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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 400 • CID 2010:50 (1 February) • FOOD SAFETY 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.