Potential Risk of Norovirus Infection Due to the Consumption of “Ready to Eat” Food
In this study, we investigated the presence of enteric viruses such as norovirus (NoV), hepatitis A virus (HAV), hepatitis E virus (HEV), and adenovirus (HAdV), in vegetables available on the Italian markets. For this aim, 110 national and international “ready to eat” samples were collected and analyzed by biomolecular tests and positive samples were confirmed by sequencing. All samples (100 %) were negative for HAV, HEV, and HAdV, while 13.6 % (15/110) were positive for NoV. Actually there is not a formal surveillance system for NoV infections in Italy but we clearly demonstrated a potential risk associated with the consumption of “ready to eat” vegetables. This study confirmed for the first time in Italy the presence of norovirus in semi-dried tomatoes by PCR technique.
KeywordsReady to eat food Sun-dried tomatoes Norovirus PCR
Viruses are increasingly recognized among the causes of foodborne outbreaks. In 2006, viral agents in Europe were reported to be for 10.2 % of foodborne outbreaks and were listed as the second most common etiologic agent, after Salmonella (EFSA 2007). It has been shown by Mead et al. (1999) that each year 67 % of the causes of acute gastroenteritis can be attributed to viral agents, thus representing the main cause. In developing countries, it has been clearly demonstrated that the viral outbreaks attributed to the consumption of fresh produce, whose cases were mostly attributed to enteric viruses such as norovirus (NoV), hepatitis A virus (HAV), human adenovirus (HAdV), and the hepatitis E virus (HEV). Recently there have been outbreaks caused by HAV in Australia (May 2009), New Zealand (May 2009), Netherlands (January 2010), and France (February 2010), as well as outbreaks due to NoV in Finland (2009) and Austria (2007) (Craven et al. 2009; Kuo et al. 2009; Maunula et al. 2009; Petrignani et al. 2010; Wadl et al. 2010). Vegetables may become contaminated by enteric viruses, during cultivation before harvest by contact with inadequately treated sewage or sewage polluted water. In addition much emphasis was also placed on the role of workers during processing, storage, distribution or final preparation (Koopmans and Duizer 2004). The importance of these routes of transmission of infection is supported by the studies that have demonstrated the possibility of transfer enteric viruses from the fingers of workers to the surface of fresh produce (10 s for a single contact) (Rzezutka and Cook 2004). The viruses does not replicate in the food but they have the ability to withstand for long periods without suffering any reduction in infectivity (Koopmans and Duizer 2004; Carter 2005) and so hygiene likely is a main requirement for microbiological quality. The purpose of this study was to verify the presence of enteric viruses in ready to eat vegetables and sun-dried tomatoes available on the Italian markets.
Materials and Methods
Primers used for PCR analyses
Type of amplification
Product size (bp)
Number of positive samples found in semi-dried tomatoes by bio-molecular tests
Country of origin
PCR positive results
Dried tomatoes in bulk
Dried tomatoes in oil
Packaged leafy green
Over the years outbreaks of NoV gastroenteritis have been mainly linked to shellfish consumption, recently also matrices like herbs and red fruits (Maunula et al. 2009) have been associated with these diseases. This study shows for the first time in Italy the detection of NoV in sun-dried tomatoes native and from Turkey. A limit due to this study is the inability to determine the infectivity of NoV found in the samples: the used methods highlight the presence of the nucleic acid of the virus but we cannot effort the vitality as the genomic RNA can persist after the virus has been inactivated and as there is no cell culture line for the laboratory growth of human NoV. A single infectious NoV has an estimated high probability of causing infection and the risk to human health is mainly present in those types of foods that do not require cooking before consumption (Teunis et al. 2008). Water quality used for agricultural irrigation and the hand of the professional working in the field affect the microbiological characteristics of products and therefore may pose a risk to the health of consumers. In particular, the transformation of sun-dried tomatoes is a process that requires much work and for this reason it is hard to detect the point-source of the viral contamination. Numerous studies have shown that enteric viruses can survive the processes usually applied to food before being put on the market and remain in a vital condition for long periods of time or at least longer than the shelf life of products (Craven et al. 2009; Butot et al. 2009; Doultree et al. 1999; Bidawid et al. 2000; Fraisse et al. 2011;) and these characteristics make it particularly dangerous to the health of the consumer. Despite this, only recently raw plant products are tested for viral contamination (Cheong et al. 2009) and these organisms are not yet considered in the regulations currently in force. Our study suggests a contact with NoV and the vegetables during the food chain but the viruses was only detected by bio-molecular technique, so it was not possible to determine the infectivity of the virus and to quantify the risk for human health. Despite the positive results, no outbreaks were noted by the local hospital. In order to protect the consumer it is necessary that the companies will undertake controls during the transformation of the products to prevent enteric virus contamination and it could be useful to start epidemiological studies for linking outbreaks with positivity to bio-molecular tests.
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