E D I T O R I A L C O M M E N TA R Y
Preventing Norovirus Transmission: How Should
We Handle Food Handlers?
Christine L. Moe
Center for Global Safe Water, Hubert Department of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia
(See the article by Malek et al. on pages 31–7)
Noroviruses are nearly perfect pathogens.
They are the most infectious agents ever
described, with an estimated median infectious dose of 18 viruses [1]. Even minute amounts of fecal matter containing
norovirus can pose a risk of transmission
via hands, food, objects, aerosols, or water.
Viral shedding can occur at extremely high
levels. Chan et al. [2] reported that the
median cDNA viral load for norovirus in
stool samples ranged from 2.2 ⫻ 10 4 to
7.7 ⫻ 1010 viruses/g. Furthermore, norovirus shedding can persist for weeks after
the (usually short-term) symptoms have
resolved. Approximately 25% of people
infected with noroviruses shed virus for
⭓3 weeks [3]. Epidemiologic evidence and
environmental studies indicate that these
viruses have a prolonged duration of survival outside of the host in the aquatic
environment [4] and on indoor surfaces
[5]. Despite evidence of genetic resistance
to 1 norovirus strain [6], most of the population appears to be highly susceptible to
noroviruses. Outbreaks of norovirus infection have high attack rates and secondReceived 23 September 2008; accepted 23 September
2008; electronically published 24 November 2008.
Reprints or correspondence: Dr. Christine L. Moe, Hubert
Dept. of Global Health, Rollins School of Public Health of
Emory University, 1518 Clifton Rd. NE, Atlanta, GA 30322
([email protected]).
Clinical Infectious Diseases 2009; 48:38–40
2008 by the Infectious Diseases Society of America. All
rights reserved.
1058-4838/2009/4801-0006$15.00
DOI: 10.1086/594119
ary transmission rates. This may be due
to the low infectious dose, but we have
also observed that ∼20% of norovirus-infected people do not have symptoms and
may continue to work and have contact
with others while oblivious of their ability
to infect them.
The reproductive number (i.e., the
mean number of susceptible persons who
become infected by an infectious individual) for norovirus is likely to vary greatly
depending on the setting and who becomes infected. In this issue of Clinical
Infectious Diseases, Malek et al. [7] describe
an outbreak of norovirus infection in
which the index case was an infected food
handler at a meat processing plant who
contaminated ready-to-eat food, resulting
in illness among 137 people who participated in river rafting trips in the Grand
Canyon. In other outbreaks involving
food handlers, such as bakers who prepared wedding cakes, the number of cases
associated with a single contamination incident has been estimated to be in the
thousands [8]. In our review of reported
outbreaks of norovirus infection in the scientific literature, we found that outbreaks
associated with food or restaurant settings
had significantly higher attack rates
(150%) than did outbreaks in other settings [9]. The Centers for Disease Control
and Prevention (CDC) estimates that
∼50% of all outbreaks of norovirus infec-
38 • CID 2009:48 (1 January) • EDITORIAL COMMENTARY
tion are linked to ill food service workers
[10].
Malek et al. [7] identify 2 critical factors
that contributed to this outbreak: (1) the
food handler who sliced the implicated
delicatessen meat returned to work 1 day
after recovering from gastroenteritis
symptoms that were clinically consistent
with norovirus infection, and (2) barehand contact with the implicated meat occurred. Because this employee was working in a meat-processing plant, the
relevant regulatory authority is the US Department of Agriculture (USDA) Food
Safety and Inspection Service. The federal
regulations that govern employee hygiene
in this setting are vague about disease control and only state that “any person who
has or appears to have an infectious disease.…must be excluded from any operations which could result in product adulteration until the condition is corrected”
[11, p. 632]. It is obvious that ill food
workers should be restricted in their activities or excluded from the workplace.
Many outbreaks of norovirus infection
have been associated with food service
workers who are ill on the premises. Cooks
and food handlers who have vomited in
sinks, in wastebaskets, and on the floors
of their workplace have infected their colleagues, contaminated the kitchen environment, and ultimately caused infection
among the patrons of the food service establishment. Yet these incidents continue
to occur, because there is no incentive for
hourly wage workers to report illness and
to lose their pay if they feel they can still
work. Perhaps the more difficult issue to
tackle is how soon after gastroenteritis
symptoms have resolved is it safe for a
food handler to return to work. The
USDA regulations do not address this issue at all.
The US Food and Drug Administration
(FDA) Food Code [12] applies to food
handlers working in food service establishments. The 2005 Food Code specifically recognizes norovirus as highly infectious and restricts any food handling by
symptomatic employees who have received
a diagnosis of norovirus infection. Asymptomatic food employees who have received
a diagnosis of norovirus infection are also
restricted from working in food establishments that serve a “highly susceptible population.” The timing of the exclusion
ranges from 24 h to 48 h, depending on
whether the food employee was symptomatic (in which case, the timing is 48 h after
symptoms have resolved) or asymptomatic. Some state and local health departments have suggested more-stringent time
restrictions, such as excluding ill food employees for at least 72 h after gastrointestinal illness symptoms subside and prohibiting contact with kitchenware or
ready-to-eat food for an additional 72 h
[13]. However, 24–72 h is not likely to be
a sufficient exclusion period for a food
handler, because it is not unusual for
someone with norovirus infection to shed
virus for 2–3 weeks. The Food Code also
notes that the food employee can be reinstated if he or she has “written medical
documentation from a health practitioner
stating that the food employee is free of a
norovirus infection” [12, p. 36]. Real-time
norovirus infection status can be determined only by detection of the virus in
stool specimens—preferably by RT-PCR
or, although it has greater speed but less
sensitivity and specificity, by electron microscopy. Several commercial ELISA kits
to detect norovirus antigen in stool specimens are still being evaluated and are not
currently available in the United States.
Therefore, it is unlikely that most health
practitioners would be equipped to get a
patient stool sample tested for norovirus
and certify that the individual is no longer
infected. A commercially available, rapid,
sensitive, and specific diagnostic test for
norovirus infection would aid in the identification of infected food handlers and
allow better prevention of virus transmission.
The other critical factor in this outbreak—and in many other foodborne outbreaks of norovirus infection—is barehand contact with ready-to-eat foods. For
120 years, the FDA Food Code has required no bare-hand contact with readyto-eat foods, and most states have adopted
this regulation, although it is controversial
[14]. Again, USDA regulations about
cleanliness and food handling are vague
and state that “all persons working in contact with product, food-contact surfaces,
and product-packaging materials must adhere to hygienic practices while on duty
to prevent adulteration of product and the
creation of insanitary conditions” [11,
p. 632].
If bare-hand contact is allowed, then
food employees must practice extraordinary hand hygiene in order to ensure that
their hands do not transmit norovirus, because of the low infectious dose and high
titers in stool. The USDA [15] has adopted
the specific guidance from the Food Code
on how, when, and where to wash and
sanitize hands. The issue is compliance
with these recommendations. Observational studies of food workers have reported improper hand washing in 73% of
restaurants [16] and that food workers
washed their hands only approximately
one-third of the time after performing activities for which hand washing is recommended [17, 18]. In addition, hand
sanitizers must be selected carefully, because some can be very effective against
noroviruses, whereas others appear to provide no measurable norovirus reduction
[19]. Extraordinary hand hygiene can be
promoted by education and training, pos-
itive incentives and reinforcement from
managers, proper location and design of
hand-washing stations, and effective
handwash agents and sanitizers. Green et
al. [20] observed that appropriate hand
washing was associated with the presence
of multiple hand sinks and a hand sink in
the worker’s sight.
Glove use is not mentioned in the
USDA regulations. The FDA Food Code
requires single-use gloves or suitable utensils for contact with ready-to-eat food and
specifies that the gloves be used for only
1 task [12]. Some food service companies
argue that single-use gloves are extremely
cumbersome in certain food service settings, such as those in which a single employee is preparing food and also working
at the cash register. Like hand washing,
food employee compliance with glove use
varies. The FDA observed a failure to prevent bare-hand contact with ready-to-eat
foods in 57% of restaurants [16]. Institutionalizing glove use and having glove
supplies readily accessible in food preparation areas have been associated with a
greater likelihood of glove use by food
workers [20].
Given the characteristics of these viruses
and the shortcomings of human behavior,
what is the most effective means to prevent
norovirus transmission by food handlers
and to reduce epidemic and endemic norovirus infection? Even in countries that
have attained the highest standards of hygiene, outbreaks of norovirus infection
continue to occur frequently. The CDC
now estimates that, in industrialized countries, noroviruses are associated with
64,000 episodes of gastroenteritis requiring hospitalization and 900,000 clinic visits among children each year, as well as up
to 200,000 deaths annually among children aged !5 years in developing countries
[21]. The substantial burden of disease associated with norovirus and the economic
costs associated with outbreaks of norovirus infection are compelling reasons to
seek more-effective prevention measures.
Our understanding of norovirus immunology has significantly improved in the
EDITORIAL COMMENTARY • CID 2009:48 (1 January) • 39
past decade, and norovirus vaccines are
currently under development. However,
there are still many unanswered questions
about the determinants of protective immunity against norovirus infection [22].
Epidemiologic evidence of temporal shifts
in predominant norovirus strains associated with epidemics of gastroenteritis suggest that it will be necessary to set up
global surveillance to track the emergence
of new norovirus stains, to inform the design of effective norovirus vaccines [23, 24,
25]. Food service workers are a logical target population to immunize against norovirus infection because of the potential
for significant public health benefit for the
general population.
Acknowledgments
We thank James Hughes and Peter Teunis, for
their reviews and comments; and Alexandra Huttinger, for her technical assistance.
Potential conflicts of interest. C.L.M has received research funding from GOJO Industries.
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