The Global Spread of Hepatitis C Virus 1a and 1b: A Phylodynamic and Phylogeographic Analysis

Magiorkinis, Gkikas; Magiorkinis, Emmanouil; Paraskevis, Dimitrios; Ho, Simon Y. W.; Shapiro, Beth; Pybus, Oliver G.; Allain, Jean‐Pierre; Hatzakis, Angelos

doi:10.1371/journal.pmed.1000198

Cited by 191 publications

(216 citation statements)

References 54 publications

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“…Previous studies have estimated the tMRCA for subtype 1a in other parts of the world, using limited segments of the genome. For instance, a previous global evolutionary analysis of subtype 1a, using the NS5B region of sequences obtained from 21 countries, placed the tMRCA at a similar time point and with a Bayesian skyline plot showing a similar pattern to that reported here for North America [1]. However, this study included a disproportionate number of North American sequences (399 vs 443 sequences from 20 other countries combined).…”

Section: Discussionsupporting

confidence: 59%

“…Hepatitis C is a chronic viral infection predominantly spread via blood-to-blood contamination during injecting drug use, with outbreaks also attributed to nonsterile medical practices, unscreened blood transfusions and sexual transmission among men who have sex with men [1][2][3][4][5]. The hepatitis C virus (HCV) genera are divided into 7 genotypes and 67 subtypes [6].…”

mentioning

confidence: 99%

“…Viral sequences and phylogenetic analysis have been used previously to infer evolutionary dynamics of Ebola and human immunodeficiency virus (HIV), as well as HCV epidemics [1,8]. Because these RNA viruses feature high mutation rates, the evolutionary and epidemiological time scales are similar.…”

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confidence: 99%

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Historical Trends in the Hepatitis C Virus Epidemics in North America and Australia

Rodrigo¹,

Eltahla²,

Bull³

et al. 2016

J Infect Dis.

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Background. Bayesian evolutionary analysis (coalescent analysis) based on genetic sequences has been used to describe the origins and spread of rapidly mutating RNA viruses, such as influenza, Ebola, human immunodeficiency virus (HIV), and hepatitis C virus (HCV).Methods. Full-length subtype 1a and 3a sequences from early HCV infections from the International Collaborative of Incident HIV and Hepatitis C in Injecting Cohorts (InC3), as well as from public databases from a time window of 1977-2012, were used in a coalescent analysis with BEAST software to estimate the origin and progression of the HCV epidemics in Australia and North America. Convergent temporal trends were sought via independent epidemiological modeling.Results. The epidemic of subtype 3a had more recent origins (around 1950) than subtype 1a (around 1920) in both continents. In both modeling approaches and in both continents, the epidemics underwent exponential growth between 1955 and 1975, which then stabilized in the late 20th century.Conclusions. Historical events that fuelled the emergence and spread of injecting drug use, such as the advent of intravenous medical therapies and devices, and growth in the heroin trade, as well as population mixing during armed conflicts, were likely drivers for the cross-continental spread of the HCV epidemics.

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Section: Discussionsupporting

confidence: 59%

mentioning

confidence: 99%

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Historical Trends in the Hepatitis C Virus Epidemics in North America and Australia

Rodrigo¹,

Eltahla²,

Bull³

et al. 2016

J Infect Dis.

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“…However, the present analysis provides tighter CIs than those reported previously for subtype 1b using two subgenomic regions (1905-1965 and 1806-1959; [12]), reflecting the increased information gained from using whole-genome reference sequences and from the inclusion of the two 1953 sequences. While direct amplification of viral genomes from archived biological samples may prove challenging using long-range PCR approaches, owing to nucleic acid degradation, modern high-throughput sequencing technologies may alleviate such difficulties, as they have done in the field of ancient DNA research [31].…”

Section: Discussioncontrasting

confidence: 49%

“…Phylogenetic analyses have suggested that the direction of spread was mainly from developed countries to the developing world, with the USA as a likely source location [12]. It is hypothesized that the global dispersal of subtypes 1a and 1b occurred in two steps, starting with widespread export of the virus from the USA to the rest of the world around 1940-1950, followed by local expansion of the exported lineages [12]. The initial step coincided with the international transportation of dried plasma units, a massive operation that involved the pooling and shipping of at least 10 million independent donations to sites of military operations over 5-10 years [13].…”

Section: Discussionmentioning

confidence: 99%

Evolutionary analysis of hepatitis C virus gene sequences from 1953

Gray

Tanaka

Takebe

et al. 2013

Phil. Trans. R. Soc. B

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Reconstructing the transmission history of infectious diseases in the absence of medical or epidemiological records often relies on the evolutionary analysis of pathogen genetic sequences. The precision of evolutionary estimates of epidemic history can be increased by the inclusion of sequences derived from ‘archived’ samples that are genetically distinct from contemporary strains. Historical sequences are especially valuable for viral pathogens that circulated for many years before being formally identified, including HIV and the hepatitis C virus (HCV). However, surprisingly few HCV isolates sampled before discovery of the virus in 1989 are currently available. Here, we report and analyse two HCV subgenomic sequences obtained from infected individuals in 1953, which represent the oldest genetic evidence of HCV infection. The pairwise genetic diversity between the two sequences indicates a substantial period of HCV transmission prior to the 1950s, and their inclusion in evolutionary analyses provides new estimates of the common ancestor of HCV in the USA. To explore and validate the evolutionary information provided by these sequences, we used a new phylogenetic molecular clock method to estimate the date of sampling of the archived strains, plus the dates of four more contemporary reference genomes. Despite the short fragments available, we conclude that the archived sequences are consistent with a proposed sampling date of 1953, although statistical uncertainty is large. Our cross-validation analyses suggest that the bias and low statistical power observed here likely arise from a combination of high evolutionary rate heterogeneity and an unstructured, star-like phylogeny. We expect that attempts to date other historical viruses under similar circumstances will meet similar problems.

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Global distribution and prevalence of hepatitis C virus genotypes

et al. 2014

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Hepatitis C virus (HCV) exhibits high genetic diversity, characterized by regional variations in genotype prevalence. This poses a challenge to the improved development of vaccines and pan-genotypic treatments, which require the consideration of global trends in HCV genotype prevalence. Here we provide the first comprehensive survey of these trends. To approximate national HCV genotype prevalence, studies published between 1989 and 2013 reporting HCV genotypes are reviewed and combined with overall HCV prevalence estimates from the Global Burden of Disease (GBD) project. We also generate regional and global genotype prevalence estimates, inferring data for countries lacking genotype information. We include 1,217 studies in our analysis, representing 117 countries and 90% of the global population. We calculate that HCV genotype 1 is the most prevalent worldwide, comprising 83.4 million cases (46.2% of all HCV cases), approximately one-third of which are in East Asia. Genotype 3 is the next most prevalent globally (54.3 million, 30.1%); genotypes 2, 4, and 6 are responsible for a total 22.8% of all cases; genotype 5 comprises the remaining <1%. While genotypes 1 and 3 dominate in most countries irrespective of economic status, the largest proportions of genotypes 4 and 5 are in lower-income countries. Conclusion: Although genotype 1 is most common worldwide, nongenotype 1 HCV cases—which are less well served by advances in vaccine and drug development—still comprise over half of all HCV cases. Relative genotype proportions are needed to inform healthcare models, which must be geographically tailored to specific countries or regions in order to improve access to new treatments. Genotype surveillance data are needed from many countries to improve estimates of unmet need. (Hepatology 2015;61:77–87)

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The Global Spread of Hepatitis C Virus 1a and 1b: A Phylodynamic and Phylogeographic Analysis

Abstract: Using phylodynamic and phylogeographic methods, Angelos Hatzakis and colleagues find that the global spread of Hepatitis C virus coincided with widespread use of transfused blood and with the expansion of intravenous drug use.

Cited by 191 publications

References 54 publications

Historical Trends in the Hepatitis C Virus Epidemics in North America and Australia

Historical Trends in the Hepatitis C Virus Epidemics in North America and Australia

Evolutionary analysis of hepatitis C virus gene sequences from 1953

Global distribution and prevalence of hepatitis C virus genotypes

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