According to the clinical symptoms, epidemiological characteristics and laboratory results, the outbreak of norovirus infectious diarrhea was determined. (1) The epidemic curve with a sharp upward slope and a gradual downward slope describes a point source outbreak. The whole school uses uniform municipal tap water and drinking water, and all the laboratory tests are qualified, which can exclude water source factors. (2) Having had take-out food is a major risk factor. (3) More than 2 cases occurred in 7 dormitories. Exposure to similar cases 72 hours before onset and the existence of case in the same dormitory were risk factors, and the time difference between the onset of the disease was as long as 10 days, which indicate that contact transmission from person to person could not be excluded in the late stage of the epidemic. (4) Moreover, we detected norovirus GⅡ.3 strain in environmental swabs samples of off-campus restaurant, as well as in rectal swabs from the food handlers using sequence analysis, which present a complete chain of evidence. (5) The outbreak was quickly quelled after the forbidden of off-campus eating, the implementation of thorough disinfection and case isolation measures, which corroborated the judgment of foodborne and contact transmission in the outbreak.
Fecal-oral spread is the primary route of norovirus transmission, and human can be infected by direct person-to-person contact, consumption of contaminated food or water, or contact with contaminated environmental surfaces as well(13). Foodborne transmission is an important source for the global spread of norovirus(14) and can happen either when food handlers contaminate food on site or during the earlier steps of food production(13, 15). During 2009-2012(8), 48% (1008/2098) of the foodborne outbreaks were caused by norovirus, among which infectious food workers were implicated as source of contamination in 364 (364/1008, 36%) in the U.S.
Poor handling practice of infected food handlers is a common source of infection in foodborne outbreak in Guangzhou. Foodborne transmission accounted for 40.74% of total norovirus outbreaks in Guangzhou from 2016 to 2018, among which kitchen workers pollution accounts for a large proportion. Personal hygiene practices of infected food handlers are considered the most important contributing factor in the spread of foodborne diseases (16).
Two studies of food handlers suggested that the norovirus infectious rate of asymptomatic food handlers ranging from 1.0 to 3.7%. Foods may be contaminated by unhygienic manipulation by a food handler excreting the virus (17), which may probably be underestimated, because it is difficult to prove(18).
Given the importance of food handling in the prevention of norovirus infections, food handlers should be advised to take special care to follow good kitchen hygiene practices, particularly hand washing. Furthermore, daily health monitoring of food handlers and cleaning and disinfection of the environment are of great importance.
Periodic monitoring with viral pathogens such as rotavirus and norovirus has been performed to assess infection status in the whole population, However, epidemiologic surveillance data on food handlers in or out of schools are scarce in China. Enhancement of the surveillance of gastrointestinal symptoms of food practitioner and timely discovery and control of disease outbreaks are critical measures to reduce the influence of such events. Recently, we have taken the first step on monitoring the norovirus infections in asymptomatic food handlers in two colleges before the new semesters in Guangzhou.
An analysis of many outbreaks has identified noroviruses of the GII genogroup as the most common strains worldwide, of which strain GII.4 has become the predominant part. This study showed that norovirus GII.3 strain was the causative agent, and the original route of transmission was foodborne means which caused infection in the primary cases. From 2012 to 2015 the strain GII.3 accounted for 12.3% of the 73 norovirus outbreaks in Guangdong province, China(19). Previous indicated that the prevalence of infecting genotypes differs between human populations and routes of transmission(13, 20). Genotype GII.4 is more often associated with transmission mediated by person-to‑person contact than with other types of transmission, whereas non-GII.4 genotypes, such as GII.3, are more often associated with foodborne transmission(14), a trait that may relate to the proposal that GII.3 strains have a higher stability in food than GII.4 strains. These results suggest that GII.3 norovirus should be paid more attention especially in suspected foodborne outbreaks of gastroenteritis.
To our knowledge this is the first study identifying norovirus as the causative agent of a foodborne outbreak caused by take-out food in China. Delivery services are common in China recent years, and the hygienic condition of the takeout food is not easy to control and guaranteed. The contamination of the food could take place in every stage from food preparation to distribution, of which the food handlers may play a significant role. The current results highlight the risk of contamination of takeout food by norovirus.
Conclusion
Food handling practices carries potential risk of acute gastroenteritis outbreaks due to a lack of surveillance and supervision. More attention should be paid to the monitoring and supervision of food handlers to reduce the incidence of norovirus-related acute gastroenteritis associated with delivery food.