Bennett & Brachman's Hospital Infections, 5th Edition

21

Foodborne Disease Prevention in Healthcare Facilities

Margarita E. Villarino

William R. Jarvis

Foodborne disease outbreaks may occur when food becomes contaminated with pathogenic organisms or toxins. When these contaminants are bacterial pathogens, food mishandling may permit proliferation of these organisms and subsequently cause illness when ingested by susceptible persons. Food service departments at hospitals and other healthcare facilities, such as nursing homes, must cope with problems associated with handling large amounts of raw food, serving many meals throughout the day, preparing and handling food for a variety of diets, and delays in serving. These challenges in food preparation and delivery in healthcare facilities are compounded by the necessity of serving many patients who are at high risk of contracting foodborne disease. Because of these problems, prevention of foodborne disease should be a high priority in healthcare facilities.

Foodborne disease outbreaks related to food service in healthcare facilities may affect patients [1,2,3,4,5,6,7,8,9], personnel [10,11], and visitors [12,13] and may involve food prepared in the facility itself [1,2,4] as well as food prepared elsewhere but served in the healthcare facility [14,15]. Generally, hospitalized persons are more likely than nonhospitalized persons to acquire disease when exposed to foodborne agents and to develop serious side effects associated with such diseases. This is most likely due to host factors (e.g., malignancy, achlorhydria, advanced age, diabetes mellitus, and acquired immunodeficiency syndrome [AIDS]) or iatrogenic factors (e.g., use of antibiotics, oximmunosuppressive agents, or antacids and gastric surgery). Small inocula of enteric pathogens that might be innocuous to most healthy people can cause disease and even death in highly susceptible patients.

Secondary transmission of foodborne pathogens also may come about when patients or healthcare facility personnel become infected and, in turn, expose other patients or personnel as a consequence of poor personal hygiene or improper patient care techniques. Epidemics resulting from person-to-person transmission occur most often in nurseries, pediatric wards, or nursing homes, where fecal-oral spread may be facilitated by difficulties in maintaining good hygiene [16]. Secondary transmission may involve persons within the healthcare facility (patients, personnel, and visitors) and others (such as family members) outside the hospital setting. Foodborne disease outbreaks affecting large numbers of hospital personnel have led to staffing problems and may hinder delivery of optimal care [11,12]. With assumptions made about the values of indirect costs, the cost of a hospital-based outbreak has been estimated to be as high as $400,000 [17].

The problems of food or dietetic services in healthcare facilities generally parallel those of large restaurants and catering firms but may be even more complex [18]. Healthcare facilities' food services typically operate 12–18 hours daily, 7 days per week. Similar to large restaurants, these institutions purchase and rapidly process quantities of food

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that require large working surfaces, numerous utensils, and many working hands. They also must adhere to tight schedules, rapidly preparing and storing a large variety of foods. In addition, food services in such facilities have unique problems created by the need for a wide assortment of special diets, including enteral feedings. Meals and supplemental feedings must be provided from a central kitchen and sometimes from decentralized kitchens on wards. Finally, food often must be transported from a central preparation area throughout the institution. If food is not held at appropriate temperatures, delays between preparation and service present opportunities for proliferation of foodborne pathogens.

Epidemiologic Aspects of Foodborne Diseases

The epidemiology of foodborne disease outbreaks in the United Kingdom, Australia, and the United States has been reviewed extensively elsewhere [19,20,21,22]. In Scotland, during the 9-year period from 1978 to 1987, some 48 foodborne outbreaks were reported from hospitals, compared with 50 outbreaks during the previous 4 years (1973 to 1977) [19]. The decline in the overall incidence of food-poisoning outbreaks was attributed to an increased recognition by dietary departments of the principles of food temperature control. Reductions were seen in the number of outbreaks caused by Clostridium perfringens and Staphylococcus species while the number of outbreaks of salmonellosis rose. The average number of persons affected per outbreak of salmonellosis increased from 36 in 1973 to 81 in 1987. In contrast, in England and Wales during 1978 to 1987, a total of 248 outbreaks of salmonellosis was reported in hospitals compared with 522 outbreaks reported during 1968 to 1977 [20]. This decline might have been a result of improved food-handling practices; environmental health officers in the United Kingdom have expanded the monitoring of hospital food service departments since 1977.

In the United States, from all foodborne outbreaks reported to the Centers for Disease Control and Prevention (CDC) during 1975 to 1992, the bacterial agents most frequently identified were Salmonella, Staphylococcus aureus, C. botulinum, and C. perfringens (Table 21-1). In healthcare facilities, Salmonella and C. perfringens are more significant than C. botulinum and S. aureus. Transmission of all four of these common foodborne bacterial pathogens was typically associated with certain food vehicles; likely sources of contamination varied for the different pathogens (Table 21-1). The number of reported foodborne outbreaks in known locations during 1975 to 1992 and the associated episodes and deaths in hospitals, nursing homes, and other known locations are shown in Table 21-2. Of these, hospitals and nursing homes accounted for 3.3% of the outbreaks, 4.8% of the episodes, and 28.9% of the deaths.

Only 123 foodborne disease outbreaks in hospitals were reported during this 17-year period. However, because foodborne disease outbreaks must be recognized, investigated, and reported to state health departments before being reported to the CDC, it is highly likely that foodborne outbreaks are underreported nationally. During 1975 to 1992, reported outbreaks in hospitals and nursing homes were significantly more likely to be caused by bacterial agents (n = 143) than by viruses, parasites, or chemicals (n = 16) (Table 21-3). Nonetheless, viral [13,23] and parasitic [24] foodborne outbreaks have been reported from healthcare facilities.

It is important to investigate foodborne disease outbreaks in hospitals, to define sources, modes of spread, and

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methods for prevention and control of nosocomial foodborne disease. Of 233 hospital-based outbreaks of infection investigated by the CDC from 1956 to 1979, gastroenteritis was the most common cause; typical organisms were Salmonella spp. and enteropathogenic Escherichia coli [25]. In adult patients, contaminated food vehicles were frequently implicated in salmonellosis outbreaks. Outbreaks attributed to cross-infection, such as gastroenteritis in nurseries due to E. coli or Salmonella, were more difficult to recognize and control than were foodborne outbreaks. Most cross-infection outbreaks were recognized because the infecting pathogen was unusual or distinguished by a unique antimicrobial resistance pattern. In England and Wales from 1978 to 1987, 71 of 235 (30%) reported outbreaks of salmonellosis in hospitals were attributed to cross-infection, compared with 57 (24%) outbreaks attributed to foodborne transmission [20]. However, foodborne outbreaks affected more persons (n = 1, 862) than did those due to cross-infection (n = 558). Since 1979, CDC investigation of such outbreaks has been uncommon.

In the United States during 1975 to 1992, 336 reported deaths were associated with foodborne disease outbreaks with known place of preparation (Table 21-4). Eighty-six (26%) took place in nursing homes and 11 (3%)

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in hospitals. Of the 97 deaths in hospitals and nursing homes, 72 (74%) were due to Salmonella. In the United States, isolation rates of Salmonella serotype enteritidis have been increasing since 1976 [26]. From 1985 to 1991, 380 S. enteritidis outbreaks were reported to the CDC, involving 13,056 ill persons, 1,512 hospitalizations, and 50 deaths [27]. Of these outbreaks, 59 (16%) were in nursing homes or hospitals, accounting for 1,512 illnesses (12%) and 45 (90%) deaths. Of 167 outbreaks in which a food vehicle was identified, 137 (82%) implicated fresh eggs in the shell. During this same period, 60% (9/15) reported nursing home outbreaks with a known vehicle implicated dishes containing shell eggs. Four (8%) of the 49 S. enteritidis outbreaks reported from January to October 31, 1990, occurred in hospitals or nursing homes, compared with 26% (20/77) of such outbreaks in 1989 [28]. This decline in hospital- and nursing home-associated S. enteritidis outbreaks may reflect efforts to improve food safety in these settings (e.g., by using pasteurized eggs).

Surveillance data can help elucidate the relative importance of various factors that contribute to the occurrence of foodborne disease outbreaks. During 1975–1992, food-handling errors were noted in 212 reported foodborne outbreaks in hospitals or nursing homes. Holding food at improper temperatures was the most common such error. Other important errors included inadequate cooking, poor personal hygiene of food handlers, use of food from unsafe sources, and use of contaminated equipment. Training personnel in proper food-handling practices can eliminate these errors and prevent outbreaks.

Food served from a healthcare facility kitchen can be contaminated before, during, or after preparation. When purchased, raw poultry and red meat might already be contaminated with organisms (e.g., Salmonella, C. perfringens, Campylobacter jejuni or, more rarely, E. coli 0157:H7). In a 1988 survey of broiler chicken specimens from 195 poultry-processing plants, the prevalence of Salmonella spp. contamination was 21% of 15,391 specimens [29]. Campylobacter jejuni typically is present in >50% of poultry carcasses at the point of sale [30]. Raw fish and shellfish can be contaminated with such pathogens as Vibrio parahaemolyticus, C. perfringens, and V. vulnificus. Shell eggs may be contaminated with S. enteritidis, either externally through fecal contamination or internally through trans-ovarian transmission [31,32]. During processing, food also may become contaminated with organisms through contact with dirty hands, infected aerosols spread by coughing or sneezing, and contaminated equipment, such as meat slicers and working surfaces [33]. Finally, bacteria may grow while food is stored (e.g., when cooked foods are stored in direct contact with raw foods or when foods are held at inadequate temperatures). Listeria monocytogenes can survive and grow in food even with adequate refrigeration [34].

Foods and the Immunocompromised Host

Patients in healthcare facilities are more susceptible to certain foodborne infections than the general population. The elderly, the immunosuppressed, and persons with chronic underlying diseases are generally at higher risk of infection and associated morbidity and mortality. In particular, outbreaks of foodborne disease in nursing homes can be associated with serious morbidity and mortality; therefore, efforts to provide the safest possible food to the elderly in nursing homes should be maximized.

Among persons in hospitals and nursing homes, increased susceptibility to foodborne infections may be caused by associated physiologic changes or therapy of underlying disease. Although the gastrointestinal tract is normally resistant to colonization, this resistance can be substantially diminished by antimicrobial therapy, mucositis from cancer treatments, decreased stomach acidity,

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impaired intestinal motility, and diminished mucosal, humoral, and cellular immunity. Even in numbers smaller than the usual infective dose, ingested microorganisms may cause systemic infection in these patients.

Because E. coli, Klebsiella spp., and Pseudomonas aeru-ginosa can contaminate fresh fruits, salads, and vegetables [35], these foods should not be served to neutropenic patients [36]. Another potential contaminant of fresh vegetables is L. monocytogenes, a gram-positive bacterium that particularly affects the elderly, pregnant women, and the severely immunosuppressed [34]. In one L. monocytogenes outbreak involving 20 patients from eight hospitals, raw vegetables served in hospital meals may have been contaminated; 10 (50%) of these patients were immunosuppressed [37]. Dairy products and any raw food of animal origin also may be contaminated with Listeria, Salmonella, or E. coli 0157:H7. Outbreaks ofE. coli 0157:H7 and Salmonella in nursing homes have been particularly devastating. In two such E. coli 0157:H7 outbreaks, 15 deaths occurred [1,38]. In an outbreak of S. enteritidisin a nursing home, 25/104 affected patients died [39].

Human immunodeficiency virus (HIV)–infected persons are at increased risk of infection with bacterial foodborne pathogens (see Chapter 42). Among persons with AIDS, the reported incidence of laboratory-confirmed salmonellosis was 20 times that reported for persons without AIDS [40]. Compared with immunocompetent persons, those with AIDS and salmonellosis are more likely to have initial and recurrent bloodstream infections [41,42]. The reported incidence of campylobacteriosis among persons with AIDS in Los Angeles County between 1983 and 1987 was 39 times higher than the rate in the general population [43]. Similarly, the incidence of listeriosis among persons with HIV infection is estimated to be 60 times that of the general population; among persons with AIDS, the relative risk is more than 140 times greater [44]. Ingestion of contaminated foods is likely to be an important source of enteric infections in persons with AIDS. All immunocompetent persons should cook raw foods of animal origin thoroughly and avoid eating raw shellfish, raw milk, raw meat, and raw eggs [45,46,47]. Dietary departments in health facilities should follow these recommendations for all hospitalized patients, particularly those who are immunocompromised.

Enteral feeding solutions are used frequently to provide nutritional support to seriously ill patients with a functional digestive tract. These solutions often are prepared in food service departments. Enteral feedings contaminated by bacteria can cause severe healthcare-associated infections (HAIs) [48,49,50]; therefore, infection control practices for their preparation and administration should be reviewed and implemented [51]. A high incidence of microbial contamination of enteral nutrition, including powdered feeds requiring reconstitution, has been described [47,48,50,52,53,54,55,56]. Contamination also can occur during assembly of a delivery system on the ward [57] or by bacteria colonizing the nasogastric tube or ascending from the patient's gut [58].

Factors contributing to the microbial contamination of enteral feeding solutions include the composition of the feeding solution, the lack of preservatives, the number of manipulations involved in the feeding process, the mode and duration of administration, and the timing of sampling [50]. Enterobacter sakazakii outbreaks in neonates have been traced to both extrinsically and intrinsically contaminated powdered infant formula [49,50,54]. Although contamination is most frequently the result of manipulation during preparation, adherence to appropriate food-handling practices is essential to minimize bacterial contamination during preparation and administration and bacterial growth during storage. Public health authorities' monitoring of recommended manufacturing procedures and of the regulations governing the bacterial content of powdered feeds has been suggested [50].

Prevention of Foodborne Transmission in Healthcare Facilities

Requirements and recommendations concerning food services are provided to hospitals and other healthcare facilities from the Joint Commission on Accreditation of Healthcare Organizations (JCAHO) and the Association for Professionals in Infection Control and Epidemiology, Inc. (APIC) (Table 21-5). Responsibilities for the inspection and certification of food service facilities in healthcare organizations vary by state. Accreditation by JCAHO does not ensure regular food service inspection or food handler training. The infection control committee of each healthcare facility has an important responsibility in the prevention of foodborne disease. This committee is responsible for cooperating with the food services department in developing written policies and procedures and for reviewing these policies at least annually [59].

To prevent foodborne disease, both the JCAHO requirements and the APIC recommendations focus prevention efforts by hospitals and other healthcare institutions in two areas: food hygiene (i.e., food preparation, storage, and distribution) and health and hygiene of food service personnel. Both of these areas need to be reinforced by specific training of food service workers in the basic principles of food safety. New personnel should receive prompt training in good food-handling practices. Food service personnel from all work shifts should receive regular in-service training stressing the prevention of foodborne diseases and appropriate food-handling practices.

General approaches to limiting contamination and destroying or inhibiting the growth of potential foodborne pathogens have been reviewed elsewhere [60,61]. Healthcare facilities should consult a dietitian with special training in food service sanitation, sanitarian, or both about

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formulating and monitoring food-handling operations and procedures. In addition, local or state health departments should be consulted about regulations and standards concerning food service personnel, food sanitation, and waste disposal.

Food Hygiene

Two factors are critical in preventing bacterial foodborne disease: holding food at appropriate temperatures (that is, either >60°C [140°F] or <5°C [41°F]) and avoiding cross-contamination of cooked food by raw food or by infected food-handling personnel [62]. In addition, pasteurized milk and pasteurized egg products should be used in place of raw milk and shell eggs. Food must be purchased from reliable sources; commercially filled unopened packages should be used when possible. Microbial contaminants on some raw foods may be kept from multiplying during processing by proper storage, thawing meat products in refrigerators (<5°C [41°F]), and adequate heat treatment. Because work surfaces, knives, slicers, pots, pans, and other kitchen equipment can convey bacteria from contaminated food to other foods, food contact surfaces of equipment and utensils must be cleaned and decontaminated between preparation of food items. Items such as slicers must be easy to disassemble to ensure proper cleaning.

Workers should be trained to operate and maintain equipment properly. Hand hygiene by food service personnel is an essential component of food hygiene. All workers must thoroughly wash their hands after handling raw poultry, meat, fish, fruits, and vegetables; after contact with unclean equipment and work surfaces, soiled clothing, washrags, and other items; and, most important, after using the bathroom. Spilled food should be cleaned up immediately. Equipment and the kitchen layout should be designed to promote rapid processing to minimize chances for cross-contamination; to avoid producing aerosols, sprays, or splashing during processing; and to facilitate cleaning and sanitizing operations [61]. Contamination by insects, rodents, sewage backflow, and drips must be prevented by screening, proper storage (including separating raw meat from processed foods), and adequate plumbing. Garbage from hospital kitchens and wards should be enclosed to protect it from insects and rodents and transported or disposed of in a sanitary manner, according to state and local regulations.

Cross-contamination can be minimized by adopting standard techniques for cleaning work surfaces and kitchen utensils and by ensuring that raw foods are processed in areas of the kitchen and on work surfaces that are not subsequently used for cooked foods. Separate cutting boards may not be required when the boards used are nonabsorbent and can be cleaned and sanitized adequately between uses for different food categories. Dishwashing- and utensil-washing equipment and techniques that sanitize service ware and prevent recontamination should be used to ensure sanitary provision of food. Disposable containers and utensils should be properly discarded after one use. Food

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hygiene procedures should be reviewed periodically and whenever physical changes in the kitchen are made or new equipment is put into use.

Foodborne disease outbreaks have resulted from poor planning and a lack of understanding of appropriate food-handling practices (e.g., not allowing enough time before cooking for poultry to thaw or assuming that thawing is complete). This problem can result in undercooking and can be compounded by keeping undercooked food in the oven after the heat has been shut off, providing ideal incubation conditions for bacteria that survived the initial cooking. Potentially harmful bacteria in foods must be destroyed by thorough cooking or reheating to the proper internal temperatures for the appropriate length of time. For example, meat and poultry should generally be cooked to heat all parts of the food to 68°C (155°F) for 15 seconds [62]. Internal meat temperatures should be measured by bayonet-type thermometers. Periodically, the internal temperature of foods in serving lines should be checked.

A common error resulting in foodborne disease outbreaks is storage of food at inappropriate temperatures; this error is most often identified in staphylococcal food poisoning outbreaks and in short- and long-incubation Bacillus cereus, C. perfringens, and Salmonella spp. outbreaks. In some outbreaks, even when refrigerator temperatures have been adequate, the center temperature of perishable foods was warm enough to permit bacteria to grow or toxin to be produced because the foods were in inadequate holding containers. When cooked foods are kept at room temperature (or are refrigerated in large quantities) for a period of 4 hours, certain pathogens remaining in the food may be able to multiply to sufficient levels or produce enough toxin to cause disease. Cooked foods have been kept too long at room temperature because of inadequate refrigerator space and failure to perceive the importance of refrigeration. In general, cooked food that requires refrigeration should be cooled from 60°C (140°F) to 21°C (70°F) within 2 hours and from 21°C (70°F) to ≤5°C (41°F) within 4 hours; storage temperature should not exceed 5°C (41°F). Food should be placed in shallow containers so that the food is no more than 4 inches deep.

Storage is a particular problem when food must be delivered from a central kitchen to peripheral areas of the healthcare facility or other buildings either by truck or on food carts. Procedures for transporting food must include a way to keep hot foods hot and cold foods cold. Thermometers used to measure holding temperatures should be standard equipment in such conveyances. Standby equipment should be on hand or alternative plans formulated to handle emergency conditions arising from equipment failure. Food delivered to a kitchen or ward should be properly stored to prevent growth of bacteria, and it should be distributed with minimum handling by ward personnel. In the event that ward personnel must handle food, they should be carefully supervised to ensure that the same high standards required of kitchen personnel are maintained.

In the past, problems have arisen because of preferences for raw or undercooked foods. Substitution of pasteurized egg products for fresh eggs in nursing homes and hospitals is strongly recommended. Several outbreaks have been traced to blenders used for both raw eggs and to pureed foods. Requiring the use of separate blenders to scramble eggs and to puree cooked foods would reduce the risk of cross-contamination. Routine disassembly and sanitation of blenders after blending raw eggs also is important. Avoiding consumption of raw milk is important in preventing outbreaks caused by Salmonella spp. and C. jejuni.

Health and Hygiene of Food Service Personnel

Supervision of food service personnel requires attention to work habits, personal hygiene, and health. The hands of food service personnel may be colonized or infected with microorganisms, such as S. aureus, or may become contaminated by organisms from raw foods (Salmonella spp., C. jejuni, or C. perfringens) or human excreta (Salmonella spp.,Shigella spp., Norovirus, or hepatitis A virus). These organisms may then contaminate food. Although thorough cooking of food just before consumption will eradicate the risk of many illnesses, staphylococcal food poisoning will not be eliminated because staphylococcal enterotoxins are heat stable.

Hand hygiene facilities should be conveniently located to permit use by employees in food preparation and utensil-washing areas and in or immediately adjacent to toilet facilities. Each hand hygiene facility should be provided a continuous supply of waterless agents, or hand-washing facilities should have clean water; a supply of hand-cleaning liquid, powder, or bar soap; and individual sanitary towels from a continuous towel system supplied with a clean towel or a heated-air hand-drying device. Common hand-drying towels are prohibited. If disposable towels are used, a waste receptacle should be located next to the hand-washing facility.

Various strategies have been used to monitor the health of food service personnel, including periodic stool examinations for certain pathogens. However, such measures may not be effective. One stool culture is not sufficient to detect the small number of organisms in the stool of an infected person who does not have diarrhea. For example, one rectal swab detected only 47% of chronic Salmonella serotype Derby carriers, and seven consecutive daily swabs were needed to detect 95% of known carriers [63]. Such extensive culturing is impractical and costly. Periodic stool cultures of food handlers may miss persons who excrete organisms intermittently or who become infected during the interval between cultures. In Jordan, a large outbreak of nosocomial salmonellosis

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caused by an asymptomatic infected food handler occurred despite the institution of routine quarterly stool cultures for kitchen employees [64].

In addition, cultures of nose and throat secretions and feces may reveal potential foodborne pathogens, such as S. aureus, but this carriage may be of no danger to others: most S. aureus carriers do not usually disseminate the organisms. Laboratory monitoring of food handlers actually could be counterproductive by instilling a false sense of security. Negative culture reports could be interpreted by the employee to indicate that he or she is not capable of contaminating food. From the management standpoint, laboratory monitoring of food handlers may convey the false impression that food safety is being enhanced. Thus, routine laboratory testing of food service personnel should not be performed [65].

The proper approach to managing the personal aspects of hygiene is to establish and pursue a policy of training food service managers and workers. The healthcare facility infection control committee should ensure a program comprising a comprehensive training course in the appropriate languages for all new employees at the onset of employment and in-service training at regular intervals for all food service personnel (see Chapter 4). As appropriate to the workers' level of responsibility, such courses should cover the basic principles of personal hygiene, emphasizing the need for good hand hygiene practices; the importance of informing supervisors of acute intestinal diseases, boils, and any skin infection, particularly on the fingers and hands; properly inspecting, handling, preparing, serving, and storing food; the proper cleaning and safe operation of equipment; general food service sanitation safety; the proper method of waste disposal; portion control; writing modified diets using the diet manual or handbook; diet instruction; and the recording of pertinent dietetic information in each patient's medical record [66]. In addition to training, a liberal medical leave policy will ensure that employees are not penalized financially when they report that they are ill.

Surveillance and Control

The responsibility for preventing, detecting, and investigating foodborne disease outbreaks rests with the healthcare facility infection control committee and the infection control professional (see Chapter 2). They can begin by carefully reviewing the results of recent hospital kitchen inspections by the local health department and the food safety training program currently in place for kitchen staff. In addition, they can ensure that, whenever possible, pasteurized eggs are used instead of shell eggs and verify that the risks of using a common blender to mix raw eggs and other foods are well understood by all employees. It is important that the infection control committee meet with the kitchen staff and communicate to them that food safety is of the highest priority.

Surveillance for illness among the kitchen staff may prevent some foodborne outbreaks and also may provide an early warning when such an outbreak occurs because they, too, eat the food. A monitoring procedure should be established to ensure that food service personnel are free from open skin lesions. Designated infection control staff should be informed of acute illnesses among food service workers that could potentially be transmitted by food. It is important to create an atmosphere that does not penalize food handlers for reporting illness. Any work restriction policy should encourage personnel to report their illnesses or exposures and not penalize them with loss of wages, benefits, or job status [67].

Appropriate culture specimens should be obtained and processed during such illnesses. In episodes of acute diarrhea, rectal swab or fecal specimens promptly inoculated onto appropriate laboratory media are recommended. Workers should not be permitted to return to their assigned jobs until their diarrhea has resolved and two stool cultures obtained ≥24 hours apart show negative results (see Chapter 33). If antimicrobial agents are used, follow-up cultures should be obtained after treatment has been completed. Personnel with boils, open sores, or cellulitis of the fingers, hands, and face should be excluded until they are adequately treated. The infection control professional's judgment should prevail in deciding when the worker can return to work.

Routine surveillance of patients and employees should detect any episodes of gastrointestinal disease related to the healthcare institution's food service. Temporal clustering of such episodes should alert the infection control personnel to the possibility of an outbreak. Promptly investigating and reporting outbreaks to the appropriate health authorities is essential to identifying and correcting food-handling error(s), preventing additional primary and secondary transmission of disease, and limiting outbreaks caused by commercially distributed foods.

References

1. Carter AO, Borczyk AA, Carlson JAK, et al. A severe outbreak of Escherichia coli0157:H7-associated hemorrhagic colitis in a nursing home. N Engl J Med 1987;317:1496–1500.
2. Lynch M, Painter J, Woodruff R, et al. Surveillance for foodborne-disease outbreaks—United States, 1998–2002. MMWR Surveill Summ2006;55:1–42.
3. Giannella RA, Brasile L. A hospital foodborne outbreak of diarrhea caused by Bacillus cereus:clinical, epidemiologic, and microbiologic studies. J Infect Dis 1979;139:366–70.
4. Telzak EE, Budnick LD, Greenberg MSZ, et al. A nosocomial outbreak of Salmonella enteritidisinfection due to the consumption of raw eggs. N Engl J Med 1990;323:394–97.
5. Thomas M, Noah ND. Hospital outbreak of Clostridium perfringensfood poisoning. Lancet 1977;1:1046–48.
6. Yamagishi T, Sakamoto K, Sakurai S, et al. A nosocomial outbreak of food poisoning caused by enterotoxigenic Clostridium perfringens. Microbiol Immunol1983;27:291–96.
7. Pavia AT, Nichols CR, Green DP, et al. Hemolytic-uremic syndrome during an outbreak of Escherichia coli0157:H7 infections in institutions for the mentally retarded: Clinical and epidemiologic observations. J Pediatr 1990;116:544–51.

P.327

8. Standaert SM, Hutcheson RH, Schaffner W. Nosocomial transmission of Salmonellagastroenteritis to laundry workers in a nursing home. Infect Control Hosp Epidemiol1994;15:22–26.
9. Holtby I, Stendon P. Food poisoning in two homes for the elderly. Communicable Dis Rep1992;2:R125–26.
10. Khatib R, Naber M, Shellum N, et al. A common source outbreak of gastroenteritis in a teaching hospital. Infect Control Hosp Epidemiol1994;15:534–35.
11. Centers for Disease Control and Prevention. Shigellosis in children's hospital—Pennsylvania. MMWR1979;28:498–99.
12. Centers for Disease Control and Prevention. Hospital-associated outbreak of Shigella dysenteriaetype 2—Maryland. MMWR 1983;32:250–52.
13. Meyers JD, Frederic JR, Tithen WS, Bryan JA. Foodborne hepatitis A in a general hospital: Epidemiologic study of an outbreak attributed to sandwiches. JAMA1975;231:1049–53.
14. Centers for Disease Control and Prevention. Multistate outbreak of salmonellosis caused by precooked roast beef. MMWR1981;30:391–92.
15. Spitalny KC, Okowitz EN, Vogt RL. Salmonellosis outbreaks at a Vermont hospital. South Med J1984;77:168–72.
16. Linnemann CC Jr., Cannon CG, Stancek JL, et al. Prolonged hospital epidemic of salmonellosis: Use of trimethoprim-sulfamethoxazole for control. Infect Control Hosp Epidemiol1985;6:221–25.
17. Yule BF, MacLeod AF, Sharp JCM, Forbes GI. Costing of a hospital-based outbreak of poultry-borne salmonellosis. Epidemiol Infect1988;100:35–42.
18. No author. Food poisoning in hospitals [editorial]. Lancet1980;1:576.
19. Collier PW, Sharp JC, MacLeod AF, et al. Food poisoning in hospitals in Scotland, 1978–1987. Epidemiol Infect1988;101:661–67.
20. Joseph CA, Palmer SR. Outbreaks of Salmonellainfection in hospitals in England and Wales, 1978–1987. Br Med J 1989;298:1161–64.
21. Dalton CB, Gregory J, Kirk MD, et al. Foodborne disease outbreaks in Australia, 1995 to 2000. Commun Dis Intell. 2004;28:211–24.
22. Bean NH, Griffin PM, Goulding JS, Ivey CB. Foodborne disease outbreaks in the United States, 1973–1987. J Food Protect1990;53:711–30.
23. Lopman BA, Reacher MH, Vipond IB, et al. Clinical manifestation of norovirus gastroenteritis in health care settings. Clin Infect Dis2004;39:318–24. Epub 2004 Jul 9.
24. Levine WC, Smart JF, Archer DL, et al. Foodborne disease outbreaks in nursing homes, 1975 to 1987. JAMA1991;266:2105–09.
25. Stamm WE, Weinstein RA, Dixon RE. Comparison of endemic and epidemic nosocomial infections. Am J Med1981;70:393–97.
26. Tauxe RV. Salmonella:A postmodern pathogen. J Food Protect 1991;54:563–68.
27. Mishu B, Koehler J, Lee LA, et al. Outbreaks of Salmonella enteritidisinfections in the United States, 1985–1991. J Infect Dis 1994;169:547–52.
28. CDC. Update: Salmonella enteritidisinfections and shell eggs—United States, 1990. MMWR 1990;39:909–12.
29. Lee L, Threatt VL, Puhr ND, et al. Antimicrobial-resistant Salmonellaspp. isolated from healthy broiler chickens after slaughter. J Am Vet Med Assoc 1993;202:752–55.
30. Tauxe RV. Epidemiology of Campylobacter jejuniinfections in the United States and other industrialized nations. In: Nachamkin T, Blaser MJ, Tompkins LS, eds. Campylobacter jejuni: Current status and future trends. Washington, DC: American Society for Microbiology, 1992:9–19.
31. St. Louis ME, Morse DL, Potter ME, et al. The emergence of grade A eggs as a major source of Salmonella enteritidis infection. JAMA1988;259:2103–07.
32. Gast RK, Beard CW. Production of Salmonella enteritidiscontaminated eggs by experimentally infected hens. Avian Dis 1990;34:438–46.
33. Jordan MC, Powell KE, Corothers TE, Murray RJ. Salmonellosis among restaurant patrons: The incisive role of a meat slicer. Am J Public Health1973;63:982–85.
34. Schucat A, Swaminathan B, Broome C. Epidemiology of human listeriosis. Clin Microbiol Rev1991;4:169–83.
35. Shooter RA, Cooke EM, Faiers MC, et al. Isolation of Escherichia coli, Pseudomonas aeruginosa,and Klebsiella from food in hospitals, canteens, and schools. Lancet1971;2:390–92.
36. Remington JS, Schimpff SC. Please don't eat the salads. N Engl J Med1981;304:433–35.
37. Ho JL, Shands KN, Fredland G, et al. An outbreak of type 4b Listeria monocytogenesinfection involving patients from eight Boston hospitals. Arch Intern Med 1986;146:520–24.
38. Ryan CA, Tauxe RV, Hosek GW, et al. Escherichia coli0157:117 diarrhea in a nursing home: Clinical, epidemiological, and pathological findings. J Infect Dis 1986;154:631–38.
39. Centers for Disease Control and Prevention. Salmonellosis—Baltimore, Maryland. MMWR1970;19:340.
40. Celum CL, Chaisson RE, Rutherford GW, et al. Incidence of salmonellosis in patients with AIDS. J Infect Dis1987;156:998–1002.
41. Gruenewald R, Blum S, Chan J. Relationship between human immunodeficiency virus infection and salmonellosis in 20- to 59-year-old residents of New York City. Clin Infect Dis1994;18:358–63.
42. Sperber SJ, Schleupner CJ. Salmonellosis during infections with human immunodeficiency virus. Rev Infect Dis1987;9:925–34.
43. Sorvillo FJ, Lieb LE, Waterman SH. Incidence of campylobacteriosis among patients with AIDS in Los Angeles County. J Acquir Immune Defic Syndr1991;4:598–602.
44. Jurado RL, Farley MM, Pereira E, et al. Increased risk of meningitis and bacteremia due to Listeria monocytogenesin patients with human immunodeficiency virus infection.Clin Infect Dis 1993;17:224–27.
45. Archer DL. Food counseling for persons infected with HIV: Strategy for defensive living. Public Health Rep1989;104:196–98.
46. Griffin PM, Tauxe RV. Food counseling for patients with AIDS [Letter]. J lnfect Dis1988;158:668.
47. Angulo FK, Swerdlow DL. Bacterial enteric infections in persons infected with human immunodeficiency virus. Clin Infect Dis1995;21 (suppl 1):S84–93.
48. Thum J, Crossley K, Gerdts A, et al. Enteral hyperalimentation as a source of nosocomial infection. J Hosp Infect1990;15:203–17.
49. Mathus-Vliegen EM, Bredius MW, Binnekade JM. Analysis of sites of bacterial contamination in an enteral feeding system. J Parenter Enteral Nutr2006;30:519–25.
50. Centers for Disease Control and Prevention (CDC). Enterobacter sakazakiiinfections associated with the use of powdered infant formula—Tennessee, 2001. MMWR Morb Mortal Wkly Rep. 2002;51:297–300
51. Levy J. Enteral nutrition: An increasingly recognized cause of nosocomial bloodstream infection. Infect Control Hosp Epidemiol1989;10:395–97.
52. Anderson KR, Norris DJ, Godfrey LB, et al. Bacterial contamination of tube feeding formula. J Parenter Enter Nutr1984;8:673–78.
53. Patchell CJ, Anderton A, MacDonald A, et al. Bacterial contamination of enteral feeds. Arch Dis Child1994;70:327–30.
54. Simmons BP, Gelfand MS, Haas M, et al. Enterobacter sakazakii infections in neonates associated with intrinsic contamination of a powdered infant formula. Infect Control Hosp Epidemiol1989;10:398–401.
55. Bowen AB, Braden CR. Invasive Enterobacter sakazakiidisease in infants. Emerg Infect Dis 2006;12:1185–89.
56. U.S. Food and Drug Administration. Bacterial contamination of enteral formula products.Washington, DC: Public Health Service, Food and Drug Administration Bulletin, 1988.
57. Anderton A, Aidov KE. The effect of handling procedures on microbial contamination of enteral feeds. J Hosp Infect1988;11:364–72.
58. de Leeuw I, Van Alsenoy L. Bacterial contamination of the feeding bag during catheter jejunostomy: Exogenous or endogenous origin? J Parenter Enter Nutr1984;9:591–92.
59. Joint Commission on Accreditation of Healthcare Organizations. Accreditation manual for hospitals, 1991.Chicago: Joint Commission on Accreditation of Healthcare Organizations, 1990.
60. Bryan FL. Prevention of foodborne diseases in food-service establishments. J Environ Health1979;41:198–206.
61. Bryan FL. Factors that contribute to outbreaks of foodborne disease. J Food Protect1978;41:816–27.

P.328

62. U.S. Department of Health and Human Services. Food code, 1993.Washington, DC: Public Health Service, Food and Drug Administration, 1993.
63. McCall CE, Martin WT, Boring JR. Efficiency of cultures of rectal swabs and faecal specimens in detecting Salmonellacarriers: Correlation with number of salmonellas excreted. J Hyg (London) 1966;64:261–69.
64. Khuri-Bulos NA, Khalaf MA, Shehabi A, Shami K. Foodhandler-associated Salmonellaoutbreak in a university hospital despite routine surveillance cultures of kitchen employees. Infect Control Hosp Epidemiol 1994;15:311–14.
65. World Health Organization. Health surveillance and management procedures for foodhandling personnel.Geneva, Switzerland: World Health Organization, 1989. (WHO Technical Report Series, no. 785.)
66. Association for Practitioners in Infection Control. APIC infection control and applied epidemiology: Principles and practice.St. Louis: Mosby-Year Book, 1996.
67. Bolyard EA, Tablan OC, Williams WW, et al. Guideline for infection control in healthcare personnel, 1998. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol1998;19:407–63.