- Email: [email protected]
Challenges in molecular epidemiology of hepatitis C virus
Journal of Clinical Virology 60 (2014) 174–176
Contents lists available at ScienceDirect
Journal of Clinical Virology journal homepage: www.elsevier.com/locate/jcv
Commentaries and Points of View
Challenges in molecular epidemiology of hepatitis C virus Livia Maria Gonc¸alves Rossi ∗ , Paula Rahal Department of Biology, Institute of Bioscience, Language and Exact Science, São Paulo State University, São José do Rio Preto, SP, Brazil
a r t i c l e
i n f o
Article history: Received 18 February 2014 Received in revised form 18 March 2014 Accepted 21 March 2014 Keywords: HCV Molecular epidemiology Evolution Outbreaks Genetic relatedness
Hepatitis C virus (HCV) infection is an important public health problem. Recent studies estimate that >180 million people are currently infected worldwide [1]. Approximately, 3–4 million new infections are reported annually [2], including 499,000 deaths [3], owned to the lack of vaccines [4], and until recently, a successful antiviral therapy [5]. Early identification of HCV infection has important clinical implications since acute cases usually exhibit higher sustained viral response (SVR) rates. Therefore, identification of transmissions events in a timely manner remains as one of the most important issues in HCV control [6], and other viral hepatitis [7,8]. However, and despite improvements in molecular methodologies, HCV molecular epidemiology still faces important challenges. Here, we highlight the main issues hindering the implementation of HCV global molecular epidemiology. Identification of cases is essential for HCV control. Implementation of serologic and nucleic acid testing (NAT), followed by appropriate care and treatment, can reduce HCV transmission [9]. Testing of high-risk groups and birth cohorts is cost effective [10], and can prevent liver disease progression [11]. Thus, development of testing capabilities for identification of active and recent infection as well as facilitating access to care and treatment is critical for HCV control. HCV transmission networks are difficult to identify due to the silent onset of disease and the absence of methods capable to discern between acute and chronic infection [12,13]. The intricate patterns of HCV molecular evolution, including genetic bottlenecks [14,15], genetic drift [16,17], staged evolution and
∗ Corresponding author at: Tel.: +55 17 3221 2200x2779; fax: +55 17 3221 2200. E-mail address: [email protected] (L.M. Gonc¸alves Rossi). http://dx.doi.org/10.1016/j.jcv.2014.03.016 1386-6532/© 2014 Elsevier B.V. All rights reserved.
temporal variations [18], further complicate the recognition of transmission events. Characterization of the HCV intrahost population commonly relies on sequence information obtained from the hypervariable region 1 (HVR1) [19–21]. However, rapid sequence divergence significantly affects genetic relatedness between isolates associated with common sources of infection [12,22,23], resulting in loss of links over time. Re-infection and superinfection among drug users can also contribute to rapid sequence divergence. Moreover, phylogenetic analyses of the E1/E2 region not always faithfully reflect epidemiological relationships between isolates from serial transmissions [24]. Therefore, improved molecular methods should be implemented to overcome these limitations. The use of other HCV subgenomic regions, such as the NS5A [25,26], and ideally the entire viral genome, is likely to improve tracking of HCV transmission over time. Conventional methodologies for assessment of the intrahost HCV genetic variation are cumbersome, expensive and provide limited sequence information [27]. Next-generation sequencing (NGS) platforms and powerful statistical approaches have significantly improved molecular characterization, and facilitated the study of HCV transmissions, helping unveil the mechanisms involved in virus spread [21,28,29]. In addition, implementation of universal laboratory methods for the characterization of the intrahost HCV variability is required to facilitate the interchange of information among laboratories in different settings. Development of inexpensive molecular approaches capable to analyze large number of specimens is also needed for optimal global HCV molecular epidemiology. Adequate molecular surveillance strategies are necessary for the identification of HCV transmission networks. Different global strategies to monitor the circulation of HCV lineages have been
L.M. Gonc¸alves Rossi, P. Rahal / Journal of Clinical Virology 60 (2014) 174–176
suggested. HCV molecular characterization in general population using volunteers has been proposed for tracking of HCV transmissions [30]. However, the usefulness of this approach is significantly hampered by the prevalence of infection. Genotype distribution has also been used to monitor HCV infection among blood donors [31–33]. In this setting, recurrent blood donors offer a unique opportunity to identify acute cases associated with recent transmissions. Importantly, testing of blood donors should be accompanied by exhaustive epidemiological investigations aimed to identify all individuals involved in the transmission network. Molecular characterization of the HCV intrahost population in infected patients, starting or undergoing antiviral treatment, is an important source of information towards global HCV molecular surveillance. Limited HCV sequence divergence among treatment naïve patients is likely to facilitate the identification of clusters in relatively recent transmissions. However, untreated patients with long-term HCV infection who undergo rapid or intermediate viral evolution would be more difficult to link to their original source of infection. Conversely, experienced or relapsing HCV cases are intriguing sentinels for the identification of transmissions. In these patients, in addition to the selective immune pressure encountered during the natural course of infection, the viral population is also subjected to the selective force imposed by the antiviral therapy [34], which can distort genetic links. The dual treatment based on interferon and ribavirin affects the pattern of HCV molecular evolution [34,35]. Upon treatment, the selective pressure exerted by the antiviral drug prompts a continuous selection of variants resulting in the swapping of viral lineages during the course of therapy [34]. Moreover, the mutagenic effects of ribavirin on the HCV infecting population also contribute to the intrahost nucleotide variability in treatment experienced patients [36]. Development of drug escape variants during the course of therapy or among relapsers might also increase the genetic distance between founder variants and subsequent progeny, diluting genetic relatedness and hampering the accurate identification of transmission events. Thus, disruption of links due to modifications in the HCV molecular evolution upon treatment with different drugs imposes a challenge in genetic relatedness studies. Additionally, the rapidly evolving field of antiHCV therapy offers a plethora of novel drugs that are likely to modify the natural course of HCV intrahost molecular evolution. Therefore, assessing the impact of new anti-HCV agents in the genetic relatedness among cases linked to a common source is needed. The massive sequence information provided by different NGS represents a major challenge requiring exceptional computational capabilities. Implementation of novel strategies for data storing is also critical in the era of next generation sequencing. Therefore, the development of global databases and algorithms capable of rapidly screening thousands of entries is necessary to establish genetic relatedness among HCV cases. In addition, approaches for data sharing between laboratory networks are indispensable for global analysis of HCV transmissions. In summary, inclusion of blood collection centers and outpatient clinics as sentinel sites for surveillance programs is likely to aid in the identification of transmission networks. Characterization of the HCV inter and intrahost population, using multiple subgenomic regions, and ideally the whole HCV genome, through large-scale routine screening of blood donors, treatment naïve, non-responder and relapsers might significantly strengthen HCV molecular surveillance. Comprehensive HCV molecular studies might close the existing gaps in transmission networks due to missing links. Development of sequence databases and data sharing is also indispensable for enhanced HCV molecular surveillance. While the challenges faced by global molecular epidemiology are daunting and numerous, the reward is well worth the efforts. Unveiling the most intimate details involved in HCV transmission should facilitate the implementation of measures aimed to control disease.
175
1. Funding Not applicable. 2. Competing interests None to be declared. 3. Ethical approval Not required. References [1] Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 2013;57:1333–42. [2] Lavanchy D. The global burden of hepatitis C. Liver Int 2009;29(Suppl. 1):74–81. [3] Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012;380:2095–128. [4] Fauvelle C, Lepiller Q, Felmlee DJ, Fofana I, Habersetzer F, Stoll-Keller F, et al. Hepatitis C virus vaccines – progress and perspectives. Microb Pathog 2013;58:66–72. [5] Wendt A, Adhoute X, Castellani P, Oules V, Ansaldi C, Benali S, et al. Chronic hepatitis C: future treatment. Clin Pharmacol 2014;6:1–17. [6] Hellinger WC, Bacalis LP, Kay RS, Thompson ND, Xia GL, Lin Y, et al. Health care-associated hepatitis C virus infections attributed to narcotic diversion. Ann Intern Med 2012;156:477–82. [7] Jasuja S, Thompson ND, Peters PJ, Khudyakov YE, Patel MT, Linchangco P, et al. Investigation of hepatitis B virus and human immunodeficiency virus transmission among severely mentally ill residents at a long term care facility. PLoS ONE 2012;7:e43252. [8] Wheeler C, Vogt TM, Armstrong GL, Vaughan G, Weltman A, Nainan OV, et al. An outbreak of hepatitis A associated with green onions. New Engl J Med 2005;353:890–7. [9] Ward JW. Testing for HCV: the first step in preventing disease transmission and improving health outcomes for HCV-infected individuals. Antivir Ther 2012;17:1397–401. [10] Rein DB, Smith BD, Wittenborn JS, Lesesne SB, Wagner LD, Roblin DW, et al. The cost-effectiveness of birth-cohort screening for hepatitis C antibody in U.S. primary care settings. Ann Intern Med 2012;156:263–70. [11] Smith BD, Morgan RL, Beckett GA, Falck-Ytter Y, Holtzman D, Teo CG, et al. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945–1965. MMWR Recomm Rep 2012;61:1–32. [12] Cruz-Rivera M, Carpio-Pedroza JC, Escobar-Gutierrez A, Lozano D, VergaraCastaneda A, Rivera-Osorio P, et al. Rapid hepatitis C virus divergence among chronically infected individuals. J Clin Microbiol 2013;51:629–32. [13] Araujo AC. Antibody- and genome-based identification of recent HCV infection. Antivir Ther 2012;17:1459–64. [14] Wang GP, Sherrill-Mix SA, Chang KM, Quince C, Bushman FD, Hepatitis C. virus transmission bottlenecks analyzed by deep sequencing. J Virol 2010;84:6218–28. [15] Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST, Chopra A, et al. Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLoS Pathog 2011;7:e1002243. [16] Kao JH, Chen PJ, Lai MY, Wang TH, Chen DS. Quasispecies of hepatitis C virus and genetic drift of the hypervariable region in chronic type C hepatitis. J Infect Dis 1995;172:261–4. [17] Allain JP, Dong Y, Vandamme AM, Moulton V, Salemi M. Evolutionary rate and genetic drift of hepatitis C virus are not correlated with the host immune response: studies of infected donor–recipient clusters. J Virol 2000;74:2541–9. [18] Ramachandran S, Campo DS, Dimitrova ZE, Xia GL, Purdy MA, Khudyakov YE. Temporal variations in the hepatitis C virus intrahost population during chronic infection. J Virol 2011;85:6369–80. [19] Forbi JC, Campo DS, Purdy MA, Dimitrova ZE, Skums P, Xia GL, et al. Intra-host diversity and evolution of hepatitis C virus endemic to Cote d’Ivoire. J Med Virol 2014;86(May (5)):765–71. [20] Campo DS, Skums P, Dimitrova Z, Vaughan G, Forbi JC, Teo CG, et al. Drug-resistance of a viral population and its individual intra-host variants during the first 48 hours of therapy. Clin Pharmacol Ther 2014, http://dx.doi.org/10.1038/clpt.2014.20. PMID: 24488144 [Epub ahead of print]. [21] Escobar-Gutierrez A, Vazquez-Pichardo M, Cruz-Rivera M, Rivera-Osorio P, Carpio-Pedroza JC, Ruiz-Pacheco JA, et al. Identification of hepatitis C virus transmission using a next-generation sequencing approach. J Clin Microb 2012;50:1461–3. [22] Kurosaki M, Enomoto N, Marumo F, Sato C. Rapid sequence variation of the hypervariable region of hepatitis C virus during the course of chronic infection. Hepatology 1993;18:1293–9.
176
L.M. Gonc¸alves Rossi, P. Rahal / Journal of Clinical Virology 60 (2014) 174–176
[23] Ray SC, Fanning L, Wang XH, Netski DM, Kenny-Walsh E, Thomas DL. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J Exp Med 2005;201:1753–9. [24] Casino C, McAllister J, Davidson F, Power J, Lawlor E, Yap PL, et al. Variation of hepatitis C virus following serial transmission: multiple mechanisms of diversification of the hypervariable region and evidence for convergent genome evolution. J Gen Virol 1999;80(Pt 3):717–25. [25] Rispeter K, Lu M, Behrens SE, Fumiko C, Yoshida T, Roggendorf M. Hepatitis C virus variability: sequence analysis of an isolate after 10 years of chronic infection. Virus Genes 2000;21:179–88. [26] Fan W, Zhu W, Wei L, Wang Q, Yin L, Du S, et al. Nonstructural 5A gene variability of hepatitis C virus (HCV) during a 10-year follow up. J Gastroenterol 2005;40:43–51. [27] Fonseca-Coronado S, Escobar-Gutierrez A, Ruiz-Tovar K, Cruz-Rivera MY, Rivera-Osorio P, Vazquez-Pichardo M, et al. Specific detection of naturally occurring hepatitis C virus mutants with resistance to telaprevir and boceprevir (protease inhibitors) among treatment-naive infected individuals. J Clin Microbiol 2012;50:281–7. [28] Gonzalez-Candelas F, Bracho MA, Wrobel B, Moya A. Molecular evolution in court: analysis of a large hepatitis C virus outbreak from an evolving source. BMC Biol 2013;11:76. [29] Cruz-Rivera M, Forbi JC, Yamasaki LH, Vazquez-Chacon CA, MartinezGuarneros A, Carpio-Pedroza JC, et al. Molecular epidemiology of viral
[30]
[31]
[32]
[33]
[34] [35]
[36]
diseases in the era of next generation sequencing. J Clin Virol 2013;57: 378–80. del Pino N, Oubina JR, Rodriguez-Frias F, Esteban JI, Buti M, Otero T, et al. Molecular epidemiology and putative origin of hepatitis C virus in random volunteers from Argentina. World J Gastroenterol 2013;19:5813–27. Oh DJ, Park YM, Seo YI, Lee JS, Lee JY. Prevalence of hepatitis C virus infections and distribution of hepatitis C virus genotypes among Korean blood donors. Ann Lab Med 2012;32:210–5. Mora MV, Romano CM, Gomes-Gouvea MS, Gutierrez MF, Carrilho FJ, Pinho JR. Molecular characterization, distribution, and dynamics of hepatitis C virus genotypes in blood donors in Colombia. J Med Virol 2010;82:1889–98. Cantaloube JF, Gallian P, Laperche S, Elghouzzi MH, Piquet Y, Bouchardeau F, et al. Molecular characterization of genotype 2 and 4 hepatitis C virus isolates in French blood donors. J Med Virol 2008;80:1732–9. Alfonso V, Mbayed VA, Sookoian S, Campos RH. Intra-host evolutionary dynamics of hepatitis C virus E2 in treated patients. J Gen Virol 2005;86:2781–6. Saludes V, Gonzalez-Candelas F, Planas R, Sola R, Ausina V, Martro E. Evolutionary dynamics of the E1-E2 viral populations during combination therapy in non-responder patients chronically infected with hepatitis C virus subtype 1b. Infect Genet Evol 2013;13:1–10. Dietz J, Schelhorn SE, Fitting D, Mihm U, Susser S, Welker MW, et al. Deep sequencing reveals mutagenic effects of ribavirin during monotherapy of hepatitis C virus genotype 1-infected patients. J Virol 2013;87:6172–81.
Contents lists available at ScienceDirect
Journal of Clinical Virology journal homepage: www.elsevier.com/locate/jcv
Commentaries and Points of View
Challenges in molecular epidemiology of hepatitis C virus Livia Maria Gonc¸alves Rossi ∗ , Paula Rahal Department of Biology, Institute of Bioscience, Language and Exact Science, São Paulo State University, São José do Rio Preto, SP, Brazil
a r t i c l e
i n f o
Article history: Received 18 February 2014 Received in revised form 18 March 2014 Accepted 21 March 2014 Keywords: HCV Molecular epidemiology Evolution Outbreaks Genetic relatedness
Hepatitis C virus (HCV) infection is an important public health problem. Recent studies estimate that >180 million people are currently infected worldwide [1]. Approximately, 3–4 million new infections are reported annually [2], including 499,000 deaths [3], owned to the lack of vaccines [4], and until recently, a successful antiviral therapy [5]. Early identification of HCV infection has important clinical implications since acute cases usually exhibit higher sustained viral response (SVR) rates. Therefore, identification of transmissions events in a timely manner remains as one of the most important issues in HCV control [6], and other viral hepatitis [7,8]. However, and despite improvements in molecular methodologies, HCV molecular epidemiology still faces important challenges. Here, we highlight the main issues hindering the implementation of HCV global molecular epidemiology. Identification of cases is essential for HCV control. Implementation of serologic and nucleic acid testing (NAT), followed by appropriate care and treatment, can reduce HCV transmission [9]. Testing of high-risk groups and birth cohorts is cost effective [10], and can prevent liver disease progression [11]. Thus, development of testing capabilities for identification of active and recent infection as well as facilitating access to care and treatment is critical for HCV control. HCV transmission networks are difficult to identify due to the silent onset of disease and the absence of methods capable to discern between acute and chronic infection [12,13]. The intricate patterns of HCV molecular evolution, including genetic bottlenecks [14,15], genetic drift [16,17], staged evolution and
∗ Corresponding author at: Tel.: +55 17 3221 2200x2779; fax: +55 17 3221 2200. E-mail address: [email protected] (L.M. Gonc¸alves Rossi). http://dx.doi.org/10.1016/j.jcv.2014.03.016 1386-6532/© 2014 Elsevier B.V. All rights reserved.
temporal variations [18], further complicate the recognition of transmission events. Characterization of the HCV intrahost population commonly relies on sequence information obtained from the hypervariable region 1 (HVR1) [19–21]. However, rapid sequence divergence significantly affects genetic relatedness between isolates associated with common sources of infection [12,22,23], resulting in loss of links over time. Re-infection and superinfection among drug users can also contribute to rapid sequence divergence. Moreover, phylogenetic analyses of the E1/E2 region not always faithfully reflect epidemiological relationships between isolates from serial transmissions [24]. Therefore, improved molecular methods should be implemented to overcome these limitations. The use of other HCV subgenomic regions, such as the NS5A [25,26], and ideally the entire viral genome, is likely to improve tracking of HCV transmission over time. Conventional methodologies for assessment of the intrahost HCV genetic variation are cumbersome, expensive and provide limited sequence information [27]. Next-generation sequencing (NGS) platforms and powerful statistical approaches have significantly improved molecular characterization, and facilitated the study of HCV transmissions, helping unveil the mechanisms involved in virus spread [21,28,29]. In addition, implementation of universal laboratory methods for the characterization of the intrahost HCV variability is required to facilitate the interchange of information among laboratories in different settings. Development of inexpensive molecular approaches capable to analyze large number of specimens is also needed for optimal global HCV molecular epidemiology. Adequate molecular surveillance strategies are necessary for the identification of HCV transmission networks. Different global strategies to monitor the circulation of HCV lineages have been
L.M. Gonc¸alves Rossi, P. Rahal / Journal of Clinical Virology 60 (2014) 174–176
suggested. HCV molecular characterization in general population using volunteers has been proposed for tracking of HCV transmissions [30]. However, the usefulness of this approach is significantly hampered by the prevalence of infection. Genotype distribution has also been used to monitor HCV infection among blood donors [31–33]. In this setting, recurrent blood donors offer a unique opportunity to identify acute cases associated with recent transmissions. Importantly, testing of blood donors should be accompanied by exhaustive epidemiological investigations aimed to identify all individuals involved in the transmission network. Molecular characterization of the HCV intrahost population in infected patients, starting or undergoing antiviral treatment, is an important source of information towards global HCV molecular surveillance. Limited HCV sequence divergence among treatment naïve patients is likely to facilitate the identification of clusters in relatively recent transmissions. However, untreated patients with long-term HCV infection who undergo rapid or intermediate viral evolution would be more difficult to link to their original source of infection. Conversely, experienced or relapsing HCV cases are intriguing sentinels for the identification of transmissions. In these patients, in addition to the selective immune pressure encountered during the natural course of infection, the viral population is also subjected to the selective force imposed by the antiviral therapy [34], which can distort genetic links. The dual treatment based on interferon and ribavirin affects the pattern of HCV molecular evolution [34,35]. Upon treatment, the selective pressure exerted by the antiviral drug prompts a continuous selection of variants resulting in the swapping of viral lineages during the course of therapy [34]. Moreover, the mutagenic effects of ribavirin on the HCV infecting population also contribute to the intrahost nucleotide variability in treatment experienced patients [36]. Development of drug escape variants during the course of therapy or among relapsers might also increase the genetic distance between founder variants and subsequent progeny, diluting genetic relatedness and hampering the accurate identification of transmission events. Thus, disruption of links due to modifications in the HCV molecular evolution upon treatment with different drugs imposes a challenge in genetic relatedness studies. Additionally, the rapidly evolving field of antiHCV therapy offers a plethora of novel drugs that are likely to modify the natural course of HCV intrahost molecular evolution. Therefore, assessing the impact of new anti-HCV agents in the genetic relatedness among cases linked to a common source is needed. The massive sequence information provided by different NGS represents a major challenge requiring exceptional computational capabilities. Implementation of novel strategies for data storing is also critical in the era of next generation sequencing. Therefore, the development of global databases and algorithms capable of rapidly screening thousands of entries is necessary to establish genetic relatedness among HCV cases. In addition, approaches for data sharing between laboratory networks are indispensable for global analysis of HCV transmissions. In summary, inclusion of blood collection centers and outpatient clinics as sentinel sites for surveillance programs is likely to aid in the identification of transmission networks. Characterization of the HCV inter and intrahost population, using multiple subgenomic regions, and ideally the whole HCV genome, through large-scale routine screening of blood donors, treatment naïve, non-responder and relapsers might significantly strengthen HCV molecular surveillance. Comprehensive HCV molecular studies might close the existing gaps in transmission networks due to missing links. Development of sequence databases and data sharing is also indispensable for enhanced HCV molecular surveillance. While the challenges faced by global molecular epidemiology are daunting and numerous, the reward is well worth the efforts. Unveiling the most intimate details involved in HCV transmission should facilitate the implementation of measures aimed to control disease.
175
1. Funding Not applicable. 2. Competing interests None to be declared. 3. Ethical approval Not required. References [1] Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 2013;57:1333–42. [2] Lavanchy D. The global burden of hepatitis C. Liver Int 2009;29(Suppl. 1):74–81. [3] Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012;380:2095–128. [4] Fauvelle C, Lepiller Q, Felmlee DJ, Fofana I, Habersetzer F, Stoll-Keller F, et al. Hepatitis C virus vaccines – progress and perspectives. Microb Pathog 2013;58:66–72. [5] Wendt A, Adhoute X, Castellani P, Oules V, Ansaldi C, Benali S, et al. Chronic hepatitis C: future treatment. Clin Pharmacol 2014;6:1–17. [6] Hellinger WC, Bacalis LP, Kay RS, Thompson ND, Xia GL, Lin Y, et al. Health care-associated hepatitis C virus infections attributed to narcotic diversion. Ann Intern Med 2012;156:477–82. [7] Jasuja S, Thompson ND, Peters PJ, Khudyakov YE, Patel MT, Linchangco P, et al. Investigation of hepatitis B virus and human immunodeficiency virus transmission among severely mentally ill residents at a long term care facility. PLoS ONE 2012;7:e43252. [8] Wheeler C, Vogt TM, Armstrong GL, Vaughan G, Weltman A, Nainan OV, et al. An outbreak of hepatitis A associated with green onions. New Engl J Med 2005;353:890–7. [9] Ward JW. Testing for HCV: the first step in preventing disease transmission and improving health outcomes for HCV-infected individuals. Antivir Ther 2012;17:1397–401. [10] Rein DB, Smith BD, Wittenborn JS, Lesesne SB, Wagner LD, Roblin DW, et al. The cost-effectiveness of birth-cohort screening for hepatitis C antibody in U.S. primary care settings. Ann Intern Med 2012;156:263–70. [11] Smith BD, Morgan RL, Beckett GA, Falck-Ytter Y, Holtzman D, Teo CG, et al. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945–1965. MMWR Recomm Rep 2012;61:1–32. [12] Cruz-Rivera M, Carpio-Pedroza JC, Escobar-Gutierrez A, Lozano D, VergaraCastaneda A, Rivera-Osorio P, et al. Rapid hepatitis C virus divergence among chronically infected individuals. J Clin Microbiol 2013;51:629–32. [13] Araujo AC. Antibody- and genome-based identification of recent HCV infection. Antivir Ther 2012;17:1459–64. [14] Wang GP, Sherrill-Mix SA, Chang KM, Quince C, Bushman FD, Hepatitis C. virus transmission bottlenecks analyzed by deep sequencing. J Virol 2010;84:6218–28. [15] Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST, Chopra A, et al. Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLoS Pathog 2011;7:e1002243. [16] Kao JH, Chen PJ, Lai MY, Wang TH, Chen DS. Quasispecies of hepatitis C virus and genetic drift of the hypervariable region in chronic type C hepatitis. J Infect Dis 1995;172:261–4. [17] Allain JP, Dong Y, Vandamme AM, Moulton V, Salemi M. Evolutionary rate and genetic drift of hepatitis C virus are not correlated with the host immune response: studies of infected donor–recipient clusters. J Virol 2000;74:2541–9. [18] Ramachandran S, Campo DS, Dimitrova ZE, Xia GL, Purdy MA, Khudyakov YE. Temporal variations in the hepatitis C virus intrahost population during chronic infection. J Virol 2011;85:6369–80. [19] Forbi JC, Campo DS, Purdy MA, Dimitrova ZE, Skums P, Xia GL, et al. Intra-host diversity and evolution of hepatitis C virus endemic to Cote d’Ivoire. J Med Virol 2014;86(May (5)):765–71. [20] Campo DS, Skums P, Dimitrova Z, Vaughan G, Forbi JC, Teo CG, et al. Drug-resistance of a viral population and its individual intra-host variants during the first 48 hours of therapy. Clin Pharmacol Ther 2014, http://dx.doi.org/10.1038/clpt.2014.20. PMID: 24488144 [Epub ahead of print]. [21] Escobar-Gutierrez A, Vazquez-Pichardo M, Cruz-Rivera M, Rivera-Osorio P, Carpio-Pedroza JC, Ruiz-Pacheco JA, et al. Identification of hepatitis C virus transmission using a next-generation sequencing approach. J Clin Microb 2012;50:1461–3. [22] Kurosaki M, Enomoto N, Marumo F, Sato C. Rapid sequence variation of the hypervariable region of hepatitis C virus during the course of chronic infection. Hepatology 1993;18:1293–9.
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L.M. Gonc¸alves Rossi, P. Rahal / Journal of Clinical Virology 60 (2014) 174–176
[23] Ray SC, Fanning L, Wang XH, Netski DM, Kenny-Walsh E, Thomas DL. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J Exp Med 2005;201:1753–9. [24] Casino C, McAllister J, Davidson F, Power J, Lawlor E, Yap PL, et al. Variation of hepatitis C virus following serial transmission: multiple mechanisms of diversification of the hypervariable region and evidence for convergent genome evolution. J Gen Virol 1999;80(Pt 3):717–25. [25] Rispeter K, Lu M, Behrens SE, Fumiko C, Yoshida T, Roggendorf M. Hepatitis C virus variability: sequence analysis of an isolate after 10 years of chronic infection. Virus Genes 2000;21:179–88. [26] Fan W, Zhu W, Wei L, Wang Q, Yin L, Du S, et al. Nonstructural 5A gene variability of hepatitis C virus (HCV) during a 10-year follow up. J Gastroenterol 2005;40:43–51. [27] Fonseca-Coronado S, Escobar-Gutierrez A, Ruiz-Tovar K, Cruz-Rivera MY, Rivera-Osorio P, Vazquez-Pichardo M, et al. Specific detection of naturally occurring hepatitis C virus mutants with resistance to telaprevir and boceprevir (protease inhibitors) among treatment-naive infected individuals. J Clin Microbiol 2012;50:281–7. [28] Gonzalez-Candelas F, Bracho MA, Wrobel B, Moya A. Molecular evolution in court: analysis of a large hepatitis C virus outbreak from an evolving source. BMC Biol 2013;11:76. [29] Cruz-Rivera M, Forbi JC, Yamasaki LH, Vazquez-Chacon CA, MartinezGuarneros A, Carpio-Pedroza JC, et al. Molecular epidemiology of viral
[30]
[31]
[32]
[33]
[34] [35]
[36]
diseases in the era of next generation sequencing. J Clin Virol 2013;57: 378–80. del Pino N, Oubina JR, Rodriguez-Frias F, Esteban JI, Buti M, Otero T, et al. Molecular epidemiology and putative origin of hepatitis C virus in random volunteers from Argentina. World J Gastroenterol 2013;19:5813–27. Oh DJ, Park YM, Seo YI, Lee JS, Lee JY. Prevalence of hepatitis C virus infections and distribution of hepatitis C virus genotypes among Korean blood donors. Ann Lab Med 2012;32:210–5. Mora MV, Romano CM, Gomes-Gouvea MS, Gutierrez MF, Carrilho FJ, Pinho JR. Molecular characterization, distribution, and dynamics of hepatitis C virus genotypes in blood donors in Colombia. J Med Virol 2010;82:1889–98. Cantaloube JF, Gallian P, Laperche S, Elghouzzi MH, Piquet Y, Bouchardeau F, et al. Molecular characterization of genotype 2 and 4 hepatitis C virus isolates in French blood donors. J Med Virol 2008;80:1732–9. Alfonso V, Mbayed VA, Sookoian S, Campos RH. Intra-host evolutionary dynamics of hepatitis C virus E2 in treated patients. J Gen Virol 2005;86:2781–6. Saludes V, Gonzalez-Candelas F, Planas R, Sola R, Ausina V, Martro E. Evolutionary dynamics of the E1-E2 viral populations during combination therapy in non-responder patients chronically infected with hepatitis C virus subtype 1b. Infect Genet Evol 2013;13:1–10. Dietz J, Schelhorn SE, Fitting D, Mihm U, Susser S, Welker MW, et al. Deep sequencing reveals mutagenic effects of ribavirin during monotherapy of hepatitis C virus genotype 1-infected patients. J Virol 2013;87:6172–81.