Nature 460, 515-519 (23 July 2009) | doi:10.1038/nature08200; Received 21 April 2009; Accepted 5 June 2009

Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz

Brandon F. Keele1,17, James Holland Jones4, Karen A. Terio5, Jacob D. Estes6, Rebecca S. Rudicell2, Michael L. Wilson7,8, Yingying Li1, Gerald H. Learn1, T. Mark Beasley3, Joann Schumacher-Stankey8, Emily Wroblewski8, Anna Mosser9, Jane Raphael9, Shadrack Kamenya9, Elizabeth V. Lonsdorf10, Dominic A. Travis11, Titus Mlengeya12, Michael J. Kinsel5, James G. Else13, Guido Silvestri14, Jane Goodall15, Paul M. Sharp16, George M. Shaw1, Anne E. Pusey8 & Beatrice H. Hahn1,2

  1. Department of Medicine,
  2. Department of Microbiology,
  3. Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama 35294, USA
  4. Department of Anthropology, Stanford University, Stanford, California 94305, USA
  5. University of Illinois Zoological Pathology Program, Maywood, Illinois 60153, USA
  6. The AIDS and Cancer Virus Program, Science Applications International Corporation-Frederick Inc., National Cancer Institute-Frederick, Frederick, Maryland 21702, USA
  7. Department of Anthropology, University of Minnesota, Minneapolis, Minnesota 55455, USA
  8. Jane Goodall Institute's Center for Primate Studies, Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul, Minnesota 55108, USA
  9. Gombe Stream Research Centre, The Jane Goodall Institute, Kigoma, Tanzania
  10. The Lester E. Fisher Center for the Study and Conservation of Apes and,
  11. Department of Conservation and Science, Lincoln Park Zoo, Chicago, Illinois 60614, USA
  12. Tanzania National Parks, Arusha, Tanzania
  13. Division of Animal Resources, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30322, USA
  14. Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19107, USA
  15. The Jane Goodall Institute, Arlington, Virginia 22203, USA
  16. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK
  17. Present address: The AIDS and Cancer Virus Program, Science Applications International Corporation-Frederick Inc., National Cancer Institute-Frederick, Frederick, Maryland 21702, USA.

Correspondence to: Beatrice H. Hahn1,2 Correspondence and requests for materials should be addressed to B.H.H. (Email: bhahn@uab.edu).

African primates are naturally infected with over 40 different simian immunodeficiency viruses (SIVs), two of which have crossed the species barrier and generated human immunodeficiency virus types 1 and 2 (HIV-1 and HIV-2)1, 2. Unlike the human viruses, however, SIVs do not generally cause acquired immunodeficiency syndrome (AIDS) in their natural hosts3. Here we show that SIVcpz, the immediate precursor of HIV-1, is pathogenic in free-ranging chimpanzees. By following 94 members of two habituated chimpanzee communities in Gombe National Park, Tanzania, for over 9 years, we found a 10- to 16-fold higher age-corrected death hazard for SIVcpz-infected (n = 17) compared to uninfected (n = 77) chimpanzees. We also found that SIVcpz-infected females were less likely to give birth and had a higher infant mortality rate than uninfected females. Immunohistochemistry and in situ hybridization of post-mortem spleen and lymph node samples from three infected and two uninfected chimpanzees revealed significant CD4+ T-cell depletion in all infected individuals, with evidence of high viral replication and extensive follicular dendritic cell virus trapping in one of them. One female, who died within 3 years of acquiring SIVcpz, had histopathological findings consistent with end-stage AIDS. These results indicate that SIVcpz, like HIV-1, is associated with progressive CD4+ T-cell loss, lymphatic tissue destruction and premature death. These findings challenge the prevailing view that all natural SIV infections are non-pathogenic and suggest that SIVcpz has a substantial negative impact on the health, reproduction and lifespan of chimpanzees in the wild.