It is important to note that as a direct result of the person-to-person transmission route, the enhanced disinfection of surfaces is not sufficient to control these outbreaks CDC, a,b; Vivancos et al. This distinguishes them from outbreaks transmitted via point source fomite contamination, which are discussed in Section IV. For outbreaks spread directly between individuals, limiting interaction between infected and uninfected persons is critical. Cohorting of patients within medical facilities, exclusion of staff for up to 72 h following an attack of gastroenteritis, and cancellation of social events have all been recommended CDC, a; Rao et al.
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The use of personal protective equipment when working with patients or patient samples has been identified as a factor affecting outbreak spread CDC, b; Ebihara et al. In addition, hand hygiene has been particularly well studied as a method of interrupting transmission of NoV during outbreaks Gilbride et al. Some studies indicate that washing with soap and water is required to eliminate NoV transmission Bidawid et al. All authors agree that the use of hand rubs is indicated where soap and water are not available CDC, a; Steinmann et al.
The pronounced environmental stability of NoV particles also contributes to the spread of outbreaks from point sources of surface contamination. All stability studies have made use of surrogate organisms to model NoV response to conditions, since the human virus is not easily grown in cell culture Duizer et al. Efforts have been made to develop methods to quantify human NoV persistence and disinfection by detection of genetic material Lamhoujeb et al.
Other more complex inanimate surfaces, such as telephone buttons and computer keyboards, support the survival of infectious FCV for 0. The particular resistance of NoV to disinfection is an additional factor in the spread of NoV infections from contaminated fomites. Table 1. Data from disinfection studies must be interpreted with care, as many demonstrate efficacy in suspension tests Beekes et al. Contact time also plays an important role, with some disinfectants exhibiting efficacy after 10 min that cannot be demonstrated after 1 min Jimenez and Chiang, ; Whitehead and McCue, These should be evaluated on a case-by-case basis, using a protocol based on their proposed use i.
More complex surfaces, such as woven fabrics, carpets, or porous materials, can be more difficult to disinfect Malik et al.
UV disinfection overcomes some of the issues with soft fabrics, but the light must reach all crevices to be effective Lee et al. The use of gas disinfection in sealed rooms is an interesting alternative to reach all areas, but this requires long incubation times and the ability to seal an area Hudson et al. There is not always a clear distinction between outbreaks transmitted via inanimate surfaces as compared to those that are linked to direct TABLE 1. The role of fomites in NoV transmission in closed settings can never be completely separated from other risk factors Wu et al. However, contaminated surfaces are associated with outbreaks in closed facilities Gallimore et al.
Outbreaks that have been linked to a point source fomite contamination are characterized by infected populations that have few or no other epidemiological links. For example, an outbreak linked to a certain seating area in a concert hall the day after a vomiting episode Evans et al. Two coach tours visiting the same hotel at different times are also linked mainly by common surfaces at the hotel Visser et al. Although school outbreaks are frequently associated with person-to-person transmission, one investigation indicated shared computers as a possible fomite source of infection CDC, The implementation of environmental swabs as a part of routine outbreak investigation would serve to highlight this potential transmission Boxman et al.
In theory, the interruption of NoV transmission after fomite contamination is straightforward: the affected objects must be disinfected. In practice, disinfection can become a complex problem. The school described above had implemented a rigorous cleaning protocol with an appropriate bleach solution but failed to consider the computer mice and keyboards for disinfection CDC, Vomiting events are particularly difficult to clean, as the contaminated area can be large, and infectious aerosols are postulated to persist in the environment Evans et al.
For NoV outbreaks, there is a strong association with food handlers and poor personal hygiene practices Baert et al. This, together with the higher incidence of secondary spread during outbreaks Martinez et al. Some characteristics of NoVs are important when considering food handlers as a transmission route. These viruses are stable in the environment and have been shown to be transmitted between surfaces, hands, and foods Bidawid et al.
Outbreaks in a variety of settings, such as 16 Kirsten Mattison hospitals, schools, catered events, and restaurants, have all been associated with infected food handlers as the source of contamination Anderson et al. Additional outbreaks have been associated with food handlers based on an indication that multiple food products were involved in a single outbreak Dominguez et al.
In addition, NoV infections result in a higher number of vomiting incidents than other foodborne pathogens Kaplan et al. Vomiting events can be difficult to manage in a food service environment, and outbreaks where food service workers have vomited may be particularly large de Wit et al. Finally, food handlers may harbor asymptomatic NoV infections Okabayashi et al. Outbreaks have been associated with foods handled by workers with no symptoms, although they may have had evidence of recent exposure to NoV Godoy et al.
Control of transmission from infected food handlers relies on an understanding and compliance with food safety procedures Clayton and Griffith, Restaurant inspections and recommendations are only effective up to a point Dominguez et al. Food safety training programs and on-site management committed to food safety can have an impact in reducing NoV outbreaks Hedberg et al.
This could limit noncompliance with policies, a possible cause of outbreaks transmitted during food preparation Anderson et al. Additional measures to prevent NoV transmission are more difficult to implement. The exclusion of asymptomatic workers known to have been exposed to NoV or after recovery from gastrointestinal illness is not always realistic when they would lose their pay Moe, There are still reports of food handlers working while symptomatic for fear of job loss Schmid et al.
Compared to surfaces, water has a protective effect for calicivirus survival, with 5. Food products provide varying degrees of protection or antiviral activity, depending on their properties. FCV has Norovirus as a Foodborne Disease Hazard 17 been shown to survive for 7 days on ham, 3—5 days on lettuce, 1—5 days on cantaloupe, 3—4 days on bell peppers, and 1 day on strawberries Mattison et al.
Temperature control is a key parameter for control of bacterial pathogens in food but less relevant for eliminating NoV Baert et al. Freezing is not suitable for control of NoV contamination, rather long-term frozen storage preserves the infectious virus. Studies have shown that there is less than a 1-log reduction of MNV after 6 months of storage on frozen onions or spinach Baert et al. Similar findings were obtained for FCV on blueberries and frozen herbs after 2 days Butot et al. FCV was inactivated after frozen storage on raspberries 1 log and strawberries 3 logs Butot et al.
Physical inactivation can also be achieved by nonthermal processing such as high pressure treatment or ultraviolet UV and gamma irradiation Baert et al. High hydrostatic pressure from — MPa can quickly reduce infectious FCV by over 5 logs in liquid media, although temperature and pH must be monitored for optimum results Buckow et al.
Food may provide some protection from high pressure treatment, but inactivation can still be achieved by a 5-min treatment Kingsley et al. UV irradiation is less useful for decontaminating foods. Food surfaces may provide some protection from UV light, as higher doses are required for inactivation of FCV, and the light must equally reach all sides of a food product Fino and Kniel, Chemical treatment of drinking water and food wash waters can also be used to reduce the presence of infectious NoV.
Although disinfection of wash water does not significantly increase the removal of viruses from produce, it can prevent cross-contamination of the next product washed Baert et al. Effective decontamination of water typically requires more disinfectant than for equivalent bacterial reductions. The concentration of chlorine is important for inactivation in short time periods.
MNV is typically inactivated by 0. FCV is sensitive to chlorine within the same concentration range Thurston-Enriquez et al. MNV inactivation has been demonstrated at 0. Ozone effectively inactivates 4 logs of FCV at less than 0. There are many peer-review publications reporting NoV outbreaks due to food and water. In spite of a recognized publication bias toward these outbreaks, there is a consensus that the scientific literature underestimates the contribution of NoV to food and waterborne disease Hall et al.
Source contamination of food and water is clearly implicated in NoV outbreaks around the world. Waterborne outbreaks have been identified in both drinking and recreational waters, although the route of entry is clearly via consumption of the contaminated water. As detection methods improve, more waterrelated outbreaks have been associated with NoV contamination Bosch et al. Recreational water outbreaks have been associated with lakes Sartorius et al.
Flood water has also been contaminated with NoV and infections resulted from direct exposure to the water Schmid et al. Drinking water has been shown to become contaminated with NoV through a variety of means. Individual wells can become contaminated and contribute to local outbreaks Nygard et al. These local outbreaks have the potential to seed secondary cases of infection in the community Beller et al. Similarly, local hotel or Norovirus as a Foodborne Disease Hazard 19 resort water distribution systems have been identified as the source of NoV outbreaks Hewitt et al. These are easily traced epidemiologically because the affected populations are infected at the same time and have no other common food intake or personal contacts.
Outbreaks in community water supplies and groundwater have only been recognized when they reach massive proportions Gallay et al. It is possible that lower levels of contamination could go undetected in the background of community acquired NoV cases throughout the year. Shellfish are the most commonly implicated food category in NoV outbreaks. These filter feeders accumulate virus if grown in contaminated waters McLeod et al.
It has been suggested that NoVs interact specifically with carbohydrate structures in the bivalve digestive diverticula Le Guyader et al. NoVs have been detected in shellfish grown around the world Boxman et al. In addition, there are numerous reports of outbreaks where viruses identified in contaminated shellfish share the same sequence as those isolated from outbreak patients David et al. In many other cases, epidemiological evidence points to oyster consumption as the cause of the outbreak, although virus cannot be detected in oyster samples Gallimore et al.
The epidemiology can be strengthened by the association of multiple viruses or genotypes with the same outbreak, a common indicator for sewage contamination in shellfish-associated outbreaks Gallimore et al. Control measures for shellfish-associated outbreaks rely on high quality growing waters. Although bacterial indicators may return to baseline levels after a contamination event, opening a shellfish harvest area too soon can lead to an NoV outbreak Huppatz et al. Frozen shellfish from contaminated waters should be clearly labeled to ensure that they are not served raw Ng et al.
If waters are known to be contaminated, additional virus-specific relaying or depuration conditions can be implemented to manage the associated risk of NoV gastroenteritis Dore et al. Consumer education is useful to reduce 20 Kirsten Mattison consumption of illegally harvested shellfish Le Guyader et al. Fresh fruits and vegetables may also be contaminated with NoV during production or processing prior to distribution. Contaminated irrigation water or wash water can transfer NoV to fresh products Bassett and McClure, ; Cheong et al. NoV has been implicated as the cause of outbreaks of gastroenteritis from salads Allwood et al.
Cooking is an effective control measure for NoV contamination but is not applicable to the fresh fruit and produce category. Washing in clean water can reduce levels of NoV contamination from 1 to 3 logs Baert et al. The most effective intervention is to prevent contamination from occurring. Appropriate treatment of irrigation and wash water can inactivate NoV Baert et al. Surveillance networks may detect point source foodborne outbreaks, and this information can be used to prevent or limit the spread of disease Koopmans et al. The difference between person-to-person and foodborne NoV transmission during outbreaks is not always clear and should not need to be defined.
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Many outbreaks that begin with contaminated food can later spread person to person and vice versa. Instead of focusing on a label for the source of NoV outbreaks, it is more important to increase overall awareness and understanding of this emerging pathogen. NoV outbreaks are spread in many different ways, including ingestion of contaminated food products. This information can be used to develop strategies for integrating public health and food safety surveillance networks that will provide alerts and interrupt transmission for all categories of NoV outbreaks.
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