{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T03:32:44Z","timestamp":1787801564223,"version":"build-2784847793"},"update-to":[{"DOI":"10.1371\/journal.ppat.1009916","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,9,24]],"date-time":"2021-09-24T00:00:00Z","timestamp":1632441600000}}],"reference-count":54,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2021,9,14]],"date-time":"2021-09-14T00:00:00Z","timestamp":1631577600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002915","name":"fondation pour la recherche m\u00e9dicale","doi-asserted-by":"crossref","award":["ECO20170637560"],"award-info":[{"award-number":["ECO20170637560"]}],"id":[{"id":"10.13039\/501100002915","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>Opioid substitution and syringes exchange programs have drastically reduced hepatitis C virus (HCV) spread in France but HCV sexual transmission in men having sex with men (MSM) has recently arisen as a significant public health concern. The fact that the virus is transmitting in a heterogeneous population, with different transmission routes, makes prevalence and incidence rates poorly informative. However, additional insights can be gained by analyzing virus phylogenies inferred from dated genetic sequence data. By combining a phylodynamics approach based on Approximate Bayesian Computation (ABC) and an original transmission model, we estimate key epidemiological parameters of an ongoing HCV epidemic among MSMs in Lyon (France). We show that this new epidemic is largely independent of the previously observed non-MSM HCV epidemics and that its doubling time is ten times lower (0.44 years <jats:italic>versus<\/jats:italic> 4.37 years). These results have practical implications for HCV control and illustrate the additional information provided by virus genomics in public health.<\/jats:p>","DOI":"10.1371\/journal.ppat.1009916","type":"journal-article","created":{"date-parts":[[2021,9,14]],"date-time":"2021-09-14T17:33:29Z","timestamp":1631640809000},"page":"e1009916","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":13,"title":["Quantifying transmission dynamics of acute hepatitis C virus infections in a heterogeneous population using sequence data"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8688-7666","authenticated-orcid":true,"given":"Gonch\u00e9","family":"Danesh","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victor","family":"Virlogeux","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1981-7155","authenticated-orcid":true,"given":"Christophe","family":"Rami\u00e8re","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4356-5146","authenticated-orcid":true,"given":"Caroline","family":"Charre","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4063-9250","authenticated-orcid":true,"given":"Laurent","family":"Cotte","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0779-9543","authenticated-orcid":true,"given":"Samuel","family":"Alizon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,9,14]]},"reference":[{"key":"ppat.1009916.ref001","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1002\/hep.27259","article-title":"Global distribution and prevalence of hepatitis C virus genotypes","volume":"61","author":"JP Messina","year":"2015","journal-title":"Hepatology"},{"issue":"5","key":"ppat.1009916.ref002","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/S2468-1253(17)30045-6","article-title":"Hepatitis C virus prevalence and level of intervention required to achieve the WHO targets for elimination in the European Union by 2030: a modelling study","volume":"2","author":"European Union HCV Collaborators","year":"2017","journal-title":"Lancet Gastroenterol Hepatol"},{"issue":"S1","key":"ppat.1009916.ref003","doi-asserted-by":"crossref","first-page":"S6","DOI":"10.1016\/j.jhep.2005.11.004","article-title":"Epidemiology of viral hepatitis and HIV co-infection","volume":"44","author":"MJ Alter","year":"2006","journal-title":"J Hepatol"},{"issue":"5","key":"ppat.1009916.ref004","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1111\/j.1468-1293.2008.00686.x","article-title":"Liver-related deaths in HIV-infected patients between 1995 and 2005 in the French GERMIVIC Joint Study Group Network (Mortavic 2005 Study in collaboration with the Mortalit\u00e9 2005 survey, ANRS EN19)","volume":"10","author":"E Rosenthal","year":"2009","journal-title":"HIV Medicine"},{"issue":"3","key":"ppat.1009916.ref005","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.jhep.2015.04.019","article-title":"High hepatic and extrahepatic mortality and low treatment uptake in HCV-coinfected persons in the Swiss HIV cohort study between 2001 and 2013","volume":"63","author":"H Kovari","year":"2015","journal-title":"J Hepatol"},{"issue":"9","key":"ppat.1009916.ref006","first-page":"1160","article-title":"Risk of End-Stage Liver Disease in HIV-Viral Hepatitis Coinfected Persons in North America From the Early to Modern Antiretroviral Therapy Eras","volume":"63","author":"MB Klein","year":"2016","journal-title":"Clin Infect Dis"},{"issue":"3","key":"ppat.1009916.ref007","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/j.jinf.2017.05.008","article-title":"Direct-acting antiviral treatment against hepatitis C virus infection in HIV-Infected patients\u2014\u201cEn route for eradication\u201d?","volume":"75","author":"P Pradat","year":"2017","journal-title":"J Infection"},{"issue":"3","key":"ppat.1009916.ref008","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1111\/liv.13528","article-title":"Trends in HCV treatment uptake, efficacy and impact on liver fibrosis in the Swiss HIV Cohort Study","volume":"38","author":"C B\u00e9guelin","year":"2018","journal-title":"Liver International"},{"issue":"1","key":"ppat.1009916.ref009","doi-asserted-by":"crossref","DOI":"10.1093\/ofid\/ofx258","article-title":"Human Immunodeficiency Virus\/Hepatits C Virus Coinfection in Spain: Elimination Is Feasible, but the Burden of Residual Cirrhosis Will Be Significant","volume":"5","author":"J Berenguer","year":"2018","journal-title":"Open Forum Infect Dis"},{"issue":"9","key":"ppat.1009916.ref010","doi-asserted-by":"crossref","first-page":"1360","DOI":"10.1093\/cid\/cix1007","article-title":"Declining Hepatitis C Virus (HCV) Incidence in Dutch Human Immunodeficiency Virus-Positive Men Who Have Sex With Men After Unrestricted Access to HCV Therapy","volume":"66","author":"A Boerekamps","year":"2018","journal-title":"Clin Infect Dis"},{"issue":"5","key":"ppat.1009916.ref011","doi-asserted-by":"crossref","first-page":"1609","DOI":"10.1053\/j.gastro.2009.02.006","article-title":"Evidence of a Large, International Network of HCV Transmission in HIV-Positive Men Who Have Sex With Men","volume":"136","author":"T van de Laar","year":"2009","journal-title":"Gastroenterology"},{"issue":"6","key":"ppat.1009916.ref012","doi-asserted-by":"crossref","first-page":"1856","DOI":"10.1002\/hep.28769","article-title":"Hepatitis C virus transmission among human immunodeficiency virus-infected men who have sex with men: Modeling the effect of behavioral and treatment interventions","volume":"64","author":"L Salazar-Vizcaya","year":"2016","journal-title":"Hepatology"},{"issue":"8","key":"ppat.1009916.ref013","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1097\/QAD.0000000000001789","article-title":"Incidence of new hepatitis C virus infection is still increasing in French MSM living with HIV","volume":"32","author":"P Pradat","year":"2018","journal-title":"AIDS"},{"issue":"1","key":"ppat.1009916.ref014","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1023\/A:1010902614443","article-title":"Prevalence of hepatitis C infection among general practice patients in the Lyon area, France","volume":"17","author":"P Pradat","year":"2001","journal-title":"Eur J Epidemiol"},{"issue":"3","key":"ppat.1009916.ref015","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1111\/j.1365-2893.2005.00583.x","article-title":"Prevalence and sexual risk of hepatitis C virus infection when human immunodeficiency virus was acquired through sexual intercourse among patients of the Lyon University Hospitals, France, 1992-2002","volume":"12","author":"JA D\u2019Oliveira","year":"2005","journal-title":"J Viral Hepat"},{"issue":"2","key":"ppat.1009916.ref016","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1093\/pubmed\/fdq071","article-title":"A randomized trial of viral hepatitis prevention among underprivileged people in the Lyon area of France","volume":"33","author":"F Sahajian","year":"2011","journal-title":"J Public Health"},{"key":"ppat.1009916.ref017","doi-asserted-by":"crossref","first-page":"2127","DOI":"10.1093\/cid\/ciz160","article-title":"Patterns of Hepatitis C Virus Transmission in Human Immunodeficiency Virus (HIV)\u2013infected and HIV-negative Men Who Have Sex With Men","volume":"69","author":"C Rami\u00e8re","year":"2019","journal-title":"Clin Infect Dis"},{"issue":"1","key":"ppat.1009916.ref018","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1186\/s12916-017-0979-1","article-title":"Modeling HIV-HCV coinfection epidemiology in the direct-acting antiviral era: the road to elimination","volume":"15","author":"V Virlogeux","year":"2017","journal-title":"BMC Medicine"},{"issue":"2","key":"ppat.1009916.ref019","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.meegid.2004.08.001","article-title":"The hepatitis C virus epidemic among injecting drug users","volume":"5","author":"OG Pybus","year":"2005","journal-title":"Inf Gen Evol"},{"issue":"4","key":"ppat.1009916.ref020","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1093\/biostatistics\/kxn004","article-title":"Estimating hepatitis C prevalence in England and Wales by synthesizing evidence from multiple data sources. Assessing data conflict and model fit","volume":"9","author":"MJ Sweeting","year":"2008","journal-title":"Biostatistics"},{"issue":"4","key":"ppat.1009916.ref021","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1097\/QAI.0b013e3181a2539a","article-title":"The Impact of Needle and Syringe Programs on HIV and HCV Transmissions in Injecting Drug Users in Australia: A Model-Based Analysis","volume":"51","author":"JA Kwon","year":"2009","journal-title":"JAIDS Journal of Acquired Immune Deficiency Syndromes"},{"key":"ppat.1009916.ref022","article-title":"Mathematical modeling of hepatitis c virus (HCV) prevention among people who inject drugs: A review of the literature and insights for elimination strategies","author":"AB Pitcher","year":"2018","journal-title":"J theor Biol"},{"issue":"9","key":"ppat.1009916.ref023","doi-asserted-by":"crossref","first-page":"e541","DOI":"10.1016\/S2214-109X(14)70188-3","article-title":"Effect of preventive and curative interventions on hepatitis C virus transmission in Egypt (ANRS 1211): a modelling study","volume":"2","author":"R Breban","year":"2014","journal-title":"Lancet Glob Health"},{"issue":"10178","key":"ppat.1009916.ref024","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1016\/S0140-6736(18)32277-3","article-title":"Scaling up prevention and treatment towards the elimination of hepatitis C: a global mathematical model","volume":"393","author":"A Heffernan","year":"2019","journal-title":"Lancet"},{"issue":"5656","key":"ppat.1009916.ref025","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1126\/science.1090727","article-title":"Unifying the epidemiological and evolutionary dynamics of pathogens","volume":"303","author":"BT Grenfell","year":"2004","journal-title":"Science"},{"issue":"3","key":"ppat.1009916.ref026","doi-asserted-by":"crossref","first-page":"e1002947","DOI":"10.1371\/journal.pcbi.1002947","article-title":"Viral phylodynamics","volume":"9","author":"EM Volz","year":"2013","journal-title":"PLoS Comput Biol"},{"key":"ppat.1009916.ref027","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.epidem.2014.09.001","article-title":"Eight challenges in phylodynamic inference","volume":"10","author":"SD Frost","year":"2015","journal-title":"Epidemics"},{"issue":"5525","key":"ppat.1009916.ref028","doi-asserted-by":"crossref","first-page":"2323","DOI":"10.1126\/science.1058321","article-title":"The epidemic behavior of the hepatitis C virus","volume":"292","author":"OG Pybus","year":"2001","journal-title":"Science"},{"issue":"12","key":"ppat.1009916.ref029","doi-asserted-by":"crossref","first-page":"e1000198","DOI":"10.1371\/journal.pmed.1000198","article-title":"The Global Spread of Hepatitis C Virus 1a and 1b: A Phylodynamic and Phylogeographic Analysis","volume":"6","author":"G Magiorkinis","year":"2009","journal-title":"PLOS Med"},{"issue":"1","key":"ppat.1009916.ref030","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1073\/pnas.1207965110","article-title":"Birth-death skyline plot reveals temporal changes of epidemic spread in HIV and hepatitis C virus (HCV)","volume":"110","author":"T Stadler","year":"2013","journal-title":"Proc Natl Acad Sci USA"},{"issue":"6","key":"ppat.1009916.ref031","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1016\/S1473-3099(16)00124-9","article-title":"The spread of hepatitis C virus genotype 1a in North America: a retrospective phylogenetic study","volume":"16","author":"JB Joy","year":"2016","journal-title":"Lancet Infect Dis"},{"issue":"4","key":"ppat.1009916.ref032","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1093\/genetics\/162.4.2025","article-title":"Approximate Bayesian Computation in Population Genetics","volume":"162","author":"MA Beaumont","year":"2002","journal-title":"Genetics"},{"issue":"3","key":"ppat.1009916.ref033","doi-asserted-by":"crossref","first-page":"e1005416","DOI":"10.1371\/journal.pcbi.1005416","article-title":"Inferring epidemiological parameters from phylogenies using regression-ABC: A comparative study","volume":"13","author":"E Saulnier","year":"2017","journal-title":"PLOS Comput Biol"},{"key":"ppat.1009916.ref034","volume-title":"Dynamics and Control","author":"RM Anderson","year":"1991"},{"issue":"2","key":"ppat.1009916.ref035","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1086\/518796","article-title":"Increase in HCV Incidence among Men Who Have Sex with Men in Amsterdam Most Likely Caused by Sexual Transmission","volume":"196","author":"TJW van de Laar","year":"2007","journal-title":"J Infect Dis"},{"issue":"10","key":"ppat.1009916.ref036","doi-asserted-by":"crossref","first-page":"1408","DOI":"10.1093\/cid\/cis694","article-title":"Hepatitis C Virus Infections in the Swiss HIV Cohort Study: A Rapidly Evolving Epidemic","volume":"55","author":"G Wandeler","year":"2012","journal-title":"Clin Infect Dis"},{"issue":"3","key":"ppat.1009916.ref037","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1002\/hep.27950","article-title":"Hepatitis C guidance: AASLD-IDSA recommendations for testing, managing, and treating adults infected with hepatitis C virus","volume":"62","author":"AASLD\/IDSA HCV Guidance Panel","year":"2015","journal-title":"Hepatology"},{"issue":"10","key":"ppat.1009916.ref038","doi-asserted-by":"crossref","first-page":"2690","DOI":"10.1073\/pnas.1522930113","article-title":"Phylogenetically resolving epidemiologic linkage","volume":"113","author":"EO Romero-Severson","year":"2016","journal-title":"Proc Nat Acad Sci USA"},{"issue":"10","key":"ppat.1009916.ref039","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.1093\/aje\/kwx182","article-title":"Shared Genomic Variants: Identification of Transmission Routes Using Pathogen Deep-Sequence Data","volume":"186","author":"CJ Worby","year":"2017","journal-title":"Am J Epidemiol"},{"issue":"3","key":"ppat.1009916.ref040","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1093\/molbev\/msx304","article-title":"PHYLOSCANNER: Inferring Transmission from Within- and Between-Host Pathogen Genetic Diversity","volume":"35","author":"C Wymant","year":"2018","journal-title":"Mol Biol Evol"},{"issue":"15","key":"ppat.1009916.ref041","doi-asserted-by":"crossref","first-page":"2147","DOI":"10.1097\/QAD.0000000000001592","article-title":"Limited overlap between phylogenetic HIV and HCV clusters illustrates the dynamic sexual","volume":"31","author":"JW Vanhommerig","year":"2017","journal-title":"AIDS"},{"issue":"4","key":"ppat.1009916.ref042","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1111\/j.1365-2893.2005.00605.x","article-title":"Changing of hepatitis C virus genotype patterns in France at the beginning of the third millenium: The GEMHEP GenoCII Study","volume":"12","author":"C Payan","year":"2005","journal-title":"Journal of Viral Hepatitis"},{"issue":"1614","key":"ppat.1009916.ref043","doi-asserted-by":"crossref","first-page":"20120198","DOI":"10.1098\/rstb.2012.0198","article-title":"Uncovering epidemiological dynamics in heterogeneous host populations using phylogenetic methods","volume":"368","author":"T Stadler","year":"2013","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"issue":"11","key":"ppat.1009916.ref044","doi-asserted-by":"crossref","first-page":"e1006546","DOI":"10.1371\/journal.pcbi.1006546","article-title":"Bayesian phylodynamic inference with complex models","volume":"14","author":"EM Volz","year":"2018","journal-title":"PLoS Comput Biol"},{"issue":"2","key":"ppat.1009916.ref045","doi-asserted-by":"crossref","first-page":"e1006895","DOI":"10.1371\/journal.ppat.1006895","article-title":"Quantifying the fitness cost of HIV-1 drug resistance mutations through phylodynamics","volume":"14","author":"D K\u00fchnert","year":"2018","journal-title":"PLoS Pathog"},{"issue":"8","key":"ppat.1009916.ref046","doi-asserted-by":"crossref","first-page":"2102","DOI":"10.1093\/molbev\/msw064","article-title":"Phylodynamics with Migration: A Computational Framework to Quantify Population Structure from Genomic Data","volume":"33","author":"D K\u00fchnert","year":"2016","journal-title":"Molecular Biology and Evolution"},{"issue":"4","key":"ppat.1009916.ref047","doi-asserted-by":"crossref","first-page":"e1003537","DOI":"10.1371\/journal.pcbi.1003537","article-title":"BEAST 2: A Software Platform for Bayesian Evolutionary Analysis","volume":"10","author":"R Bouckaert","year":"2014","journal-title":"PLoS Comput Biol"},{"key":"ppat.1009916.ref048","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1186\/1471-2148-11-131","article-title":"The mode and tempo of hepatitis C virus evolution within and among hosts","volume":"11","author":"RR Gray","year":"2011","journal-title":"BMC Evol Biol"},{"key":"ppat.1009916.ref049","first-page":"599","article-title":"How generation intervals shape the relationship between growth rates and reproductive numbers","volume":"274","author":"J Wallinga","year":"2007","journal-title":"Proc R Soc Lond B"},{"key":"ppat.1009916.ref050","article-title":"Simulating trajectories and phylogenies from population dynamics models with TiPS","author":"G Danesh","year":"2020","journal-title":"bioRxiv"},{"issue":"4","key":"ppat.1009916.ref051","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/0021-9991(76)90041-3","article-title":"A general method for numerically simulating the stochastic time evolution of coupled chemical reactions","volume":"22","author":"DT Gillespie","year":"1976","journal-title":"J Comput Physics"},{"issue":"3","key":"ppat.1009916.ref052","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1093\/sysbio\/syv116","article-title":"Characterizing and comparing phylogenies from their laplacian spectrum","volume":"65","author":"E Lewitus","year":"2016","journal-title":"Syst Biol"},{"key":"ppat.1009916.ref053","article-title":"abc: an R package for approximate Bayesian computation (ABC)","author":"K Csillery","year":"2012","journal-title":"Methods Ecol Evol"},{"issue":"2","key":"ppat.1009916.ref054","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1111\/j.1467-9868.2005.00503.x","article-title":"Regularization and Variable Selection via the Elastic Net","volume":"67","author":"H Zou","year":"2005","journal-title":"J R Stat Soc B"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1009916","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,9,24]],"date-time":"2021-09-24T00:00:00Z","timestamp":1632441600000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1009916","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,24]],"date-time":"2021-09-24T18:08:07Z","timestamp":1632506887000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1009916"}},"subtitle":[],"editor":[{"given":"Nels C.","family":"Elde","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,9,14]]},"references-count":54,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9,14]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1009916","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.ppat.1009916","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,14]]}}}