Martine Peeters

Université de Montpellier 1, Montpelhièr, Languedoc-Roussillon, France

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Publications (206)1084.45 Total impact

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    ABSTRACT: Humans are ecosystems containing trillions of microorganisms, but the evolutionary history of this microbiome is obscured by a lack of knowledge about microbiomes of African apes. We sequenced the gut communities of hundreds of chimpanzees, bonobos, and gorillas and developed a phylogenetic approach to reconstruct how present-day human microbiomes have diverged from those of ancestral populations. Compositional change in the microbiome was slow and clock-like during African ape diversification, but human microbiomes have deviated from the ancestral state at an accelerated rate. Relative to the microbiomes of wild apes, human microbiomes have lost ancestral microbial diversity while becoming specialized for animal-based diets. Individual wild apes cultivate more phyla, classes, orders, families, genera, and species of bacteria than do individual humans across a range of societies. These results indicate that humanity has experienced a depletion of the gut flora since diverging from Pan.
    Proceedings of the National Academy of Sciences of the United States of America. 11/2014;
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    ABSTRACT: Populations of an organism living in marked geographical or evolutionary isolation from other populations of the same species are often termed subspecies and expected to show some degree of genetic distinctiveness. The common chimpanzee (Pan troglodytes) is currently described as four geographically delimited subspecies: the western (P. t. verus), the nigerian-cameroonian (P. t. ellioti), the central (P. t. troglodytes) and the eastern (P. t. schweinfurthii) chimpanzees. Although these taxa would be expected to be reciprocally monophyletic, studies have not always consistently resolved the central and eastern chimpanzee taxa. Most studies, however, used data from individuals of unknown or approximate geographic provenance. Thus, genetic data from samples of known origin may shed light on the evolutionary relationship of these subspecies. We generated microsatellite genotypes from noninvasively collected fecal samples of 185 central chimpanzees that were sampled across large parts of their range and analyzed them together with 283 published eastern chimpanzee genotypes from known localities. We observed a clear signal of isolation by distance across both subspecies. Further, we found that a large proportion of comparisons between groups taken from the same subspecies showed higher genetic differentiation than the least differentiated between-subspecies comparison. This proportion decreased substantially when we simulated a more clumped sampling scheme by including fewer groups. Our results support the general concept that the distribution of the sampled individuals can dramatically affect the inference of genetic population structure. With regard to chimpanzees, our results emphasize the close relationship of equatorial chimpanzees from central and eastern equatorial Africa and the difficult nature of subspecies definitions. Am J Phys Anthropol, 2014. © 2014 Wiley Periodicals, Inc.
    American Journal of Physical Anthropology 10/2014; · 2.48 Impact Factor
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    ABSTRACT: Thirty years after the discovery of HIV-1, the early transmission, dissemination, and establishment of the virus in human populations remain unclear. Using statistical approaches applied to HIV-1 sequence data from central Africa, we show that from the 1920s Kinshasa (in what is now the Democratic Republic of Congo) was the focus of early transmission and the source of pre-1960 pandemic viruses elsewhere. Location and dating estimates were validated using the earliest HIV-1 archival sample, also from Kinshasa. The epidemic histories of HIV-1 group M and nonpandemic group O were similar until ~1960, after which group M underwent an epidemiological transition and outpaced regional population growth. Our results reconstruct the early dynamics of HIV-1 and emphasize the role of social changes and transport networks in the establishment of this virus in human populations.
    Science 10/2014; 346(6205):56-61. · 31.20 Impact Factor
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    ABSTRACT: Vector-borne parasites of the genus Leishmania are responsible for severe human diseases. Cutaneous leishmaniasis, a common form of the disease, is most often caused by the transmission of Leishmania major to humans by female phlebotomine sandflies. Recently, Apes are increasingly seen as source of zoonotic diseases including malaria and rickettsiosis. To examine the possibility whether gorillas harbor Leishmania spp., we screened fecal samples from wild western lowland gorillas (Gorilla gorilla gorilla) in Cameroon for the presence of these pathogens. Of 91 wild gorilla feces samples, 12 contained Leishmania parasites and 4 contained phlebotomine sand fly vectors. The molecular identity was determined by running three different PCR tests as L. major. Next, fluorescence in situ hybridization (FISH) was performed to visualize L. major parasites in the feces of the gorillas. Both promastigote and amastigote forms of the parasite were found. This work strongly suggests that wild gorillas carry pathogenic Leishmania parasites.
    The Journal of infectious diseases. 07/2014;
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    ABSTRACT: The existence and genetic make-up of most primate retroviruses was revealed by studies of bushmeat and fecal samples from unhabituated primate communities. For these, detailed data on intra-and within-species contact rates are generally missing, which makes identification of factors influencing transmission a challenging task. Here we present an assessment of 12 years of research on primate retroviruses in the Taï National Park area, Côte d'Ivoire. We discuss insights gained into the prevalence, within-and cross-species transmission of primate retroviruses (including towards local human populations) and the importance of virus–host interactions in determining cross-species transmission risk. Finally we discuss how retroviruses ecology and evolution may change in a shifting environment and identify avenues for future research.
    Virology 07/2014; 460-461:147-153. · 3.35 Impact Factor
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    ABSTRACT: Despite recent declines in HIV incidence, sub-Saharan Africa remains the most heavily affected region in the global HIV/AIDS epidemic. Estimates of HIV prevalence in African military personnel are scarce and inconsistent. We conducted a serosurvey between June and September 2007 among 4043 Armed Forces personnel of the Democratic Republic of Congo (FARDC) stationed in Kinshasa, Democratic Republic of Congo (DRC) to determine the prevalence of HIV and syphilis infections and describe associated risk behaviours. Participants provided blood for HIV and syphilis testing and responded to a demographic and risk factor questionnaire. The prevalence of HIV was 3.8% and the prevalence of syphilis was 11.9%. Women were more likely than men to be HIV positive, (7.5% vs. 3.6% respectively, aOR: 1.66, 95% C.I: 1.21-2.28, p < 0.05). Factors significantly associated with HIV infection included gender and self-reported genital ulcers in the 12 months before date of enrollment. The prevalence of HIV in the military appears to be higher than the general population in DRC (3.8% vs. 1.3%, respectively), with women at increased risk of infection.
    International Journal of STD & AIDS 05/2014; · 1.00 Impact Factor
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    ABSTRACT: We tested 114 faecal samples from wild simian immunodeficiency virus (SIV)-positive (n = 43) and SIV-negative (n = 71) chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon for the presence of gastrointestinal parasites by direct smear. We observed cysts from different protozoa (Entamoeba coli and Entamoeba histolytica / Entamoeba dispar, Endolimax nana, Iodamoeba butschlii, Chilomastix mesnili, Balantidium coli and Blastocystis cells) and trophozoites from Troglodytella abrassarti and Balantidium coli. Eggs from different helminths (strongylids, Ascaris lumbricoides, Abbreviata caucasica, Trichuris sp., Capillaria sp., Enterobius anthropopeci, Bertiella sp., Hymenolepis diminuta and an undetermined fluke) were also observed. Finally, we observed eggs that could not be properly identified and classified. We did not observe any differences between the SIV + and SIV - samples except for the unidentified eggs. The studied chimpanzees were highly parasitised by strongylid (85.1 % of prevalence), Troglodytella (43.8 %) and Blastocystis (2.9 %), and the frequency of the other parasites ranged from 0.9 to 8.8 %. These high levels of parasite infections could represent an additional burden in a population where there is a high rate of the SIV virus in circulation.
    Parasitology Research 04/2014; · 2.85 Impact Factor
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    ABSTRACT: Not Applicable.
    AIDS research and human retroviruses 03/2014; · 2.18 Impact Factor
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    ABSTRACT: Enteroviruses (EVs) are a genetically and antigenically diverse group of viruses infecting humans. A mostly distinct set of EV variants have additionally been documented to infect wild apes and several, primarily captive, Old World monkey (OWM) species. To investigate the prevalence and genetic characteristics of EVs infecting OWMs in the wild, faecal samples from mandrills (Mandrillus sphinx) and other species collected in remote regions of Southern Cameroon were screened for EV RNA. Remarkably high rates of EV positivity were detected in M.sphinx (100 from 102 screened), Cercocebus torquatus (7/7) and Cercopithecus cephus (2/4), with high viral loads indicative of active infection. Genetic characterisation in VP4/VP2 and VP1 regions allowed EV variants to be assigned to simian species H (EV-H), EV-J (including one or more new types) while seven matched simian EV-B variants, SA5 and EV110 (chimpanzee). Sequences from the remaining 70 formed a new genetic group distinct in VP4/2 and VP1 region from all currently recognised human or simian EV species. Complete genome sequences were obtained from three to determine their species assignment. In common with EV-J and the EV-A A13 isolate, new group sequences were chimaeric, being most closely related to EV-A in capsid genes and to EV-B in the non-structural gene region. Further recombination events created different groupings in 5' and 3' untranslated regions. While clearly a distinct EV group, the hybrid nature of new variants prevented their unambiguous classification as either members of a new species or as divergent members of EV-A using current ICTV assignment criteria. This study is the first large scale investigation of the frequency of infection and diversity of enteroviruses (EVs) infecting monkeys (primarily mandrills) in the wild. Findings demonstrate extremely high frequencies of active infection (95%) among mandrills and other Old World monkey species inhabiting remote regions of Cameroon without human contact. EV variants detected were distinct from those infecting human populations, comprising members of enterovirus species B, J and H and a large novel group of viruses that potentially represent a candidate new EV species. The viral sequences obtained contribute substantially to our growing understanding of the genetic diversity of EVs and the existence of inter-species chimaerism that characterises the novel variants in the current study, as well as in previously characterised species A and J viruses infecting monkeys. The latter findings will contribute to future development of consensus criteria for species assignments in enteroviruses and other picornavirus genera.
    Journal of Virology 03/2014; · 5.08 Impact Factor
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    ABSTRACT: To understand the evolutionary histories and conservation potential of wild animal species it is useful to assess whether taxa are genetically structured into different populations and identify the underlying factors responsible for any clustering. Landscape features such as rivers may influence genetic population structure, and analysis of structure by sex can further reveal effects of sex-specific dispersal. Using microsatellite genotypes obtained from noninvasively collected fecal samples we investigated the population structure of 261 western lowland gorillas (WLGs) (Gorilla gorilla gorilla) from seven locations spanning an approximately 37,000 km2 region of mainly continuous rain forest within Central African Republic (CAR), Republic of Congo and Cameroon. We found our sample to consist of two or three significantly differentiated clusters. The boundaries of the clusters coincided with courses of major rivers. Moreover, geographic distance detoured around rivers better-explained variation in genetic distance than straight line distance. Together these results suggest that major rivers in our study area play an important role in directing WLG gene flow. The number of clusters did not change when males and females were analyzed separately, indicating a lack of greater philopatry in WLG females than males at this scale. Am. J. Primatol. © 2014 Wiley Periodicals, Inc.
    American Journal of Primatology 03/2014; · 2.46 Impact Factor
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    ABSTRACT: Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.
    Nature Communications 02/2014; 5:3346. · 10.74 Impact Factor
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    ABSTRACT: Dried blood spots (DBS) can be used in developing countries to alleviate the logistic constraints of using blood plasma specimens for viral load (VL) and HIV drug resistance (HIVDR) testing, but they should be assessed under field conditions. Between 2009 and 2011, we collected paired plasma-DBS samples from treatment-experienced HIV-1-infected adults in Burkina Faso, Cameroon, Senegal, Togo, Thailand, and Vietnam. The DBS were stored at an ambient temperature for 2 to 4 weeks and subsequently at -20°C before testing. VL testing was performed on the plasma samples and DBS using locally available methods: the Abbott m2000rt HIV-1 test, generic G2 real-time PCR, or the NucliSENS EasyQ version 1.2 test. In the case of virological failure (VF), i.e., a plasma VL of ≥1,000 copies/ml, HIVDR genotyping was performed on paired plasma-DBS samples. Overall, we compared 382 plasma-DBS sample pairs for DBS VL testing accuracy. The sensitivities of the different assays in different laboratories for detecting VF using DBS varied from 75% to 100% for the m2000rt test in labs B, C, and D, 91% to 93% for generic G2 real-time PCR in labs A and F, and 85% for the NucliSENS test in lab E. The specificities varied from 82% to 97% for the m2000rt and NucliSENS tests and reached only 60% for the generic G2 test. The NucliSENS test showed good agreement between plasma and DBS VL but underestimated the DBS VL. The lowest agreement was observed for the generic G2 test. Genotyping was successful for 96/124 (77%) DBS tested, and 75/96 (78%) plasma-DBS pairs had identical HIVDR mutations. Significant discrepancies in resistance interpretations were observed in 9 cases, 6 of which were from the same laboratory. DBS can be successfully used as an alternative to blood plasma samples for routine VL and HIVDR monitoring in African and Asian settings. However, the selection of an adequate VL measurement method and the definition of the VF threshold should be considered, and laboratory performance should be monitored.
    Journal of clinical microbiology 02/2014; 52(2):578-86. · 4.16 Impact Factor
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    ABSTRACT: Although gorillas regarded as the largest extant species of primates and have a close phylogenetic relationship with humans, eukaryotic communities have not been previously studied in these populations. Herein, 35 eukaryotic primer sets targeting the 18S rRNA gene, internal transcribed spacer gene and other specific genes were used firstly to explore the eukaryotes in a fecal sample from a wild western lowland gorilla (Gorilla gorilla gorilla). Then specific real-time PCRs were achieved in additional 48 fecal samples from 21 individual gorillas to investigate the presence of human eukaryotic pathogens. In total, 1,572 clones were obtained and sequenced from the 15 cloning libraries, resulting in the retrieval of 87 eukaryotic species, including 52 fungi, 10 protozoa, 4 nematodes and 21 plant species, of which 52, 5, 2 and 21 species, respectively, have never before been described in gorillas. We also reported the occurrence of pathogenic fungi and parasites (i.e. Oesophagostomum bifurcum (86%), Necator americanus (43%), Candida tropicalis (81%) and other pathogenic fungi were identified). In conclusion, molecular techniques using multiple primer sets may offer an effective tool to study complex eukaryotic communities and to identify potential pathogens in the gastrointestinal tracts of primates.
    Scientific reports. 01/2014; 4:6417.
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    ABSTRACT: The Simian Immunodeficiency Virus (SIV) mus/mon/gsn lineage is a descendant of one of the precursor viruses to the HIV-1/SIVcpz/gor viral lineage. SIVmus and SIVgsn were sequenced from mustached and greater spot nosed monkeys in Cameroon and SIVmon from mona monkeys in Cameroon and Nigeria. In order to further document the genetic diversity of SIVmus, we analyzed two full-length genomes of new strains identified in Gabon. The whole genomes obtained showed the expected reading frames for gag, pol, vif, vpr, tat, rev, env, nef, and also for a vpu gene. Analyses showed that the Gabonese SIVmus strains were closely related and formed a monophyletic clade within the SIVmus/mon/gsn lineage. Nonetheless, within this lineage, the position of both new SIVmus differed according to the gene analyzed. In pol and nef gene, phylogenetic topologies suggested different evolutions for each of the two new SIVmus strains whereas in the other nucleic fragments studied, their positions fluctuated between SIVmon, SIVmus-1, and SIVgsn. In addition, in C1 domain of env, we identified an insertion of seven amino acids characteristic for the SIVmus/mon/gsn and HIV‑1/SIVcpz/SIVgor lineages. Our results show a high genetic diversity of SIVmus in mustached monkeys and suggest cross-species transmission events and recombination within SIVmus/mon/gsn lineage. Additionally, in Central Africa, hunters continue to be exposed to these simian viruses, and this represents a potential threat to humans.
    Viruses. 01/2014; 6(7):2880-2898.
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    ABSTRACT: Wild apes are considered to be the most serious reservoir and source of zoonoses. However, little data are available about the gut microbiota and pathogenic bacteria in gorillas. For this propose, a total of 48 fecal samples obtained from 21 Gorilla gorilla gorilla individuals (as revealed via microsatellite analysis) were screened for human bacterial pathogens using culturomics and molecular techniques. By applying culturomics to one index gorilla and using specific media supplemented by plants, we tested 12,800 colonies and identified 147 different bacterial species, including 5 new species. Many opportunistic pathogens were isolated, including 8 frequently associated with human diseases; Mycobacterium bolletii, Proteus mirabilis, Acinetobacter baumannii, Klebsiella pneumoniae, Serratia marcescens, Escherichia coli, Staphylococcus aureus and Clostridium botulinum. The genus Treponema accounted for 27.4% of the total reads identified at the genus level via 454 pyrosequencing. Using specific real-time PCR on 48 gorilla fecal samples, in addition to classical human pathogens, we also observed the fastidious bacteria Bartonella spp. Borrelia spp., Coxiella burnetii and Tropheryma whipplei in the gorilla population. We estimated that the prevalence of these pathogens vary between 4.76% and 85.7%. Therefore, gorillas share many bacterial pathogens with humans suggesting that they could be a reservoir for their emergence.
    Scientific reports. 01/2014; 4:7174.
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    ABSTRACT: A total of 139 stool samples from wild chimpanzees, gorillas and bonobos in Cameroon and Democratic Republic of Congo (DRC) were screened for enteroviruses (EVs) by RT-PCR. EV RNA was detected in 10% of samples, comprising 8 from 58 sampled chimpanzees (13.8%), 1/40 bonobos (2.5%) and 5/40 gorillas (12.2%). Three chimpanzee variants grouped with human isolate EV-A89 while four (4 chimpanzee, 1 gorilla) represented a newly identified type, EV-A119. These species A virus types overlapped with those circulating in human populations in the same area. The remaining six strains comprised a new species D type, EV-D120, infecting one chimpanzee and 4 gorillas, and a single EV variant infecting a bonobo that was remarkably divergent from other EVs and potentially constitutes a new enterovirus species. The study demonstrates both the circulation of genetically divergent EV variants in apes and monkeys as well as those shared with local human populations.
    Journal of General Virology 11/2013; · 3.13 Impact Factor
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    ABSTRACT: The aim of this study was to evaluate the use for HIV-1 drug resistance testing dried blood spots collected in remote areas and sent under field conditions to a reference laboratory and also to document virological failure in patients with suspected treatment failure. Samples were collected from patients receiving first line ART at 11 hospital sites around country, kept at room temperature (<37°C) and sent within 15 days maximum to the reference laboratory. Viral nucleic acids were obtained by magnetic extraction with NucliSENS (bioMérieux, Marcy l'Etoile, France). Genotyping of HIV-1 pol gene was performed using the ANRS protocol. Drug resistance mutations were analyzed according to the Stanford University HIV database version 6.0.8. Two hundred thirty one HIV-infected adults' on HAART first line regimen composed study population. The median time on ART was 18 months (range 6-68). Regardless of the treatment duration, the overall rate of virological failure (VL ≥ 3 log10 cp/ml) was 23.8% (n = 55/231). HIV genotypes were obtained successfully in 94.5% (n = 52/55). Drug resistance mutation was found in 41/52 patients in virological failure, for 17.7% (n = 41/231) an overall rate of drug resistance mutations. M184V/I was the most frequent mutation occurring, followed by K103N. Phylogenetic analysis of the 52 genotyped viral isolates showed the predominance of CRF02_AG with 62% (n = 32/52). Use of a DBS specimen is suitable to assist national programs for monitoring in remote areas HIV drug resistance in resources limited-settings. J. Med. Virol. © 2013 Wiley Periodicals, Inc.
    Journal of Medical Virology 10/2013; · 2.37 Impact Factor
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    ABSTRACT: Background. The limited access to virological monitoring in developing countries is a major weakness of the current antiretroviral treatment (ART) strategy in these settings. We conducted a large cross-sectional study in Burkina-Faso, Cameroon, Cote d'Ivoire, Senegal, Togo, Thailand and Vietnam to assess virological failure (VF) and drug resistance mutations (DRMs) after 12 or 24 months of ART. Methods. Between 2009 and 2011, we recruited adult-patients attending ART centers for their medical visit at month 12±2 (M12) or 24±2 (M24). Demographic and clinical data were collected on site, and viral load (VL) was performed. Samples with VL≥1000 copies/ml, considered as the failure threshold, were genotyped for drug resistance assessment. Results. Overall, 3935 patients were recruited, 2060 at month 12 and 1875 at month 24 since starting ART. Median ages varied from 32 to 42 years. Median CD4 values at ART initiation were low, 99 to 172 cells/μl. Main ART regimens included stavudine/zidovudine plus lamivudine plus nevirapine/efavirenz. Overall, VF frequency was 11.1% for M12 and 12.4% for M24 patients, and 71.0% to 86.1% of these patients selected drug resistant virus. Across sites, VF varied from 2.9% to 20.6% in M12 and 3.7% to 26.0% in M24 patients. Predominant DRMs were associated with ART regimens, but several patients accumulated DRMs to drugs not received as abacavir, didanosine, tenofovir, etravirine and rilpivirine. Conclusions. Our findings show heterogeneous virological failure and illustrate that in addition to routine access to VL, good ART-programme management is even more critical to improve treatment outcome in resource-limited countries.
    Clinical Infectious Diseases 09/2013; · 9.37 Impact Factor
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    ABSTRACT: Circulating and unique recombinant HIV-1 strains continue to be identified and their number increases over time, suggesting that co-infection with multiple HIV-1 is frequent. In this study we analysed to what extent dual infections with different HIV-1 variants occur in a population group with high risk behaviour, high HIV-1 prevalence and in an area where multiple HIV-1 subtypes and Circulating Recombinant Forms (CRFs) co-circulate. We studied 69 MSM with our recently developed multi-region hybridization assay (MHA), based on fluorescent probe detection for eight common variants circulating in West and West Central Africa. At least 11 (15.9%) of the 69 patients were simultaneously infected with two different HIV-1 subtypes and/or CRFs. Among the 29 samples identified as subtype C by MHA in gag, 15 (57.7%) reacted with both C1 and C2 probes. Sequence analysis suggests that the majority of the samples reactive with C1 and C2 probes are most likely infected with two different subtype C clades. Single genome amplification and DNA dilutions confirmed dual infection with subtype D and C for MSM1193, triple infection with two different C subtype strains and one CRF02_AG strain in MSM1157 and showed that MSM3017 is at least co-infected with CRF06_cpx and CRF02_AG and another strain that could not be classified. Comparison of all subtype C sequences from the MSM population and from the general population from this and previous studies confirmed the intermixing of HIV-1 variants between low-risk women and high-risk men as shown by the intermixing of subtype C variants from MSM1157 and a female patient (02SN-HALD478). Comparison of dual infection rates between the general population and MSM in Senegal, show also clearly the importance of high HIV prevalence and high risk behaviour in dual infections and subsequent intermixing of HIV-1 variants which can lead to emergence and spread of new recombinants (CRFs).
    Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 09/2013; · 3.22 Impact Factor
  • Martine Peeters, Matthieu Jung, Ahidjo Ayouba
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    ABSTRACT: HIV-1 in humans resulted from at least four cross-species transmissions of simian immunodeficiency viruses (SIVs) from chimpanzees and gorillas in West Central Africa, while HIV-2 viruses resulted from at least eight independent transmissions of SIVs infecting sooty mangabeys in West Africa only, where one of these transmissions (HIV-1 group M) is responsible for the global epidemic. HIV-1 M is subdivided into nine subtypes and a wide diversity of circulating recombinant forms (CRFs) and unique recombinant forms. The heterogenic HIV-1 M subtype/CRF distribution is the result of founder effects. The genetic diversity of HIV-1 continues to increase overtime due to demographic factors such as travel and migration and frequent co/superinfections. In addition, the expanded access to antiretrovirals leads to an increasing number of drug-resistant strains, especially in resource limited countries.
    Expert Review of Anticancer Therapy 09/2013; · 3.22 Impact Factor

Publication Stats

5k Citations
1,084.45 Total Impact Points


  • 2003–2014
    • Université de Montpellier 1
      Montpelhièr, Languedoc-Roussillon, France
    • University of Strasbourg
      Strasburg, Alsace, France
  • 2002–2014
    • Institute of Research for Development
      Marsiglia, Provence-Alpes-Côte d'Azur, France
    • Cheikh Anta Diop University, Dakar
      Dakar, Dakar, Senegal
  • 2013
    • Royal Society of Edinburgh
      Edinburgh, Scotland, United Kingdom
    • University of Pennsylvania
      • Perelman School of Medicine
      Philadelphia, PA, United States
  • 2012
    • Université René Descartes - Paris 5
      Lutetia Parisorum, Île-de-France, France
  • 2011–2012
    • International Centre of Medical Research of Franceville
      Franceville, Haut-Ogooué, Gabon
    • Wellcome Trust Sanger Institute
      • Malaria Programme
      Cambridge, England, United Kingdom
    • State University of New York
      New York City, New York, United States
  • 2006–2012
    • Universität Ulm
      • • Institute of Molecular Virology
      • • Institute of Virology
      Ulm, Baden-Wuerttemberg, Germany
    • Institut de Recherche en Cancerologie de Montpellier
      Montpelhièr, Languedoc-Roussillon, France
    • Institut de France
      Lutetia Parisorum, Île-de-France, France
  • 2010–2011
    • The University of Edinburgh
      • Edinburgh Infectious Diseases
      Edinburgh, SCT, United Kingdom
    • Global Viral Forecasting Initiative
      San Francisco, California, United States
    • University of Helsinki
      • Haartman Institute
      Helsinki, Southern Finland Province, Finland
    • University of Yaounde I
      Jaúnde, Centre Region, Cameroon
  • 2004–2010
    • University of Alabama at Birmingham
      • Department of Medicine
      Birmingham, AL, United States
  • 2009
    • Institute of Agricultural Research for Development
      Jaúnde, Centre Region, Cameroon
  • 2008–2009
    • Tsinghua University
      Peping, Beijing, China
  • 2003–2007
    • University of Nottingham
      • Centre for Sports Medicine
      Nottingham, ENG, United Kingdom
  • 2002–2007
    • University of Leuven
      • Department of Microbiology and Immunology
      Louvain, Flanders, Belgium
  • 2005–2006
    • Institute of Tropical Medicine
      Antwerpen, Flanders, Belgium
  • 2003–2005
    • Institut de Recherches Mathematiques , Cote d'Ivoire, Abidjan
      Abijan, Lagunes, Ivory Coast
  • 2002–2003
    • National Hospital of Niamey
      Niamey, Niamey, Niger
  • 1993
    • Claude Bernard University Lyon 1
      Villeurbanne, Rhône-Alpes, France