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INVITED ARTICLE
FOOD SAFETY
Frederick J. Angulo, Section Editor
Gastroenteritis and Food-Borne Disease in Elderly People
Living in Long-Term Care
Martyn D. Kirk,1,2 Mark G. Veitch,3 and Gillian V. Hall1
1
National Centre for Epidemiology and Population Health, The Australian National University, 2OzFoodNet, Office of Health Protection, Australian Government
Department of Health and Ageing, Canberra, and 3Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology,
The University of Melbourne, Melbourne, Australia
Elderly people in long-term care facilities (LTCFs) may be more vulnerable to infectious gastroenteritis and food-borne disease
and more likely to experience serious outcomes. We review the epidemiology of gastroenteritis and food-borne diseases in
elderly residents of LTCFs to inform measures aimed at preventing sporadic disease and outbreaks. Gastroenteritis in elderly
people is primarily acquired from other infected persons and contaminated foods, although infections may also be acquired
when residents have poor personal hygiene, have contaminated living environments or water, or have contact with infected
pets. Early recognition of outbreaks and implementation of control measures is critical to reduce the effects on LTCF residents
and staff members. Although outbreaks among LTCF residents are common, they are challenging to investigate, and there
are still major gaps in our knowledge, particularly in regards to controlling noroviruses, the incidence and causes of specific
infections, and sources of food-borne disease.
The number of people aged 165 years is increasing globally [1,
2]. Elderly people may be vulnerable to gastroenteritis and
food-borne infections because of changes in immune response
[3, 4], gastrointestinal physiology [5], use of immunosuppressive or acid-suppressive medications [6, 7], and comorbid conditions [6] associated with aging. One subpopulation at higher
risk of food-borne diseases are elderly people living in longterm care facilities (LTCFs) [8, 9]. In the United States between
1994–1998, LTCF residents were 4 times more likely to die from
gastroenteritis than people living in the community [10], and
17.5% of deaths involving gastroenteritis occurred in LTCFs
[11]. In the 1980s, the Food and Drug Administration recommended that LTCFs, where the case fatality rate was 70 times
that of other settings, not feed residents unpasteurized eggs
because of Salmonella Enteritidis outbreaks; the recommendation resulted in a subsequent decrease in outbreak and associated deaths [12].
LTCF residents tend to have poorer health status [9, 13] with
higher prevalence of chronic diseases [1] and greater use of
Received 15 June 2009; accepted 28 August 2009; electronically published 4 January 2010.
Reprints or correspondence: Mr Martyn Kirk, The Australian National University, Canberra,
Australian Capital Territory 0200, Australia ([email protected]).
Clinical Infectious Diseases 2010; 50:397–404
2010 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2010/5003-0016$15.00
DOI: 10.1086/649878
antibiotics and other medication [9]. In the United States,
18,000 facilities house ∼1.6 million predominantly female residents with a median age of 83 years (National Nursing Home
Survey 2004, Centers for Disease Control and Prevention, unpublished data) [1]. The close living arrangements of elderly
people and contact with visitors and staff make LTCFs a unique
environment for the spread of infectious agents [9, 13, 14]. In
addition, centralized preparation and service of food to LTCF
residents has inherent risks for transmission of food-borne
agents [15, 16].
METHODS AND DEFINITIONS
The aim of this review was to describe the epidemiology of
gastroenteritis and food-borne diseases in elderly residents of
LTCFs, to inform measures aimed at preventing sporadic disease and outbreaks. We considered both gastroenteritis due to
all modes of transmission and food-borne infections presenting
with nongastrointestinal symptoms. We searched PubMed and
the Web of Science for articles published in English language
from 1970 through mid-2009, using a variety of search terms
relating to LTCFs, enteric pathogens, and modes of transmission. One of us (M.D.K.) evaluated articles for relevance to the
review and extracted information into an Endnote, Version 11
(Thomson Reuters), database, which resulted in 1200 articles
(search strategy and full reference list available on request).
FOOD SAFETY • CID 2010:50 (1 February) • 397
Despite many studies published in the literature, there is a
paucity of information from well-designed trials, and evidence
is largely derived from outbreak investigations, which are often
deficient. We considered persons aged165 years to be “elderly”
[1]. In this article, LTCFs are institutions providing short- or
long-term health care to elderly people who, because of disability, frailty, or illness, are unable to live in the community
[17], and we restrict our discussion to the developed world.
CHARACTERISTICS OF GASTROENTERITIS
AND FOOD-BORNE DISEASE
The major causes of gastroenteritis and food-borne diseases in
LTCF residents are shown in Table 1.
Difficulty of diagnosing infectious gastroenteritis. Signs
and symptoms of infectious disease may be atypical in elderly
persons, making early recognition of illness difficult [6, 9, 27].
Infectious diarrhea may be difficult to distinguish from fecal
incontinence, fecal impaction with overflow, aperient use, irritable bowel syndrome, or drug-induced diarrhea [27]. Similarly, vomiting may be attributable to many other causes [30,
31], and fever may be absent in elderly people [32]. To assist
with diagnosis, the Infectious Diseases Society of America has
established clinical practice guidelines for evaluation of fever
and infection in LTCF residents [32] and management of infectious diarrhea [33].
Invasive and complicated food-borne illnesses. Foodborne infections may manifest with nongastrointestinal manifestations, such as septicemia, meningitis, pneumonia, septic
arthritis, and osteomyelitis [7, 23, 34]. Listeria monocytogenes
causes meningitis and septicemia in elderly persons, particularly
those who are immunocompromised [7]. Elderly people have
higher rates of invasive Salmonella infection [35], with 13 (45%)
of 29 deaths due to invasive infection in United States surveillance sites occurring in people aged 160 years [35]. Clostridium species, including Clostridium perfringens, may cause
pseudomembranous colitis in elderly residents [27, 36]. Elderly
people more commonly experiencing invasive infection and
serious sequelae, such as acute renal failure, although data are
lacking to contrast risks for people living in LTCFs with those
for people in the community.
Treatment. The Infectious Diseases Society of America
practice guidelines for gastroenteritis [33] emphasize supportive treatment and rehydration, which may be difficult in LTCF
residents [37]. Antibiotics are not generally indicated for residents with gastroenteritis, except where there is a higher likelihood of bacteremia [38]. Overuse of antibiotics in LTCF residents may lead to endemic Clostridium difficile [39]. Treatment
with antimotility agents may result in toxic megacolon when
infected with C. difficile [38] or hemolytic uremic syndrome
when infected with Escherichia coli O157:H7 [33, 40].
Incidence. LTCF residents experience 0.04–1.9 episodes of
398 • CID 2010:50 (1 February) • FOOD SAFETY
gastroenteritis per 1000 bed days [41, 42], equating to 1 episode
every 3–100 years. This incidence is lower than for elderly
people living in the community [43], although differing study
methods and study populations make comparison difficult. The
incidence of gastroenteritis among LTCF residents is lower than
that of respiratory and urinary tract infections but similar to
that of skin and soft-tissue infections [9].
Surveillance in LTCFs. A primary reason to conduct infection surveillance in LTCF is to detect outbreaks; surveillance
is mandatory in some countries as part of licensing and accreditation [17]. Case definitions developed at a Canadian consensus conference in 1991 recommended that a case have ⭓2
diarrheal stools or vomits within 24 h or fecal tests indicating
enteric pathogens with consistent symptoms. Conference participants expressed reservations about the definition [44], and
validation studies have not been published. Definitions are
probably applied loosely, where the priority of surveillance is
to identify cases and establish control. Nosocomial surveillance
in LTCFs is challenging because of difficulties diagnosing sporadic infections, high patient-to-staff ratios, training requirements, lack of nurses with experience in surveillance [45], and
high staff workloads.
DISEASE OUTBREAKS
Summaries of outbreak investigations in LTCFs have provided
insights into food-borne disease and gastroenteritis in LTCF residents [13, 15, 24, 46]. Improved surveillance and new diagnostic
tests have highlighted the burden of outbreak-associated gastroenteritis in LTCF residents [18, 47]. In Australia in 2007, 1010
(54%) of 1882 outbreaks of gastroenteritis occurred in LTCFs
(K. Fullerton [OzFoodNet], personal communication), representing 60% (939 of 1556) of outbreaks spread from person to
person [48]. In other countries, 12%–57% of all gastroenteritis
outbreaks occur in LTCFs [24, 49, 50].
In recent years, noroviruses have emerged as the main cause
of epidemic gastroenteritis in LTCFs and hospitals and have
challenged traditional measures to manage infectious diseases
[18, 47, 51]. Reports of norovirus outbreaks in LTCFs have
increased because of improved surveillance and global circulation of 2 strains of GII.4 norovirus, designated 2006a and
2006b [52, 53]. In LTCFs, norovirus outbreaks are predominantly spread from person to person [46, 53]. Noroviruses are
highly infectious [54] and pose risks for residents, visitors, and
staff members [55].
C. difficile is spread from person to person or via contaminated living environments and can result in serious outbreaks
[39]. C. difficile infection presents with highly variable symptoms, from mild diarrhea to colitis, toxic megacolon, and death
[28, 56]. Colonization and asymptomatic carriage amongst
LTCF residents is common and may be associated with prior
C. difficile infection or exposure to antibiotics [29]. In a study
Bloody diarrhea, abdominal pains, hemolytic
uremic syndrome,
thrombotic thrombocytopenic purpura
Diarrhea, vomiting, blood
I, 24–72 h; D, 4–7 days;
in stool, abdominal pain,
S, 1–21 days
fever
Shiga toxin–
producing
Escherichia
coli
Salmonella
enterica
Diarrhea, colitis, fever, abdominal pain,
leucocytosis
Headache, fever, myalgia, I, 130 days; D, variable;
S, NA
chills, abdominal pain,
and coma. Presentations include non-specific bacteremia, meningitis and focal infections
Clostridium
difficile
Listeria
I, 1–10 days; D, variable;
S, NA
Food-borne
Person-toperson
Food-borne
Watery diarrhea, abdominal pain, nausea
Clostridium
perfringens
I, 8–16 h; D, 24–48 h; S,
NA
Food-borne
Food-borne,
with some
person-toperson
Food-borne,
with some
person-toperson
Person-toperson
Person to person, with
some foodborne
Main mode of
transmission
Campylobacter Diarrhea, vomiting, blood
I, 2–5 days; D, 2–10
in stool, abdominal pain,
days; S, 1–69 days
fever
I, 2–12 days; D, 4–14
days; S, 1 day–3
months
I, 24–72 h; D, 1–5 days;
S, 1–20 days
Diarrhea, vomiting, fever
Rotavirus
I, 24–48 h; D, 12–60 h;
S, 2–45 days
Vomiting (⭓50% of affected), nausea, abdominal pain, anorexia,
diarrhea
Signs and symptoms
Norovirus
Agent
Incubation period (I), duration (D), and shedding
(S) following cessation
of symptoms
Comments
Food safety program; appropriate dietary assessment to avoid high-risk foods in vulnerable elderly residents
Environmental decontamination; increased infection control; cease offending antibiotic
treatment
Food safety program; minimize holding food at
inappropriate temperatures and reuse of foods
from day to day.
Food safety program; thoroughly cook poultry
products and minimize cross contamination;
avoid unpasteurized milk and untreated water
[18, 19]
References
Occasional cause of food-borne disease outbreaks in LTCF residents that may propagate
person to person after introduction to facility;
severity of illness can vary markedly
[27–29]
[24–26]
[23]
A single case in an LTCF requires assessment of [7]
food exposures and clinical history; case fatality rate in elderly people 20%–30%; 75% of infections occur in people who are
immunocompromised
Common cause of antibiotic-associated diarrhea
and causes wide spectrum of illness; high rate
of asymptomatic carriage of C. difficile with
4%–10% of LTCF residents colonized; in outbreak settings ∼50% of residents without
symptoms have positive stools
Routine testing of stool in pathology laboratories
will not detect C. perfringens; duration of C.
perfringens outbreaks much shorter than for
other pathogens, which may be a hallmark for
this etiology; may cause recurrent diarrhea or
antibiotic associated diarrhea in LTCF residents
Occasional cause of sporadic infections in LTCF
residents
[23]
[21, 22]
Infections can occur throughout the year, but out- [20]
breaks occur commonly in winter
Major cause of gastroenteritis outbreaks in facility residents; course of illness may be complicated and duration of illness or recovery may
be prolonged in hospital patients; incubation
period during person-to-person outbreaks difficult to assess
Evaluate food-borne sources; avoid undercooked Presentation can be complicated in immunocommeats, raw egg dishes, unpasteurized milk and
promised residents
juices, and untreated water; increased infection
control
Investigate food-borne sources; avoid undercooked hamburgers, unpasteurized milk or
juice, and some raw fruits and vegetables; increased infection control
Infection control; cohort ill patients
Infection control; intense environmental sanitation; cohort ill patients; restrict ill staff from
working
Main control measures
Table 1. Key Features of Main Pathogens Causing Gastroenteritis and Food-Borne Disease Affecting Long-Term Care Facility (LTCF) Residents
Figure 1. Risk-based approach for preventing, detecting, and managing gastroenteritis in long-term care facility residents based on means of
acquisition. Animal- and water-borne disease were combined because of the relative rarity of these modes of transmission.
in Ohio, the rate of C. difficile detection in stool samples of
hospital patients was 3 times higher than for LTCF residents,
in whom the rate of detection was 0.2–0.3 per 1000 bed days
[57]. Controlling C. difficile transmission in acute care settings
is vital for preventing infections in LTCF residents who are
more likely to have recently been hospitalized [58].
Two reviews of food-borne disease outbreaks highlight Salmonella as a common cause of food-borne disease outbreaks
in LTCFs, causing 25 (43%) of 58 outbreaks in the United
Kingdom [24] and 27 (23%) of 115 outbreaks in the United
States [15]. The case fatality rate for Salmonella outbreaks
ranged from 3% to 4% [15, 24]. Toxin-based illnesses were
also common, with C. perfringens responsible for 23 (40%) of
58 food-borne outbreaks in LTCFs in the United Kingdom [24]
and 6 (5%) of 115 in the United States. Staphylococcus aureus
also caused 12 (10%) of 115 outbreaks in the United States
[15]. The importance of C. perfringens may be underappreciated because of difficulties in microbiological diagnosis of
intoxications. Despite gastroenteritis normally having a mild
presentation, multiple deaths in LTCF residents may occur during a single outbreak of E. coli O157, Salmonella, or C. perfringens infections [15, 24].
Highly infectious norovirus may be transmitted by food
when catering or food service staff work while ill [55]. Outbreaks due to agents, such as Shiga toxin–producing E. coli and
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Salmonella, spread initially in food can subsequently spread
from infected persons or contaminated environments when
infection control is poor [21, 59]. Shigella, Yersinia, Giardia
[60], Cryptosporidium, rotaviruses, adenoviruses, sapoviruses,
and astroviruses [20, 24] cause occasional outbreaks in LTCFs,
although little is known about the introduction or propagation
of these agents.
PREVENTION, DETECTION, AND MANAGEMENT
OF OUTBREAKS
Prevention. Despite the commonness of outbreaks, few studies have assessed measures to prevent food-borne diseases or
gastroenteritis in LTCFs. A systematic review of 75 published
outbreaks in LTCFs concluded that data were insufficient for
quantitative assessment and made only general recommendations [46]. Prevention of gastroenteritis outbreaks in LTCF residents can be understood in terms of interrupting the possible
transmission pathways as shown in Figure 1. Pathogens may
be transmitted within a facility by ingestion of microorganisms
or toxins via exposure to (1) an infected person, (2) contaminated food or (3) water, (4) contaminated objects in the residential environment, or (5) infected animals.
Facilities are vulnerable to the introduction of infections due
to a complex traffic of people between the community, hos-
Table 2. Key Research Gaps in the Literature Regarding Foodborne Disease and Gastroenteritis in Long-Term Care Facility
(LTCF) Residents
1. What is the incidence, cause and cost of gastroenteritis and
food-borne disease in LTCF residents compared to elderly
people living in the community?
2. What are the best practices to manage outbreaks of
gastroenteritis in LTCFs?
3. What is the relative contribution of different microbiological
agents to gastroenteritis in LTCF residents?
4. What is the most appropriate means of conducting for surveillance for gastroenteritis in LTCFs, including validation of case
definitions?
5. How can gastroenteritis and food-borne disease be prevented
within LTCFs and what strategies should be in place relating to
architecture & fittings (including toilets), food handling, cleaning,
and response to single cases?
6. What is the most useful diagnostic strategy for a case of
gastroenteritis in an LTCF resident?
7. What factors facilitate introduction and initial transmission of
enteric agents, such as norovirus, within LTCFs?
8. What are the risks posed to different categories of LTCF
workers from infectious gastroenteritis?
9. What is the role of contaminated living environments for
transmission of enteric agents?
pitals, and other establishments and LTCFs. One means of
transmission occurs when a resident, staff member, or visitor
infects another person [13]. Infected residents then transmit
the agent to visitors or staff, or vice versa, during routine contact and care, such as clinical assessment, bathing, or feeding
[61]. Similarly, preventing people who are ill from visiting residents reduces the attack rates among residents during norovirus outbreaks [53]. Larger LTCFs experience respiratory or
gastrointestinal disease outbreaks more commonly, with a 71%
increase in risk per 100-bed increase in size [62]. LTCF staff
who work while ill may prolong outbreaks [63] or transmit
gastroenteritis to other facilities if they work in multiple institutions [64] or units [62]. Paid sick-leave programs for employees significantly reduce the risk of outbreaks [62].
While food may become contaminated outside the facility,
many outbreaks result from contamination occurring within
the LTCF from food handling errors during storage and preparation or unintentional contamination by residents [16, 46,
53]. Many foods have caused food-borne disease outbreaks in
LTCFs, including eggs, poultry, salads, cornmeal, powdered
milk and protein supplements, red-meats, peanut butter, and
water [12, 15, 24, 65]. The vulnerability of residents needs to
be considered in risk-based food safety programs, such as Hazard Analysis and Critical Control Points plans, along with
ongoing food safety education for staff [66]. Foods prepared
for residents may be at higher risk of contamination because
of the following: (1) preparation of large batches making cooling difficult; (2) holding foods at incorrect temperatures for
long periods allowing growth of microorganisms, such as C.
perfringens and S. aureus [25]; (3) use of equipment that increases the surface area for bacterial growth and dissemination
of pathogens when pureeing food for residents on soft diets;
(4) reusing leftover foods for pureed diets [46]; (5) cross-contamination during manual food preparation processes [66, 67];
(6) cooling foods to avoid burning residents; and (7) feeding
residents foods posing higher risks, such as raw eggs [12] and
sprouts.
In particular, pureed or blended food commonly causes bacterial or toxin-mediated outbreaks [12, 15, 25, 68], and investigators should swab blenders, because they are difficult to clean
and microorganisms colonize seals surrounding the blades (A.
Tan [University of Melbourne], personal communication).
Public health agencies have recognized increasing numbers
of outbreaks associated with fresh produce [69], such as spinach
[21], tomatoes, melons, and lettuce [69]. However, surveys in
the United Kingdom show that microbiological contamination
of salads and fruits is relatively rare, with the exception of
Listeria on precut fruit containing melons [70]. Facility managers should evaluate the benefits of serving these and other
higher-risk foods to LTCF residents, particularly those who are
immunocompromised [71]. Managers’ awareness about foodborne disease occurrence and management may be low [67],
resulting in poor uptake of food safety measures, such as using
irradiated meats and avoiding unpasteurized products [16].
Poor personal hygiene among residents, which leads to fomites or bedroom or bathroom environments becoming contaminated with persistent agents, is probably under-recognized
as a source of enteric infection [39, 59, 72]. LTCF residents
may be infected after consuming contaminated drinking water
during community-wide outbreaks [73] or from dedicated water supplies [74]. Infected pets in facilities are a possible source
of enteric infections, such as Salmonella and Campylobacter
infections [75]. In a survey of dogs visiting Canadian hospitals,
toxigenic C. difficile was isolated from 41 (40%) of 102 fecal
samples [76].
Detection and management. A Netherlands trial found that
LTCFs reporting norovirus outbreaks to public health agencies
within 3 days of the first patient becoming ill was associated with
more effective control measures [53]. In particular, LTCFs reporting early had lower attack rates among staff, along with
reductions in attack rates among residents and duration of outbreaks; the results just failed to reach statistical significance [53].
Unfortunately, detection of outbreaks may be difficult because
of residents having different physicians, lack of access to laboratories to confirm etiology, reluctance to investigate, and absence
of registers of resident and staff illnesses [27].
LTCFs should develop outbreak plans outlining management
arrangements for outbreaks, which may require involvement
of public health agencies [77]. A facility outbreak control team
FOOD SAFETY • CID 2010:50 (1 February) • 401
led by a physician or nurse [77] and including facility managers
and domestic staff should aim to minimize the early spread of
the outbreak. A sensitive definition of ⭓2 cases of gastroenteritis occurring in a facility in a week may be appropriate to
trigger an outbreak response, given the low background incidence of gastroenteritis [9, 31].
The etiology and likely mode of transmission of outbreaks
can guide control measures (Table 1 and Figure 1). Facility
outbreak plans should include stool sample test kits [78] to
allow collection of 4–6 fecal specimens from ill residents, to
increase the probability of confirming the etiology [78, 79].
Clinicians should consult laboratorians, because pathogens
such as C. difficile, C. perfringens, and norovirus require specialized tests [23]. Isolating agents, such as C. difficile, that may
be carried asymptomatically can cause confusion, and it is important to consider whether clinical features are characteristic
of the pathogen [80]. The team should maintain a line list of
affected residents and staff and review it daily [77].
Outbreaks with a high proportion of residents and staff experiencing vomiting may indicate norovirus spread from person to person, whereas tightly clustered onset of diarrheal illness
without vomiting among residents but not staff may indicate
food-borne C. perfringens [46, 81]. Outbreaks of longer duration affecting both staff and residents may be caused by agents
spread from person to person [22, 82] or may be from a persisting food-borne source [61].
Investigating outbreaks in LTCFs is challenging. Patients usually cannot recall consuming specific foods, and food intake
may not be recorded in detail [12]. During the investigation,
outbreak teams should formally evaluate food preparation and
service, facility cleanliness, waste management, hand hygiene,
laundry cleaning, and infection control to identify how the
outbreak occurred and to prevent future occurrences [46].
Control. Noroviruses are incredibly difficult to control because of their infectivity and environmental persistence [31, 53,
54, 72] and can be detected in residents’ stool samples an
average of 28 days after cessation of symptoms [19, 30]. Both
acutely ill and convalescent patients pose infectious hazards in
hospitals and LTCFs [83]. Staff must be made aware of and
communicate this risk, without jeopardizing the care and accommodation of the case patient [32]. For highly transmissible
agents, such as norovirus and Salmonella, exposure to vomit
and diarrhea pose an infectious risk for staff, including those
working in the laundry [53, 54, 84]. Friesma et al [53] reported
that attack rates were lower among staff during norovirus outbreaks in which a toilet was dedicated for ill persons for ⭓7
days following recovery, face masks were used during contact
with vomit, and staff worked in the first unit affected within
the LTCF. Many guidelines mention cohorting ill residents [46],
but implementation is difficult because residents may be difficult to shift during outbreaks [53]. It is preferable to close
402 • CID 2010:50 (1 February) • FOOD SAFETY
the unit to new admissions or limit exchange of staff [53, 83].
Outbreak control teams may restrict staff from working in certain parts of a facility and limit access by health care workers
or visitors [83]. LTCF staff with gastroenteritis should not return to work until ⭓48 h after symptoms resolve [53, 85].
Some agents that cause gastroenteritis are persistent in the
environment and difficult to eradicate [39, 72]. Vomit and feces
on surfaces or floors should be initially cleaned away with a
detergent-soaked cloth or mop. The soiled area should then be
disinfected with a solution containing 1000 parts per million
of available chlorine [86]. Some evidence suggests that higher
concentrations may be required (15000 parts per million) to
effect a substantial reduction of norovirus [72]. Persons cleaning must be protected by standard precautions, supplemented
by a gown, gloves, and eye protection. Soiled carpet is problematic; steam cleaning is required. Ineffective cleaning with
cloths may spread norovirus within a facility [72], whereas C.
difficile spores require high compliance with protocol and an
effective disinfectant [39].
The best approach to hand hygiene in the setting of an outbreak of gastroenteritis in a LTCF is unclear. Alcohol-based
hand hygiene products have been widely adopted in many
health care settings [87]. Concerns have been raised as to
whether the concentration and type of alcohol in a typical
product are sufficient to adequately reduce the concentration
of norovirus or C. difficile on contaminated hands [88, 89].
The alternative approach, hand washing with soap and water,
may be compromised in LTCFs if taps and basins are not easily
accessible [90]. Well-controlled studies are needed to evaluate
which approach is most effective in practice during outbreaks
in LTCFs. Staff caring for infected residents should use personal
protective equipment, such as gowns, gloves, and surgical masks
[53]. Once the etiology of the outbreak has been identified,
infection control measures should specifically target the infective agent [39, 55].
CONCLUSION
The key means of preventing gastroenteritis in LTCF residents
are well-functioning infection control programs and food-safety
plans, although there is a paucity of data on the most-effective
approaches [53]. To further our knowledge about gastroenteritis
and food-borne diseases in LTCF residents, there is a need for
more research to address key gaps in the literature (Table 2).
Acknowledgments
We would like to thank Drs Jenny Firman and Elaine Scallan for their
helpful comments on this article.
Financial support. National Health & Medical Research Council Postgraduate Scholarship (M.D.K.).
Potential conflicts of interest. All authors: no conflicts.
References
1. Kinsella K, He W. An Aging World: 2008. International Population Reports. Washington, DC: US Census Bureau, 2009.
2. Kirkwood TB. A systematic look at an old problem. Nature 2008; 451:
644–647.
3. McGlauchlen KS, Vogel LA. Ineffective humoral immunity in the elderly.
Microbes Infect 2003; 5:1279–1284.
4. Nikolich-Zugich J. Ageing and life-long maintenance of T-cell subsets in
the face of latent persistent infections. Nat Rev Immunol 2008; 8:512–522.
5. Slotwiner-Nie PK. Infectious diarrhea in the elderly. Gastroenterol Clin
North Am 2001; 30:625–635.
6. Gavazzi G. Ageing and infection. Lancet Infect Dis 2002; 2:659–666.
7. Swaminathan B, Gerner-Smidt P. The epidemiology of human listeriosis.
Microbes Infect 2007; 9:1236–1243.
8. Djuretic T, Ryan MJ, Fleming DM, Wall PG. Infectious intestinal disease
in elderly people. Commun Dis Rep CDR Rev 1996; 6:R107–R112.
9. Garibaldi RA. Residential care and the elderly: the burden of infection.
J Hosp Infect 1999; 43:S9–S18.
10. Frenzen PD. Mortality due to gastroenteritis of unknown etiology in the
United States. J Infect Dis 2003; 187:441–452.
11. Frenzen PD. Deaths due to unknown foodborne agents. Emerg Infect
Dis 2004; 10:1536–1543.
12. Mishu B, Koehler J, Lee LA, et al. Outbreaks of Salmonella enteritidis
infections in the United States, 1985–1991. J Infect Dis 1994; 169:547–552.
13. Strausbaugh LJ, Sukumar SR, Joseph CL. Infectious disease outbreaks in
nursing homes: an unappreciated hazard for frail elderly persons. Clin
Infect Dis 2003; 36:870–876.
14. Garibaldi RA, Brodine S, Matsumiya S. Infections among patients in
nursing homes: policies, prevalence, problems. N Engl J Med 1981; 305:
731–735.
15. Levine WC, Smart JF, Archer DL, Bean NH, Tauxe RV. Foodborne disease outbreaks in nursing homes, 1975 through 1987. JAMA 1991; 266:
2105–2109.
16. Nelson JM, Bednarczyk R, Nadle J, et al. FoodNet survey of food use
and practices in long-term care facilities. J Food Prot 2008; 71:365–372.
17. Smith PW, Bennett G, Bradley S, et al. SHEA/APIC guideline: infection
prevention and control in the long-term care facility, July 2008. Infect
Control Hosp Epidemiol 2008; 29:785–814.
18. Green KY, Belliot G, Taylor JL, et al. A predominant role for Norwalklike viruses as agents of epidemic gastroenteritis in Maryland nursing
homes for the elderly. J Infect Dis 2002; 185:133–146.
19. Tu ET, Bull RA, Kim MJ, et al. Norovirus excretion in an aged-care
setting. J Clin Microbiol 2008; 46:2119–2121.
20. Svraka S, Duizer E, Vennema H, et al. Etiological role of viruses in
outbreaks of acute gastroenteritis in the Netherlands from 1994 through
2005. J Clin Microbiol 2007; 45:1389–1394.
21. Reiss G, Kunz P, Koin D, Keeffe EB. Escherichia coli O157:H7 infection
in nursing homes: review of literature and report of recent outbreak. J
Am Geriatr Soc 2006; 54:680–684.
22. Afza M, Hawker J, Thurston H, Gunn K, Orendi J. An outbreak of
Escherichia coli O157 gastroenteritis in a care home for the elderly. Epidemiol Infect 2006; 134:1276–1281.
23. American Medical Association; American Nurses Association–American
Nurses Foundation; Centers for Disease Control and Prevention; Center
for Food Safety and Applied Nutrition, Food and Drug Administration;
Food Safety and Inspection Service, US Department of Agriculture. Diagnosis and management of foodborne illnesses: a primer for physicians
and other health care professionals. MMWR Rep Recomm Rep 2004;
53:1–33.
24. Ryan MJ, Wall PG, Adak GK, Evans HS, Cowden JM. Outbreaks of
infectious intestinal disease in residential institutions in England and
Wales 1992–1994. J Infect 1997; 34:49–54.
25. Tallis G, Ng S, Ferreira C, Tan A, Griffith J. A nursing home outbreak
of Clostridium perfringens associated with pureed food. Aust N Z J Public
Health 1999; 23:421–423.
26. Sparks SG, Carman RJ, Sarker MR, McClane BA. Genotyping of enter-
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
otoxigenic Clostridium perfringens fecal isolates associated with antibioticassociated diarrhea and food poisoning in North America. J Clin Microbiol 2001; 39:883–888.
Trinh C, Prabhakar K. Diarrheal diseases in the elderly. Clin Geriatr Med
2007; 23:833–856, vii.
Bartlett JG, Gerding DN. Clinical recognition and diagnosis of Clostridium
difficile infection. Clin Infect Dis 2008; 46(Suppl 1):S12–S18.
Riggs MM, Sethi AK, Zabarsky TF, Eckstein EC, Jump RL, Donskey CJ.
Asymptomatic carriers are a potential source for transmission of epidemic
and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin Infect Dis 2007; 45:992–998.
Said MA, Perl TM, Sears CL. Healthcare epidemiology: gastrointestinal
flu: norovirus in health care and long-term care facilities. Clin Infect Dis
2008; 47:1202–1208.
Lopman BA, Reacher MH, Vipond IB, Sarangi J, Brown DW. Clinical
manifestation of norovirus gastroenteritis in health care settings. Clin
Infect Dis 2004; 39:318–324.
High KP, Bradley SF, Gravenstein S, et al. Clinical practice guideline for
the evaluation of fever and infection in older adult residents of longterm care facilities: 2008 update by the Infectious Diseases Society of
America. Clin Infect Dis 2009; 48:149–171.
Guerrant RL, Van Gilder T, Steiner TS, et al. Practice guidelines for the
management of infectious diarrhea. Clin Infect Dis 2001; 32:331–351.
Chen PL, Chang CM, Wu CJ, et al. Extraintestinal focal infections in
adults with nontyphoid Salmonella bacteraemia: predisposing factors and
clinical outcome. J Intern Med 2007; 261:91–100.
Vugia DJ, Samuel M, Farley MM, et al. Invasive Salmonella infections in
the United States, FoodNet, 1996–1999: incidence, serotype distribution,
and outcome. Clin Infect Dis 2004; 38:S149-S156.
Bos J, Smithee L, McClane B, et al. Fatal necrotizing colitis following a
foodborne outbreak of enterotoxigenic Clostridium perfringens type A
infection. Clin Infect Dis 2005; 40:e78–e83.
Kayser-Jones J, Schell ES, Porter C, Barbaccia JC, Shaw H. Factors contributing to dehydration in nursing homes: inadequate staffing and lack
of professional supervision. J Am Geriatr Soc 1999; 47:1187–1194.
Thielman NM, Guerrant RL. Clinical practice: acute infectious diarrhea.
N Engl J Med 2004; 350:38–47.
Gerding DN, Muto CA, Owens RC Jr. Measures to control and prevent
Clostridium difficile infection. Clin Infect Dis 2008; 46(Suppl 1):S43–S49.
Tarr PI, Gordon CA, Chandler WL. Shiga-toxin-producing Escherichia
coli and haemolytic uraemic syndrome. Lancet 2005; 365:1073–1086.
Heudorf U, Schulte D. Surveillance of nosocomial infections in a longterm care facility: incidence and risk factors [in German]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2009; 52:723–743.
Jacobson C, Strausbaugh LJ. Incidence and impact of infection in a
nursing home care unit. Am J Infect Control 1990; 18:151–159.
Scallan E, Majowicz SE, Hall G, et al. Prevalence of diarrhoea in the
community in Australia, Canada, Ireland, and the United States. Int
J Epidemiol 2005; 34:454–460.
McGeer A, Campbell B, Emori TG, et al. Definitions of infection for
surveillance in long-term care facilities. Am J Infect Control 1991; 19:
1–7.
Smith PW. Infection control in long-term care facilities. Infect Dis Clin
Pract 1998; 7:91–95.
Greig JD, Lee MB. Enteric outbreaks in long-term care facilities and
recommendations for prevention: a review. Epidemiol Infect 2009; 137:
145–155.
Lopman BA, Reacher M, Gallimore C, Adak GK, Gray JJ, Brown DW.
A summertime peak of “winter vomiting disease”: surveillance of noroviruses in England and Wales, 1995 to 2002. BMC Public Health
2003; 3:13.
Monitoring the incidence and causes of diseases potentially transmitted
by food in Australia: annual report of the Ozfoodnet Network, 2006.
Commun Dis Intell 2007; 31:345–365.
Krause G, Altmann D, Faensen D, et al. SurvNet electronic surveillance
system for infectious disease outbreaks, Germany. Emerg Infect Dis
2007; 13:1548–1555.
FOOD SAFETY • CID 2010:50 (1 February) • 403
50. van Duynhoven YT, de Jager CM, Kortbeek LM, et al. A one-year
intensified study of outbreaks of gastroenteritis in The Netherlands.
Epidemiol Infect 2005; 133:9–21.
51. Doyle TJ, Stark L, Hammond R, Hopkins RS. Outbreaks of noroviral gastroenteritis in Florida, 2006–2007. Epidemiol Infect 2008; 137:
617–625.
52. Tu ET, Bull RA, Greening GE, et al. Epidemics of gastroenteritis during
2006 were associated with the spread of norovirus GII.4 variants 2006a
and 2006b. Clin Infect Dis 2008; 46:413–420.
53. Friesma IH, Vennema H, Heijne JC, et al. Norovirus outbreaks in
nursing homes: the evaluation of infection control measures. Epidemiol
Infect 2009; 137:1722–1733.
54. Teunis PF, Moe CL, Liu P, et al. Norwalk virus: how infectious is it?
J Med Virol 2008; 80:1468–1476.
55. Koopmans M. Progress in understanding norovirus epidemiology. Curr
Opin Infect Dis 2008; 21:544–552.
56. Moshkowitz M, Ben Baruch E, Kline Z, Shimoni Z, Niven M, Konikoff
F. Risk factors for severity and relapse of pseudomembranous colitis
in an elderly population. Colorectal Dis 2006; 9:173–177.
57. Campbell RJ, Giljahn L, Machesky K, et al. Clostridium difficile infection
in Ohio hospitals and nursing homes during 2006. Infect Control Hosp
Epidemiol 2009; 30:526–533.
58. Laffan AM, Bellantoni MF, Greenough WB 3rd, Zenilman JM. Burden
of Clostridium difficile-associated diarrhea in a long-term care facility.
J Am Geriatr Soc 2006; 54:1068–1073.
59. Olsen SJ, DeBess EE, McGivern TE, et al. A nosocomial outbreak of
fluoroquinolone-resistant Salmonella infection. N Engl J Med 2001;
344:1572–1579.
60. White KE, Hedberg CW, Edmonson LM, Jones DB, Osterholm MT,
MacDonald KL. An outbreak of giardiasis in a nursing home with
evidence for multiple modes of transmission. J Infect Dis 1989; 160:
298–304.
61. Frank C, Buchholz U, Maass M, et al. Protracted outbreak of S. enteritidis PT 21c in a large Hamburg nursing home. BMC Public Health
2007; 7:243.
62. Li J, Birkhead GS, Strogatz DS, Coles FB. Impact of institution size,
staffing patterns, and infection control practices on communicable disease outbreaks in New York State nursing homes. Am J Epidemiol 1996;
143:1042–1049.
63. Milazzo A, Tribe IG, Ratcliff R, Doherty C, Higgins G, Givney R. A
large, prolonged outbreak of human calicivirus infection linked to an
aged-care facility. Commun Dis Intell 2002; 26:261–264.
64. Rodriguez EM, Parrott C, Rolka H, Monroe SS, Dwyer DM. An outbreak of viral gastroenteritis in a nursing home: importance of excluding
ill employees. Infect Control Hosp Epidemiol 1996; 17:587–592.
65. Multistate outbreak of Salmonella infections associated with peanut
butter and peanut butter-containing products–United States,
2008–2009. MMWR Morb Mortal Wkly Rep 2009; 58:85–90.
66. Angelillo IF, Viggiani NM, Greco RM, Rito D. HACCP and food hygiene in hospitals: knowledge, attitudes, and practices of food-services
staff in Calabria, Italy. Collaborative Group. Infect Control Hosp Epidemiol 2001; 22:363–369.
67. Sneed J, Strohbehn C, Gilmore SA,Mendonca A. Microbiological evaluation of foodservice contact surfaces in Iowa assisted-living facilities.
J Am Diet Assoc 2004; 104:1722–1724.
68. Layton MC, Calliste SG, Gomez TM, Patton C, Brooks S. A mixed
foodborne outbreak with Salmonella heidelberg and Campylobacter jejuni in a nursing home. Infect Control Hosp Epidemiol 1997; 18:
115–121.
69. Lynch MF, Tauxe RV, Hedberg CW. The growing burden of foodborne
outbreaks due to contaminated fresh produce: risks and opportunities.
Epidemiol Infect 2009; 137:307–315.
70. Little CL, Gillespie IA. Prepared salads and public health. J Appl Microbiol 2008; 105:1729–1743.
71. Engelhart S, Glasmacher A, Kaufmann F, Exner M. Protecting vul-
404 • CID 2010:50 (1 February) • FOOD SAFETY
72.
73.
74.
75.
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
nerable groups in the home: the interface between institutions and the
domestic setting. J Infect 2001; 43:57–59; discussion, 59–60.
Barker J, Vipond IB, Bloomfield SF. Effects of cleaning and disinfection
in reducing the spread of norovirus contamination via environmental
surfaces. J Hosp Infect 2004; 58:42–49.
McAnulty JM, Keene WE, Leland D, et al. Contaminated drinking
water in one town manifesting as an outbreak of cryptosporidiosis in
another. Epidemiol Infect 2000; 125:79–86.
Anon. OzFoodNet: enhancing foodborne disease surveillance across
Australia: quarterly report, January to March 2005. Commun Dis Intell
2005; 29:198–201.
Lefebvre SL, Reid-Smith R, Boerlin P, Weese JS. Evaluation of the risks
of shedding salmonellae and other potential pathogens by therapy dogs
fed raw diets in Ontario and Alberta. Zoonoses Public Health 2008;
55:470–480.
Lefebvre SL, Waltner-Toews D, Peregrine AS, et al. Prevalence of zoonotic agents in dogs visiting hospitalized people in Ontario: implications for infection control. J Hosp Infect 2006; 62:458–466.
Eastwood K, Osbourn M, Francis L, et al. Improving communicable
disease outbreak preparedness in residential aged care facilities using
an interventional interview strategy. Australas J Ageing 2008; 27:
143–149.
Jones TF, Bulens SN, Gettner S, et al. Use of stool collection kits
delivered to patients can improve confirmation of etiology in foodborne disease outbreaks. Clin Infect Dis 2004; 39:1454–1459.
Duizer E, Pielaat A, Vennema H, Kroneman A, Koopmans M. Probabilities in norovirus outbreak diagnosis. J Clin Virol 2007; 40:38–42.
Koo HL, Ajami NJ, Jiang ZD, et al. A nosocomial outbreak of norovirus
infection masquerading as Clostridium difficile infection. Clin Infect
Dis 2009; 48:e75–e77.
Hedberg CW, Palazzi-Churas KL, Radke VJ, Selman CA, Tauxe RV.
The use of clinical profiles in the investigation of foodborne outbreaks
in restaurants: United States, 1982–1997. Epidemiol Infect 2008; 136:
65–72.
Lopman BA, Adak GK, Reacher MH, Brown DW. Two epidemiologic
patterns of norovirus outbreaks: surveillance in England and wales,
1992–2000. Emerg Infect Dis 2003; 9:71–77.
Vanderpas J, Louis J, Reynders M, Mascart G, Vandenberg O. Mathematical model for the control of nosocomial norovirus. J Hosp Infect
2009; 71:214–222.
Standaert SM, Hutcheson RH, Schaffner W. Nosocomial transmission
of Salmonella gastroenteritis to laundry workers in a nursing home.
Infect Control Hosp Epidemiol 1994; 15:22–26.
Mody L, Langa KM, Saint S, Bradley SF. Preventing infections in nursing homes: a survey of infection control practices in southeast Michigan. Am J Infect Control 2005; 33:489–492.
Sehulster LM, Chinn RYW, Arduino MJ, et al. Guidelines for environmental infection control in health-care facilities. Recommendations
from CDC and the Healthcare Infection Control Practices Advisory
Committee (HICPAC). Chicago IL: American Society for Healthcare
Engineering/American Hospital Association, 2004.
Pittet D, Allegranzi B, Boyce J; the World Health Organization World
Alliance for Patient Safety First Global Patient Safety Challenge Core
Group of Experts. The World Health Organization Guidelines on Hand
Hygiene in Health Care and their consensus recommendations. Infect
Control Hosp Epidemiol 2009; 30:611–622.
Lages SL, Ramakrishnan MA, Goyal SM. In-vivo efficacy of hand sanitisers against feline calicivirus: a surrogate for norovirus. J Hosp Infect
2008; 68:159–163.
World Health Organization guidelines on hand hygiene in health care.
Geneva: The World Health Organization, 2009.
Smith A, Carusone SC, Loeb M. Hand hygiene practices of health care
workers in long-term care facilities. Am J Infect Control 2008; 36:
492–494.