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Acquired Immune Deficiency Syndrome (AIDS) was first recognized as a new disease in 1981 when increasing numbers of young homosexual men succumbed to unusual opportunistic infections and rare malignancies (CDC 1981; Greene 2007). 2011); however, 80% of adults acquire HIV-1 following exposure at mucosal surfaces, and AIDS is thus primarily a sexually transmitted disease (Hladik and Mc Elrath 2008; Cohen et al. Since its first identification almost three decades ago, the pandemic form of HIV-1, also called the main (M) group, has infected at least 60 million people and caused more than 25 million deaths (Merson et al. Developing countries have experienced the greatest HIV/AIDS morbidity and mortality, with the highest prevalence rates recorded in young adults in sub-Saharan Africa (
A retrovirus, now termed human immunodeficiency virus type 1 (HIV-1), was subsequently identified as the causative agent of what has since become one of the most devastating infectious diseases to have emerged in recent history (Barre-Sinoussi et al. Although antiretroviral treatment has reduced the toll of AIDS- related deaths, access to therapy is not universal, and the prospects of curative treatments and an effective vaccine are uncertain (Barouch 2008; Richman et al. Thus, AIDS will continue to pose a significant public health threat for decades to come. These relationships provided the first evidence that AIDS had emerged in both humans and macaques as a consequence of cross-species infections with lentiviruses from different primate species (Sharp et al. Indeed, subsequent studies confirmed that SIVmac was not a natural pathogen of macaques (which are Asian primates), but had been generated inadvertently in US primate centers by inoculating various species of macaques with blood and/or tissues from naturally infected sooty mangabeys (Apetrei et al. Similarly, it became clear that HIV-1 and HIV-2 were the result of zoonotic transfers of viruses infecting primates in Africa (Hahn et al. In this article, we summarize what is known about the simian precursors of HIV-1 and HIV-2, and retrace the steps that led to the AIDS pandemic. Old World monkeys are naturally infected with more than 40 different lentiviruses, termed simian immunodeficiency viruses (SIVs) with a suffix to denote their primate species of origin (e.g., SIVsmm from sooty mangabeys).
To address this, a prospective study was initiated in Gombe National Park, Tanzania, the only field site where SIVcpz infected chimpanzees are habituated and so can be observed in their natural habitat.
Gombe is located in northwestern Tanzania on the shores of Lake Tanganyika. SIVcpz also appears to be transmitted from infected mothers to their infants, and in rare cases, possibly by aggression (Keele et al. Migration of infected females constitutes a major route of virus transmission between communities (Rudicell et al. Behavioral and virological studies also provided insight into the pathogenicity of SIVcpz.
The first isolates of SIVcpz were all derived from animals housed in primate centers or sanctuaries, although infection was rare in these populations. 2005), this finding raised doubts about whether chimpanzees represented a true SIV reservoir. These technical innovations, combined with genotyping methods for species and subspecies confirmation as well as individual identification, permitted a comprehensive analysis of wild-living chimpanzee populations throughout central Africa.
Collective analyses of nearly 2,000 wild-caught or captive-born apes identified fewer than a dozen SIVcpz positive individuals (Sharp et al. Because other primate species, such as sooty mangabeys and African green monkeys, are much more commonly infected, both in captivity and in the wild (Fultz et al. To resolve this conundrum, our laboratory developed noninvasive diagnostic methods that detect SIVcpz specific antibodies and nucleic acids in chimpanzee fecal and urine samples with high sensitivity and specificity (Santiago et al. Chimpanzees are classified into two species, the common chimpanzee (). These studies have identified common chimpanzees as a natural SIVcpz reservoir, but also revealed important differences between the epidemiology of SIVcpz and that of other primate lentiviruses.
Most of these transfers resulted in viruses that spread in humans to only a limited extent.
Figure 3A summarizes current molecular epidemiological data derived from the analysis of over 7,000 chimpanzee fecal samples collected at nearly 90 field sites (Santiago et al. The upper panel depicts the ranges of the four subspecies of the common chimpanzee (, brown) gorillas (map courtesy of Lilian Pintea, The Jane Goodall Institute). Moreover, there is no evidence that chimpanzees harbor any other SIV, although they, as well as bonobos, are routinely exposed to SIVs through their hunting behavior (Mitani and Watts 1999; Surbeck and Hohmann 2008; Leendertz et al. Initially, SIVcpz was thought to be harmless for its natural host.
Data were compiled from several studies (Santiago et al. This was because none of the few captive apes that were naturally SIVcpz infected suffered from overt immunodeficiency, although in retrospect this conclusion was based on the immunological and virological analyses of only a single naturally infected chimpanzee (Heeney et al. In addition, SIV-infected sooty mangabeys and African green monkeys showed no sign of disease despite high viral loads in blood and lymphatic tissues (Paiardini et al.
That is, viral sequences from members of the same species form a monophyletic clade in evolutionary trees.
This host-specific clustering indicates that the great majority of transmissions occur among members of the same species; however, there are also numerous documented instances when SIVs have crossed between species. Thus, it is clear that in addition to more long-standing virus/host relationships, a number of naturally occurring SIVs have emerged more recently as a result of cross-species transmission and recombination.