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

Brandon F. Keele, James Holland Jones, Karen A. Terio, Jacob D. Estes, Rebecca S. Rudicell, Michael L. Wilson, Yingying Li, Gerald H. Learn, T. Mark Beasley, Joann Schumacher-Stankey, Emily Wroblewski, Anna Mosser, Jane Raphael, Shadrack Kamenya, Elizabeth V. Lonsdorf, Dominic A. Travis, Titus Mlengeya, Michael J. Kinsel, James G. Else, Guido SilvestriJane Goodall, Paul M. Sharp, George M. Shaw, Anne E. Pusey, Beatrice H. Hahn

Research output: Contribution to journalArticle

236 Citations (Scopus)

Abstract

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). Unlike the human viruses, however, SIVs do not generally cause acquired immunodeficiency syndrome (AIDS) in their natural hosts. 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.

Original languageEnglish (US)
Pages (from-to)515-519
Number of pages5
JournalNature
Volume460
Issue number7254
DOIs
StatePublished - Jul 23 2009

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Pan troglodytes
Acquired Immunodeficiency Syndrome
Simian Immunodeficiency Virus
HIV-1
Mortality
HIV-2
Follicular Dendritic Cells
Viruses
T-Lymphocytes
Premature Mortality
Tanzania
Infant Mortality
Lymphoid Tissue
Virus Diseases
Primates
In Situ Hybridization
Reproduction
Spleen
Lymph Nodes
Immunohistochemistry

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Keele, B. F., Jones, J. H., Terio, K. A., Estes, J. D., Rudicell, R. S., Wilson, M. L., ... Hahn, B. H. (2009). Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature, 460(7254), 515-519. https://doi.org/10.1038/nature08200

Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. / Keele, Brandon F.; Jones, James Holland; Terio, Karen A.; Estes, Jacob D.; Rudicell, Rebecca S.; Wilson, Michael L.; Li, Yingying; Learn, Gerald H.; Beasley, T. Mark; Schumacher-Stankey, Joann; Wroblewski, Emily; Mosser, Anna; Raphael, Jane; Kamenya, Shadrack; Lonsdorf, Elizabeth V.; Travis, Dominic A.; Mlengeya, Titus; Kinsel, Michael J.; Else, James G.; Silvestri, Guido; Goodall, Jane; Sharp, Paul M.; Shaw, George M.; Pusey, Anne E.; Hahn, Beatrice H.

In: Nature, Vol. 460, No. 7254, 23.07.2009, p. 515-519.

Research output: Contribution to journalArticle

Keele, BF, Jones, JH, Terio, KA, Estes, JD, Rudicell, RS, Wilson, ML, Li, Y, Learn, GH, Beasley, TM, Schumacher-Stankey, J, Wroblewski, E, Mosser, A, Raphael, J, Kamenya, S, Lonsdorf, EV, Travis, DA, Mlengeya, T, Kinsel, MJ, Else, JG, Silvestri, G, Goodall, J, Sharp, PM, Shaw, GM, Pusey, AE & Hahn, BH 2009, 'Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz', Nature, vol. 460, no. 7254, pp. 515-519. https://doi.org/10.1038/nature08200
Keele, Brandon F. ; Jones, James Holland ; Terio, Karen A. ; Estes, Jacob D. ; Rudicell, Rebecca S. ; Wilson, Michael L. ; Li, Yingying ; Learn, Gerald H. ; Beasley, T. Mark ; Schumacher-Stankey, Joann ; Wroblewski, Emily ; Mosser, Anna ; Raphael, Jane ; Kamenya, Shadrack ; Lonsdorf, Elizabeth V. ; Travis, Dominic A. ; Mlengeya, Titus ; Kinsel, Michael J. ; Else, James G. ; Silvestri, Guido ; Goodall, Jane ; Sharp, Paul M. ; Shaw, George M. ; Pusey, Anne E. ; Hahn, Beatrice H. / Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. In: Nature. 2009 ; Vol. 460, No. 7254. pp. 515-519.
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