Raw and Undercooked : A Danger of Salmonellosis

C.-T. Jordan Lin, Roberta A. Morales, and Katherine Ralston (202) 842-7600 (919) 515-4670 (202) 501-6766

icrobial pathogens of the CDC, the proportion of cases of sal- way in the public and private sec- genus are monellosis due to Salmonella enteri- tors to prevent consumer exposure M among the leading causes tidis increased from 5 percent in to contaminated eggs and to educate of foodborne illness in the United 1976 to 26 percent in 1994 when consumers about safe practices for States. Between 696,000 and compared to all reported cases of preparation and consumption. 3,840,000 cases of foodborne salmo- salmonellosis reported to CDC. The However, our review of data from nellosis occur each year, causing CDC also reported that, between four recent surveys suggests some mild to acute gastrointestinal symp- 1985 and 1995, there were 582 consumers are still consuming raw toms, such as abdominal pain, fre- Salmonella enteritidis outbreaks (two or undercooked eggs. Thorough quent diarrhea, vomiting, fever, and or more people became ill from eat- of eggs until both white and chills. Infants, the elderly, and peo- ing the same food), which accounted are firm greatly reduces the ple with compromised immune sys- for 24,058 cases of illness, 2,290 hos- chances of human infection. Proper tems are particularly vulnerable, pitalizations, and 70 deaths. While refrigeration can prevent prolifera- and death from salmonellosis may many more people may have suf- tion of the pathogen in contami- occur in these high-risk population fered the illness than what the out- nated eggs. Thus, further improve- groups. These human illness cases break data suggest, few seek med- ments in egg production, handling, and deaths cost society between ical help, so large numbers of cases and preparation practices can $600 million and $3.5 billion each probably are not reported to the reduce the number of illnesses year in medical treatment, lost pro- CDC. caused by Salmonella enteritidis due ductivity, and loss of life. Raw or undercooked eggs and to the consumption of contaminated Since the mid-1980’s, Salmonella foods containing them have been eggs and the costs these cases enteritidis has been one of the most implicated in about 80 percent of impose on society. frequently implicated species of the those Salmonella enteritidis outbreaks genus Salmonella in human illness in which a food source was identi- Outbreaks From Eggs cases reported to the National fied. And, 87 percent of the out- Prepared Away From Salmonella Surveillance System, breaks between 1990 and 1994 were which is administered by the associated with eggs prepared in Home Declining Centers for Disease Control and foodservice and in institutions, such A major cause of the Salmonella Prevention (CDC). According to the as nursing homes and hospitals. enteritidis illness in foodservice and Eggs can become contaminated institutions is the pooling of shell with the pathogen before laying and eggs for quick preparation of foods, before the shell is formed. Patho- such as omelets and . gens carried in fecal material or dirt A single infected egg can contami- may also contaminate the shell exte- nate a large pooled batch with rior and then move through cracks Salmonella enteritidis and increase the Lin is a senior associate with CSR, Inc. Morales is or shell pores to the inner surface. chances of human infection. More- a research associate at the Department of Agricul- The pathogen can be found in the tural and Resource Economics, North Carolina State University. Ralston is an agricultural economist yolk or . Efforts are under- with the Food and Consumer Economics Division, Economic Research Service, USDA.

January-April 1997 27 Food Safety over, when pooled eggs are left sit- stituted pasteurized egg products pasteurized egg products will ting at room temperature for an for shell eggs because they are less increase by another 12 eggs to 28 extended period of time, the patho- likely to be contaminated with eggs per capita by the year 2000. gen multiplies. pathogens and are thus safer. For Due to the emergence of Salmo- example, United Airlines and nella enteritidis outbreaks with shell American Airlines have eliminated But Risk From Eggs eggs prepared outside the home, the shell eggs from all of their flight Prepared at Home CDC has been strongly recommend- kitchens and catering sources. Large Increasing ing since 1989 that foodservice and hotel corporations such as Marriot institutions use pasteurized eggs, and Hyatt have also substituted pas- Although the number of foodser- particularly when high-risk popula- teurized egg products for shell eggs vice and institutional outbreaks tion groups are served or when in recipes that call for raw or lightly appears to have declined in recent recipes call for pooling shell eggs. cooked eggs. Fastfood chains such years, the CDC data suggest more The pathogen can be killed by pas- as Burger King and McDonald’s outbreaks are occurring at home teurization—the heat treatment of have also switched from shell eggs (fig. 1). And, the number of sporadic shell eggs or egg products (liquid, to pasteurized liquid eggs in their (single) cases has been rising since frozen, or dried). In August 1990, breakfast menus when possible. 1992. the Food and Drug Administration Recent data from the CDC suggest To assess the prevalence of unsafe (FDA) issued recommended guide- that foodservice and institutional egg preparation and consumption lines for refrigerating, pooling, and Salmonella enteritidis outbreaks are practices, particularly at home, we cooking eggs, and advocated substi- becoming less frequent (fig. 1). The examined four recent national con- tuting pasteurized eggs for shell decline may be related to this sumer surveys: the 1992-95 Menu eggs by foodservice and institutions increased use of pasteurized eggs Census survey, the 1996-97 Food when possible. Currently, the and egg products by this segment of Consumption and Preparation Diary USDA’s Egg Products Inspection Act the market. In 1992, foodservice and (FCPD), the 1993 Food Safety requires that all liquid, frozen, or institutions used 16 pasteurized Survey, and the 1994 Continuing dried egg products be pasteurized to eggs per capita, compared with 10 in Survey of Food Intakes by destroy pathogens. 1980. If this trend continues, the Individuals (CSFII) (see box for In response, many foodservice American Egg Board predicts that details about the surveys). Taken and institution operators have sub- foodservice and institutional use of together, these surveys shed light on different aspects of how consumers prepare and use shell eggs and on the demographics of those who are exposed to home-prepared raw or Figure 1 Outbreaks of Salmonella enteritidis Illness From Eggs Prepared undercooked eggs. Away From Home May Be Declining, But Home-Related Outbreaks The surveys provide information May Be Increasing on the consumption of two cate- Number of outbreaks gories of potentially unsafe eggs: 70 “raw or near raw” are raw eggs and uncooked or lightly heated foods 60 Foodservice and Institutions containing eggs as ingredients, such 50 as egg drinks, egg-based sauces, salad dressings, and desserts; 40 “undercooked” are eggs prepared as 30 a main dish (referred to here as egg dishes), which are not thoroughly 20 Home cooked until both white and yolk 10 are firm, such as a with a “runny” yolk. 0 1990 1991 1992 1993 1994

Notes: "Foodservice and institutions" include restaurants, delicatessens, bakeries, nursing homes, chronic-care facilities, hospitals, homeless shelters, shelters for children, daycare centers, drug rehabilitation centers, camps, school cafeterias, other cafeterias, vending trucks, school classes, cruise ships, submarines, airplanes, and country clubs. "Home" also includes receptions, churches, and picnics.

FoodReview 28 Food Safety

Raw or Near-Raw Eggs period, it would not have been own consumption of specific foods Used as Ingredients recorded. In contrast, respondents in over an unspecified period of time. the Food Safety Survey, all of them A respondent who indicated eating According to the Menu Census adults, were asked to recall their such foods could have been refer- survey, 5 percent of the households surveyed in 1992-95 ate raw or near- raw eggs at least once a year. Most of the times that those foods were eaten (about 40 percent) occurred Sources of Information between July and September, while April-June was the least likely sea- This article is based on four data from the year-long study— son of the year such foods were con- national consumer surveys because March-July 1996. During these 5 sumed. no individual survey provides all months, 830 households returned the information needed for this arti- the survey with information on The Menu Census survey also cle. 2,282 people. indicates that frosting accounted for 1992-95 Menu Census. USDA’s 1993 Food Safety Survey. This 53 percent of the times that raw or Economic Research Service (ERS) national telephone survey, con- near-raw eggs were used as ingredi- acquired from a commercial mar- ducted by FDA and USDA’s Food ents (table 1). Salad dressing was the keting research firm tabulations of Safety and Inspection Service, pro- next most popular use (18 percent). data on consumption of raw and vides information on consumption The data suggest the typical con- undercooked eggs among a nation- of specific foods containing raw sumer of raw or near-raw eggs ally weighted sample of 16,500 peo- eggs. The survey was administered tended to be a 15- to 24-year-old ple in 6,000 households. The data to 1,620 English-speaking adults in white male who lived in the West. were derived from a 14-consecu- late 1992 and early 1993. He came from a household earning tive-day menu census survey Respondents in the survey were administered continuously through- asked: “Do you ever eat foods that an annual income of $15,000-$24,999 out a year by the firm between July contain raw eggs, such as home- or $50,000 and above. The head of 1992 and June 1995. The home- made cookie batter, homemade the household had not attained a maker in the household recorded all frosting with raw egg, Caesar salad, college education. foods and beverages consumed by or homemade , homemade The prevalence of raw or near-raw every household member and , homemade ice cream, egg consumption appears to be guests, as well as how each food shakes with raw egg, or homemade higher when based on the Food item was prepared and the ingredi- ?” and what the Safety Survey. In this survey, 53 per- ents used. foods were, if any of them were cent of the respondents said they 1996-97 Food Consumption and ever eaten. had ever eaten a food containing Preparation Diary (FCPD). To 1994 Continuing Survey of Food raw eggs, such as homemade cookie assess the prevalence of unsafe Intakes by Individuals (CSFII). preparation practices of selected USDA’s Agricultural Research batter and homemade ice cream. Of foods often associated with food- Service conducted this survey using those, 27 percent mentioned cookie borne illness, ERS is also obtaining personal interviews. The survey col- batter as a specific raw egg food from the same firm information on lected details of food and beverage (table 1). Other reported foods con- how shell eggs are prepared from a consumption on 2 nonconsecutive taining raw eggs included ice cream, base sample of about 2,000 nation- days by a nationally representative eggnog, and Caesar salad dressing. ally representative households. sample of 5,589 people. The CSFII A typical consumer of foods con- Homemakers in these households yielded less information than the taining raw eggs was white, 18-29 are asked to fill out a Food other three surveys regarding con- years old, and attained a post-grad- Consumption and Preparation sumption of specific raw or under- uate education. Diary, which accompanies the 14- cooked eggs or foods containing The two surveys, however, are not day Menu Census survey. them. But, we combined cooking Participants record how eggs are practice information from the FCPD comparable. The Menu Census data cooked (poached, scrambled, sunny and demographic information from were based on reports by the home- side up, over easy, hard boiled, or the CSFII to obtain estimates of how maker of all foods every adult, soft boiled), the appearance when frequently undercooked egg dishes child, and guest of participating cooked (runny, runny yolk, runny were eaten and by whom. This was households ate over a 14-day white, or firm yolk and white), done because of insufficient infor- period. If consumption of raw or name of the food item, and who ate mation on the demographics of near-raw eggs occurred outside that the food item. This article reports households participating in the findings from the latest available FCPD survey.

January-April 1997 29 Food Safety ring to an experience that occurred a Table 1 long time ago. Besides, consumption Raw or Undercooked Eggs in a Variety of Homemade Foods of raw cookie batter is more likely to be reported in the Food Safety Frosting was the most common use of raw or near-raw eggs as ingredients by Survey than in the Menu Census households participating in the Menu Census survey1 survey. The respondents in the Food Safety Survey were prompted with Percent of raw egg eating occasions specific food items and, therefore, Ingredient: were more likely to recall such expe- Frosting 52 riences than were the respondents in Salad dressing 18 the Menu Census survey. Flavored milk beverages 16 Ice cream 6 Sauces 5 Undercooked Egg Dishes Other 3 Also Popular

According to the FCPD survey, 27 Cookie batter topped the list of foods containing raw eggs eaten by FSS percent of all egg dishes consumed respondents2 were undercooked—described as either “runny yolk,” “runny,” or Percent of all foods mentioned “runny white.” Each person on Food: average consumed undercooked Cookie batter 27 eggs 20 times a year. Ice cream 19 Eggs fried “over easy” and Eggnog 16 “sunny side up” accounted for Caesar salad dressing 12 almost half (49 percent) of the Frosting 11 undercooked eggs eaten (fig. 2). This Other 15 reflects both the relative popularity Notes: 1Based on the 1992-95 Menu Census data. 2Based on the 1993 Food Safety of fried eggs and the relatively high Survey. probability that they will be under- cooked. Eggs fried “over easy” and “sunny side up” accounted for over one-quarter (27 percent) of all eggs

Figure 2 Fried Eggs Accounted for Nearly Half of ...In Part, Because They Were Eaten Frequently Undercooked Eggs...

Consumption of undercooked eggs Consumption of all eggs

Fried eggs 27% 49%

Hard-boiled eggs 47% 2% Soft-boiled eggs 7% 14% Scrambled eggs Poached eggs and omelets 13% 4% 29% 8%

FoodReview 30 Food Safety

Figure 3 Teenage Boys, Adult Men, and Elderly Women Ate Undercooked Egg Dishes Most Frequently

Number of times per year 100 All eggs Undercooked 80

60

40

20

0 Under 6 years 6-12 Men ages Women ages Men age 65 Women age 65 All groups years 13-64 13-64 and over and over

Age/sex group

Notes: The frequency of egg consumption by demographic classification was estimated from the 1994 CSFII. These data were used because the demographic data are incomplete for the preliminary data from the 1996-97 FCPD. The overall estimated frequency of egg consumption from the FCPD was similar to that from the CSFII.

consumed by households participat- elderly men had among the lowest year. While consumers in the ing in the FCPD survey, and nearly probabilities of consuming their Midwest ate a higher percentage of half of these dishes were described eggs undercooked (17 percent). By their eggs undercooked (31 percent), as “runny,” “runny yolk,” or “runny comparison, teenage boys and adult western consumers ate eggs of all white.” Scrambled eggs and omelets men consumed the highest propor- styles more often. accounted for only 29 percent of tion of their eggs undercooked (30 undercooked eggs. While these eggs percent), but they ate those foods were the most popular style of eggs less frequently. Children under 6 Safe Practices and consumed, they were not as likely as years of age, who are also more sus- Pasteurized Shell Eggs fried eggs to be undercooked. ceptible to foodborne illness, had Minimize Risk Based on the combined data of the the lowest frequencies for consum- CSFII and the FCPD survey, teenage ing undercooked eggs (8 times per Some consumers may not be boys and adult men (13-64 years year). aware of the risk of Salmonella enteri- old) and elderly women (over 65 FCPD respondents with annual tidis illness and its association with years) had the highest frequencies of household incomes below $15,000 raw or undercooked eggs. In the consuming undercooked egg dishes, ate undercooked eggs more fre- Food Safety Survey, only 17 percent at 23 and 21 times per year, respec- quently than any other income of the respondents had heard of tively (fig. 3). Of these two groups, group, at 24 times per year. Salmonella as “a problem in food” elderly women present the more Although the percentage of eggs and could identify eggs and their serious concern for foodborne ill- eaten undercooked does not differ products as related to the pathogen. ness, because they are more likely to dramatically across income groups To inform consumers about the risk have weakened immune systems. (between 25 and 29 percent), low- of Salmonella enteritidis illness from Women over 65 consumed 25 per- income respondents ate eggs more eating raw or undercooked eggs and cent of their egg dishes under- often than the average for all income foods containing them, USDA, FDA, cooked, slightly less than the aver- groups (92 times versus 71 times per CDC, and the egg industry are pro- age of all age/sex groups (27 year). This is a potential public- viding information to consumers on percent). However, they ate eggs health concern for foodborne illness safe practices for egg storage, prepa- more frequently than did most other because the poor tend to have less ration, and cooking. groups, except elderly men. Elderly access to medical care. In the near future, consumers may men consumed eggs more fre- Consumers in the West ate under- also be able to select pasteurized quently than did elderly women (88 cooked eggs more frequently than in shell eggs. In April 1996, Minnea- versus 83 times per year), but the any other region, at 21 times per polis-based Michael Foods began

January-April 1997 31 Food Safety test-marketing pasteurized shell Federal funding to USDA for Salmo- growth and inadequate for protect- eggs—marked with a stylized “P” nella control, and USDA discontin- ing consumers. The 1991 amend- for easy identification by shoppers, ued its involvement in the traceback ment requires an ambient tempera- packaged in a clear plastic carton, program. FDA currently has respon- ture of 45 oF for storing shell eggs. and sealed with shrink-wrap allow- sibility for the Federal program. However, in practice, an ambient ing visual inspection. These eggs are The first of the programs initiated temperature of 45 oF does not neces- priced at $1.39-$1.59 per dozen, by industry, the Pennsylvania Egg sarily reflect the temperature inside compared with about $1.00 per Quality Assurance Program, began an egg, which may often be higher dozen for nonpasteurized shell eggs in April 1992. This is a cooperative than the ambient temperature. in the test-market area. effort between the Pennsylvania Scientific research has shown that The New Hampshire-based poultry industry, USDA, Pennsyl- internal egg temperatures of 45 oF or Pasteurized Eggs, L.P., recently vania Department of Agriculture, lower are necessary to reduce the received preliminary FDA clearance and two universities to reduce the risk of Salmonella enteritidis multipli- for its process. number of eggs contaminated with cation. According to the firm, the process is Salmonella enteritidis. Producer par- As with most food-safety prob- expected to cost 12 cents per dozen ticipation in the program is volun- lems, the public-health risk from of shell eggs, and the firm has just tary. Salmonella enteritidis in eggs needs to begun to make their equipment Since then, other egg quality- be addressed at every stage from the available to egg producers. assurance programs have emerged, farm to the table. Producers and such as the Maine/New England consumers working together can Pathogen Control Also Risk Program, the reduce the risk of Salmonella enteri- California Egg Quality Assurance tidis illness from egg consumption. Reduces Risk Program, and the United Egg Producers are working to develop In 1990, USDA instituted two new Producers’ Five-Star Program. effective quality-assurance pro- programs aimed at controlling Salmonella enteritidis control mea- grams. Consumers can take protec- Salmonella enteritidis in egg laying sures used in each of these quality- tive actions, such as not eating raw operations. First, mandatory testing assurance programs vary widely or undercooked eggs, and thor- of breeder flocks for the pathogen and may include testing for the oughly cooking all foods containing was begun to eliminate transmission pathogen, cleaning and disinfecting eggs. of the pathogen to laying hens and houses and equipment, rodent and their environments. Second, a trace- pest control, and refrigerating eggs References back program to identify flocks immediately after collection. implicated in human foodborne out- USDA and FDA recently an- The Centers for Disease Control breaks of salmonellosis was initi- nounced plans to initiate rulemak- and Prevention. “Outbreaks of ated. Under this traceback program, ing to establish science-based stan- Salmonella Serotype Enteritidis In- if the pathogen was detected at the dards for proper refrigeration of fection Associated with Consump- farm of origin of the implicated shell eggs from farm to retail. This tion of Raw Shell Eggs—United eggs, then eggs from that source joint effort is aimed at replacing a States, 1994-1995,” Morbidity and could not be sold as shell eggs. 1991 amendment to the Egg Products Mortality Weekly Report, Vol. 45, No. These eggs could, however, be pas- Inspection Act that USDA viewed as 34, Aug. 30, 1996, pp. 737-42. teurized and subsequently sold as ineffective in minimizing bacterial either hard-cooked eggs or pasteur- Lin, C.-T. Jordan, Tanya Roberts, ized egg products. Furthermore, and Milton Madison. “Producing producers whose hens tested posi- Safer Poultry: Modernizing the tive for Salmonella enteritidis could Methods,” Agricultural Outlook, AO- resume the sale of shell eggs only 198, July 1993, pp. 33-38. after compliance with USDA requirements which included elimi- Mishu, Ban, Jane Koehler, Lisa A. nating flocks infected with Salmonel- Lee, Daniel Rodrigue, Frances la enteritidis and cleaning and disin- Hickman Brenner, Paul Blake, and fecting the premises prior to restock- Robert V. Tauxe. “Outbreaks of ing with uninfected birds. In Octob- Salmonella enteritidis Infections in the er 1995, as private and State-level United States, 1985- 1991,” The Salmonella enteritidis control pro- Journal of Infectious Diseases, Vol. 169, grams emerged, Congress deferred Michael Foods’ logo provides easy iden- No. 3, March 1994, pp. 547-52. tification of their pasteurized shell eggs.

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