Improving inclusion and exclusion criteria in foodborne illness outbreak investigations: a case study.

The practice of foodborne illness outbreak investigations has evolved, shifting away from large-scale community case-control studies towards more focused case exposure assessments and sub-cluster investigations to identify contaminated food sources. Criteria to include or exclude cases are established to increase the efficiency of epidemiological analyses and traceback activities, but these criteria can also affect the investigator's ability to implicate a suspected food vehicle. A 2010 outbreak of Salmonella ser. Hvittingfoss infections associated with a chain of quick-service restaurants (Chain A) provided a useful case study on the impact of exclusion criteria on the ability to identify a food vehicle. In the original investigation, a case-control study of restaurant-associated cases and well meal companions was conducted at the ingredient level to identify a suspected food vehicle; however, 21% of cases and 22% of well meal companions were excluded for eating at Chain A restaurants more than once during the outbreak. The objective of this study was to explore how this decision affected the results of the outbreak investigation.

Developing a risk management framework to improve public health outcomes by enumerating Salmonella in ground turkey.

Salmonella spp. continue to be a leading cause of foodborne morbidity worldwide. To assess the risk of foodborne disease, current national regulatory schemes focus on prevalence estimates of Salmonella and other pathogens. The role of pathogen quantification as a risk management measure and its impact on public health is not well understood. To address this information gap, a quantitative risk assessment model was developed to evaluate the impact of pathogen enumeration strategies on public health after consumption of contaminated ground turkey in the USA. Public health impact was evaluated by using several dose-response models for high- and low-virulent strains to account for potential under- or overestimation of human health impacts. The model predicted 2705-21 099 illnesses that would result in 93-727 reported cases of salmonellosis. Sensitivity analysis predicted cooking an unthawed product at home as the riskiest consumption scenario and microbial concentration the most influential input on the incidence of human illnesses. Model results indicated that removing ground turkey lots exceeding contamination levels of 1 MPN/g and 1 MPN in 25 g would decrease the median number of illnesses by 86-94% and 99%, respectively. For a single production lot, contamination levels higher than 1 MPN/g would be needed to result in a reported case to public health officials. At contamination levels of 10 MPN/g, there would be a 13% chance of detecting an outbreak, and at 100 MPN/g, the likelihood of detecting an outbreak increases to 41%. Based on these model prediction results, risk management strategies should incorporate pathogen enumeration. This would have a direct impact on illness incidence linking public health outcomes with measurable food safety objectives.

Factors associated with recovery of meat products following recalls due to Shiga toxin-producing Escherichia coli.

Food-product recall data for recalls due to Shiga toxin-producing Escherichia coli (STEC) from 2000 to 2012 were obtained for establishments regulated by the United States Department of Agriculture, Food Safety and Inspection Service (FSIS). Statistical tests were used to assess the factors associated with recovery of product following STEC recalls along with the relationship between cluster detection and jurisdictions. Our results indicated that the percentage of recalled product recovered following a recall action due to STEC was dependent on the complexity of distribution, type of distribution, amount of time between production and recall dates, and the number of pounds of product recalled. Illness-related STEC recalls were associated with a lower percentage of product recovery which was probably impacted by larger amounts of product recalled, broader production scope, and delays from epidemiological and traceback investigations. Further, detection of illnesses related to STEC recalls seemed to be enhanced in states with additional resources and a history of successful foodborne investigations. This makes an argument for additional resources dedicated to public health agencies specifically for the surveillance of foodborne illnesses.

The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities.

Foodborne outbreaks from contaminated fresh produce have been increasingly recognized in many parts of the world. This reflects a convergence of increasing consumption of fresh produce, changes in production and distribution, and a growing awareness of the problem on the part of public health officials. The complex biology of pathogen contamination and survival on plant materials is beginning to be explained. Adhesion of pathogens to surfaces and internalization of pathogens limits the usefulness of conventional processing and chemical sanitizing methods in preventing transmission from contaminated produce. Better methods of preventing contamination on the farm, or during packing or processing, or use of a terminal control such as irradiation could reduce the burden of disease transmission from fresh produce. Outbreak investigations represent important opportunities to evaluate contamination at the farm level and along the farm-to-fork continuum. More complete and timely environmental assessments of these events and more research into the biology and ecology of pathogen-produce interactions are needed to identify better prevention strategies.

Analysis of the FoodNet case-control study of sporadic Salmonella serotype Enteritidis infections using persons infected with other Salmonella serotypes as the comparison group.

Use of well persons as the comparison group for laboratory-confirmed cases of sporadic salmonellosis may introduce ascertainment bias into case-control studies. Data from the 1996-1997 FoodNet case-control study of laboratory-confirmed Salmonella serogroups B and D infection were used to estimate the effect of specific behaviours and foods on infection with Salmonella serotype Enteritidis (SE). Persons with laboratory-confirmed Salmonella of other serotypes acted as the comparison group. The analysis included 173 SE cases and 268 non-SE controls. SE was associated with international travel, consumption of chicken prepared outside the home, and consumption of undercooked eggs prepared outside the home in the 5 days prior to diarrhoea onset. SE phage type 4 was associated with international travel and consumption of undercooked eggs prepared outside the home. The use of ill controls can be a useful tool in identifying risk factors for sporadic cases of Salmonella.

The use of clinical profiles in the investigation of foodborne outbreaks in restaurants: United States, 1982-1997.

Improving the efficiency of outbreak investigation in restaurants is critical to reducing outbreak-associated illness and improving prevention strategies. Because clinical characteristics of outbreaks are usually available before results of laboratory testing, we examined their use for determining contributing factors in outbreaks caused by restaurants. All confirmed foodborne outbreaks reported to the Centers for Disease Control and Prevention (CDC) from 1982 to 1997 were reviewed. Clinical profiles were developed based on outbreak characteristics. We compared the percentage of contributing factors by known agent and clinical profile to their occurrence in outbreaks of unclassified aetiology. In total, 2246 foodborne outbreaks were included: 697 (31%) with known aetiology and 1549 (69%) with aetiology undetermined. Salmonella accounted for 65% of outbreaks with a known aetiology. Norovirus-like clinical profiles were noted in 54% of outbreaks with undetermined aetiology. Improper holding times and temperatures were associated with outbreaks caused by Clostridium perfringens, Bacillus cereus, Staphylococcus aureus, and Salmonella, and also with outbreaks of undetermined aetiology that fitted diarrhoea-toxin and vomiting-toxin clinical profiles. Poor personal hygiene was associated with norovirus, Shigella, and Salmonella, and also with outbreaks that fitted norovirus-like and vomiting-toxin clinical profiles. Contributing factors were similar for outbreaks with known aetiology and for those where aetiology was assigned by corresponding clinical profile. Rapidly categorizing outbreaks by clinical profile, before results of laboratory testing are available, can help identification of factors which contributed to the occurrence of the outbreak and will promote timely and efficient outbreak investigations.

Disinfection of fabrics and carpets artificially contaminated with calicivirus: relevance in institutional and healthcare centres.

Fabrics and carpets are used widely as surface coverings or linens in healthcare settings and are prone to contamination with infectious agents such as noroviruses (NoVs). Laundering, water cleaning and vacuuming are considered to be adequate for routine cleaning of these materials, but no standard procedure for their disinfection is available in case of contamination. Testing disinfectants for their efficacy against NoVs is difficult because these viruses cannot be cultivated in vitro. Therefore, feline calicivirus (FCV) has gained acceptance as a surrogate model for NoVs in disinfectant efficacy testing. The present study evaluated five disinfectants against FCV on various fabrics or carpets. FCV was dried on fabrics and carpets, followed by treatment with a given disinfectant for a defined contact time of 1, 5 or 10 min. The surviving virus was then eluted and titrated in Crandell-Reese feline kidney cells to determine virus inactivation. A disinfectant was considered to be effective if it inactivated at least 99% of the applied virus. Metricide, an activated dialdehyde-based product, was found to be the most effective disinfectant on all types of fabric and carpet, inactivating more than 99.99% of the virus in 1-10 min. In general, effectiveness of disinfectants increased with an increase in exposure time from 1 to 10 min. The disinfection of carpets was more difficult than the disinfection of fabrics; 100% polyester was the least amenable to disinfection. Only Metricide and Microbac-II (a phenolic compound) were able to inactivate 99% of FCV on 100% polyester. In summary, activated dialdehyde was found to be uniformly active against FCV on all types of material tested.

Efficacy of commonly used disinfectants for the inactivation of calicivirus on strawberry, lettuce, and a food-contact surface.

Norwalk and Norwalk-like viruses (NLVs) are important causes of foodborne gastroenteritis in restaurant-related outbreaks. Efficacy of common disinfection methods against these viruses on food-contact surfaces and fresh produce is not known partially because of their nonculturability. Seven commercial disinfectants for food-contact surfaces and three sanitizers for fruits and vegetables were tested against cultivable feline calicivirus (FCV). Disks of stainless steel, strawberry, and lettuce were contaminated with known amounts of FCV. The disinfectants were applied at one, two, and four times the manufacturer's recommended concentrations for contact times of 1 and 10 min. The action of disinfectant was stopped by dilution, and the number of surviving FCVs was determined by titration in cell cultures. An agent was considered effective if it reduced the virus titer by at least 3 log10 from an initial level of 10(7) 50% tissue culture infective dose. None of the disinfectants was effective when used at the manufacturer's recommended concentration for 10 min. Phenolic compounds, when used at two to four times the recommended concentration, completely inactivated FCV on contact surfaces. A combination of quaternary ammonium compound and sodium carbonate was effective on contact surfaces at twice the recommended concentration. Rinsing of produce with water alone reduced virus titer by 2 log10. On artificially contaminated strawberry and lettuce, peroxyacetic acid and hydrogen peroxide was the only effective formulation when used at four times the manufacturers' recommended concentration for 10 min. These findings suggest that FCV and perhaps NLVs are very resistant to commercial disinfectants. However, phenolic compounds at two to four times their recommended concentrations appear to be effective at decontaminating environmental surfaces and may help control foodborne outbreaks of calicivirus in restaurants.

Use of molecular subtyping in surveillance for Salmonella enterica serotype typhimurium.

BACKGROUND: Because Salmonella enterica serotype typhimurium is the most common serotype isolated from persons with salmonellosis in the United States, it is difficult to detect unusual clusters or outbreaks. To determine whether molecular subtyping could be useful in public health surveillance for S. enterica serotype typhimurium, the Minnesota Department of Health initiated the routine use of pulsed-field gel electrophoresis (PFGE) of isolates. METHODS: Beginning in 1994, all S. enterica serotype typhimurium isolates submitted by clinical laboratories to the Department of Health were subtyped by PFGE. A standard questionnaire was used to interview patients about possible sources of infection. RESULTS: From 1994 through 1998, 998 cases of infection with S. enterica serotype typhimurium were reported to the Minnesota Department of Health (4.4 cases per 100,000 person-years). PFGE was performed on 958 of the isolates (96 percent), and 174 different patterns were identified. Sixteen outbreaks with a common source were identified, accounting for 154 cases. PFGE subtyping made it possible to confirm 10 outbreaks that involved small numbers of cases in institutional settings. Of six larger, community-based outbreaks, four would probably not have been recognized without PFGE subtyping. These four outbreaks accounted for 96 of the 154 culture-confirmed outbreak cases (62 percent). Fifty-six of 209 isolates tested for antimicrobial susceptibility (27 percent) were resistant to at least five antimicrobial agents. The multidrug-resistant isolates identified had unique PFGE patterns. CONCLUSIONS: Routine molecular subtyping of S. enterica serotype typhimurium by PFGE can improve the detection of outbreaks and aid in the identification of multidrug-resistant strains. Combining routine molecular subtyping with a method of rapid communication among public health authorities can improve surveillance for S. enterica serotype typhimurium infections.

Epidemiologic profiling: evaluating foodborne outbreaks for which no pathogen was isolated by routine laboratory testing: United States, 1982-9.

The objective was to evaluate foodborne outbreaks of undetermined aetiology by comparing them to pathogen-specific epidemiologic profiles of laboratory-confirmed foodborne outbreaks. National foodborne outbreak data reported to CDC during 1982-9 were categorized by clinico-epidemiologic profiles based on incubation, duration, percent vomiting, fever and vomiting to fever ratio. From the pathogen-specific profiles, five syndromes were developed: a vomiting-toxin syndrome resembling Bacillus cereus and Staphylococcus aureus; a diarrhoea-toxin syndrome characteristic of Clostridium perfringens, a diarrhaeogenic Escherichia coli syndrome, a Norwalk-like virus syndrome, and a salmonella like syndrome. Of 712 outbreaks, 624 (87.6%) matched one of five syndromes; 340 (47.8%) matched the Norwalk-like syndrome and 83 (11.7%) matched the salmonella-like syndrome. After combining information on known pathogens and epidemiologic profiles, only 88 (12.4%) outbreaks remained unclassified. Norwalk-like virus outbreaks appear as common as salmonella-like outbreaks. We conclude that profiling can help classify outbreaks, guide investigations and direct laboratory testing to help detect new and emerging pathogens.

The impact of foodborne calicivirus disease: the Minnesota experience.

The first outbreaks of Norwalk virus gastroenteritis in Minnesota were confirmed in 1982. Since then, Norwalk-like caliciviruses have been recognized to be the most common cause of foodborne disease outbreaks, accounting for 41% of all confirmed foodborne outbreaks in Minnesota from 1981-1998. Although laboratory confirmation of caliciviruses in stool samples was not attempted in most of these outbreaks, all conformed to epidemiologic criteria for defining outbreaks of Norwalk virus. Since 1996, the availability of polymerase chain reaction testing at the Minnesota Department of Health has allowed for the confirmation of calicivirus infection among patients involved in epidemiologically defined outbreaks of viral gastroenteritis. Results have confirmed the usefulness of characterizing foodborne disease outbreaks by epidemiologic criteria and also confirmed the importance of human caliciviruses as the leading cause of foodborne disease outbreaks in Minnesota.

Outbreaks of salmonellosis associated with eating uncooked tomatoes: implications for public health. The Investigation Team.

Laboratory-based surveillance of salmonella isolates serotyped at four state health departments (Illinois, Michigan, Minnesota and Wisconsin) led to the identification of multistate outbreaks of salmonella infections during 1990 (176 cases of S. javiana) and 1993 (100 cases of S. montevideo). Community-based case-control studies and product traceback implicated consumption of tomatoes from a single South Carolina tomato packer (Packer A) MOR 16.0; 95% CI2.1, 120.6; P < 0.0001 in 1990 and again in 1993 (MOR 5.7; 95 % CI 1.5, 21.9; P = 0.01) as the likely vehicle. Contamination likely occurred at the packing shed, where field grown tomatoes were dumped into a common water bath. These outbreaks represent part of a growing trend of large geographically dispersed outbreaks caused by sporadic or low-level contamination of widely distributed food items. Controlling contamination of agricultural commodities that are also ready-to-eat foods, particularly fruits and vegetables, presents a major challenge to industry, regulators and public health officials.

Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. Investigation Team.

BACKGROUND: Increasing resistance to quinolones among campylobacter isolates from humans has been reported in Europe and Asia, but not in the United States. We evaluated resistance to quinolones among campylobacter isolates from Minnesota residents during the period from 1992 through 1998. METHODS: All 4953 campylobacter isolates from humans received by the Minnesota Department of Health were tested for resistance to nalidixic acid. Resistant isolates and selected sensitive isolates were tested for resistance to ciprofloxacin. We conducted a case-comparison study of patients with ciprofloxacin-resistant Campylobacter jejuni isolated during 1996 and 1997. Domestic chicken was evaluated as a potential source of quinolone-resistant campylobacter. RESULTS: The proportion of quinolone-resistant C. jejuni isolates from humans increased from 1.3 percent in 1992 to 10.2 percent in 1998 (P<0.001). During 1996 and 1997, infection with quinolone-resistant C. jejuni was associated with foreign travel and with the use of a quinolone before the collection of stool specimens. However, quinolone use could account for no more than 15 percent of the cases from 1996 through 1998. The number of quinolone-resistant infections that were acquired domestically also increased during the period from 1996 through 1998. Ciprofloxacin-resistant C. jejuni was isolated from 14 percent of 91 domestic chicken products obtained from retail markets in 1997. Molecular subtyping showed an association between resistant C. jejuni strains from chicken products and domestically acquired infections in Minnesota residents. CONCLUSIONS: The increase in quinolone-resistant C. jejuni infections in Minnesota is largely due to infections acquired during foreign travel. However, the number of quinolone-resistant infections acquired domestically has also increased, largely because of the acquisition of resistant strains from poultry. The use of fluoroquinolones in poultry, which began in the United States in 1995, has created a reservoir of resistant C. jejuni.

A statewide survey of immunization rates in Minnesota school age children: implications for targeted assessment and prevention strategies.

BACKGROUND: A retrospective statewide immunization survey of the 69115 Minnesota children who entered kindergarten in 1992 was conducted. METHODS: Information was collected from school immunization records on date of birth, dates of vaccination for each dose of vaccine, address of residence and race/ethnicity (when available). Immunization rates were assessed retrospectively for each month of a child's life from 2 to 48 months of age. Age-appropriate immunization was defined as receipt of all scheduled vaccines within 30 days of the recommended age. RESULTS: Immunization levels varied by vaccine, age of the child and race/ethnicity. For example at 19 months of age, 73% of students had received measles, mumps, rubella vaccine; however, only 39% had received their fourth dose of diphtheria, tetanus and pertussis vaccine. White, non-Hispanic students consistently had higher vaccination rates than children of other racial/ ethnic groups. For example 45% of white, non-Hispanic students were age-appropriately vaccinated at 16 months of age compared with 25% of Blacks, 30% of American Indians, 30% of white Hispanics and 28% of Asian-Pacific Islanders (Mantel-Haenzel chi square, P < 0.001 for each comparison). Furthermore coverage rates frequently varied significantly by neighborhood, thereby identifying pockets of underimmunization within communities. CONCLUSION: Our data demonstrate that vaccination rates can vary substantially by age, race/ ethnicity and neighborhood. Detailed immunization assessment is necessary so that effective targeted interventions can be developed.

An outbreak of foodborne illness caused by Escherichia coli O39:NM, an agent not fitting into the existing scheme for classifying diarrheogenic E. coli.

An outbreak of gastrointestinal illness with clinical and epidemiologic features of enterotoxigenic Escherichia coli (ETEC) occurred among patrons of a restaurant during April 1991. Illnesses among several groups of patrons were characterized by diarrhea (100%) and cramps (79%-88%) lasting a median of 3-5 days. Median incubation periods ranged from 50 to 56 h. A nonmotile strain of E. coli (E. coli O39), which was negative for heat-labile (LT) and heat-stable (STa, STb) ETEC toxins, was isolated only from ill patrons. This organism produced enteroaggregative E. coli heat-stable enterotoxin 1 and contained the enteropathogenic E. coli gene locus for enterocyte effacement; it did not display mannose-resistant adherence, but produced attaching and effacing lesions in the absence of mannose on cultured HEp-2 cells. E. coli that are not part of highly characterized but narrowly defined groups may be important causes of foodborne illness.

Surveillance for Escherichia coli O157:H7 infections in Minnesota by molecular subtyping.

BACKGROUND: Escherichia coli O157:H7 is a leading cause of diarrhea and the hemolytic-uremic syndrome. Current public health surveillance for E. coli O157:H7 requires considerable resources; traditional methods lack the sensitivity and specificity to detect outbreaks effectively. METHODS: During 1994 and 1995, the Minnesota Department of Health requested that all clinical isolates of E. coli O157:H7 be submitted to our laboratory. Isolates were subtyped by pulsed-field gel electrophoresis (PFGE), and patients were interviewed about potential sources of infection. RESULTS: In 1994 and 1995, 344 cases of E. coli O157:H7 infection were reported to the Minnesota Department of Health; 317 (92 percent) were subtyped by PFGE, and 143 distinct PFGE patterns were identified. Ten outbreaks of E. coli O157:H7 were identified; these accounted for 56 (18 percent) of the 317 subtyped cases. Four outbreaks were detected solely as a result of subtype-specific surveillance. In 11 two-week periods, the number of reported cases of E. coli O157:H7 doubled from the previous two weeks. In eight of these instances, the patterns identified were dissimilar and there were no outbreaks. Two of the remaining three increases resulted from multiple simultaneous outbreaks. CONCLUSIONS: Subtype-specific surveillance for E. coli O157:H7 can identify outbreaks that are not detected by traditional methods and can ascertain whether sudden increases in reported cases are due to sporadic isolated cases or to one or more outbreaks.