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Volume 16, Number 11—November 2010

Hepatitis E Virus Infection in Sheltered Homeless Persons, France

Mamadou Kaba, Philippe Brouqui, Hervé Richet, Sekené Badiaga, Pierre Gallian, Didier Raoult, and Philippe ColsonComments to Author 
Author affiliations: Centre Hospitalo–Universitaire Timone, Marseille, France (M. Kaba, P. Colson); Université de la Méditerranée, Marseille (M. Kaba, P. Brouqui, H. Richet, S. Badiaga, D. Raoult, P. Colson); Hôpital Nord, Marseille (P. Brouqui, S. Badiaga); d Etablissement Français du Sang Alpes-Méditerranée, Marseille (P. Gallian)

Cite This Article


To determine the prevalence of hepatitis E virus (HEV) infection among sheltered homeless persons in Marseille, France, we retrospectively tested 490 such persons. A total of 11.6% had immunoglobulin (Ig) G and 2.5% had IgM against HEV; 1 person had HEV genotype 3f. Injection drug use was associated with IgG against HEV.

Initially considered a leading cause of acute hepatitis in tropical and subtropical countries, hepatitis E virus (HEV) is endemic to industrialized countries (1). Although substantial data indicate that HEV infection is a porcine zoonosis, more information is needed about the epidemiology and transmission of this virus in industrialized countries (13). Homeless persons are at higher risk than other persons for viral hepatitis (A, B, and C) because their lifestyle might include injection drug use (IDU) and poor hygiene (4), but data on HEV prevalence among them are scarce (5,6). In Marseille in southeastern France, ≈1,500 persons are homeless (4). Since 2000, shelter-based surveys have been conducted yearly to monitor infectious diseases in homeless persons (4). This work determined the prevalence of HEV infection in this population.

The Study

The surveys were reviewed and approved by the Institutional Review Board (CCPPCRB99/76) (Comité de Protection des Personnes Sud-Méditerranée II; and the Ethics Committee of the Medical School, University of the Mediterranean, Marseille). Participating homeless persons were examined by a physician and interviewed by using a standardized questionnaire, and serum samples were collected from each participant for laboratory testing. Epidemiologic, clinical, and biologic data that were collected varied from 1 year to another.

Serum samples collected from 490 homeless persons in 2003, 2005, and 2006 in 2 shelters in Marseille (Appendix Table) were tested retrospectively for immunoglobulin (Ig) G and IgM (EIAgen HEV kits; Adaltis Italia SpA, Rome, Italy) against HEV and for HEV RNA by using an in-house real-time reverse transcription–PCR specific for open reading frame 2 (7). HEV RNA sequencing was performed when HEV RNA was detected, and genotype was assigned through phylogenetic analysis of open reading frame 2 partial sequences (7). Serologic testing for hepatitis A, B, and C and for HIV were performed by using Axsym Abbott assays (Abbott Diagnostics Division, Wiesbaden, Germany). Statistical analysis was performed by using STATA version 10.1 software (StataCorp, College Station, TX, USA). Pearson χ2 test, Fisher exact test, Kruskal-Wallis test, or logistic regression model were used when appropriate.

Mean ± SD age of homeless persons was 43 ± 14 years, and their mean ± SD duration of homelessness was 49 ± 84 months. Most (96.3%) were men and were born in North Africa (40.2%) or in France (33.3%) (Appendix Table). Previous or ongoing IDU was reported for 4/176 (2.3%). Overall prevalence of anti-HEV IgG and IgM was 11.6% (95% confidence interval [CI] 8.9%–14.8%) (57/490) and 2.5% (95% CI 1.3%–4.2%) (12/490), respectively. Mean optical density ratio (optical density/cutoff value) was 3.0 (range 1.1–6.9) and 2.0 (range 1.1–4.6) for IgG and IgM, respectively. Three (0.6%; 95% CI 0.1%–1.8%) homeless persons were concurrently positive for HEV IgM and IgG, whereas 9 (1.8%; 95% CI 0.8%–3.5%) were positive only for IgM and 54 (11%; 95% CI 8.4%–14.1%) were positive only for IgG.


Thumbnail of Phylogenetic tree based on partial nucleotide sequences (275 bp) corresponding to the 5′-end open reading frame 2 region of the hepatitis E virus (HEV) genome. Phylogenetic analysis included HEV sequence recovered in the present study (black circle, boldface and underlined; GenBank accession no. FJ71877) and sequences corresponding to the HEV sequences hits with the highest BLASTn score ( to this sequence (black triangles), previously recovered in our l

Figure. Phylogenetic tree based on partial nucleotide sequences (275 bp) corresponding to the 5′-end open reading frame 2 region of the hepatitis E virus (HEV) genome. Phylogenetic analysis included HEV sequence recovered...

HEV RNA was detected in 1 homeless person, a 50-year-old man from Romania concurrently seronegative for HEV IgM and IgG and for hepatitis B and C viruses. He reported excessive alcohol intake but no IDU. HEV genotype was 3f (Figure), and sequence analysis showed 98% nt identity with sequences previously recovered from persons in Spain and France. Alanine aminotransferase (ALT) level had been assessed in only 2/12 HEV IgM–positive homeless persons and was elevated in 1 person (177 IU/L), in association with an increased γ-glutamyl transferase level (788 IU/L). Among the 19 homeless persons sampled in 2 different years, 1 seroconverted; he was seronegative for HEV IgM and IgG in 2005 then positive in 2006 (optical density ratio 1.14 and 4.3, respectively). Results of HEV RNA testing were negative in both serum samples, and ALT level had not been tested.

The prevalence of HEV IgG or IgM in homeless persons did not differ by year of survey; sex; place of birth; or serologic status for hepatitis A, B, or C viruses (Appendix Table). In addition, mean age, duration of homelessness, and ALT, aspartate aminotransferase, and γ-glutamyl transferase levels did not differ among homeless persons who were positive or negative for HEV antibodies (Table). In the univariate analysis, previous or ongoing IDU (3/4 vs. 19/172; p = 0.006), HIV seropositivity (2/3 vs. 16/183; p = 0.03), and having scabies (6/20 vs. 48/462; p = 0.02) were significantly associated with HEV IgG. In multivariate analysis that used variables that were statistically significant in the univariate analysis as covariates, only IDU was independently associated with anti-HEV IgG (adjusted odds ratio 26.3, 95% CI 2.5–267.1; p = 0.006).


We found that 11.6% (95% CI 8.9%–14.8%) of homeless persons in Marseille were positive for HEV IgG, whereas 2.6% (95% CI 1.3%–4.2%) had HEV IgM or HEV RNA, indicating recent or ongoing HEV infection. The HEV IgG prevalence is similar to that previously found (6) in homeless persons in Los Angeles, California, USA (13.5%), and much lower than that found in 98 homeless children in Cochabamba, Bolivia (66.3%) (5). This prevalence falls between seroprevalences recently assessed among blood donors in northern (3.2%) and southwestern (16.6%) France (8,9).

These comparisons should take into account the use of different serologic assays, in addition to differences in epidemiologic settings. Indeed, substantial differences have been observed regarding the performances of some HEV IgG tests (10). Moreover, the sensitivity and specificity of the HEV IgG assay used in our study have not been previously evaluated, which warrants a cautious interpretation of the results. A preliminary study conducted in 2008 of 194 blood donors in Marseille with the same assay as that used in the present study found that the prevalence of HEV IgG was 9% (P. Gallian, unpub. data), which is similar to the seroprevalence we found in homeless persons. The HEV IgM assay we used showed good performance in patients with HEV genotype 3 infections in reference to PCR testing (11). Thus, sensitivity, specificity, and negative predictive value were 90%, 100%, and 98.8%, respectively. In addition, sensitivities and specificities of this test and of the HEV IgM ELISA 3.0 (MP Diagnostics, Singapore) did not differ significantly.

Although based on a small subset of homeless persons, our finding of the association of IDU with serologic results indicating past HEV infection is intriguing. This result is surprising because the proportion of IDUs in our homeless population was low (2.3%) and much lower than proportions previously reported (9%–83% (1215). HEV IgG prevalence of 2.2%–62% has been described in IDUs, but a significant difference with the control group was found in only 2 of these studies (1215). HEV IgG prevalence in Sweden was 62% (21/34) in patients who acquired acute hepatitis B through IDU compared with 25% (9/36) in patients with sexually acquired hepatitis B (p<0.005) (13). Moreover, in Italy, the prevalence was 5.4% (16/179) in IDUs compared with 2.6% (49/1,889) in the general population (p<0.00001) (12). In summary, our data indicate that HEV infection occurs in homeless persons, and further studies are needed to determine whether IDU is responsible for HEV transmission.

Dr Kaba works at Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, Facultés de Médecine et de Pharmacie, Université de la Méditerranée, and at the Pôle des Maladies Infectieuses et Tropicales Clinique et Biologique, Fédération de Bactériologie-Hygiène-Virologie, Centre Hospitalo-Universitaire Timone, in Marseille, France. His primary field of interest is viral hepatitis.



This study was supported by the Conseil General des Bouches-du-Rhône (Conseil General 13), France, and the Programme Hospitalier de Recherche Clinique, Marseille, France.



  1. Dalton  HR, Bendall  R, Ijaz  S, Banks  M. Hepatitis E: an emerging infection in developed countries. Lancet Infect Dis. 2008;8:698709. DOIPubMedGoogle Scholar
  2. Lu  L, Li  C, Hagedorn  CH. Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol. 2006;16:536. DOIPubMedGoogle Scholar
  3. Teo  CG. Hepatitis E indigenous to economically developed countries: to what extent a zoonosis? Curr Opin Infect Dis. 2006;19:4606. DOIPubMedGoogle Scholar
  4. Badiaga  S, Raoult  D, Brouqui  P. Preventing and controlling emerging and reemerging transmissible diseases in the homeless. Emerg Infect Dis. 2008;14:13539. DOIPubMedGoogle Scholar
  5. Leon  P, Venegas  E, Bengoechea  L, Rojas  E, Lopez  JA, Elola  C, Prevalence of infections by hepatitis B, C, D and E viruses in Bolivia. Rev Panam Salud Publica. 1999;5:14451. DOIPubMedGoogle Scholar
  6. Smith  HM, Reporter  R, Rood  MP, Linscott  AJ, Mascola  LM, Hogrefe  W, Prevalence study of antibody to ratborne pathogens and other agents among patients using a free clinic in downtown Los Angeles. J Infect Dis. 2002;186:16736. DOIPubMedGoogle Scholar
  7. Kaba  M, Davoust  B, Marie  JL, Barthet  M, Henry  M, Tamalet  C, Frequent transmission of hepatitis E virus among piglets in farms in Southern France. J Med Virol. 2009;81:17509. DOIPubMedGoogle Scholar
  8. Boutrouille  A, Bakkali-Kassimi  L, Cruciere  C, Pavio  N. Prevalence of anti-hepatitis E virus antibodies in French blood donors. J Clin Microbiol. 2007;45:200910. DOIPubMedGoogle Scholar
  9. Mansuy  JM, Legrand-Abravanel  F, Calot  JP, Peron  JM, Alric  L, Agudo  S, High prevalence of anti-hepatitis E virus antibodies in blood donors from South West France. J Med Virol. 2008;80:28993. DOIPubMedGoogle Scholar
  10. Bendall  R, Ellis  V, Ijaz  S, Ali  R, Dalton  H. A comparison of two commercially available anti-HEV IgG kits and a re-evaluation of anti-HEV IgG seroprevalence data in developed countries. J Med Virol. 2010;82:799805. DOIPubMedGoogle Scholar
  11. Legrand-Abravanel  F, Thevenet  I, Mansuy  JM, Saune  K, Vischi  F, Peron  JM, Good performance of immunoglobulin M assays in diagnosing genotype 3 hepatitis E virus infections. Clin Vaccine Immunol. 2009;16:7724. DOIPubMedGoogle Scholar
  12. Gessoni  G, Manoni  F. Hepatitis E virus infection in north-east Italy: serological study in the open population and groups at risk. J Viral Hepat. 1996;3:197202. DOIPubMedGoogle Scholar
  13. Sylvan  SP. The high rate of antibodies to hepatitis E virus in young, intravenous drug-abusers with acute hepatitis B virus infection in a Swedish community: a study of hepatitis markers in individuals with intravenously or sexually acquired hepatitis B-virus infection. Scand J Infect Dis. 1998;30:42930.PubMedGoogle Scholar
  14. Christensen  PB, Engle  RE, Jacobsen  SE, Krarup  HB, Georgsen  J, Purcell  RH. High prevalence of hepatitis E antibodies among Danish prisoners and drug users. J Med Virol. 2002;66:4955. DOIPubMedGoogle Scholar
  15. Thomas  DL, Yarbough  PO, Vlahov  D, Tsarev  SA, Nelson  KE, Saah  AJ, Seroreactivity to hepatitis E virus in areas where the disease is not endemic. J Clin Microbiol. 1997;35:12447.PubMedGoogle Scholar




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DOI: 10.3201/eid1611.091890

Table of Contents – Volume 16, Number 11—November 2010

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Please use the form below to submit correspondence to the authors or contact them at the following address:

Philippe Colson, Pôle des Maladies Infectieuses et Tropicales Cliniques et Biologiques, Fédération de Bactériologie-Hygiène-Virologie, Centre Hospitalo-Universitaire Timone, 264 rue Saint-Pierre, 13385 Marseille CEDEX 05, France

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