This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Boutrouille, A.
Right arrow Articles by Pavio, N.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Boutrouille, A.
Right arrow Articles by Pavio, N.

 Previous Article  |  Next Article 

Journal of Clinical Microbiology, June 2007, p. 2009-2010, Vol. 45, No. 6
0095-1137/07/$08.00+0     doi:10.1128/JCM.00235-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Prevalence of Anti-Hepatitis E Virus Antibodies in French Blood Donors{triangledown}

Annie Boutrouille, Labib Bakkali-Kassimi, Catherine Crucière, and Nicole Pavio*

UMR 1161 (INRA, AFSSA, ENVA), Ecole Nationale Vétérinaire d'Alfort, 7 avenue du Général de Gaulle, 94704 Maisons-Alfort Cedex, France

Received 30 January 2007/ Returned for modification 1 April 2007/ Accepted 16 April 2007


arrow
ABSTRACT
 
Accumulating evidence suggests that hepatitis E virus (HEV) infection is an emerging disease in regions where HEV is nonendemic. In France, the prevalence of anti-HEV antibodies in the general population has never been studied. Using blood donors' samples, we have found a prevalence of 3.20%, which is similar to that of other industrialized countries.


arrow
TEXT
 
Hepatitis E virus (HEV) is responsible for acute hepatitis in humans and associated with large waterborne epidemics in Asia and Africa, where it is endemic (3). To a lesser extent, HEV infection leads, in 1 to 2% of cases, to lethal fulminating hepatitis, and this level reaches 20% in pregnant women infected during their third term in areas of endemicity (8). In the industrialized countries of the United States, Europe, and Japan, HEV is responsible for sporadic cases, and genotyping combined with phylogenetic analysis has shown that the origin of these cases is mostly autochthonous, thus suggesting that the virus is present locally (1). In Europe (The Netherlands, the United Kingdom, Spain, Italy, and Sweden), the prevalence of anti-HEV antibodies ranges from 2.20 to 9.30% (2, 5, 6, 10). In France, the National Reference Centre reports 40 to 60 autochthonous cases every year, but the prevalence of HEV is not yet known. HEV serology or detection is not systematically performed in cases of acute hepatitis, even if HAV or HBV infection is ruled out. HEV is still considered an imported disease from regions of endemicity, and without a recent history of travel in these regions, a diagnosis of HEV infection is made only occasionally. In the southern part of France, acute hepatitis associated with HEV infection seems to be becoming more frequent than that due to HAV, suggesting that HEV is an emerging virus (7).

In contrast to regions of endemicity where the water vector has been well characterized, very little is known about the mode of transmission in regions where HEV is nonendemic. Unlike the other hepatitis viruses, HEV has animal reservoirs. Several lines of evidence, such as phylogenetic analysis and direct contamination through infected food products (wild boar or deer) (4, 9), have shown that animal-to-human transmission occurs and that HEV is in some cases a zoonotic virus. Among risk factors associated with hepatitis E, contact with swine seems to increase HEV prevalence. In the United States and Sweden, studies on HEV prevalence among swine handlers and veterinarian workers have shown higher prevalences in these populations (13% versus 9.3% for control subjects in Sweden) (5, 6).

To determine whether hepatitis E is a frequent disease in France and to establish a starting point for further studies on HEV epidemiology, HEV prevalence was estimated in the general population using sera from blood donors from two regions of France. The first region, Ile de France, is located near Paris, in an urban area, and the second one, Pays de Loire, is located in the west of France, in a rural area with many swine herds.

Sera from 998 blood donors from Ile de France and 1,000 sera from Pays de Loire were obtained from the Établissement Française du Sang. Information on sex, age, and travel to regions of HEV endemicity were provided.

Prevalence of anti-HEV antibodies (immunoglobulin G [IgG]) was determined by an HEV enzyme-linked immunosorbent assay (Genelabs Diagnostics, St. Ingbert, Germany). This technique had been validated by the French HEV National Reference Center. Every sample with an optical density (OD) value greater than the cutoff value was tested at least twice before it was considered positive. Among the 1,998 serum samples analyzed, a total of 64 were found to be positive for anti-HEV IgG (Table 1), corresponding to a prevalence of 3.20%. In a comparison of the prevalence in Ile de France (2.91%) with that of Pays de Loire (3.50%), no significant difference was observed (P = 0.45). The prevalence in female subjects was 3.27%, with 3.31% in Ile de France versus 3.21% in Pays de Loire. The prevalence in male subjects was similar to that in female subjects, at 3.14%, but a slightly higher prevalence was observed among males from Pays de Loire (3.72%) than in males from Ile de France (2.42%), suggesting that exposure to HEV might be more frequent in this region. No data on work activities of the donors were available, but it would be interesting to know whether some of them had occupations related to swineherds. Another possibility is that sanitation may play a more prominent role in urban than rural areas. None of the positive donors had a recent history of travel in regions of endemicity, but the possibility that they had traveled outside France a long time ago and been exposed to HEV cannot be excluded. Thus, it is not possible to conclude that HEV was acquired locally.


View this table:
[in this window]
[in a new window]

 
TABLE 1. Prevalence of anti-HEV IgG in blood donors from two areas in France

Hepatitis E is observed in young adults in regions of endemicity, but in industrialized countries, HEV seems to be more frequent in older adults. To characterize this epidemiological feature of HEV infection in France, the data of four age groups were analyzed: ≤24, 25 to 34, 35 to 44, and ≥45 years of age. Globally, HEV prevalence was higher (5.17%) in people who were ≥45 years of age, regardless of their geographical region of origin (4.60% in Ile de France and 5.42% in Pays de Loire) or gender (female, 5.11%; male, 5.22%) (Table 2). Thus, the probability of being exposed to HEV seems to increase with age. However, the possibility cannot be totally excluded that many years ago HEV infection was more prevalent than it is today and as a result the group of subjects who were ≥45 years of age had the highest prevalence. While prevalence was heterogeneous in the 35- to 44-year-old age group in the two regions (from 0 to 5.21%), the prevalence in female subjects was higher than that in males, without any particular epidemiological factor that could explain why females might be more frequently exposed than men. In the 25- to 34-year-old age group, some variability was also observed, with the highest prevalence found in male subjects from Pays de Loire (4.95%). Along the same line, male subjects from Pays de Loire may have occupations involving swine and, thus, might be more frequently exposed.


View this table:
[in this window]
[in a new window]

 
TABLE 2. Age-related prevalence of anti-HEV IgG in male and female blood donors from two areas in France

In young adults (≤24 years old) from the two regions, prevalences ranged between 1.49% and 3.06%. These low values underscore that HEV epidemiology in regions of nonendemicity is fundamentally different from that in regions of endemicity. Young women do not demonstrate any increased risk for HEV infection, thus limiting the risk of major liver failure during pregnancy.

In conclusion, these first data collected in France indicate that the HEV seroprevalence is similar to that of other European countries. These data constitute a starting point in HEV surveillance and will help to determine whether HEV is an emerging disease and needs increased attention. These data also underscore that both male and female subjects over 45 years of age have a higher risk of exposure to HEV. Women between 35 and 44 years of age are also more frequently exposed than men of the same age. An extended study on these populations with a detailed questionnaire may contribute to the identification of risk factors associated with HEV infection and the identification of transmission pathways in regions where HEV is nonendemic.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: UMR 1161, Ecole Nationale Vétérinaire d'Alfort, Bâtiment Bressou, 7 avenue du Général de Gaulle, 94704 Maisons-Alfort Cedex, France. Phone: 33 143 96 72 09. Fax: 33 143 96 73 96. E-mail: npavio{at}vet-alfort.fr Back

{triangledown} Published ahead of print on 25 April 2007. Back


arrow
REFERENCES
 
    1
  1. Banks, M., R. Bendall, S. Grierson, G. Heath, J. Mitchell, and H. Dalton. 2004. Human and porcine hepatitis E virus strains, United Kingdom. Emerg. Infect. Dis. 10:953-955.[Medline]
  2. 2
  3. Clemente-Casares, P., S. Pina, M. Buti, R. Jardi, M. MartIn, S. Bofill-Mas, and R. Girones. 2003. Hepatitis E virus epidemiology in industrialized countries. Emerg. Infect. Dis. 9:448-454.[Medline]
  4. 3
  5. Emerson, S. U., and R. H. Purcell. 2004. Running like water—the omnipresence of hepatitis E. N. Engl. J. Med. 351:2367-2368.[Free Full Text]
  6. 4
  7. Masuda, J., K. Yano, Y. Tamada, Y. Takii, M. Ito, K. Omagari, and S. Kohno. 2005. Acute hepatitis E of a man who consumed wild boar meat prior to the onset of illness in Nagasaki, Japan. Hepatol. Res. 31:178-183.[CrossRef][Medline]
  8. 5
  9. Meng, X. J., B. Wiseman, F. Elvinger, D. K. Guenette, T. E. Toth, R. E. Engle, S. U. Emerson, and R. H. Purcell. 2002. Prevalence of antibodies to hepatitis E virus in veterinarians working with swine and in normal blood donors in the United States and other countries. J. Clin. Microbiol. 40:117-122.[Abstract/Free Full Text]
  10. 6
  11. Olsen, B., D. Axelsson-Olsson, A. Thelin, and O. Weiland. 2006. Unexpected high prevalence of IgG-antibodies to hepatitis E virus in Swedish pig farmers and controls. Scand. J. Infect. Dis. 38:55-58.[CrossRef][Medline]
  12. 7
  13. Peron, J. M., J. M. Mansuy, H. Poirson, C. Bureau, E. Dupuis, L. Alric, J. Izopet, and J. P. Vinel. 2006. Hepatitis E is an autochthonous disease in industrialized countries. Analysis of 23 patients in South-West France over a 13-month period and comparison with hepatitis A. Gastroenterol. Clin. Biol. 30:757-762.
  14. 8
  15. Singh, S., A. Mohanty, Y. K. Joshi, D. Deka, S. Mohanty, and S. K. Panda. 2003. Mother-to-child transmission of hepatitis E virus infection. Indian J. Pediatr. 70:37-39.[Medline]
  16. 9
  17. Tei, S., N. Kitajima, K. Takahashi, and S. Mishiro. 2003. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362:371-373.[CrossRef][Medline]
  18. 10
  19. Widdowson, M. A., W. J. Jaspers, W. H. van der Poel, F. Verschoor, A. M. de Roda Husman, H. L. Winter, H. L. Zaaijer, and M. Koopmans. 2003. Cluster of cases of acute hepatitis associated with hepatitis E virus infection acquired in the Netherlands. Clin. Infect. Dis. 36:29-33.[CrossRef][Medline]


Journal of Clinical Microbiology, June 2007, p. 2009-2010, Vol. 45, No. 6
0095-1137/07/$08.00+0     doi:10.1128/JCM.00235-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.




This article has been cited by other articles:

  • Galiana, C., Fernandez-Barredo, S., Garcia, A., Gomez, M. T., Perez-Gracia, M. T. (2008). Occupational Exposure to Hepatitis E Virus (HEV) in Swine Workers. Am J Trop Med Hyg 78: 1012-1015 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Boutrouille, A.
Right arrow Articles by Pavio, N.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Boutrouille, A.
Right arrow Articles by Pavio, N.