Volume 17, Number 11—November 2011
CME ACTIVITY
Close Similarity between Sequences of Hepatitis E Virus Recovered from Humans and Swine, France, 2008−2009
Jérôme Bouquet, Sophie Tessé, Aurélie Lunazzi, Marc Eloit, Nicolas Rose, Elisabeth Nicand, and Nicole Pavio
Suggested citation for this article Abstract
Frequent zoonotic transmission of hepatitis E virus (HEV) has been suspected, but data supporting the animal origin of autochthonous cases are still sparse. We assessed the genetic identity of HEV strains found in humans and swine during an 18-month period in France. HEV sequences identified in patients with autochthonous hepatitis E infection (n = 106) were compared with sequences amplified from swine livers collected in slaughterhouses (n = 43). Phylogenetic analysis showed the same proportions of subtypes 3f (73.8%), 3c (13.4%), and 3e (4.7%) in human and swine populations. Furthermore, similarity of >99% was found between HEV sequences of human and swine origins. These results indicate that consumption of some pork products, such as raw liver, is a major source of exposure for autochthonous HEV infection.Hepatitis E virus (HEV) is a causative agent of enterically transmitted acute hepatitis in humans (1). It is a major public health issue in developing countries, where it causes large waterborne epidemics (2). In industrialized countries, it is an emerging problem, as an increasing number of sporadic cases for which the origins are still unclear (3) have been reported for patients who have not traveled to HEV-endemic areas.
HEV is a nonenveloped virus with a single-stranded positive RNA genome of 7.2 kb composed of 3 open reading frames (ORFs). HEV is the sole member of the family Hepeviridae (4) and has been classified into 4 major genotypes and 24 subtypes. Genotype 1 is divided into 5 subtypes (1a to 1e), genotype 2 into 2 subtypes (2a and 2b), genotype 3 into 10 subtypes (3a to 3j), and genotype 4 into 7 subtypes (4a to 4g) (5). Although genotypes 1 and 2 are endemic to developing countries, genotypes 3 and 4 are the cause of sporadic cases. HEV is the only hepatitis virus that is also found in a wide variety of animals (6). Genotype 3 can infect humans as well as swine, wild boar, deer, and mongoose (7–10). It is generally agreed that swine are widely infected all over the world (6). HEV seroprevalence varies greatly depending on countries; 22.7% to 88.4% of pigs are seropositive at 6 months of age (11,12). Among pigs slaughtered at ≈25 weeks of age, the prevalence of HEV fecal excretion ranges from 4% to 41% (13,14). Viral RNA sequences from pigs and humans can be closely related (15,16), and cross-species infection of genotypes 3 and 4 from human to pig and pig to nonhuman primate has been demonstrated experimentally (17). To date, only 2 cases of zoonotic transmission from consumption of raw or undercooked sika deer and wild boar meat have been clearly identified in Japan with near or 100% homology between the sequences from the patient and the consumed meat (7,8).
A few reports have shown close phylogenetic relationships between sequences identified in swine and in humans. However, these studies were based on limited numbers of sequences with little geographic or temporal data (18–21).
In France, HEV seroprevalence in the human population ranges from 3.2% to 16.6%, depending on the geographic regions studied (22,23). The number of reported viral hepatitis E cases is increasing. Although only 38 cases were reported in 2006, a total of 340 cases were diagnosed in 2010, of which 70% were declared autochthonous with no recent history of patients traveling abroad (French National Reference Laboratory, unpub. data). In the swine reservoir, a recent nationwide survey performed at slaughterhouses showed high prevalence of HEV. HEV seroprevalence in swine ranges from 31% at the individual level to 65% at the farm level. In that study, HEV prevalence in pig liver was estimated at 4%, meaning that HEV-infected pig livers can enter the food chain (24). Moreover, it has been shown that regional products made from raw pig liver may contain HEV (25). In France, pork is the most widely eaten type of meat (26) and could represent an HEV reservoir with a high risk for zoonotic transmission.
To assess the zoonotic risk for transmission from swine to humans in France, we studied HEV sequences in both hosts. HEV sequences collected from every human autochthonous case of hepatitis E infection and HEV-positive pig livers collected at slaughterhouses, both within 18 months, were analyzed. Epidemiologic and spatial–temporal data corresponding to phylogenetic analyses of partial ORF2 sequences were used to investigate whether swine are a major source of HEV contamination in France.
HEV is a nonenveloped virus with a single-stranded positive RNA genome of 7.2 kb composed of 3 open reading frames (ORFs). HEV is the sole member of the family Hepeviridae (4) and has been classified into 4 major genotypes and 24 subtypes. Genotype 1 is divided into 5 subtypes (1a to 1e), genotype 2 into 2 subtypes (2a and 2b), genotype 3 into 10 subtypes (3a to 3j), and genotype 4 into 7 subtypes (4a to 4g) (5). Although genotypes 1 and 2 are endemic to developing countries, genotypes 3 and 4 are the cause of sporadic cases. HEV is the only hepatitis virus that is also found in a wide variety of animals (6). Genotype 3 can infect humans as well as swine, wild boar, deer, and mongoose (7–10). It is generally agreed that swine are widely infected all over the world (6). HEV seroprevalence varies greatly depending on countries; 22.7% to 88.4% of pigs are seropositive at 6 months of age (11,12). Among pigs slaughtered at ≈25 weeks of age, the prevalence of HEV fecal excretion ranges from 4% to 41% (13,14). Viral RNA sequences from pigs and humans can be closely related (15,16), and cross-species infection of genotypes 3 and 4 from human to pig and pig to nonhuman primate has been demonstrated experimentally (17). To date, only 2 cases of zoonotic transmission from consumption of raw or undercooked sika deer and wild boar meat have been clearly identified in Japan with near or 100% homology between the sequences from the patient and the consumed meat (7,8).
A few reports have shown close phylogenetic relationships between sequences identified in swine and in humans. However, these studies were based on limited numbers of sequences with little geographic or temporal data (18–21).
In France, HEV seroprevalence in the human population ranges from 3.2% to 16.6%, depending on the geographic regions studied (22,23). The number of reported viral hepatitis E cases is increasing. Although only 38 cases were reported in 2006, a total of 340 cases were diagnosed in 2010, of which 70% were declared autochthonous with no recent history of patients traveling abroad (French National Reference Laboratory, unpub. data). In the swine reservoir, a recent nationwide survey performed at slaughterhouses showed high prevalence of HEV. HEV seroprevalence in swine ranges from 31% at the individual level to 65% at the farm level. In that study, HEV prevalence in pig liver was estimated at 4%, meaning that HEV-infected pig livers can enter the food chain (24). Moreover, it has been shown that regional products made from raw pig liver may contain HEV (25). In France, pork is the most widely eaten type of meat (26) and could represent an HEV reservoir with a high risk for zoonotic transmission.
To assess the zoonotic risk for transmission from swine to humans in France, we studied HEV sequences in both hosts. HEV sequences collected from every human autochthonous case of hepatitis E infection and HEV-positive pig livers collected at slaughterhouses, both within 18 months, were analyzed. Epidemiologic and spatial–temporal data corresponding to phylogenetic analyses of partial ORF2 sequences were used to investigate whether swine are a major source of HEV contamination in France.
Close Similarity between Sequences of Hepatitis E Virus Recovered from Humans and Swine, France, 2008−2009 - Vol. 17 No. 11 - November 2011 - Emerging Infectious Disease journal - CDC
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