Recency-Weighted Statistical Modeling Approach to Attribute Illnesses Caused by 4 Pathogens to Food Sources Using Outbreak Data, United States.

Foodborne illness source attribution is foundational to a risk-based food safety system. We describe a method for attributing US foodborne illnesses caused by nontyphoidal Salmonella enterica, Escherichia coli O157, Listeria monocytogenes, and Campylobacter to 17 food categories using statistical modeling of outbreak data. This method adjusts for epidemiologic factors associated with outbreak size, down-weights older outbreaks, and estimates credibility intervals. On the basis of 952 reported outbreaks and 32,802 illnesses during 1998-2012, we attribute 77% of foodborne Salmonella illnesses to 7 food categories (seeded vegetables, eggs, chicken, other produce, pork, beef, and fruits), 82% of E. coli O157 illnesses to beef and vegetable row crops, 81% of L. monocytogenes illnesses to fruits and dairy, and 74% of Campylobacter illnesses to dairy and chicken. However, because Campylobacter outbreaks probably overrepresent dairy as a source of nonoutbreak campylobacteriosis, we caution against using these Campylobacter attribution estimates without further adjustment.

Antimicrobial resistance among invasive nontyphoidal Salmonella enterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996 to 2007.

Nontyphoidal salmonellae (NTS) are important causes of community-acquired bloodstream infection. We describe patterns of antimicrobial resistance among invasive NTS in the United States. We compared bloodstream NTS isolates with those from stool submitted to the National Antimicrobial Resistance Monitoring System (NARMS) from 1996 to 2007. We describe antimicrobial resistance among invasive strains by serogroup and serotype. Of the 19,302 NTS isolates, 17,804 (92.2%) were from stool or blood. Of these, 1,050 (5.9%) were bloodstream isolates. The median ages (ranges) of patients with and without bacteremia were 36 (<1 to 97) years and 20 (<1 to 105) years, respectively (P < 0.001). Males (odds ratio [OR], 1.21; 95% confidence interval [CI], 1.06 to 1.38) and those ≥65 years of age were at greater risk for invasive disease. Salmonella enterica serotypes Enteritidis, Typhimurium, and Heidelberg were the most common serotypes isolated from blood; S. enterica serotypes Dublin, Sandiego, and Schwarzengrund were associated with the greatest risk for bloodstream isolation. Of invasive isolates, 208 (19.8%) were resistant to ampicillin, 117 (11.1%) to chloramphenicol, and 26 (2.5%) to trimethoprim-sulfamethoxazole; 28 (2.7%) isolates were resistant to nalidixic acid and 26 (2.5%) to ceftriaxone. Antimicrobial resistance to traditional agents is common. However, the occurrence of nalidixic acid and ceftriaxone resistance among invasive NTS is cause for clinical and public health vigilance.

A waterborne outbreak of gastroenteritis with multiple etiologies among resort island visitors and residents: Ohio, 2004.

BACKGROUND: The implementation of treated municipal water systems in the 20th century led to a dramatic decrease in waterborne disease in the United States. However, communities with deficient water systems still experience waterborne outbreaks. In August 2004, we investigated an outbreak of gastroenteritis on South Bass Island, Ohio, an island of 900 residents that is visited by >500,000 persons each year. METHODS: To identify the source of illness, we conducted a case-control study and an environmental investigation. A case was defined as diarrhea in a person who traveled to the island during the period from May 1 through 30 September 2004 and became ill within 2 weeks after the visit. Healthy travel companions served as matched control subjects. We also performed an environmental assessment and extensive testing of island water sources. RESULTS: Among the 1450 persons reporting illness, Campylobacter jejuni, norovirus, Giardia intestinalis, and Salmonella enterica serotype Typhimurium were identified in 16, 9, 3, and 1 persons, respectively. We interviewed 100 case patients and 117 matched control subjects. Case patients were more likely to drink water on the island than control subjects (68% vs. 35%; matched odds ratio, 4.3; 95% confidence interval, 2.2-9.3). Sampling of ground water wells indicated contamination with multiple fecal microbes, including Escherichia coli, C. jejuni, Salmonella species, and Giardia species. Irregularities in sewage disposal practices that could have contaminated the underground aquifer were noted. CONCLUSIONS: The combined epidemiological and environmental investigation indicated that sewage-contaminated ground water was the likely source of this large outbreak. Long-term changes to the island's water supply and sewage management infrastructure are needed.

An outbreak of Escherichia coli O157:H7 infections among visitors to a dairy farm.

BACKGROUND: Outbreaks of Escherichia coli O157:H7 infections have involved direct transmission from animals and their environment to humans. We describe an outbreak among visitors to a Pennsylvania dairy and petting farm that provides public access to animals. METHODS: We conducted both a case-control study among visitors to a farm to identify risk factors for infection and a household survey to determine the rates of diarrheal illness among these visitors. We performed an extensive environmental study to identify sources of E. coli O157:H7 on the farm. RESULTS: Fifty-one patients with confirmed or suspected E. coli O157:H7 infection were enrolled in the case-control study. The median age of the patients was four years, and the hemolytic-uremic syndrome developed in eight. Contact with calves and their environment was associated with an increased risk of infection, whereas hand washing was protective. The household survey indicated that visitors to the farm during the outbreak had higher than expected rates of diarrhea. Environmental studies showed that 28 of the 216 cattle on the farm (13 percent) were colonized with E. coli O157:H7 that had the same distinct pattern on pulsed-field gel electrophoresis that was found in isolates from the patients. This organism was also recovered from surfaces that were accessible to the public. CONCLUSIONS: In a large outbreak of E. coli O157:H7 infections among visitors to a dairy farm, predominantly children, high rates of carriage of E. coli O157:H7 among calves and young cattle most likely resulted in contamination of both the animals' hides and the environment.

Multistate outbreak of Listeriosis linked to turkey deli meat and subsequent changes in US regulatory policy.

BACKGROUND: Listeriosis, a life-threatening foodborne illness caused by Listeria monocytogenes, affects approximately 2500 Americans annually. Between July and October 2002, an uncommon strain of L. monocytogenes caused an outbreak of listeriosis in 9 states. METHODS: We conducted case finding, a case-control study, and traceback and microbiological investigations to determine the extent and source of the outbreak and to propose control measures. Case patients were infected with the outbreak strain of L. monocytogenes between July and November 2002 in 9 states, and control patients were infected with different L. monocytogenes strains. Outcome measures included food exposure associated with outbreak strain infection and source of the implicated food. RESULTS: Fifty-four case patients were identified; 8 died, and 3 pregnant women had fetal deaths. The case-control study included 38 case patients and 53 control patients. Case patients consumed turkey deli meat much more frequently than did control patients (P = .008, by Wilcoxon rank-sum test). In the 4 weeks before illness, 55% of case patients had eaten deli turkey breast more than 1-2 times, compared with 28% of control patients (odds ratio, 4.5; 95% confidence interval, 1.3-17.1). Investigation of turkey deli meat eaten by case patients led to several turkey processing plants. The outbreak strain was found in the environment of 1 processing plant and in turkey products from a second. Together, the processing plants recalled > 30 million pounds of products. Following the outbreak, the US Department of Agriculture's Food Safety and Inspection Service issued new regulations outlining a L. monocytogenes control and testing program for ready-to-eat meat and poultry processing plants. CONCLUSIONS: Turkey deli meat was the source of a large multistate outbreak of listeriosis. Investigation of this outbreak helped guide policy changes designed to prevent future L. monocytogenes contamination of ready-to-eat meat and poultry products.

Salmonella enterica Infections in the United States and Assessment of Coefficients of Variation: A Novel Approach to Identify Epidemiologic Characteristics of Individual Serotypes, 1996-2011.

BACKGROUND: Despite control efforts, salmonellosis continues to cause an estimated 1.2 million infections in the United States (US) annually. We describe the incidence of salmonellosis in the US and introduce a novel approach to examine the epidemiologic similarities and differences of individual serotypes. METHODS: Cases of salmonellosis in humans reported to the laboratory-based National Salmonella Surveillance System during 1996-2011 from US states were included. Coefficients of variation were used to describe distribution of incidence rates of common Salmonella serotypes by geographic region, age group and sex of patient, and month of sample isolation. RESULTS: During 1996-2011, more than 600,000 Salmonella isolates from humans were reported, with an average annual incidence of 13.1 cases/100,000 persons. The annual reported rate of Salmonella infections did not decrease during the study period. The top five most commonly reported serotypes, Typhimurium, Enteritidis, Newport, Heidelberg, and Javiana, accounted for 62% of fully serotyped isolates. Coefficients of variation showed the most geographically concentrated serotypes were often clustered in Gulf Coast states and were also more frequently found to be increasing in incidence. Serotypes clustered in particular months, age groups, and sex were also identified and described. CONCLUSIONS: Although overall incidence rates of Salmonella did not change over time, trends and epidemiological factors differed remarkably by serotype. A better understanding of Salmonella, facilitated by this comprehensive description of overall trends and unique characteristics of individual serotypes, will assist in responding to this disease and in planning and implementing prevention activities.

A recurrent, multistate outbreak of salmonella serotype agona infections associated with dry, unsweetened cereal consumption, United States, 2008.

An outbreak of Salmonella enterica serotype Agona infections associated with nationwide distribution of cereal from Company X was identified in April 2008. This outbreak was detected using PulseNet, the national molecular subtyping network for foodborne disease surveillance, which coincided with Company X's voluntary recall of unsweetened puffed rice and wheat cereals after routine product sampling yielded Salmonella Agona. A case patient was defined as being infected with the outbreak strain of Salmonella Agona, with illness onset from 1 January through 1 July 2008. Case patients were interviewed using a standard questionnaire, and the proportion of ill persons who reported eating Company X puffed rice cereal was compared with Company X's market share data using binomial testing. The Minnesota Department of Agriculture inspected the cereal production facility and collected both product and environmental swab samples. Routine surveillance identified 33 case patients in 17 states. Of 32 patients interviewed, 24 (83%) reported eating Company X puffed rice cereal. Company X puffed rice cereal represented 0.063% of the total ready-to-eat dry cereal market share in the United States at the time of the investigation. Binomial testing suggested that the proportion of exposed case patients would not likely occur by chance (P < 0.0001). Of 17 cereal samples collected from case patient homes for laboratory testing, 2 (12%) yielded Salmonella Agona indistinguishable from the outbreak strain. Twelve environmental swabs and nine product samples from the cereal plant yielded the outbreak strain of Salmonella Agona. Company X cereal was implicated in a similar outbreak of Salmonella Agona infection in 1998 with the same outbreak strain linked to the same production facility. We hypothesize that a recent construction project at this facility created an open wall near the cereal production area allowing reintroduction of Salmonella Agona into the product, highlighting the resilience of Salmonella in dry food production environments.

Outbreak of Salmonella Wandsworth and Typhimurium infections in infants and toddlers traced to a commercial vegetable-coated snack food.

OBJECTIVE: Human outbreaks of Salmonella infection have been attributed to a variety of food vehicles. Processed snack foods are increasingly consumed by children. In May 2007, state and local health departments and the Centers for Disease Control and Prevention investigated human infections from Salmonella Wandsworth, an extremely rare serotype. MATERIALS AND METHODS: Serotyping and pulsed-field gel electrophoresis were used to identify outbreak-associated illnesses. Food history questionnaires and open-ended interviews were used to generate exposure hypotheses. A nationwide case-control study was conducted to epidemiologically implicate a source. Public health laboratories cultured implicated product from patient homes and retail stores. RESULTS: Sixty-nine patients from 23 states were identified; 93% were aged 10 months to 3 years. Eighty-one percent of child patients had bloody diarrhea; 6 were hospitalized. No deaths were reported. The case-control study strongly associated illness with a commercial puffed vegetable-coated ready-to-eat snack food (mOR = 23.3, P = 0.0001), leading to a nationwide recall. Parents of 92% of interviewed case-children reported that children consumed the food during the week before their illness began; 43% reported daily consumption. Salmonella Wandsworth, 3 additional Salmonella serotypes and Chronobacter (formerly Enterobacter) sakazaki were all cultured from this product, leading to the identification of 18 human outbreak-related Salmonella Typhimurium illnesses. CONCLUSIONS: This report documents a nationwide outbreak associated with a commercial processed ready-to-eat snack food. Cases occurred primarily in infants and toddlers, many of whom frequently consumed the food. Measures are needed to ensure that ingredients added to ready-to-eat foods after the final lethal processing step are free of pathogens.

Clinical response and outcome of infection with Salmonella enterica serotype Typhi with decreased susceptibility to fluoroquinolones: a United States foodnet multicenter retrospective cohort study.

Patients with typhoid fever due to Salmonella enterica serotype Typhi strains for which fluoroquinolones MICs are elevated yet that are classified as susceptible by the current interpretive criteria of the Clinical and Laboratory Standards Institute may not respond adequately to fluoroquinolone therapy. Patients from seven U.S. states with invasive Salmonella serotype Typhi infection between 1999 and 2002 were enrolled in a multicenter retrospective cohort study. Patients infected with Salmonella serotype Typhi isolates with ciprofloxacin MICs of 0.12 to 1 microg/ml (decreased ciprofloxacin susceptibility but not resistant to ciprofloxacin [DCS]) were compared with patients infected with isolates with ciprofloxacin MICs <0.12 microg/ml for fever clearance time and treatment failure. Of 71 patients, 30 (43%) were female and 24 (34%) were infected with Salmonella serotype Typhi with DCS; the median age was 14 years (range, 1 to 51 years). Twenty-one (88%) of 24 isolates with DCS were resistant to nalidixic acid. The median antimicrobial-related fever clearance times in the DCS and non-DCS groups were 92 h (range, 21 to 373 h) and 72 h (range, 19 to 264 h) (P = 0.010), respectively, and the fluoroquinolone-related fever clearance times in the DCS and non-DCS groups were 90 h (range, 9 to 373 h) and 64 h (range, 34 to 204 h) (P = 0.153), respectively. Four (17%) of 24 patients in the DCS group and 2 (4%) of 46 patients in the non-DCS group (relative risk, 2.5; 95% confidence interval, 1.2 to 5.1) experienced treatment failure. Associations persisted after adjustment for potential confounders. We demonstrate that patients infected with Salmonella serotype Typhi isolates with DCS show evidence of a longer time to fever clearance and more frequent treatment failure. Nalidixic acid screening does not detect all isolates with DCS.

Household based treatment of drinking water with flocculant-disinfectant for preventing diarrhoea in areas with turbid source water in rural western Kenya: cluster randomised controlled trial.

OBJECTIVE: To compare the effect on prevalence of diarrhoea and mortality of household based treatment of drinking water with flocculant-disinfectant, sodium hypochlorite, and standard practices in areas with turbid water source in Africa. DESIGN: Cluster randomised controlled trial over 20 weeks. SETTING: Family compounds, each containing several houses, in rural western Kenya. PARTICIPANTS: 6650 people in 605 family compounds. INTERVENTION: Water treatment: flocculant-disinfectant, sodium hypochlorite, and usual practice (control). MAIN OUTCOME MEASURES: Prevalence of diarrhoea and all cause mortality. Escherichia coli concentration, free residual chlorine concentration, and turbidity in household drinking water as surrogates for effectiveness of water treatment. RESULTS: In children < 2 years old, compared with those in the control compounds, the absolute difference in prevalence of diarrhoea was -25% in the flocculant-disinfectant arm (95% confidence interval -40 to -5) and -17% in the sodium hypochlorite arm (-34 to 4). In all age groups compared with control, the absolute difference in prevalence was -19% in the flocculant-disinfectant arm (-34 to -2) and -26% in the sodium hypochlorite arm (-39 to -9). There were significantly fewer deaths in the intervention compounds than in the control compounds (relative risk of death 0.58, P = 0.036). Fourteen per cent of water samples from control compounds had E coli concentrations < 1 CFU/100 ml compared with 82% in flocculant-disinfectant and 78% in sodium hypochlorite compounds. The mean turbidity of drinking water was 8 nephelometric turbidity units (NTU) in flocculant-disinfectant households, compared with 55 NTU in the two other compounds (P < 0.001). CONCLUSIONS: In areas of turbid water, flocculant-disinfectant was associated with a significant reduction in diarrhoea among children < 2 years. This health benefit, combined with a significant reduction in turbidity, suggests that the flocculant-disinfectant is well suited to areas with highly contaminated and turbid water.

Outbreaks of Escherichia coli O157 infections at multiple county agricultural fairs: a hazard of mixing cattle, concession stands and children.

Escherichia coli O157 infections cause an estimated 60 deaths and 73 000 illnesses annually in the United States. A marked summer peak in incidence is largely unexplained. We investigated an outbreak of E. coli O157 infections at an agricultural fair in Ohio and implicated consumption of beverages made with fairground water and sold by a geographically localized group of vendors who were all on the same branch of the fairground water distribution system. To examine county fair attendance as a risk factor for infection, we conducted two further epidemiological studies. In the first, we enhanced surveillance for E. coli O157 infections in 15 Northeast Ohio counties during the 2000 agricultural fair season and showed increased risk of E. coli O157 infection among fair attendees. In the second study, we examined Ohio Public Health Laboratory Information Service (PHLIS) data for 1999 using a time-varying covariate proportional hazards model and demonstrated an association between agricultural fairs and E. coli O157 infections, by county. Agricultural fair attendance is a risk factor for E. coli O157 infection in the United States and may contribute to the summer peak in incidence. Measures are needed to reduce transmission of enteric pathogens at agricultural fairs.