Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir

Yingying Li, Jean Bosco Ndjango, Gerald H. Learn, Miguel A. Ramirez, Brandon F. Keele, Frederic Bibollet-Ruche, Weimin Liu, Juliet L. Easlick, Julie M. Decker, Rebecca S. Rudicell, Bila Isia Inogwabini, Steve Ahuka-Mundeke, Fabian H. Leendertz, Vernon Reynolds, Martin N. Muller, Rebecca L. Chancellor, Aaron S. Rundus, Nicole Simmons, Michael Worobey, George M. ShawMartine Peeters, Paul M. Sharp, Beatrice H. Hahna

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

Chimpanzees in west central Africa (Pan troglodytes troglodytes) are endemically infected with simian immunodeficiency viruses (SIVcpzPtt) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa (Pan troglodytes schweinfurthii) are also infected with SIVcpz; however, their viruses (SIVcpzPts) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos (Pan paniscus) in the DRC, a species not previously tested for SIV in the wild. Fecal samples (n=3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km2. In this region, SIVcpzPts was common and widespread, with seven field sites exhibiting infection rates of 30% or greater. The overall prevalence of SIVcpzPts infection was 13.4% (95% confidence interval, 10.7% to 16.5%). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpzPts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpzPts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.

Original languageEnglish (US)
Pages (from-to)10776-10791
Number of pages16
JournalJournal of Virology
Volume86
Issue number19
DOIs
StatePublished - Oct 2012

Fingerprint

Pan paniscus
Simian immunodeficiency virus
Simian Immunodeficiency Virus
Pan troglodytes
Gorilla gorilla
Democratic Republic of the Congo
antibodies
Antibodies
Gorilla
Infection
Troglodytes troglodytes
infection
Rwanda
Viruses
Congo
Central Africa
sampling
Eastern Africa
viruses
Western Africa

ASJC Scopus subject areas

  • Immunology
  • Virology

Cite this

Li, Y., Ndjango, J. B., Learn, G. H., Ramirez, M. A., Keele, B. F., Bibollet-Ruche, F., ... Hahna, B. H. (2012). Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. Journal of Virology, 86(19), 10776-10791. https://doi.org/10.1128/JVI.01498-12

Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. / Li, Yingying; Ndjango, Jean Bosco; Learn, Gerald H.; Ramirez, Miguel A.; Keele, Brandon F.; Bibollet-Ruche, Frederic; Liu, Weimin; Easlick, Juliet L.; Decker, Julie M.; Rudicell, Rebecca S.; Inogwabini, Bila Isia; Ahuka-Mundeke, Steve; Leendertz, Fabian H.; Reynolds, Vernon; Muller, Martin N.; Chancellor, Rebecca L.; Rundus, Aaron S.; Simmons, Nicole; Worobey, Michael; Shaw, George M.; Peeters, Martine; Sharp, Paul M.; Hahna, Beatrice H.

In: Journal of Virology, Vol. 86, No. 19, 10.2012, p. 10776-10791.

Research output: Contribution to journalArticle

Li, Y, Ndjango, JB, Learn, GH, Ramirez, MA, Keele, BF, Bibollet-Ruche, F, Liu, W, Easlick, JL, Decker, JM, Rudicell, RS, Inogwabini, BI, Ahuka-Mundeke, S, Leendertz, FH, Reynolds, V, Muller, MN, Chancellor, RL, Rundus, AS, Simmons, N, Worobey, M, Shaw, GM, Peeters, M, Sharp, PM & Hahna, BH 2012, 'Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir', Journal of Virology, vol. 86, no. 19, pp. 10776-10791. https://doi.org/10.1128/JVI.01498-12
Li Y, Ndjango JB, Learn GH, Ramirez MA, Keele BF, Bibollet-Ruche F et al. Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. Journal of Virology. 2012 Oct;86(19):10776-10791. https://doi.org/10.1128/JVI.01498-12
Li, Yingying ; Ndjango, Jean Bosco ; Learn, Gerald H. ; Ramirez, Miguel A. ; Keele, Brandon F. ; Bibollet-Ruche, Frederic ; Liu, Weimin ; Easlick, Juliet L. ; Decker, Julie M. ; Rudicell, Rebecca S. ; Inogwabini, Bila Isia ; Ahuka-Mundeke, Steve ; Leendertz, Fabian H. ; Reynolds, Vernon ; Muller, Martin N. ; Chancellor, Rebecca L. ; Rundus, Aaron S. ; Simmons, Nicole ; Worobey, Michael ; Shaw, George M. ; Peeters, Martine ; Sharp, Paul M. ; Hahna, Beatrice H. / Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. In: Journal of Virology. 2012 ; Vol. 86, No. 19. pp. 10776-10791.
@article{4b304fbf94e14a16a633bb2c1dd407b7,
title = "Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir",
abstract = "Chimpanzees in west central Africa (Pan troglodytes troglodytes) are endemically infected with simian immunodeficiency viruses (SIVcpzPtt) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa (Pan troglodytes schweinfurthii) are also infected with SIVcpz; however, their viruses (SIVcpzPts) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos (Pan paniscus) in the DRC, a species not previously tested for SIV in the wild. Fecal samples (n=3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km2. In this region, SIVcpzPts was common and widespread, with seven field sites exhibiting infection rates of 30{\%} or greater. The overall prevalence of SIVcpzPts infection was 13.4{\%} (95{\%} confidence interval, 10.7{\%} to 16.5{\%}). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpzPts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpzPts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.",
author = "Yingying Li and Ndjango, {Jean Bosco} and Learn, {Gerald H.} and Ramirez, {Miguel A.} and Keele, {Brandon F.} and Frederic Bibollet-Ruche and Weimin Liu and Easlick, {Juliet L.} and Decker, {Julie M.} and Rudicell, {Rebecca S.} and Inogwabini, {Bila Isia} and Steve Ahuka-Mundeke and Leendertz, {Fabian H.} and Vernon Reynolds and Muller, {Martin N.} and Chancellor, {Rebecca L.} and Rundus, {Aaron S.} and Nicole Simmons and Michael Worobey and Shaw, {George M.} and Martine Peeters and Sharp, {Paul M.} and Hahna, {Beatrice H.}",
year = "2012",
month = "10",
doi = "10.1128/JVI.01498-12",
language = "English (US)",
volume = "86",
pages = "10776--10791",
journal = "Journal of Virology",
issn = "0022-538X",
publisher = "American Society for Microbiology",
number = "19",

}

TY - JOUR

T1 - Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir

AU - Li, Yingying

AU - Ndjango, Jean Bosco

AU - Learn, Gerald H.

AU - Ramirez, Miguel A.

AU - Keele, Brandon F.

AU - Bibollet-Ruche, Frederic

AU - Liu, Weimin

AU - Easlick, Juliet L.

AU - Decker, Julie M.

AU - Rudicell, Rebecca S.

AU - Inogwabini, Bila Isia

AU - Ahuka-Mundeke, Steve

AU - Leendertz, Fabian H.

AU - Reynolds, Vernon

AU - Muller, Martin N.

AU - Chancellor, Rebecca L.

AU - Rundus, Aaron S.

AU - Simmons, Nicole

AU - Worobey, Michael

AU - Shaw, George M.

AU - Peeters, Martine

AU - Sharp, Paul M.

AU - Hahna, Beatrice H.

PY - 2012/10

Y1 - 2012/10

N2 - Chimpanzees in west central Africa (Pan troglodytes troglodytes) are endemically infected with simian immunodeficiency viruses (SIVcpzPtt) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa (Pan troglodytes schweinfurthii) are also infected with SIVcpz; however, their viruses (SIVcpzPts) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos (Pan paniscus) in the DRC, a species not previously tested for SIV in the wild. Fecal samples (n=3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km2. In this region, SIVcpzPts was common and widespread, with seven field sites exhibiting infection rates of 30% or greater. The overall prevalence of SIVcpzPts infection was 13.4% (95% confidence interval, 10.7% to 16.5%). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpzPts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpzPts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.

AB - Chimpanzees in west central Africa (Pan troglodytes troglodytes) are endemically infected with simian immunodeficiency viruses (SIVcpzPtt) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa (Pan troglodytes schweinfurthii) are also infected with SIVcpz; however, their viruses (SIVcpzPts) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos (Pan paniscus) in the DRC, a species not previously tested for SIV in the wild. Fecal samples (n=3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km2. In this region, SIVcpzPts was common and widespread, with seven field sites exhibiting infection rates of 30% or greater. The overall prevalence of SIVcpzPts infection was 13.4% (95% confidence interval, 10.7% to 16.5%). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpzPts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpzPts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.

UR - http://www.scopus.com/inward/record.url?scp=84869015088&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84869015088&partnerID=8YFLogxK

U2 - 10.1128/JVI.01498-12

DO - 10.1128/JVI.01498-12

M3 - Article

C2 - 22837215

AN - SCOPUS:84869015088

VL - 86

SP - 10776

EP - 10791

JO - Journal of Virology

JF - Journal of Virology

SN - 0022-538X

IS - 19

ER -