Assessment of the risk of foodborne transmission and burden of hepatitis E in Switzerland

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Highlights

  • The prevalence of HEV RNA detection in Swiss pig livers at slaughter is 1.3% (95% CI 0.3%; 4.4%).

  • The annual number of human hepatitis E cases due to high risk products was estimated as 176 (95% CI 64; 498).

  • The total burden due to Hepatitis E in the canton Ticino was > 50 DALY per 100,000 inhabitants in 2015.

Abstract

The objective of this study was i) to quantify the risk of hepatitis E for Swiss consumers by specified pork products and ii) to estimate the total burden of human food-borne hepatitis E in Switzerland. A quantitative risk assessment from slaughter to consumption was carried out according to the Codex Alimentarius framework. In the hazard characterization, assumptions were made due to the lack of a dose-response relationship for oral exposure to hepatitis E virus (HEV). The prevalence of HEV in 160 pig livers of 40 different Swiss fattening farms was examined and determined to be 1.3% (CI 0.3%; 4.4%). This result was used as input in the risk assessment model, together with data from other published studies. The annual burden of hepatitis E was estimated in terms of Disability Adjusted Life Years (DALY), using data about hepatitis E cases diagnosed between 2010 and 2015 at two major hospitals located in the canton Ticino. Only the risk of foodborne hepatitis E from products containing pork liver was evaluated, as those containing only pork meat could not be evaluated because of lack of data on HEV load in pork. Assuming that successful oral infection occurs in 1% of servings contaminated with high HEV loads (> 105 genome copies), and that acute illness develops in 5% of susceptible consumers, the most likely annual number of foodborne hepatitis E cases in Switzerland was estimated to be 1481 (95% CI 552; 4488) if all products containing pork liver were considered. If only high-risk products, such as plain pork liver and liver sausages (e.g. Saucisse au Foie), were considered, the annual number of cases was estimated to be 176 (95% CI 64; 498). We were unable to calculate the total burden of hepatitis E in Switzerland due to lack of data. Yet, for the canton Ticino, it was shown that a significant increase had occurred from < 5 DALY per 100,000 inhabitants before 2012 to > 50 DALY per 100,000 inhabitants in 2015. This change could partly be due to an increased reporting and higher awareness among medical practitioners. Extrapolation to other regions could be accomplished if detailed information on food consumption patterns were available. Notification of HEV cases and attempts of cases source attribution would improve the basis for risk assessments.

Introduction

Hepatitis E virus (HEV) is a relatively recently discovered hepatotropic virus (Reyes et al., 1991). To date, four genotypes (GT) affecting humans have been identified; GT3, and to a lesser extent GT4 represent the most common genotypes found in industrialized countries (Dalton et al., 2013). The clinical presentation is indistinguishable from Hepatitis A with classical symptoms including jaundice, anorexia, abdominal pain accompanied by fever, nausea and vomiting (Emerson and Purcell, 2003). Hepatitis E is usually self-limiting, but chronic infections have been described in immune-depressed patients (Bihl and Negro, 2009) and organ transplant recipients (Arends et al., 2014, Kamar et al., 2012). Fulminant and fatal HEV GT3 cases have also been reported in Europe and Japan, often in older males with underlying chronic liver diseases (Lewis et al., 2010). In pregnant women, the proportion of fulminant cases were only described for GT1 strains circulating predominantly in developing countries (Smith, 2001).

While Hepatitis E was originally considered to be endemic only in areas of Asia, Africa and Mexico (WHO, 2010), sporadic cases were recently observed in developed countries, including Europe. These were initially considered to be imported, however, enhanced Hepatitis E surveillance has detected an increasing number of non-travel associated infections (Dalton et al., 2008), e.g. in France (Nicand et al., 2009), in the United Kingdom (Ijaz et al., 2014) and in Germany (Robert Koch Institut, 2015). The exact transmission routes for autochthonous HEV cases remain unknown, but foodborne transmission was identified as an emerging concern (EFSA, 2011). Contaminated products mostly include pork products (e.g. pork pies, under-cooked or raw pork meat and liver pate), but also deer meat, wild boar meat, offal, shellfish and some ethnic foods are described (Lewis et al., 2010). Few outbreak investigations have been performed so far. Some of them confirmed the role of specific pork items such as figatellu, a traditional dried pig liver sausage widely eaten in France and commonly consumed raw (Colson et al., 2010), and undercooked pig liver–based stuffing (Guillois et al., 2015).

In Switzerland, no specific surveillance is in place and Hepatitis E is not a notifiable disease, therefore the exact number of diagnosed cases is not known (EDI, 2015). Few case reports confirmed that two autochthonous cases—including one acute case—with unknown exposure were diagnosed in the canton Geneva in 2004 (Sudre et al., 2005) and 12 acute autochthonous cases were diagnosed in the canton Vaud in 2013 (Hiroz et al., 2013). Recently, two acute cases were reported in the canton Nidwalden of a hunter who consumed deer and wild boar meat (Joller and Gaudenz, 2015), and in the canton Saint Gallen of a person who took part in a nature walk, during which wild, possibly contaminated herbs were collected and consumed (Sawatzki et al., 2015). One chronic case was also identified among a Swiss cohort of HIV patients (Kenfak-Foguena et al., 2011). However, Hepatitis E is likely to be underdiagnosed in Switzerland as the awareness for the disease is low among medical practitioners (Joller and Gaudenz, 2015). The occurrence of HEV is probably widespread as shown by a seroprevalence study conducted among blood donors in the Vaud canton (Kaufmann et al., 2011); depending on the diagnostic test used, the seroprevalence was estimated to be between 4.2% and 21.8% (Schnegg et al., 2013).

No quantitative data about the occurrence or the load of HEV in food is currently available in Switzerland. The seroprevalence of Hepatitis E in slaughtered pigs was estimated to be 49% at animal levels and 60% at farm level (Wacheck et al., 2012). A recent study covering the period of 2006–2011 confirmed HEV seroprevalence to be 58.1% in domestic pigs, and 12.5% in wild boars (Burri et al., 2014). The impact of this in terms of risk for the consumer of pork or wild boar is unknown.

In 2011, EFSA recommended to develop a risk assessment framework for specific HEV-commodity combinations and target populations, in order to identify specific data gaps, and to target research efforts (EFSA, 2011). In response to this recommendation we developed a population-based risk assessment framework for human Hepatitis E infection. More particularly, the specific study objectives were i) to assess the risk of hepatitis E from the consumption of pork and wild boar products, and ii) to estimate the overall burden of human hepatitis E in Switzerland.

Section snippets

Material and methods

The quantitative risk assessment was carried out according to Codex Alimentarius Framework (Cac/Gl 63, 2007). Fig. 1 illustrates the framework of the risk assessment of hepatitis E infection by the consumption of pork and wild boar products.

Exposure assessment

Out of 160 pig livers of 40 different Swiss fattening farms, two yielded a positive result, with a HEV load of 102.033 and 104.047 gc/g. The prevalence was therefore established to be 1.25% (95% CI 0.3%; 4.4%). The highest prevalence of HEV contamination was estimated as 18.38% (95% CI 13.93%; 23.97%) for wild boar liver or products thereof (category 1). The HEV prevalence of other category 1 products consisting of pork liver was estimated as 3.37% (95% CI 2.86%; 3.98%) (Appendix Table A.1. and

Discussion

The exposure assessment showed that HEV prevalence in Swiss pork livers was slightly lower, but still within the range of prevalence described in other European countries (Berto et al., 2012, Bouwknegt et al., 2007, Di Bartolo et al., 2012). At retail, we estimated that < 6% of the products containing pork liver (categories 1 and 2), and < 3% of the products containing pork meat could be contaminated with HEV genetic material. These values are below the range of 6% to 22% recently described in

Acknowledgements

The authors would like to thank the Swiss hospitals and accredited laboratories for their collaboration and sharing data on Hepatitis E cases in Switzerland, in particular Dr. Martinetti Lucchini from the microbiology service of the Ticino cantonal hospital, as well as Prof. Dr. med. Cerny and Ms. Fossati from the Fondazione Epatocentro Ticino. This research was supported by a grant of the Swiss Confederation, Federal Food Safety and Veterinary Office, Project number 4.15.c.

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