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      Frequent and Recent Human Acquisition of Simian Foamy Viruses Through Apes' Bites in Central Africa

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          Abstract

          Human infection by simian foamy viruses (SFV) can be acquired by persons occupationally exposed to non-human primates (NHP) or in natural settings. This study aimed at getting better knowledge on SFV transmission dynamics, risk factors for such a zoonotic infection and, searching for intra-familial dissemination and the level of peripheral blood (pro)viral loads in infected individuals. We studied 1,321 people from the general adult population (mean age 49 yrs, 640 women and 681 men) and 198 individuals, mostly men, all of whom had encountered a NHP with a resulting bite or scratch. All of these, either Pygmies (436) or Bantus (1085) live in villages in South Cameroon. A specific SFV Western blot was used and two nested PCRs ( polymerase, and LTR) were done on all the positive/borderline samples by serology. In the general population, 2/1,321 (0.2%) persons were found to be infected. In the second group, 37/198 (18.6%) persons were SFV positive. They were mostly infected by apes (37/39) FV (mainly gorilla). Infection by monkey FV was less frequent (2/39). The viral origin of the amplified sequences matched with the history reported by the hunters, most of which (83%) are aged 20 to 40 years and acquired the infection during the last twenty years. The (pro)viral load in 33 individuals infected by a gorilla FV was quite low (<1 to 145 copies per 10 5 cells) in the peripheral blood leucocytes. Of the 30 wives and 12 children from families of FV infected persons, only one woman was seropositive in WB without subsequent viral DNA amplification. We demonstrate a high level of recent transmission of SFVs to humans in natural settings specifically following severe gorilla bites during hunting activities. The virus was found to persist over several years, with low SFV loads in infected persons. Secondary transmission remains an open question.

          Author Summary

          Most of the viral pathogens that have emerged in humans during the last decades have a zoonotic origin. After the initial interspecies transmission, these viruses have followed different evolutionary routes and have spread among humans through distinct mechanisms. The understanding of the initial steps of the emergence of several viruses and associated diseases often remains quite poor. Human infection by simian foamy viruses (SFV) can be acquired by persons occupationally exposed to non-human primates (NHP) or in natural settings. Epidemiological and microbiological studies in specific high-risk populations are necessary to gain new insights into the early events of the emergence process, and the potential to spread or cause disease among humans. The present study found that hunting is still a very common and risky activity for SFV infection in forest areas of South Cameroon. Indeed, recent interspecies transmission of SFVs to young adults is still very frequent, as 1 person out of 5 among the hunters who have reported a bite or scratch by a non-human primate and 2 persons out of a thousand in the general population are persistently infected by a SFV, mostly from an ape. Secondary transmission to other family members and presence of a disease in infected persons are still open questions that are being investigated.

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          Most cited references71

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          A new human immunodeficiency virus derived from gorillas.

          We have identified a new human immunodeficiency virus in a Cameroonian woman. It is closely related to gorilla simian immunodeficiency virus (SIVgor) and shows no evidence of recombination with other HIV-1 lineages. This new virus seems to be the prototype of a new HIV-1 lineage that is distinct from HIV-1 groups M, N and O. We propose to designate it HIV-1 group P.
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            Ancient co-speciation of simian foamy viruses and primates.

            Although parasite-host co-speciation is a long-held hypothesis, convincing evidence for long-term co-speciation remains elusive, largely because of small numbers of hosts and parasites studied and uncertainty over rates of evolutionary change. Co-speciation is especially rare in RNA viruses, in which cross-species transfer is the dominant mode of evolution. Simian foamy viruses (SFVs) are ubiquitous, non-pathogenic retroviruses that infect all primates. Here we test the co-speciation hypothesis in SFVs and their primate hosts by comparing the phylogenies of SFV polymerase and mitochondrial cytochrome oxidase subunit II from African and Asian monkeys and apes. The phylogenetic trees were remarkably congruent in both branching order and divergence times, strongly supporting co-speciation. Molecular clock calibrations revealed an extremely low rate of SFV evolution, 1.7 x 10(-8) substitutions per site per year, making it the slowest-evolving RNA virus documented so far. These results indicate that SFVs might have co-speciated with Old World primates for at least 30 million years, making them the oldest known vertebrate RNA viruses.
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              Human immunodeficiency viruses: SIV infection in wild gorillas.

              Chimpanzees (Pan troglodytes troglodytes) from west central Africa are recognized as the reservoir of simian immunodeficiency viruses (SIVcpzPtt) that have crossed at least twice to humans: this resulted in the AIDS pandemic (from human immunodeficiency virus HIV-1 group M) in one instance and infection of just a few individuals in Cameroon (by HIV-1 group N) in another. A third HIV-1 lineage (group O) from west central Africa also falls within the SIVcpzPtt radiation, but the primate reservoir of this virus has not been identified. Here we report the discovery of HIV-1 group O-like viruses in wild gorillas.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                October 2011
                October 2011
                27 October 2011
                : 7
                : 10
                : e1002306
                Affiliations
                [1 ]Unit of Epidemiology and Pathophysiology of Oncogenic Viruses, Department of Virology, Institut Pasteur, Paris, France
                [2 ]Centre National de la Recherche Scientifique (CNRS), URA 3015, Paris, France
                [3 ]Faculty of Medicine and Biomedical Sciences, University of Yaounde I, Yaounde, Cameroun
                [4 ]Institute of Research for Development, Musée de l'Homme, Paris, France
                SAIC-Frederick, United States of America
                Author notes

                Conceived and designed the experiments: EB RR AG. Performed the experiments: EB RR. Analyzed the data: EB RR PT AG. Contributed reagents/materials/analysis tools: EB AF PT. Wrote the paper: EB AG. Advices regarding biostatistical analysis: AF.

                Article
                PPATHOGENS-D-11-01201
                10.1371/journal.ppat.1002306
                3203161
                22046126
                afe29eed-16b8-4c0e-b931-860514a47d13
                Betsem et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 3 June 2011
                : 24 August 2011
                Page count
                Pages: 15
                Categories
                Research Article
                Biology
                Microbiology
                Virology
                Emerging Viral Diseases
                Viral Transmission and Infection

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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