Association of Schistosomiasis and HIV Infection in Tanzania

Jennifer A. Downs Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Govert J. van Dam Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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John M. Changalucha Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Paul L. A. M. Corstjens Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Robert N. Peck Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Claudia J. de Dood Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Heejung Bang Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Aura Andreasen Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Samuel E. Kalluvya Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Lisette van Lieshout Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Warren D. Johnson Jr. Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Daniel W. Fitzgerald Department of Medicine, Weill Cornell Medical College, New York, New York; Department of Medicine, Bugando Medical Centre, Mwanza, Tanzania; Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands; National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania; Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands; Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, California; Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom

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Animal and human studies suggest that Schistosoma mansoni infection may increase risk of human immunodeficiency virus (HIV) acquisition. Therefore, we tested 345 reproductive age women in rural Tanzanian villages near Lake Victoria, where S. mansoni is hyperendemic, for sexually transmitted infections (STIs) and schistosomiasis by circulating anodic antigen (CAA) serum assay. Over one-half (54%) had an active schistosome infection; 6% were HIV-seropositive. By univariate analysis, only schistosome infection predicted HIV infection (odds ratio [OR] = 3.9, 95% confidence interval = [1.3–12.0], P = 0.015) and remained significant using multivariate analysis to control for age, STIs, and distance from the lake (OR = 6.2 [1.7–22.9], P = 0.006). HIV prevalence was higher among women with more intense schistosome infections (P = 0.005), and the median schistosome intensity was higher in HIV-infected than -uninfected women (400 versus 15 pg CAA/mL, P = 0.01). This finding suggests that S. mansoni infection may be a modifiable HIV risk factor that places millions of people worldwide at increased risk of HIV acquisition.

Author Notes

* Address correspondence to Jennifer A. Downs, Center for Global Health, Weill Cornell Medical College, 440 East 69th Street, New York, NY 10065. E-mail: jna2002@med.cornell.edu

Financial support: This work was supported by the 2009 Merle A. Sande/Pfizer Fellowship Award in International Infectious Diseases, which is awarded annually by the Infectious Diseases Society of America Education & Research Foundation and the National Foundation for Infectious Diseases. This work was also supported by Agency for Healthcare Research and Quality Grant T32HS000066, National Institute for Allergy and Infectious Diseases Grant T32AI007613, and Clinical and Translational Science Center at Weill Cornell Medical College Grant UL1-RR024996 (to J.A.D.). Various improvements of the upconverting phosphor-LF assay for circulating anodic antigen detection, involving the implementation of dry reagents (allowing worldwide shipping), increased sensitivity, and handheld upconverting phosphor readers, were developed, in part, with financial support from US National Institutes of Health Grant UO1DE017855 and the University of Georgia Research Foundation, Inc. (Schistosomiasis Consortium for Operational Research and Evaluation [SCORE] project).

Authors' addresses: Jennifer A. Downs, Robert N. Peck, Warren D. Johnson Jr., and Daniel W. Fitzgerald, Center for Global Health, Weill Cornell Medical College, New York, NY, E-mails: jna2002@med.cornell.edu, rnp2002@med.cornell.edu, wdjohnso@med.cornell.edu, and dfitzgerald@gheskio.org. Govert J. van Dam and Lisette van Lieshout, Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands, E-mails: G.J.van_Dam@lumc.nl and E.A.van_Lieshout@lumc.nl. John M. Changalucha, National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania, E-mail: jchangalucha@yahoo.com. Paul L. A. M. Corstjens and Claudia J. de Dood, Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands, E-mails: P.Corstjens@lumc.nl and C.J.de_Dood@lumc.nl. Heejung Bang, Division of Biostatistics, Department of Public Health Sciences, University of California, Davis, CA, E-mail: hbang@phs.ucdavis.edu. Aura Andreasen, Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom; and Mwanza Interventional Trials Unit, Mwanza, Tanzania, E-mail: aura.andreasen@mitu.or.tz. Samuel E. Kalluvya, Department of Internal Medicine, Bugando Medical Centre, Mwanza, Tanzania, E-mail: samuelkalluvya@yahoo.com.

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