Boucher JL, Wherry EJ, Bushman FD, Allen JE, Virgin HW, Artis D, 2014. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 345: 578–582.

    • Search Google Scholar
    • Export Citation
  • 23.

    Ayash-Rashkovsky M, Chenine A-L, Steele LN, Lee SJ, Song R, Ong H, Rasmussen RA, Hofmann-Lehmann R, Else JG, Augostini P, McClure HM, Secor WE, Ruprecht RM, 2007. Coinfection with Schistosoma mansoni reactivates viremia in rhesus macaques with chronic simian-human immunodeficiency virus clade C infection. Infect Immun 75: 1751–1756.

    • Search Google Scholar
    • Export Citation
  • 24.

    Leutscher PDC, Ramarokoto C-E, Hoffmann S, Jensen JS, Ramaniraka V, Randrianasolo B, Raharisolo C, Migliani R, Christensen N, 2008. Coexistence of urogenital schistosomiasis and sexually transmitted infection in women and men living in an area where Schistosoma haematobium is endemic. Clin Infect Dis 47: 775–782.

    • Search Google Scholar
    • Export Citation
  • 25.

    Smith JH, Kamel IA, Elwi A, Von Lichtenberg F, 1974. A quantitative post mortem analysis of urinary schistosomiasis in Egypt. I. Pathology and pathogenesis. Am J Trop Med Hyg 23: 1054–1071.

    • Search Google Scholar
    • Export Citation
  • 26.

    Leutscher PDC, Pedersen M, Raharisolo C, Jensen JS, Hoffmann S, Lisse I, Ostrowski SR, Reimert CM, Mauclere P, Ullum H, 2005. Increased prevalence of leukocytes and elevated cytokine levels in semen from Schistosoma haematobium-infected individuals. J Infect Dis 191: 1639–1647.

    • Search Google Scholar
    • Export Citation
  • 27.

    Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA, 2011. Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl Trop Dis 5: e1396.

    • Search Google Scholar
    • Export Citation
  • 28.

    Kroidl I, Saathof E, Maganga L, Makunde WH, Hoerauf A, Geldmacher C, Clowes P, Maboko L, Hoelscher M, 2016. Effect of Wuchereria bancrofti infection on HIV incidence in southwest Tanzania (EMINI): a prospective cohort study. Lancet 388: 1912–1920.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Schistosomiasis and Human Immunodeficiency Virus in Men in Tanzania

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  • 1 Department of Medicine, Center for Global Health, Weill Cornell Medicine, New York, New York.
  • 2 Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania.
  • 3 Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands.
  • 4 Cornell University, Ithaca, New York.
  • 5 Catholic University of Health and Allied Sciences, Mwanza, Tanzania.
  • 6 National Institute for Medical Research-Mwanza Research Centre, Mwanza, Tanzania.
  • 7 Department of Parasitology, Leiden University Medical Centre, Leiden, The Netherlands.

Schistosomiasis is a parasitic worm infection that affects over 260 million individuals worldwide. Women with schistosome infections have been demonstrated to have a 4-fold increase in the odds of human immunodeficiency virus (HIV) infection compared with women without schistosome infections. A relationship between schistosome and HIV infections has not been clearly defined in men. Among 674 men aged 18–50 years living in rural Tanzania, we identified 429 (63.6%) who had a schistosome infection as defined by serum positivity for schistosome circulating anodic antigen, visualization of parasite eggs in urine or stool, or both. HIV infection was identified in 38 (5.6%). The odds of HIV infection was 1.3 [95% confidence interval = 0.6–2.5] (P = 0.53) among men with any schistosome infection (Schistosoma haematobium or Schistosoma mansoni), and it was 1.4 [0.6–3.3] (P = 0.43) among men with S. haematobium infection. Men with S. haematobium infection were significantly more likely to report the symptom of hemospermia than men without S. haematobium infection. We conclude that schistosome infections appear to have little to no association with HIV infection in men.

Author Notes

* Address correspondence to Jennifer A. Downs, Department of Medicine, Center for Global Health, Weill Cornell Medicine, 402 E 67th Street, Second Floor, New York, NY 10065. E-mail: jna2002@med.cornell.edu

Financial support: This study was supported by grants from the National Institutes of Health (K23 AI 110238 to JAD; K24 AI 098627 to DWF).

Authors' addresses: Jennifer A. Downs, Hannah E. Dee, Megan McGeehan, Myung Hee Lee, and Daniel W. Fitzgerald, Department of Medicine, Center for Global Health, Weill Cornell Medicine, New York, NY, E-mail: jna2002@med.cornell.edu, hed2011@med.cornell.edu, mam2167@med.cornell.edu, myl2003@med.cornell.edu, and dfitzgerald@gheskio.org. Claudia J. de Dood and Paul L. A. M. Corstjens, Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands, E-mails: c.j.de_Dood@lumc.nl and p.corstjens@lumc.nl. Hijab Khan and Abena Marenga, Human Ecology, Cornell University, Ithaca, NY, E-mails: hak58@cornell.edu and mam674@cornell.edu. Patrick E. Adel, Edward Faustine, Benson Issarow, Emmanuel F. Kisanga, Godfrey Alfred Kisigo, Salvius Ngahyolerwa, and Frank Zahoro, Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania, E-mails: adel87.pa@gmail.com, eddo1566@gmail.com, issarowjr@gmail.com, kisanga.emmanuel@gmail.com, godkisigo@gmail.com, salvius19@gmail.com, and fredfrank743@gmail.com. Donald Miyaye, Ruth Gideon Magawa, and Julius Mngara, National Institute for Medical Research-Mwanza Research Centre, Mwanza, Tanzania, E-mails: miyaye64@yahoo.com, ruthmagawa@gmail.com, and juliusmngara@yahoo.com. Govert J. van Dam, Department of Parasitology, Leiden University Medical Centre, Leiden, The Netherlands, E-mail: g.j.van_Dam@lumc.nl.

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