High Prevalence of Simian Immunodeficiency Virus Infection in a Community of Savanna Chimpanzees

Abstract

Simian immunodeficiency virus of chimpanzees (SIVcpz) has a significant negative impact on the health, reproduction, and life span of chimpanzees, yet the prevalence and distribution of this virus in wild-living populations are still only poorly understood. Here, we show that savanna chimpanzees, who live in ecologically marginal habitats at 10-to 50-fold lower population densities than forest chimpanzees, can be infected with SIVcpz at high prevalence rates. Fecal samples were collected from nonhabituated eastern chimpanzees (Pan troglodytes schweinfurthii) in the Issa Valley (n ‫؍‬ 375) and Shangwa River (n ‫؍‬ 6) areas of the Masito-Ugalla region in western Tanzania, genotyped to determine the number of sampled individuals, and tested for SIVcpz-specific antibodies and nucleic acids. None of 5 Shangwa River apes tested positive for SIVcpz; however, 21 of 67 Issa Valley chimpanzees were SIVcpz infected, indicating a prevalence rate of 31% (95% confidence interval, 21% to 44%). Two individuals became infected during the 14-month observation period, documenting continuing virus spread in this community. To characterize the newly identified SIVcpz strains, partial and full-length viral sequences were amplified from fecal RNA of 10 infected chimpanzees. Phylogenetic analyses showed that the Ugalla viruses formed a monophyletic lineage most closely related to viruses endemic in Gombe National Park, also located in Tanzania, indicating a connection between these now separated communities at some time in the past. These findings document that SIVcpz is more widespread in Tanzania than previously thought and that even very low-density chimpanzee populations can be infected with SIVcpz at high prevalence rates. Determining whether savanna chimpanzees, who face much more extreme environmental conditions than forest chimpanzees, are more susceptible to SIVcpz-associated morbidity and mortality will have important scientific and conservation implications.Among the many lentiviruses known to infect Old World primates in sub-Saharan Africa, simian immunodeficiency virus of chimpanzees (SIVcpz) is of particular interest because it is the immediate precursor of human immunodeficiency virus type 1 (HIV-1), the causative agent of AIDS (8, 16). However, SIVcpz is also an important pathogen in its own right, since it causes significant morbidity and mortality in its chimpanzee host (6, 15, 37). Recent natural history studies in Gombe National Park in western Tanzania showed that infected chimpanzees have a 10-to 16-fold increased risk of death compared to uninfected chimpanzees (15). SIVcpz-infected females were less likely to give birth and their infants had a much higher mortality rate than those of uninfected females (15). Most importantly, postmortem analyses showed that SIVcpz can cause CD4 ϩ T lymphocyte depletion and histopathological findings consistent with end-stage AIDS (15). These results demonstrated that SIVcpz has a substantial negative impact on the health, reproduction, and life span of chimpanzees, a conclusion ...

Eastern Chimpanzees, but Not Bonobos, Represent a Simian Immunodeficiency Virus Reservoir

“…This is because previous field studies in Uganda, Rwanda, and Tanzania failed to uncover infected apes at most locations, except for communities in Gombe National Park and the Masito-Ugalla region of western Tanzania (29,54,55,59,60,66). However, since these areas of east Africa comprise only a small part of the P. t. schweinfurthii range (Fig.…”

“…Briefly, partially overlapping subgenomic fragments were amplified from fecal RNA, gel purified, and sequenced directly. Chromatograms were examined for positions of base mixtures, and ambiguous sites were resolved as previously reported (7,55,72,73). For positions that did not affect the corresponding amino acid, the predominant nucleotide (highest amplitude in the sequence chromatogram or the most frequent nucleotide in repeat sequencing reactions) was chosen.…”

“…Inspection of the BF1167 consensus sequence revealed uninterrupted open reading frames for all structural and regulatory proteins as well as intact regulatory elements. BF1167 also contained all previously identified SIVcpzPts signatures (55,58,73), including three amino acid insertions in Gag p24, a conserved PPLP Vif motif, a short Vpr protein of 95 amino acids, a 5-amino-acid deletion at the C terminus of Nef, and an insertion in the ectodomain of gp41. Phylogenetic analysis of full-length Gag, Pol, and Env proteins showed that BF1167 fell within the SIVcpzPts radiation (Fig.…”

“…Examining the molecular epidemiology of SIVcpz in the wild, we found that only two of the four currently recognized subspecies (9), i.e., central (Pan troglodytes troglodytes) and eastern (Pan troglodytes schweinfurthii) chimpanzees but not western (Pan troglodytes verus) and Nigeria-Cameroonian (Pan troglodytes ellioti) chimpanzees, are naturally infected by SIVcpz (30,35,55,58,59,78). We also found that SIVcpz is unevenly distributed among wild apes, with high prevalence rates (up to 50%) in some communities and rare or absent infection in others (29,30,54,55,59,78). Molecular studies of existing SIVcpz strains revealed that they cluster in accordance to their subspecies origin in two highly divergent lineages, termed SIVcpzPtt and SIVcpzPts (65).…”

“…However, extensive field studies in east Africa revealed a surprising paucity of SIVcpzPts infections. Although infected chimpanzees were identified in Gombe National Park (GM) (29,54,59,60) and the Ugalla region (UG) of western Tanzania (55), communities in the Budongo Forest (BG) in northern Uganda, the Kibale National Park (KB) in western Uganda, the Bwindi Impenetrable Forest (BW) in southern Uganda, and Mahale Mountains National Park (MH) in Tanzania seemed free of SIVcpz infection (55,59,66). Moreover, none of over 300 fecal samples from the Nyungwe Forest Reserve (NY) in western Rwanda was virus positive (66).…”