Food Quality and Preference 16 (2005) 401–412 www.elsevier.com/locate/foodqual Awareness of foodborne pathogens among US consumers Chung-Tung Jordan Lin a a,1 , Kimberly L. Jensen b,2 , Steven T. Yen b,* Division of Market Studies, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, College Park, MD 20740, United States b Department of Agricultural Economics, University of Tennessee, Knoxville, TN 37996-4518, United States Received 5 May 2004; received in revised form 25 June 2004; accepted 14 July 2004 Available online 11 September 2004 Abstract Each year in the United States, microbial pathogens cause millions of cases of foodborne disease and result in many hospitalizations and deaths. Effective consumer education programs to promote safer food handling practices and other averting behaviors may benefit from consumer awareness of microbial pathogens. This paper investigates US consumers awareness of four major microbial pathogens (Salmonella, Campylobacter, Listeria and Escherichia coli) as food safety problems, using a multivariate probit model. The awareness varies among pathogens and the variations appear to be related to differences in the number and severity of illnesses associated with these pathogens. Our findings suggest that awareness of microbial pathogens is associated with food safety perceptions, awareness of potentially risky foods and substances associated with potential food safety hazards, food safety related behaviors, and demographics. There are differentiated effects of variables on awareness of the four pathogens. 2004 Elsevier Ltd. All rights reserved. Keywords: Consumer awareness; Foodborne pathogens; Multivariate probit 1. Introduction Each year, microbial pathogens cause as many as 76 million cases of foodborne illness, 324,000 hospitalizations, and 5200 deaths in the United States (Mead et al., 1999). The more common pathogens associated with foodborne illness include Salmonella, Campylobacter jejuni, and Escherichia coli O157:H7 (Table 1). Some victims of E. coli O157:H7 caused illness, particularly the very young, have developed hemolytic uremic syndrome (HUS), characterized by renal failure and hemolytic anemia which can lead to permanent loss of kidney function (FDA-CFSAN, 2003a). Foodborne illness associated with Listeria monocytogenes, though * Corresponding author. Tel.: +1 865 974 7474; fax: +1 865 974 4829. E-mail addresses: [email protected] (C.-T.J. Lin), [email protected] (K.L. Jensen), [email protected] (S.T. Yen). 1 Tel.: +1 301 436 1831; fax: +1 301 436 2626. 2 Tel.: +1 865 974 3716; fax: +1 865 974 4829. 0950-3293/$ - see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodqual.2004.07.001 relatively low in number (Table 1), is associated with many deaths (CAST, 1994; FDA-CFSAN, 2003a). Also, listeriosis in pregnant women can result in miscarriage, fetal death, and severe illness or death of a newborn infant (FDA-CFSAN, 2003d). Annual costs of foodborne illness in the United States have been estimated between $10 and $83 billion (FDA-CFSAN, 2003c). The US Department of Agricultures Economic Research Service estimates that the costs associated with five major pathogens alone (Escherichia coli O157:H7, other Shiga toxin-producing E. coli (STECs), Campylobacter, Listeria monocytogenes, and Salmonella) amount to at least $6.9 billion annually (USDA-ERS, 2000). While practices of food suppliers and food service establishments play an important role in reducing foodborne illness (CAST, 1994), existing research suggests that a substantial proportion of foodborne illness is attributable to improper in-home food handling, preparation, and consumption practices by consumers (CAST, 1994; Redmond & Griffith, 2003). Improper 402 C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 Table 1 Four major foodborne pathogens: incidence, associated foods, and symptoms Bacterial organism US cases annually Associated foods Symptoms of illness Salmonella 2–4 million Raw meats, poultry, eggs, milk and dairy products, fish, shrimp, frog legs, yeast, coconut, sauces and salad dressing, cake mixes, cream-filled desserts and toppings, dried gelatin, peanut butter, cocoa, and chocolate Nausea, vomiting, abdominal cramps, diarrhea, fever, and headache. Chronic consequences—arthritic symptoms may follow 3–4 weeks after onset of acute symptoms Campylobacter jejuni At least 2–4 million Raw chicken, raw milk, non-chlorinated water Diarrhea, fever, abdominal pain, nausea, headache and muscle pain. The illness usually occurs 2–5 days after ingestion. Illness generally lasts 7–10 days, but relapses are not uncommon (about 25% of cases) Escherichia coli O157:H7 20,000 and 40,000 Undercooked or raw hamburger (ground beef), alfalfa sprouts, unpasteurized fruit juices, dry-cured salami, lettuce, game meat, cheese curds, raw milk Severe cramping (abdominal pain) and diarrhea that becomes grossly bloody. Occasionally vomiting occurs. Fever is either low-grade or absent Lasts for an average of 8 days Listeria monocytogenes 1600 cases (Foods with high or moderate risk) Unpasteurized and pasteurized fluid milk, deli meats, frankfurters (not reheated), cheeses (particularly soft-ripened varieties), high-fat and other dairy products, pâté and meat spreads, smoked seafood, cooked and ready-to-eat crustaceans Septicemia, meningitis (or meningo-encephalitis), encephalitis, spontaneous abortion or stillbirth, fever, nausea, vomiting, and diarrhea Source: FDA-CFSAN (2003a,b,c). practices include, but are not limited to, inadequate cooking, inadequate cooling and storage of foods, cross-contamination of raw and cooked foods, inadequate personal hygiene such as hand washing, and consumption of raw, undercooked, or unsafe foods (CAST, 1994; Doyle et al., 2000; Medeiros, Hillers, Kendall, & Mason, 2001; Redmond & Griffith, 2003). Thus, consumer food handling and preparation behaviors are important means to reduce foodborne illness. Awareness of foodborne pathogens may play a positive role in reducing foodborne illness. McIntosh, Christensen, and Acuff (1994) reported that a higher number of five bacteria that Texan consumers had heard of were associated with (1) awareness of dangers related to the degree of doneness in cooking hamburger patties, and (2) preference toward hamburger patties prepared more than less done. The five pathogens asked were Salmonella, Campylobacter, E. coli, Listeria, and Clostridium perfringens. Similarly, US adult residents who had heard of Salmonella as a problem in food and volunteered a probable food vehicle related to the pathogen were more likely than others to know that ‘‘cooking meat until well-done reduces the risk of food poisoning’’ (Altekruse, Street, Fein, & Levy, 1996). In addition, Altekruse et al. (1996) found that those who had heard of Salmonella and volunteered a probable food vehicle related to Salmonella were more likely than others to (1) wash hands after handling raw meat, (2) wash or change cutting board after cutting raw meat or poultry, (3) think washing hands reduces risk of food poisoning, (4) think serving steak on a plate that held raw steaks increases risk of food poisoning, and (5) think cooking meat ‘‘well-done’’ decreases food poisoning. Nevertheless, the hamburgers served were no more or less ‘‘done’’ in either groups homes. Hence, these studies suggest that awareness of foodborne pathogens goes hand in hand with better knowledge of safe food handling and preparation principles and safer food handling and preparation practices; both should ultimately contribute to a reduction in foodborne illness. Consumer education programs are often used to promote safer food handling and preparation practices, and increasing the level of awareness of foodborne pathogens appears to be helpful in enhancing the outcomes of consumer education. In particular, consumer education programs may target individuals who are less likely to be aware of foodborne pathogens as a food safety problem, and thus may practice less safe food handling and preparation behaviors. This in turn requires an understanding of which consumers are aware of pathogens and what factors, such as, food safety perceptions, attitudes and information, and demographic characteristics, are associated with their awareness. C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 This study built on existing research and investigated consumer awareness of four major foodborne pathogens, Salmonella, Campylobacter, Listeria, and E. coli. By using data collected in a 2001 national telephone survey of US adults, the study examined the relationships between the awareness and its explanatory variables for each pathogen simultaneously and the differential relationships among the four different pathogens. Two major features of this study distinguish it from the literature. First, we included two categories of explanatory variables to gain a better understanding of the awareness. One category of explanatory variables reflect consumers perceptions related to food safety, such as whether food safety problems are most likely to occur at homes or not and how serious of a food safety problem is contamination of food by micro-organisms. The other category of explanatory variables represent consumers awareness of potentially risky substances in food such as mercury and potentially risky foods such as sprouts. We hypothesized that consumers with higher risk perceptions or awareness of foods and substances associated with food safety problems would pay more attention to food safety information and therefore more likely to be aware of foodborne pathogens. The second distinguishing feature of this study is that we used an econometric technique to simultaneously examine the relationships between each of the pathogens and a common set of explanatory variables. If there are unobserved and unmeasured common factors underlying the different awareness, then the univariate (single-equation) technique as used in previous research would be more prone to biases caused by the common factors. Our approach explicitly recognizes and controls for the potential correlation among awareness and thus can offer more accurate estimates of relationships between awareness and its explanatory variables. 403 in the household, the most-recent-birthday method was used to select a respondent. Interviews began on April 30, 2001 and ended on August 28, 2001. A total of 4482 adults were successfully interviewed, yielding a response rate of 46.5% (per the Response Rate 5 defined by the American Association for Public Opinion Research (AAPOR, 2004)). We created a sample of 2992 observations, consisting of the respondents who provided usable responses to all survey questions included in the analysis (observations with responses like ‘‘dont know’’ or ‘‘refuse’’ were removed from the sample). The data were weighted to adjust for probability of selection (number of residential telephone numbers and number of adults in the household) and to adjust the sample distributions of race, education, and gender to that of the 2001 Current Population Survey (US Census, 2001). In the current analysis, both descriptive statistics and regression results were based on weighted data. As shown in Table 2, 12% of the sample are Black, 9% are Hispanic, 4% are of other races, 22% are in the 18–29-year age group, 44% are in the 30–49-year age group, 18% have at least one child under 5 years of age in the household, 52% are female, 52% have had at least some college education, 18% reside in the Northeast region, 24% in the Midwest region, and 18% in the West region. In comparison, the 2001 Current Population Survey (CPS) estimated the distributions among US adults were 52% female, 12% Black, 11% Hispanic, and 51% with at least some college education. The CPS estimated that, among all US households, 18% were in the Northeast region, 23% in the Midwest region, and 22% in the West region (US Census, 2001). Therefore, our sample closely resembles the US population in these characteristics. 2.2. Questionnaire 2. Sample and methods 2.1. Sample We used data from the 2001 Food Safety Survey (FSS) sponsored jointly by the US Food and Drug Administration (FDA) and the US Department of Agriculture (USDA) and conducted by a private contractor (FDA-CFSAN, 2002). The FSS is a random-digit-dialing survey using the ComputerAssisted-Telephone-Interviewing (CATI) technique on a nationally representative sample of American consumers. The sample is based on a single-stage sample of telephone numbers, listed and unlisted, generated from the GENESYS Sampling System (Marketing Systems Group, 2004). Eligible respondents were adults (18 years of age or older) in the 48 contiguous states and the District of Columbia. When there were more than one adult The questionnaire covered awareness of pathogens as problems in food, food safety perceptions, food handling and consumption practices, perceived vulnerability from unsafe food handling and consumption practices, awareness and consumption of potentially risky foods, awareness of new food processing technologies, food allergies, foodborne illness experience, and demographics. In this study, we focused on the analysis of awareness of four different pathogens (Salmonella, Campylobacter, Listeria, and E. coli). Specifically, the survey asked ‘‘Have you ever heard of (a pathogen) as a problem in food?’’ The possible responses were ‘‘yes’’ and ‘‘no’’. 2.3. Methods Our statistical model postulated that pathogen awareness is related to food safety perceptions, awareness of 404 C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 Table 2 Variable definitions and weighted sample means Variable Definition and code Mean Dependent variables AWARE_SAL AWARE_CAM AWARE_LIS AWARE_ECO 1 = ever 1 = ever 1 = ever 1 = ever 0.94 0.07 0.32 0.90 heard heard heard heard of of of of Salmonella as a problem in food, 0 = otherwise Campylobacter as a problem in food, 0 = otherwise Listeria as a problem in food, 0 = otherwise E. coli as a problem in food, 0 = otherwise Explanatory variables—risk perceptions FROMHOME 1 = homes are where food safety problems are most likely to occur; 0 = otherwise HOMERISK How common it is for people in the US to become sick because of the way food is handled or prepared in their homes; 1 = very common or somewhat common, 0 = not very common GERMRISK How serious of a food safety problem is contamination of food by micro-organisms; 1 = very serious or serious, 0 = somewhat a problem or not a problem at all VULNERABLE Average of perceived likelihood of getting sick from unsafe food handling practices ((a) forgetting to wash hands before beginning cooking, (b) letting vegetables that will be eaten raw touch raw meat or chicken, (c) eating meat or chicken not thoroughly cooked, and (d) leaving cooked food out of the refrigerator for more than 2 h after it has finished cooking); each likelihood is measured on a 1 (not at all likely) to 5 (very likely) scale; recoded as 1 if average = 3 or higher, and 0 otherwise Food safety practices WASHHANDS HAMBURGER STOPBUY Frequency of washing hands with soap before preparing food, 1 = all of the time, 0 = otherwise 1 = hamburgers are usually served well-done or medium (brown all the way through) at home; 0 = served medium (still have some pink in the middle) or rare 1 = has stopped buying specific kinds of food that the respondent is especially worried about because of their safety, 0 = otherwise Awareness of other food safety issues SPROUTS 1 = has heard or read about possible health problems related to eating sprouts, such as alfalfa or bean sprouts, 0 = otherwise JUICES 1 = has heard or read about possible health problems related to drinking juice that has not been pasteurized or unpasteurized juice, 0 = otherwise MERCURY 1 = has heard or read about possible health problems related to mercury as a problem in some fish, 0 = otherwise Foodborne illness and other diseases ILLNESS 1 = respondent or someone in the household has had some kind of sickness that the respondent thought might be caused by eating spoiled or unsafe food (except food allergies), 0 = otherwise HEALTH 1 = has one or more of the following health conditions: liver disease, diabetes, reduced gastric acidity, HIV, AIDS, a weakened immune system, or currently receiving chemotherapy or radiation therapy, 0 = otherwise 0.17 0.62 0.54 0.67 0.76 0.83 0.23 0.15 0.29 0.69 0.30 0.12 Meal preparation MEALPREP 1 = prepares the main meal in respondents household all or nearly all of the time, 0 = otherwise 0.55 Demographics INCOME2 INCOME3 INCOME4 HHSIZE2 HHSIZE3 HHSIZE4 CHILD5 FEMALE COLLEGE BLACK HISPANIC OTHER RACE AGE1829 AGE3049 MIDWEST WEST NORTHEAST Household income is $20,001–$50,000 (reference = $20,000 and under) Household income is $50,001–$100,000 Household income is more than $100,000 Household size is two persons (reference = household with one person) Household size is 3–4 persons Household size is more than 4 persons 1 = if children under age 5 in household, 0 = other 1 = female, 0 = male 1 = at least some college education, 0 = other 1 = black race, 0 = otherwise (reference = White) 1 = Hispanic origin, 0 = otherwise 1 = Other race, 0 = otherwise 1 = age 18–29, 0 = other (reference = 50 and older) 1 = age 30–49, 0 = other 1 = Midwest region, 0 = other (reference = south region) 1 = West region, 0 = other 1 = Northeast region, 0 = other 0.42 0.32 0.10 0.31 0.41 0.19 0.18 0.52 0.52 0.12 0.09 0.04 0.22 0.44 0.24 0.18 0.18 Source: FDA Food Safety Survey, 2001. C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 potentially risky foods and substances associated with potential food safety hazards, food safety related behaviors and experience, and demographics. 2.3.1. Food safety perceptions We hypothesized that consumers who perceive higher risk of foodborne illness are more likely to be aware of the pathogens because they may pay more attention to food safety information and be more motivated to learn about food safety, such as the causes of foodborne illness. Answers to the following survey questions were used to construct four binary explanatory variables to represent food safety perceptions. First, ‘‘Where do you think food safety problems are most likely to occur, would you say farms, food processing plants, warehouses, supermarkets, restaurants, or homes’’ (FROMHOME). Second, ‘‘How common do you think it is for people in the United States to become sick because of the way food is handled or prepared in their homes’’ (HOMERISK). Third, ‘‘Do you think contamination of food by micro-organisms, such as germs, is a very serious food safety problem, a serious food safety problem, somewhat of a problem, or not a food safety problem at all’’ (GERMRISK). The fourth variable, VULNERABLE, is a binary variable constructed from responses to four questions: (1) ‘‘If you forget to wash your hands before you begin cooking, how likely are you to get sick’’, (2) ‘‘If vegetables you will eat raw happen to touch raw meat or chicken, how likely are you to get sick’’, (3) ‘‘If you eat meat or chicken that is not thoroughly cooked, how likely are you to get sick’’, and (4) ‘‘If you happen to leave cooked food out of the refrigerator for more than 2 hours after it has finished cooking, how likely are you to get sick’’ (see Table 2 for variable codes). 2.3.2. Awareness of potentially-risky foods and substances We hypothesized that consumers who are aware of potentially risky foods and substances are also more likely to be aware of the pathogens. Again, this relationship is expected because these consumers may pay more attention to food safety information and are more motivated to learn about food safety. The association between pathogen awareness and awareness of high risk foods may also arise because when consumers hear or read about certain potentially risky foods, they are likely to hear or read about the source of the risk, i.e., the pathogens. The survey asked respondents whether they had heard or read about any possible health problems related to ‘‘eating sprouts (such as alfalfa or bean sprouts)’’ (SPROUTS), ‘‘drinking juice that has not been pasteurized, that is, unpasteurized juice’’ (JUICES), and ‘‘mercury as a problem in some fish’’ (MERCURY). In the late 1990s and early 2000s, raw sprouts and unpasteurized juices were implicated in a number of foodborne illness outbreaks in the United 405 States. For instance, from 1996 to 2000, four major outbreaks were related to unpasteurized juices contaminated with Salmonella or E. coli O157:H7 (USDHHS, 2001). A Salmonella-related outbreak in four Western states in early 2001 was related to sprouts (CDC, 2002). Mercury occurs naturally in the environment and can also be released into the air through industrial pollution; the pollutant falls from the air and can accumulate and is turned into methylmercury in the water. Major foodborne illness outbreaks receive a lot of media attention and news stories often mention the pathogens implicated (see, e.g., Ollinger-Synder & Matthews, 1994). Food safety authorities, such as the FDA and the USDA, also issue consumer advisories and food recall notices that often mention the specific pathogen(s) related to a risk (FDA-CFSAN, 1998; USDHHS, 1999). Hence, consumers who have heard or read of the high risk foods or substances are hypothesized to have higher likelihood of having heard of foodborne pathogens. 2.3.3. Other explanatory variables Previous studies have suggested that awareness of foodborne pathogens is related to better knowledge of safe food handling and preparation principles and safer food handling and preparation practices (Altekruse et al., 1996; McIntosh et al., 1994). Based on these findings, we hypothesized that pathogen awareness is higher among consumers who have safer food handling and preparation practices. Two questions in the survey were used. First, ‘‘Before you begin preparing food, how often do you wash your hands with soap? Would you say all of the time, most of the time, some of the time, or rarely’’ (WASHHANDS). Second, ‘‘In your home, are hamburgers usually served rare, medium, or welldone’’ (HAMBURGER). Those who said ‘‘medium’’ were further asked whether they meant ‘‘brown all the way through’’ or ‘‘still have some pink in the middle’’. We also hypothesized that consumers are more likely to have heard of the pathogens if they have stopped buying specific kinds of food due to safety concern (STOPBUY), think they themselves or someone in the household have had suspected foodborne illness (ILLNESS), have one or more health conditions that may weaken their immunity (HEALTH), are the primary meal preparers in the household (MEALPREP), are older, are female (FEMALE), or reside in a household with young children (CHILD5). These consumers would have greater awareness of pathogens because they may pay more attention to food safety. Finally, we included in the model several demographic characteristics, i.e., race/ethnicity, household size, education, income, and geographic region. In particular, we hypothesized that more educated consumers and consumers who come from higher income households have greater access to food safety information and greater capability to use the information and therefore 406 C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 would likely be more aware of the pathogens. We also hypothesized that awareness of pathogens differs among geographic regions. Two possible causes of the difference are: (1) the number of outbreaks differ among geographic regions (CDC, 2000b) and (2) the number of cases of some highly publicized outbreaks also differ in various parts of the country. For example, cases in the 1993 E. coli O157:H7 outbreak associated with undercooked hamburgers concentrated in four Western US states (CDC, 1993). density /(e1, e2, . . ., en; R). The likelihood contribution for an observation is the n-variate standard normal probability Prðy 1 ; . . . ; y n j xÞ Z ð2y 1 1Þx0 b1 Z ¼ 1 Z ð2y 2 1Þx0 b2 1 ð2y n 1Þx0 bn /ðe1 ; e2 ; . . . ; en ; Z 0 RZÞden de2 de1 ; 1 ð2Þ 2.4. Statistical model We used descriptive analysis to characterize the sample (i.e., means). We applied a weighting factor to the data for the descriptive analysis, using the weighting procedure described above. The SAS PROC MEANS procedure was used for the analysis (SAS Institute Inc., 2001). To analyze the relationships between awareness of the four pathogens and the explanatory variables, we used a multivariate probit econometric technique. Chisquare analysis has been used to investigate awareness of a single pathogen (Herrmann & Warland, 2000). McIntosh et al. (1994) applied the ordinary least-squares econometric technique with the dependent variable defined as the sum of ones (‘‘heard of’’) and zeros (‘‘not heard of’’) for five pathogens (Salmonella, Campylobacter, E. coli, Listeria, and Clostridium perfringens). Another approach would be to model each pathogen individually, i.e., using a univariate technique such as probit analysis for discrete dependent variables. Univariate techniques, however, ignore the potential correlation among the unobserved disturbances in the awareness, and thus may compromise statistical efficiency. If there are unobserved and unmeasured common factors underlying the different awareness, then the univariate technique, as used in previous research, would be more prone to biases caused by neglecting common factors. To overcome the shortcoming in univariate techniques, we adopted a multivariate probit econometric technique in this study. Drawing upon the statistics literature (Ashford & Sowden, 1970), the multivariate probit econometric model is characterized by a set of n binary dependent variables yi (with observation subscripts suppressed) such that yi ¼ 1 ¼0 if x0 bi þ ei > 0; if x0 bi þ ei 6 0; i ¼ 1; 2; . . . ; n; ð1Þ where x is a vector of explanatory variables, b1, b2, . . ., bn are conformable parameter vectors, and random error terms e1, e2, . . ., en are distributed as multivariate normal distribution with zero means, unitary variance and an n · n contemporaneous correlation matrix R = [qij], with where Z = diag[2y11, . . ., 2yn 1]. Maximum-likelihood estimation was carried out by maximizing the sample likelihood function, which is the product of probabilities (2) across sample observations. To quantify the marginal effects of explanatory variables, the awareness probability for each pathogen Prðy i ¼ 1Þ ¼ Uðx0 bi Þ; i ¼ 1; 2; . . . ; n; ð3Þ can be differentiated, where U(Æ) is the univariate standard normal cumulative distribution function. Because all explanatory variables are binary, the effects of each variable on the awareness probabilities (3) were calculated by simulating a finite change in the variable (i.e., from 0 to 1) while holding all other variables at the sample means. We estimated the multivariate probit model by programming the log-likelihood function in GAUSS (Aptech, 1997). Numerical maximization of the loglikelihood was accomplished with the Broyden–Fletcher–Goldfarb–Shanno (BFGS) algorithm (Luenberger, 1984). The current application to four pathogens involved a four-variate (one for each pathogen) standard normal probability for each observation, which was evaluated with a simulation technique known as the GHK probability simulator (Hajivassiliou, 1994). The asymptotic standard errors of the maximum-likelihood estimates were calculated by inverting the outer products of the numerical gradients (Berndt, Hall, Hall, & Hausman, 1974). Some of the behavioral variables may be endogenous, causing simultaneous-equation bias in the statistical estimates. Potential endogeneity of WASHHANDS, HAMBURGER and STOPBUY was investigated by estimating a simultaneous-equation probit model for each of these pathogens, one at a time, in which significance of the error correlation would suggest presence of endogeneity (Rivers & Vuong, 1988). The hypothesis of exogeneity cannot be rejected for STOPBUY in any equation. However, there is some evidence of endogeneity for WASHHANDS in the Campylobacter (p-value < 0.01) and Listeria (p-value < 0.01) equations, and for HAMBURGER in the Listeria (p-value = 0.01) and E. Coli (p-value = 0.05) equations, respectively. Estimation of the model without the WASHHANDS C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 and HAMBURGER variables, however, produces very similar results, in terms of signs and significance of explanatory variables, as those reported here. Results of this alternative specification and simultaneous-equation estimates for endogeneity tests are available upon request from the authors. As in more traditional regression models, multicollinearity among the explanatory variables can lead to imprecise parameter estimates (Kleinbaum, Kupper, & Muller, 1988). To explore potential multicollinearity among the explanatory variables, we calculated the variance inflation factor (VIF) for each explanatory variable. The VIFs range from <0.01 to 2.75, which do not reach conventional thresholds (10 or higher) used in the regression diagnosis literature (Kleinbaum et al., 1988). Hence, multicollinearity does not appear to be a problem in the current analysis. 3. Results The majority of US consumers said they had heard of Salmonella (94%) and E. coli (90%) as a problem in food (Table 2). In contrast, about one third of them were aware of Listeria (32%) and only 7% were aware of Campylobacter. About 17% of US consumers thought homes were where food safety problems were most likely to occur. Sixty-two percent thought it was very common or somewhat common for people in the United States to become sick because of the way food was handled or prepared in their homes. About half of US consumers considered food contamination by micro-organisms a very serious or serious food safety problem. They perceived themselves to be somewhat likely to get sick from four unsafe food handling practices. Sixty-seven percent of the consumers perceived at least a moderate likelihood of getting sick from unsafe food handling practices (see VULNERABLE defined above and in Table 2). Most consumers claimed they always washed their hands before preparing food, and the hamburgers served at their homes were usually thoroughly cooked (i.e., well-done or brown all the way through). About one quarter (23%) of consumers had stopped buying specific foods because of food safety concern. As to awareness of other food safety issues, while a large portion of consumers (69%) said they had heard or read about possible health problems related to mercury in some fish, much fewer consumers said they had heard or read about possible health problems of eating sprouts (15%) or about health problems of drinking unpasteurized juice (29%). One in three consumers thought they themselves or someone in the household had been sick from eating spoiled or unsafe food; 12% of the consumers said they had one or more health conditions, including liver disease, diabetes, reduced gastric acidity, HIV, AIDS, a weakened immune system, or were under chem- 407 otherapy or radiation therapy. Fifty-five percent of consumers were main meal preparers in their households. We estimated the multivariate probit model and, for comparison, a univariate probit model for each of the four pathogens. The univariate probit models together can be viewed as a restricted version of the multivariate probit with all off-diagonal error correlations set to zeros (i.e., qij = 0 for i > j). Based on the log-likelihood values of the multivariate and univariate probit models, a likelihood ratio test (Engle, 1984) suggested joint significance of the error correlations (v2 = 97.01, d.f. = 6, p-value < 0.001), justifying estimation of the multivariate probit vis-à-vis univariate probit models. This test result is consistent with the significance of the error correlation coefficients between Listeria and Campylobacter (0.43), and between E. coli and Salmonella (0.59), respectively. A comparison of the multivariate and univariate probit results, available from the authors upon request, however, suggests qualitatively similar effects of explanatory variables, in terms of signs and significance levels, between the two models. The rest of the analysis is based on the multivariate probit estimates. Table 3 shows the estimated relationships between pathogen awareness and explanatory variables. As typical in cross-sectional analysis, the pseudo R-squareds (Wooldridge, 2002, p. 463) for the probit equations are fairly low, ranging from 0.07 for Campylobacter to 0.14 for Salmonella. However, for binary-choice models, it is more important to examine the predictive power, defined as the percentage of times the predicted 0–1 outcome matches the actual 0–1 outcome. Specifically, de^, note the maximum-likelihood estimator of bi as b i then the outcome of yi is predicted to be unity when ^ Þ > 0:5 and zero when Uðx0 b ^ Þ 6 0:5 (Wooldridge, Uðx0 b i i 2002, p. 465). The predicted powers of the estimated models are fairly high, ranging from 67.75% correct predictions for Listeria to 96.46% for Salmonella. In addition, based on results from a randomly selected 80% sub-sample, the model performs well in out-of-sample prediction (with the remaining 20% of the sample), with predicted powers ranging from 66.56% correct predictions for Listeria to 94.98% for Salmonella. Based on estimated marginal effects, awareness of Salmonella is more likely among consumers who perceive homes are where food safety problems are most likely to occur, who perceive it is very common or somewhat common that people get sick from food handled or prepared at home, who consider pathogen contamination as a very serious or serious food safety problem, who perceive higher risk from unsafe food handling practices, or who always wash hands with soap before food preparation. Those who have heard of possible health problems related to drinking unpasteurized juices or related to mercury in some fish are also more likely to be aware of Salmonella. Consumers from homes that usually serve thoroughly cooked (well-done or brown 408 C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 Table 3 Multivariate probit estimates of consumer awareness Salmonella Coefficient CONSTANT Risk perceptions FROMHOME HOMERISK GERMRISK VULNERABLE Food safety practices WASHHANDS HAMBURGER STOPBUY Campylobacter Marg. effect INCOME3 INCOME4 HHSIZE2 HHSIZE3 HHSIZE4 CHILD5 FEMALE COLLEGE BLACK Coefficient E. coli Marg. effect 1.444*** (0.154) 0.303* (0.163) 0.184** (0.085) 0.232** (0.097) 0.166* (0.100) 0.010** (0.004) 0.008** (0.004) 0.010** (0.004) 0.007* (0.004) 0.136 (0.109) 0.051 (0.096) 0.114 (0.086) 0.044 (0.098) 0.015 (0.013) 0.005 (0.010) 0.012 (0.009) 0.004 (0.010) 0.398*** (0.105) 0.215 (0.148) 0.142 (0.113) 0.021*** (0.007) 0.008* (0.004) 0.006 (0.006) 0.130 (0.105) 0.170 (0.113) 0.147 (0.092) 0.013 (0.010) 0.016* (0.010) 0.016 (0.011) 0.453*** (0.095) 0.220*** (0.086) 0.190* (0.114) 0.061*** (0.016) 0.025** (0.011) 0.019* (0.011) Foodborne illness and other diseases ILLNESS 0.130 0.005 (0.103) (0.004) HEALTH 0.199 0.010 (0.123) (0.007) Demographics INCOME2 Marg. effect 2.823*** (0.300) 0.253 (0.262) Awareness of other food safety issues SPROUTS 0.130 0.005 (0.223) (0.008) JUICES 0.348*** 0.013*** (0.140) (0.005) MERCURY 0.743*** 0.044*** (0.106) (0.009) Meal preparation MEALPREP Coefficient Listeria 0.059 (0.064) 0.030 (0.045) 0.104** (0.046) 0.083* (0.051) 0.043 (0.053) 0.041 (0.062) 0.011 (0.054) Coefficient Marg. effect 0.117 (0.292) 0.018 (0.020) 0.009 (0.014) 0.031** (0.014) 0.025* (0.015) 0.013 (0.016) 0.012 (0.019) 0.003 (0.016) 0.603*** (0.068) 0.289*** (0.052) 0.181*** (0.053) 0.206*** (0.027) 0.091*** (0.017) 0.053*** (0.015) 0.083 (0.080) 0.160*** (0.060) 0.036 (0.062) 0.152*** (0.061) 0.015 (0.015) 0.029** (0.014) 0.006 (0.011) 0.028** (0.014) 0.002 (0.065) 0.190** (0.081) 0.129* (0.069) 0.000 (0.012) 0.037* (0.020) 0.024* (0.014) 0.250** (0.127) 0.322*** (0.091) 0.593*** (0.076) 0.040 (0.025) 0.053** (0.022) 0.122*** (0.034) 0.011 (0.092) 0.092 (0.148) 0.001 (0.009) 0.009 (0.014) 0.127*** (0.049) 0.014 (0.068) 0.039*** (0.016) 0.004 (0.021) 0.091 (0.072) 0.039 (0.078) 0.016 (0.013) 0.007 (0.015) 0.034 (0.096) 0.001 (0.004) 0.003 (0.093) 0.000 (0.010) 0.081* (0.049) 0.024* (0.015) 0.009 (0.064) 0.002 (0.011) 0.324*** (0.111) 0.554*** (0.135) 0.197 (0.215) 0.069 (0.184) 0.090 (0.192) 0.341* (0.204) 0.366*** (0.140) 0.464*** (0.112) 0.181 (0.120) 0.616*** (0.143) 0.013*** (0.005) 0.019*** (0.005) 0.007 (0.007) 0.003 (0.007) 0.004 (0.008) 0.018 (0.013) 0.012*** (0.004) 0.020*** (0.005) 0.008 (0.005) 0.042*** (0.013) 0.220 (0.157) 0.235 (0.166) 0.312 (0.207) 0.007 (0.198) 0.039 (0.196) 0.014 (0.219) 0.050 (0.120) 0.160* (0.096) 0.545*** (0.097) 0.197 (0.139) 0.023 (0.017) 0.026 (0.020) 0.040 (0.031) 0.001 (0.020) 0.004 (0.020) 0.001 (0.023) 0.005 (0.013) 0.016 (0.010) 0.057*** (0.011) 0.018 (0.011) 0.142** (0.067) 0.283*** (0.071) 0.354*** (0.097) 0.016 (0.105) 0.171 (0.106) 0.290*** (0.112) 0.179*** (0.065) 0.053 (0.051) 0.303*** (0.046) 0.372*** (0.067) 0.043** (0.021) 0.089*** (0.023) 0.117*** (0.035) 0.005 (0.032) 0.051* (0.031) 0.081*** (0.030) 0.056*** (0.021) 0.016 (0.016) 0.091*** (0.014) 0.100*** (0.017) 0.375*** (0.075) 0.493*** (0.087) 0.354*** (0.138) 0.030 (0.124) 0.141 (0.122) 0.235* (0.131) 0.167** (0.079) 0.227*** (0.067) 0.247*** (0.069) 0.426*** (0.077) 0.064*** (0.023) 0.079*** (0.029) 0.052** (0.026) 0.005 (0.023) 0.026 (0.024) 0.046 (0.030) 0.028** (0.014) 0.041** (0.018) 0.044** (0.021) 0.092*** (0.030) C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 409 Table 3 (continued) Salmonella HISPANIC OTHER RACE AGE1829 AGE3049 MWEST WEST NEAST % predicted Pseudo R2 Campylobacter Listeria E. coli Coefficient Marg. effect Coefficient Marg. effect Coefficient Marg. effect Coefficient Marg. effect 1.057*** (0.142) 0.660** (0.285) 0.175 (0.151) 0.384*** (0.132) 0.144 (0.131) 0.037 (0.118) 0.220 (0.148) 96.46 0.137 0.108*** (0.024) 0.052 (0.036) 0.007 (0.005) 0.015*** (0.005) 0.006 (0.005) 0.002 (0.005) 0.008* (0.005) 0.199 (0.185) 0.581*** (0.144) 0.115 (0.126) 0.062 (0.102) 0.088 (0.107) 0.249** (0.123) 0.024 (0.115) 90.68 0.070 0.018 (0.015) 0.091*** (0.032) 0.013 (0.015) 0.006 (0.011) 0.009 (0.010) 0.023** (0.010) 0.002 (0.012) 0.070 (0.081) 0.264*** (0.106) 0.045 (0.072) 0.164*** (0.055) 0.070 (0.058) 0.376*** (0.069) 0.007 (0.060) 67.75 0.109 0.021 (0.023) 0.087** (0.037) 0.013 (0.021) 0.050*** (0.017) 0.021 (0.018) 0.103*** (0.018) 0.002 (0.018) 0.775*** (0.102) 0.385** (0.167) 0.116 (0.090) 0.134* (0.078) 0.008 (0.077) 0.040 (0.086) 0.197** (0.089) 93.38 0.085 0.195*** (0.043) 0.085** (0.039) 0.020 (0.016) 0.024 (0.015) 0.001 (0.014) 0.007 (0.016) 0.032** (0.017) Note: Log-likelihood = 3452.268. Asymptotic standard errors in parentheses. Levels of statistical significance: *** = 1%, ** = 5%, * = 10%. all the way through) hamburgers are less likely to be aware of Salmonella (though the probability difference is negligible, 0.008). As for Campylobacter, consumers are more likely to have heard of it if thoroughly-cooked hamburgers are usually served in their homes. In addition, awareness of health problems related to eating sprouts, drinking unpasteurized juices, or mercury in some fish is also associated with a larger probability of having heard of Campylobacter. Likewise, the same awareness is associated with the probability of having heard of Listeria. Meanwhile, those who perceive pathogen contamination as a very serious or serious food safety problem, who perceive higher likelihood of getting sick from unsafe practices, who have household member(s) with sickness possibly caused by eating spoiled or unsafe food, or who are the main meal preparers in their households are also more likely to be aware of the pathogen. Having heard of the pathogen E. coli is more likely among those who think it is very common or somewhat common for people in the United States to become sick because of the way food is handled or prepared in their homes, who perceive higher likelihood of getting sick from unsafe food handling practices, who are from a household where thoroughly-cooked hamburgers are usually served, or who have heard about possible health problems related to drinking unpasteurized juices or related to mercury in some fish. But awareness of E. coli is less likely among consumers who have stopped buying specific kinds of food due to safety concern. Awareness of a pathogen is also associated with demographic characteristics. Consumers with at least some college education are more likely to have heard of any one of the four pathogens, except for Salmonella, than those with less education. Female consumers are more aware of Salmonella or E. coli than males. Awareness of Salmonella, Listeria, or E. coli is higher among those who have one or more children younger than 5 years old in their households or who come from households with annual income above $20,000. Consumers age 30 to 49 have higher awareness of Salmonella or Listeria than older consumers (50 and above). Compared to White consumers, Black, Hispanic, and other-race consumers are generally less aware of the pathogens, particularly Salmonella and E. coli. Northeastern consumers are more aware of Salmonella and E. coli and Western consumers less aware of Campylobacter or Listeria, than South consumers. 4. Discussion and conclusion Similar to findings by Altekruse et al. (1996), our results suggest that self-reported awareness of Salmonella is associated with safer self-reported hand washing practice. Specifically, we found the relationship in hand washing before meal preparation while they found the relationship in hand washing after handling raw meat. Hence, it appears that safer hand washing behavior is a consistent predictor of Salmonella awareness. Furthermore, this study finds that awareness of Campylobacter or E. coli is associated with serving thoroughly-cooked hamburgers, while McIntosh et al. (1994) reported that a higher number of five bacteria Texas consumers reported having heard of was associated with reported preference toward more cooked hamburger patties. We find that serving thoroughly-cooked hamburgers is associated with a statistically significant but practically insignificant decrease in the probability of having heard of Salmonella. By comparison, Altekruse et al. (1996) 410 C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 found that the awareness of Salmonella was not associated with the degree of doneness in hamburgers served. Therefore, despite that pathogen awareness is different from safe practices and higher awareness does not necessarily mean better practices, the totality of available evidence suggests that raising pathogen awareness can be a potentially useful approach to advocating safer food handling and preparation practices. As shown in this and previous research, pathogen awareness can have no or negative, albeit negligible, relationship with how hamburgers are served. Hence, the evidence also seems to suggest that higher awareness of pathogens does not necessarily translate into safer practices when a practice may affect the taste of a food. This phenomenon appears plausible since taste often plays a more important role in food preferences than food safety. Therefore, pathogen awareness could be less useful in promoting safer cooking practices than safer hand washing practices. It is noteworthy that the co-existence of both positive and negative as well as both significant and insignificant awareness-behavior relationships may also be attributable to the fact that all existing research is based on self-reports rather than objectively verifiable measures. As expected, awareness of pathogens, except Campylobacter, is in general higher among those who perceive homes, rather than other places, are where food safety problems are most likely to occur, it is very or somewhat common for people in the United States to become sick because of how food is handled or prepared in their homes, microorganism contamination is a very serious or serious food safety problem, or higher vulnerability to unsafe practices. In addition, pathogen awareness is positively related to awareness of potentially-risky foods and substances (sprouts, unpasteurized juices, and mercury). Therefore, the data appear to suggest that those who pay more attention to food safety information and are also more motivated to learn about food safety are more likely to be aware of the pathogens. We caution, however, that the almost uniform pattern of relationships between pathogen awareness and awareness of potentially-risky foods and substances, both based on self-reports, may be vulnerable to the ‘‘social desirability bias’’ (Maccoby & Maccoby, 1954). In other words, some survey respondents might have given answers that were believed to be intelligent or desirable. Compared to previous studies, our findings suggest two things about the prevalence of pathogen awareness. First, more US consumers said they had heard of Salmonella, E. coli, and Listeria in 2001 than in the early 1990s. As high as 94% consumers had heard of Salmonella in 2001, while the corresponding figure for 1993 and 1991 was approximately 80% (Altekruse et al., 1996; McIntosh et al., 1994). The awareness of E. coli was 90% in 2001, much higher than the 30% reported in McIntosh et al. (1994). Differences also exist in the awareness of Listeria among this study (32%), McIntosh et al. (1994) (21%), and Herrmann and Warland (2000) (52%). Note, however, Herrmann and Warland (2000) used a mail rather than a telephone survey and asked a different question (‘‘are you concerned about Listeria bacteria, or is that something you never have heard of’’). Thus, the notably different results in Herrmann and Warland (2000) could be attributable to differences in the mode of data collection, question wording, and time. Second, the percentage ranking in awareness among the four pathogens remained relatively stable between the early 1990s and 2001. Salmonella had consistently been the most widely heard pathogen, E. coli second, Listeria next, and Campylobacter least. The availability heuristic is a possible explanation for the differences over time in the awareness of Salmonella, E. coli, and Listeria and the consistent pattern of order ranking in the awareness. The availability heuristic, a simplified judgmental rule, posits that, in assessing the frequency of a risk, individuals often base their decisions on how easy it is to recall the risk and how recent occurrences of the risk are (Tversky & Kahneman, 1982, Chapter 1). Food safety incidents, especially those affecting many consumers and those resulting in deaths, are often reported by the media (IFICF, 2002; OllingerSynder & Matthews, 1994). Many consumers receive information about food safety through mass media such as newspapers, magazines, and television (ADA/ConAgra, 2000a). Hence, it is possible that, when asked whether they have heard of a pathogen, consumers would report awareness if the pathogen name is readily available in the memory and there are recent events related to the pathogen. The numbers of outbreaks associated with Salmonella, E. coli, and Listeria were all higher in 2001 than in 1992 (CDC, 2004). There had been several recent large and highly publicized foodborne illness outbreaks since the early 1990s, such as the 1993 E. coli O157:H7 outbreak related to undercooked hamburgers and in which four children died (CDC, 1993). In addition, the number of voluntary recalls of foods due to potential risk of pathogen contamination was also higher in 2000 than in early 1990s. For example, the number of recalls doubled from 1994 to 2000 for FSIS-inspected meat and poultry products due to Listeria contamination (USDA-FSIS, 1994, 2000). Availability heuristic may also explain why Salmonella is most heard of, E. coli second, Listeria next, and Campylobacter least. Epidemiological data show that, from 1993 to 2000, the annual numbers of outbreaks and cases are highest for Salmonella, second for E. coli, third for Campylobacter, and lowest for Listeria (CDC, 2000a; CDC, 2004). In addition, the awareness of Listeria could have been higher than that of Campylobacter because the death rate is higher among listeriosis victims than among campylobacteriosis victims. C.-T.J. Lin et al. / Food Quality and Preference 16 (2005) 401–412 Thus, our data suggest that self-reported awareness of the four pathogens is strongly influenced by the prevalence and visibility of foodborne illnesses associated with these pathogens. This finding, though reasonable, raises the possibility that the level of awareness varies according to what and when publicized foodborne illnesses occur. Insofar as such incidents are unpredictable and most foodborne illness cases go unreported (CAST, 1994), it would be useful to reach out to consumers with pathogen information and make the information widely and constantly available as higher awareness may be associated with safer food handling and preparation practices. Our findings suggest that awareness of different pathogens is related to college education and higher household income. This may be because less-educated or low-income consumers have less access to food safety information and less capacity to use the information. This may also suggest that less-educated or lower-income consumers may have put themselves under higher risk of foodborne illness due to lack of basic knowledge of microbial food safety. How to increase the awareness of these consumers therefore calls for more attention in food safety education. On the other hand, one cannot rule out the possibility that socially desirable responses may have prevented the disclosure of more genuine relationships between pathogen awareness and education and income in this as well as other survey-based studies. Two other demographic subgroups appear to have less awareness of pathogens—males and non-White consumers. The finding that males are less likely to have heard of Salmonella or E. coli is not surprising as previous food safety studies have repeatedly shown that male consumers, in general, are less interested than females in food safety issues and less likely to handle or prepare food safely (Adu-Nyako, Kunda, & Ralston, 2003; Albrecht, 1995; Altekruse et al., 1996; Klontz, Timbo, Fein, & Levy, 1995). But the finding does signal a potential area that deserves more attention in food safety education. Since these pathogens are major sources of foodborne illness and male consumers handle a lot of food preparation and grilling, especially in the summer (ADA/ConAgra, 2000b), increasing male consumers awareness can help reduce foodborne illness. NonWhite consumers are less likely to report awareness of pathogens, especially Salmonella and E. Coli. While the cause of this difference is worth investigation, the effectiveness of food safety education may benefit from paying special attention to non-White consumers. This is particularly important to Hispanics as they are now the largest minority in the United States and their number is expected to grow rapidly (Pew Hispanic Center, 2002), yet they may be more likely to engage in risky food consumption practices than other race/ethnic groups (FDA/USDA, 1999). The age variation indicates that middle-age consumers, 30–49 years old, are more aware of Salmonella and 411 Listeria than others. Meanwhile, there is a significant association between Salmonella, Listeria, and E. coli awareness and the presence of young children. Taken together, these findings suggest that many consumers who have just started a family or are raising children have some knowledge of microbial food safety. Since these consumers may be preparing foods for multiple household members, including young children, their food handling and preparation practices can affect not only their own health but also the health of other household members. Thus, it is important for food safety education to maintain or even increase food safety knowledge among these consumers, including awareness of foodborne pathogens. In conclusion, this study finds that there are noticeable variations in US consumers awareness of four major foodborne pathogens. The prevalence of awareness also changed between 2001 and the early 1990s. The variations and change appear to be related to the number and severity of illnesses associated with these pathogens. The study also finds that the awareness is associated with food safety perceptions, awareness of potentially risky foods and substances, food safety related behaviors, and demographics. 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