Prevalence, serotype, and antimicrobial resistance of Salmonella on broiler carcasses postpick and postchill in 20 U.S. processing plants.

The objective of this study was to measure the effect of broiler processing on the prevalence, serotype, and antimicrobial resistance profiles of salmonellae. Twenty U.S. commercial processing plants representing eight integrators in 13 states were included in the survey. In each of four replications, 10 carcasses from one flock were collected at rehang and 10 more carcasses were collected at postchill; each carcass was sampled by whole-carcass rinse. Salmonella organisms were isolated from carcass rinses by standard cultural techniques, serotypes were determined, and the resistance to 15 antimicrobials was measured. Overall, Salmonella was detected on 72% of carcasses at rehang (ranging from 35 to 97%) and on 20% of carcasses postchill (ranging from 2.5 to 60%). In every instance, a significant (P < 0.05) decrease in Salmonella prevalence was noted between rehang and postchill. The four most common serotypes, accounting for 64% of all Salmonella isolates, were Kentucky, Heidelberg, Typhimurium, and Typhimurium var. 5-; most isolates of Kentucky (52%), Heidelberg (79%), and Typhimurium (54%) serotypes were susceptible to all antimicrobial drugs tested. However, only 15% of the Typhimurium var. 5- isolates were pansusceptible; more than one-half of the isolates of this serotype were resistant to three or more drugs. No isolate of any serotype exhibited resistance to amikacin, ceftriaxone, ciprofloxacin, or trimethoprim-sulfamethoxazole. These data demonstrate that although processing lessens carcass contamination with Salmonella, antimicrobial-resistant isolates may still be present.

Prevalence and numbers of Campylobacter on broiler carcasses collected at rehang and postchill in 20 U.S. processing plants.

Campylobacter is a human pathogen associated with chicken and chicken meat products. This study was designed to examine the prevalence and number of Campylobacter on broiler chicken carcasses in commercial processing plants in the United States. Carcass samples were collected from each of 20 U.S. plants four times, roughly approximating the four seasons of 2005. At each plant on each sample day, 10 carcasses were collected at rehang (prior to evisceration), and 10 carcasses from the same flock were collected postchill. A total of 800 carcasses were collected at rehang and another 800 were collected postchill. All carcasses were subjected to a whole-carcass rinse, and the rinse diluent was cultured for Campylobacter. The overall mean number of Campylobacter detected on carcasses at rehang was 2.66 log CFU per ml of carcass rinse. In each plant, the Campylobacter numbers were significantly reduced by broiler processing; the mean concentration after chill was 0.43 log CFU/ml. Overall prevalence was also reduced by processing from a mean of > or =30 of 40 carcasses at rehang to > or =14 of 40 carcasses at postchill. Seven different on-line reprocessing techniques were applied in the test plants, and all techniques resulted in <1 log CFU/ml after chilling. Use of a chlorinated carcass wash before evisceration did not affect the postchill Campylobacter numbers. However, use of chlorine in the chill tank was related to lower numbers on postchill carcasses. Overall, U.S. commercial poultry slaughter operations are successful in significantly lowering the prevalence and number of Campylobacter on broiler carcasses during processing.

Assessment of post-Hurricane Katrina recovery in poultry slaughter establishments.

Control of bacterial contamination during poultry slaughter can be compromised by natural disaster. In October 2005, disaster recovery was evaluated in 11 broiler slaughter establishments 1 month after operations were disrupted by Hurricane Katrina. A questionnaire was administered to characterize the establishment's operational disruption. Carcass rinses were collected at the early and late stage of the slaughter process (rehang and postchill). Counts for generic Escherichia coli were determined for all rinses. Salmonella culture and serotyping were performed on postchill samples. Historical U.S. Food Safety and Inspection Service data on the presence of Salmonella also were examined. The mean duration of disruption was 6.3 days (range, 3 to 9 days). Loss of utilities (electricity and water) was the cause of prolonged recoveries. Most establishments (64%) did not exceed the m performance criteria threshold for generic E. coli (>2 log or 100 CFU/ml) during the recovery period. The mean reduction in E. coli counts between rehang and postchill was 2.3 log or 200 CFU/ml (range, 0.9 to 3.1 log CFU/ ml). Rinse samples from 5 of 11 establishments were positive for Salmonella. Of 12 Salmonella isolates that were recovered, eight were Salmonella Kentucky. Salmonella Heidelberg and Salmonella Thompson were recovered from one establishment, and two isolates of Salmonella Typhimurium were isolated from another. This study provided empirical reassurance that the establishments' processes controlled bacterial contamination. Data on reductions in E. coli counts during poultry slaughter may help establishments control microbial contamination. Other data (e.g., Salmonella and Campylobacter enumeration) may also have merit for this purpose.

A model to estimate the optimal sample size for microbiological surveys.

Estimating optimal sample size for microbiological surveys is a challenge for laboratory managers. When insufficient sampling is conducted, biased inferences are likely; however, when excessive sampling is conducted valuable laboratory resources are wasted. This report presents a statistical model for the estimation of the sample size appropriate for the accurate identification of the bacterial subtypes of interest in a specimen. This applied model for microbiology laboratory use is based on a Bayesian mode of inference, which combines two inputs: (ii) a prespecified estimate, or prior distribution statement, based on available scientific knowledge and (ii) observed data. The specific inputs for the model are a prior distribution statement of the number of strains per specimen provided by an informed microbiologist and data from a microbiological survey indicating the number of strains per specimen. The model output is an updated probability distribution of strains per specimen, which can be used to estimate the probability of observing all strains present according to the number of colonies that are sampled. In this report two scenarios that illustrate the use of the model to estimate bacterial colony sample size requirements are presented. In the first scenario, bacterial colony sample size is estimated to correctly identify Campylobacter amplified restriction fragment length polymorphism types on broiler carcasses. The second scenario estimates bacterial colony sample size to correctly identify Salmonella enterica serotype Enteritidis phage types in fecal drag swabs from egg-laying poultry flocks. An advantage of the model is that as updated inputs from ongoing surveys are incorporated into the model, increasingly precise sample size estimates are likely to be made.

Pathogenic and fecal Escherichia coil strains from turkeys in a commercial operation.

The biochemical phenotypes and antimicrobial susceptibility patterns of 105 clinical Escherichia coli isolates from flocks with colibacillosis in a turkey operation were compared with 1104 fecal E. coli isolates from 20 flocks in that operation. Clinical isolates and 194 fecal isolates with biochemical phenotypes or minimum inhibitory concentrations for gentamicin and sulfamethoxazole similar to clinical isolates were tested for somatic antigens and the potential virulence genes hylE, iss, tsh, and K1. The predominant biochemical phenotype of clinical isolates contained 21 isolates including 14 isolates belonging to serogroup 078 with barely detectable beta-D-glucuronidase activity. Thirty-five fecal isolates had biochemical phenotypes matching common phenotypes of clinical isolates. Sixty-six (63%) clinical isolates exhibited intermediate susceptibility or resistance to gentamicin and sulfamethoxazole compared with 265 (24%) fecal isolates (P < 0.001). Seventy-seven clinical isolates reacted with O-antisera, of which 51 (66%) belonged to the following serogroups: O1, O2, O8, O25, O78, O114, and O119. In comparison, 8 of 35 (23%) fecal isolates subtyped on the basis of biochemical phenotype belonged to these serogroups and four of 167 (2%) fecal isolates subtyped on the basis of their antimicrobial resistance patterns belonged to these serogroups. Iss, K1, and tsh genes were detected more often among clinical isolates than these fecal isolates (P < 0.05). In summary, a small subgroup of E. coli strains caused most colibacillosis infections in this operation. These strains existed at low concentration in normal fecal flora of healthy turkeys in intensively raised flocks. The data suggest that colibacillosis in turkey operations may be due to endogenous infections caused by specialized pathogens.

Evaluation of safe food-handling instructions on raw meat and poultry products.

Every year in the United States, millions of people become ill, thousands of people die, and substantial economic costs are incurred from foodborne diseases. As a measure to prevent foodborne diseases, since July 1994, the U.S. Department of Agriculture has required that safe food-handling labels be placed on retail packages of raw or partially cooked meat and poultry products. Through selected states' Behavioral Risk Factor Surveillance System (BRFSS) interviews, survey data were collected to determine the proportion of adults aware of the label and adults who reported changing their raw meat-handling practices because of the label. Fifty-one percent of the 14,262 respondents reported that they had seen the label. Of these, 79% remembered reading the label, and 37% of persons who reported that they had seen and read the label reported changing their raw meat preparation methods because of the label. Women were more likely than men to have read the label, as were persons who are at least 30 years of age compared to younger adults (P < 0.05). Both label awareness and risky food-handling behaviors increased with education and income, suggesting that safe food-handling labels have limited influence on consumer practices. Our results also suggest that the labels might be more effective in discouraging cross-contamination than in promoting thorough cooking practices. We suggest that the label is only one component among many food safety education programs that are needed to inform consumers about proper food-handling and preparation practices and to motivate persons who have risky food-handling and preparation behaviors to change these behaviors.

Vibrio gastroenteritis in the US Gulf of Mexico region: the role of raw oysters.

We examined clinical and epidemiological features of 575 laboratory-confirmed cases of vibrio gastroenteritis in Alabama, Florida, Louisiana, and Texas from 1988 to 1997 (the US Gulf of Mexico Regional Vibrio Surveillance System). Illnesses occurred year round, with peaks in spring and autumn. Illnesses lasted a median of 7 days and included fever in half of patients and bloody stools in 25% of patients with relevant information. Seventy-two percent of patients reported no underlying illnesses. In the week before onset, 236 (53%) of 445 patients for whom data were available ate raw oysters, generally at a restaurant or bar. Educational efforts should address the risk of vibrio gastroenteritis for raw oyster consumers, including healthy individuals. Further studies should examine environmental conditions affecting vibrio counts on seafood and processing technologies to enhance the safety of raw oysters.

An increase in sporadic and outbreak-associated Salmonella enteritidis infections in Wisconsin: the role of eggs.

In Wisconsin, reported Salmonella enterica serotype enteritidis (SE) infections during 1997 more than doubled compared with the previous 9 years. A case-control study was conducted to determine risk factors for sporadic infections, and results of outbreak investigations were reviewed. Eating raw eggs (matched odds ratio [MOR]=14.5; 95% confidence interval [CI], 1.7-591.6), eating raw or undercooked eggs (MOR=5.8; 95% CI, 1.3-28.0), eating any eggs (MOR=4.2; 95% CI, 1.2-16.2), and dining at a restaurant (MOR=4.7; 95% CI, 1.4-18.4) were associated with infection in the case-control study. For 3 of the 8 outbreaks, a probable source was identified, in each instance, foods containing eggs. Human infections decreased after eggs were diverted from implicated flocks. This epidemic demonstrates the continuing need for quality assurance on egg farms and enhanced education of consumers and commercial food preparers regarding safe handling of eggs.

A Mexican restaurant-associated outbreak of Salmonella Enteritidis type 34 infections traced to a contaminated egg farm.

In May 1996, the Georgia Division of Public Health was notified about a cluster of persons with Salmonella Enteritidis (SE) infections in Waycross, Georgia. A matched pair case-control study to determine risk factors for illness found a statistically significant association of SE infection with a history of having eaten at Restaurant A during the 5 days before onset of illness (relative risk = 13 [95% confidence interval (CI) = 3-62, P < 0.01]). In a second case-control study, to determine specific food exposures, consumption of a deep-fried Mexican dish (chile relleno) (4 of 21 cases vs. 0 of 26 controls, odds ratio undefined, 95% CI > 1.46, P = 0.034) was found to be significantly associated with SE infection. An environmental investigation found evidence of suboptimal food storage and cooking temperatures at Restaurant A; cross contamination of foods may have contributed to the low attributable risk identified for chile rellenos. Five of 37 Restaurant A food and environment specimens yielded SE strains. All five positive specimens were from chiles rellenos. Of the seven outbreak-associated strains (six patient isolates and one food isolate from Restaurant A) for which phage typing was conducted, all were phage type 34. A FDA traceback investigation through Restaurant A's single-egg supplier identified the potential source as three interrelated farms in South Carolina. Environmental culture from one of these farms yielded SE phage type 34. As a result of this outbreak, FDA helped institute a statewide egg quality-assurance programme in South Carolina to minimize SE contamination of eggs.

A multi-state survey of consumer food-handling and food-consumption practices.

INTRODUCTION: In the United States, foodborne infections cause an estimated 6.5-33 million illnesses a year. Also included in the burden of foodborne illnesses are sequelae such as hemolytic uremic syndrome, Guillain-Barré syndrome, and reactive arthritis. Surveillance for risky food-handling and food-consumption practices can be used to identify high-risk populations, develop educational efforts, and evaluate progress toward risk reduction. DESIGN: In 1995 and 1996, Behavioral Risk Factor Surveillance System interviews of 19,356 adults in eight states (1995: Colorado, Florida, Missouri, New York, and Tennessee; 1996: Indiana, New Jersey, and South Dakota) included questions related to food-handling and/or food-consumption practices. Risky food-handling and food-consumption practices were not uncommon. Overall, 19% of respondents did not adequately wash hands or cutting boards after contact with raw meat or chicken. During the previous year, 20% ate pink hamburgers, 50% ate undercooked eggs, 8% ate raw oysters, and 1% drank raw milk. Men were more likely to report risky practices than women. The prevalence of most risky behaviors increased with increasing socioeconomic status. CONCLUSION: Targeted education efforts may reduce the frequency of these behaviors. Periodic surveillance can be used to assess effectiveness. In addition to consumer education, prevention efforts are needed throughout the food chain including on the farm, in processing, distribution, and at retail.

Campylobacter jejuni--an emerging foodborne pathogen.

Campylobacter jejuni is the most commonly reported bacterial cause of foodborne infection in the United States. Adding to the human and economic costs are chronic sequelae associated with C. jejuni infection--Guillian-Barré syndrome and reactive arthritis. In addition, an increasing proportion of human infections caused by C. jejuni are resistant to antimicrobial therapy. Mishandling of raw poultry and consumption of undercooked poultry are the major risk factors for human campylobacteriosis. Efforts to prevent human illness are needed throughout each link in the food chain.

Deaths from hematopoietic and other cancers in relation to permanent hair dye use in a large prospective study (United States).

OBJECTIVES: To assess in a large prospective study whether women who used permanent hair dye, especially dark dye for many years, experienced increased death rates from hematopoietic and other cancers that have been associated with hair dye use in some previous reports. METHODS: In 1982, 547,586 women provided information on use of permanent hair dye and other lifestyle factors when enrolled in an American Cancer Society (ACS) prospective study. We extended mortality follow-up from 7 to 12 years. Using Cox proportional hazards modeling we compared death rates from hematopoietic and other cancers among women according to their hair dye use at baseline with death rates in unexposed women. RESULTS: The adjusted death rate from all cancers combined was marginally lower among women who ever used hair dye than nonusers (relative risk [RR] = 0.9; 95% confidence interval [CI] = 0.9-1.0). Mortality from all hematopoietic cancers was marginally higher among users than nonusers (RR = 1.1; CI = 1.0-1.2), and increased with an index that combined duration of use and darker coloration (test of trend p = 0.02). Women who used black or brown dye for 10 or more years experienced somewhat higher death rates from non-Hodgkin's lymphoma and (for black dye only) multiple myeloma. The temporal increase in death rates from non-Hodgkin's lymphoma and multiple myeloma between 1982-88 and 1989-94 was similar for women in our study who never used hair dyes to the increase among all US women. CONCLUSIONS: If prolonged use of dark permanent hair dyes contributes to death rates from non-Hodgkin's lymphoma and multiple myeloma, then the increase is small and difficult to detect reliably even in large prospective studies. The use of permanent hair dye is unlikely to be a major contributor to the temporal rise in non-Hodgkin's lymphoma and multiple myeloma in the US.

Cheese-associated outbreaks of human illness in the United States, 1973 to 1992: sanitary manufacturing practices protect consumers.

To identify contributing factors for cheese-associated outbreaks, we reviewed all cheese-associated outbreaks of human illness reported to the Centers for Disease Control and Prevention (CDC) with onsets during 1973 to 1992. The infrequency of large, cheese-associated outbreaks was notable because such outbreaks had been a frequent public health problem before the mid-20th century. Of 32 reported cheese-associated outbreaks, 11 attributed to manufacturing errors caused most of the illnesses and hospitalizations and all 58 deaths. Important factors in these 11 outbreaks were manufacturing cheese with raw or improperly pasteurized milk and postpasteurization contamination. If current Food and Drug Administration sanitary requirements for cheesemaking had been met, these outbreaks would have been preventable. In two outbreaks of Salmonella infections, fewer than 10 Salmonella per 100 g of cheese were detected. In two outbreaks of Brucella infections, efforts to recover the pathogen from the implicated cheese were unsuccessful, emphasizing the inadequacy of end product testing for assuring consumer safety. Curing cheeses kills most bacteria present in cheeses; however, evidence from sources other than the CDC Foodborne Disease Outbreak Surveillance System suggests that curing alone may not be a sufficient pathogen control step to eliminate Salmonella, Listeria, and E. coli O157:H7 from cheese.

Multistate surveillance for food-handling, preparation, and consumption behaviors associated with foodborne diseases: 1995 and 1996 BRFSS food-safety questions.

PROBLEM/CONDITION: In 1995, CDC, the Food and Drug Administration (FDA), and several state health departments collaboratively developed questions regarding food safety. This set of questions was used to collect data about food-handling, preparation, and consumption behaviors that have been associated with foodborne diseases in adults. These data will help characterize persons at high risk for foodborne illness and assist in developing food-safety education strategies for consumers and foodhandlers that are intended to reduce foodborne illness. REPORTING PERIOD COVERED: January 1995-December 1996. DESCRIPTION OF SYSTEM: Data were collected by using the 12 food-safety questions, which were administered with the 1995 Behavioral Risk Factor Surveillance Systems (BRFSS) in Colorado, Florida, Missouri, New York, and Tennessee, and the 1996 BRFSS in Indiana and New Jersey. In addition, data were collected in South Dakota from two of the standardized questions that deal with consumption of undercooked eggs and pink hamburgers. The BRFSS is a state-based system that surveys noninstitutionalized adults by telephone about their health behaviors and practices. RESULTS: This study included 19,356 completed questionnaires (2,461 in Colorado; 3,335 in Florida; 2,212 in Indiana; 1,572 in Missouri; 3,149 in New Jersey; 2,477 in New York; 2,110 in South Dakota; and 2,040 in Tennessee). During the previous 12 months, 50.2% of respondents reported eating undercooked eggs (95% confidence interval [CI] = 49.2-51.2); 23.8% reported eating home-canned vegetables (95% CI = 22.5-24.5); 19.7% reported eating pink hamburgers (95% CI = 18.9-20.5); 8.0% reported eating raw oysters (95% CI = 7.5-8.5); and 1.4% reported drinking raw milk (95% CI = 1.2-1.6). The prevalence of not washing hands with soap after handling raw meat or chicken and not washing a cutting board with soap or bleach after using it for cutting raw meat or chicken were 18.6% (95% CI = 17.8-19.4) and 19.5% (95% CI = 18.6-20.4), respectively. Less than half of respondents (45.4%, 95% CI = 44.2-46.6) reported seeing safe food-handling label information on raw meat products. In addition, among those persons who reported they remembered seeing the label information, 77.2% (95% CI = 76.0-78.4) remembered reading the label information, and 36.7% reported changing their meat and poultry preparation habits because of the labels (95% CI = 35.2-38.2). When population characteristics were considered in the analysis, all high-risk food-handling, preparation, and consumption behaviors were more prevalent in men than in women. Eating pink hamburgers during the previous 12 months was more commonly reported by whites (22.3%) than by blacks (6.5%). The prevalence of reported consumption of pink hamburgers during the previous. 12 months decreased with age (18-29 years: 21.8%, 30-59 years: 21.9%, and 60-99 years: 13.2%); increased with education (less than grade 12: 12.0%, high school graduate: 16.5%, and any college education: 24.0%); and increased with income (< $15,000: 11.8%, $15,000-$34,999: 17.6%, $35,000-$49,999: 22.0%, and > or = $50,000: 28.6%). INTERPRETATION: During 1995-1996, several high-risk food-handling, preparation, and consumption behaviors were common, and some were particular to specific population groups. Based on this analysis, interventions are needed to reduce the prevalence of these risky behaviors. All consumers and foodhandlers could benefit from food-safety education. ACTIONS TAKEN: Behavioral surveillance systems can provide data that identify persons or groups in which behaviors associated with foodborne diseases are more common and who are at higher risk for foodborne illness. State-specific data can assist in developing food-safety education programs and, if collected periodically, can be used to evaluate program effectiveness.

The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992.

OBJECTIVES: This study describes the epidemiology of raw milk-associated outbreaks reported to the Centers for Disease Control and Prevention from 1973 through 1992. METHODS: Surveillance data for each reported raw milk-associated outbreak were reviewed. A national survey was conducted to determine the legal status of intrastate raw milk sales for the period 1973 through 1995. RESULTS: Forty-six raw milk-associated outbreaks were reported during the study period; 40 outbreaks (87%) occurred in states where the intrastate sale of raw milk was legal. CONCLUSIONS: Consumption of raw milk remains a preventable cause of foodborne disease outbreaks.

Factors in the emergence of food borne diseases.

Food borne diseases are an important public health problem. Over the past two decades, the epidemiology of food borne diseases has changed rapidly as a consequence of changes in the social environment and the ability of pathogens to adapt to new niches. Several newly recognized pathogens have emerged and well-recognized pathogens have increased in prevalence or become associated with new food vehicles. Several factors have contributed to the changing patterns of food borne diseases, and addressing food borne diseases will require rapid surveillance and effective prevention strategies. This article examines these factors and briefly addresses prevention and control of food borne diseases.

Microbial food borne pathogens. Campylobacter jejuni.

Campylobacter jejuni is the most common food borne bacterial pathogen and leading cause of food borne disease in humans in the United States and other industrialized nations. Approximately four million cases of human campylobacteriosis occur each year in the United States. Although the majority of cases consist of limited diarrheal illness, severe sequelae can affect a small portion of patients with campylobacteriosis that may include reactive arthritis and Guillain-Barré syndrome. Animal reservoirs primarily include poultry (C. jejuni) and swine (C. coli). Pathogen reduction during poultry processing and safe handling of raw poultry in the kitchen are needed to prevent illness.

Foodborne diseases. Emerging pathogens and trends.

The epidemiology of foodborne diseases is rapidly changing. In the past 15 years, new foodborne pathogens, such as Campylobacter jejuni and Escherichia coli O157:H7, have emerged as important public health problems. Well-recognized pathogens, such as Salmonella serotype Enteritidis, have increased in prevalence or become associated with new vehicles, and pathogens such as C. jejuni and S. Typhimurium are becoming increasingly resistant to antimicrobial agents. Evolving trends in foodborne diseases are being driven by the same factors that have led to the emergence of other infectious diseases: changes in demographic characteristics of the population, human behavior, industry, and technology and the shift toward a global economy, microbial adaptation, and breakdown in the public health infrastructure. Addressing emerging foodborne disease will require more sensitive and timely surveillance, enhanced methods of laboratory identification and subtyping, and identification of effective prevention and control strategies.