Foods Implicated in U.S. Outbreaks Differ from the Types Most Commonly Consumed.

ABSTRACT: Foodborne disease outbreak investigations identify foods responsible for illnesses. However, it is not known the degree to which foods implicated in outbreaks reflect the distribution of food consumption in the U.S. population or the risk associated with their consumption. We compared the distribution of 24 categories of foods implicated in outbreaks with the distribution of foods consumed by the U.S. population. Beef, chicken, eggs, fish, herbs, mollusks, pork, sprouts, seeded vegetables, and turkey were implicated in outbreaks significantly more often than expected based on the frequency of their consumption by the general population, suggesting a higher risk of contamination or mishandling from foods in these categories than from foods in other categories. In contrast, pasteurized dairy, fruits, grains and beans, oils and sugars, and root and underground vegetables were less frequently implicated in outbreaks than their frequency of consumption by the general population, suggesting a lower health risk associated with these food categories.

Epidemiologic patterns of human Salmonella serotype diversity in the USA, 1996-2016.

Although researchers have described numerous risk factors for salmonellosis and for infection with specific common serotypes, the drivers of Salmonella serotype diversity among human populations remain poorly understood. In this retrospective observational study, we partition records of serotyped non-typhoidal Salmonella isolates from human clinical specimens reported to CDC national surveillance by demographic, geographic and seasonal characteristics and adapt sample-based rarefaction methods from the field of community ecology to study how Salmonella serotype diversity varied within and among these populations in the USA during 1996-2016. We observed substantially higher serotype richness in children <2 years old than in older children and adults and steadily increasing richness with age among older adults. Whereas seasonal and regional variation in serotype diversity was highest among infants and young children, variation by specimen source was highest in adults. Our findings suggest that the risk for infection from uncommon serotypes is associated with host and environmental factors, particularly among infants, young children and older adults. These populations may have a higher proportion of illness acquired through environmental transmission pathways than published source attribution models estimate.

Post-Campylobacter Guillain Barré Syndrome in the USA: secondary analysis of surveillance data collected during the 2009-2010 novel Influenza A (H1N1) vaccination campaign.

Guillain Barré syndrome (GBS), which is triggered by autoantibodies produced in response to antigenic stimuli such as certain infections and vaccinations, is the most common cause of acute flaccid paralysis worldwide. Campylobacter, the most common bacterial enteric infection in the USA, is reported to be the most commonly diagnosed antecedent of GBS, yet little information is available about the risk of post-Campylobacter GBS. Data collected through active, population-based surveillance in the Emerging Infections Program during the 2009-2010 novel Influenza A (H1N1) vaccination campaign allowed us to compare confirmed and probable GBS cases to non-cases to determine whether antecedent Campylobacter infection (or a diarrhoeal illness consistent with campylobacteriosis) was more common among cases and to assess the risk of GBS following Campylobacter infection. We estimate that 8-12% of GBS cases in the USA are attributable to Campylobacter infection (or a diarrhoeal illness consistent with campylobacteriosis), with 434-650 cases of post-diarrhoeal GBS annually and about 49 cases of GBS per 100 000 Campylobacter infections. These results provide updated estimates for post-Campylobacter GBS incidence in the USA and highlight an important benefit of effective measures to prevent Campylobacter infections.

Temporal patterns in principal Salmonella serotypes in the USA; 1996-2014.

Analysing temporal patterns in foodborne illness is important to designing and implementing effective food safety measures. The reported incidence of illness due to Salmonella in the USA. Foodborne Diseases Active Surveillance Network (FoodNet) sites has exhibited no declining trend since 1996; however, there have been significant annual trends among principal Salmonella serotypes, which may exhibit complex seasonal patterns. Data from the original FoodNet sites and penalised cubic B-spline regression are used to estimate temporal patterns in the reported incidence of illness for the top three Salmonella serotypes during 1996-2014. Our results include 95% confidence bands around the estimated annual and monthly curves for each serotype. The results show that Salmonella serotype Typhimurium exhibits a statistically significant declining annual trend and seasonality (P < 0.001) marked by peaks in late summer and early winter. Serotype Enteritidis exhibits a significant annual trend with a higher incidence in later years and seasonality (P < 0.001) marked by a peak in late summer. Serotype Newport exhibits no significant annual trend with significant seasonality (P < 0.001) marked by a peak in late summer.

Use of random forest to estimate population attributable fractions from a case-control study of Salmonella enterica serotype Enteritidis infections.

To design effective food safety programmes we need to estimate how many sporadic foodborne illnesses are caused by specific food sources based on case-control studies. Logistic regression has substantive limitations for analysing structured questionnaire data with numerous exposures and missing values. We adapted random forest to analyse data of a case-control study of Salmonella enterica serotype Enteritidis illness for source attribution. For estimation of summary population attributable fractions (PAFs) of exposures grouped into transmission routes, we devised a counterfactual estimator to predict reductions in illness associated with removing grouped exposures. For the purpose of comparison, we fitted the data using logistic regression models with stepwise forward and backward variable selection. Our results show that the forward and backward variable selection of logistic regression models were not consistent for parameter estimation, with different significant exposures identified. By contrast, the random forest model produced estimated PAFs of grouped exposures consistent in rank order with results obtained from outbreak data, with egg-related exposures having the highest estimated PAF (22·1%, 95% confidence interval 8·5-31·8). Random forest might be structurally more coherent and efficient than logistic regression models for attributing Salmonella illnesses to sources involving many causal pathways.

An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years.

We explored the overall impact of foodborne disease caused by seven leading foodborne pathogens in the United States using the disability adjusted life year (DALY). We defined health states for each pathogen (acute illness and sequelae) and estimated the average annual incidence of each health state using data from public health surveillance and previously published estimates from studies in the United States, Canada and Europe. These pathogens caused about 112 000 DALYs annually due to foodborne illnesses acquired in the United States. Non-typhoidal Salmonella (32 900) and Toxoplasma (32 700) caused the most DALYs, followed by Campylobacter (22 500), norovirus (9900), Listeria monocytogenes (8800), Clostridium perfringens (4000), and Escherichia coli O157 (1200). These estimates can be used to prioritize food safety interventions. Future estimates of the burden of foodborne disease in DALYs would be improved by addressing important data gaps and by the development and validation of US-specific disability weights for foodborne diseases.

Attributing sporadic and outbreak-associated infections to sources: blending epidemiological data.

Common sources of shiga toxin-producing Escherichia coli (STEC) O157 infection have been identified by investigating outbreaks and by case-control studies of sporadic infections. We conducted an analysis to attribute STEC O157 infections ascertained in 1996 and 1999 by the Foodborne Diseases Active Surveillance Network (FoodNet) to sources. Multivariable models from two case-control studies conducted in FoodNet and outbreak investigations that occurred during the study years were used to calculate the annual number of infections attributable to six sources. Using the results of the outbreak investigations alone, 27% and 15% of infections were attributed to a source in 1996 and 1999, respectively. Combining information from both data sources, 65% of infections in 1996 and 34% of infections in 1999 were attributed. The results suggest that methods to incorporate data from multiple surveillance systems and over several years are needed to improve estimation of the number of illnesses attributable to exposure sources.

Tuberculosis screening by tuberculosis skin test or QuantiFERON-TB Gold In-Tube Assay among an immigrant population with a high prevalence of tuberculosis and BCG vaccination.

RATIONALE: Each year 1 million persons acquire permanent U.S. residency visas after tuberculosis (TB) screening. Most applicants undergo a 2-stage screening with tuberculin skin test (TST) followed by CXR only if TST-positive at > 5 mm. Due to cross reaction with bacillus Calmette-Guérin (BCG), TST may yield false positive results in BCG-vaccinated persons. Interferon gamma release assays exclude antigens found in BCG. In Vietnam, like most high TB-prevalence countries, there is universal BCG vaccination at birth. OBJECTIVES: 1. Compare the sensitivity of QuantiFERON-TB Gold In-Tube Assay (QFT) and TST for culture-positive pulmonary TB. 2. Compare the age-specific and overall prevalence of positive TST and QFT among applicants with normal and abnormal CXR. METHODS: We obtained TST and QFT results on 996 applicants with abnormal CXR, of whom 132 had TB, and 479 with normal CXR. RESULTS: The sensitivity for tuberculosis was 86.4% for QFT; 89.4%, 81.1%, and 52.3% for TST at 5, 10, and 15 mm. The estimated prevalence of positive results at age 15-19 years was 22% and 42% for QFT and TST at 10 mm, respectively. The prevalence increased thereafter by 0.7% year of age for TST and 2.1% for QFT, the latter being more consistent with the increase in TB among applicants. CONCLUSIONS: During 2-stage screening, QFT is as sensitive as TST in detecting TB with fewer requiring CXR and being diagnosed with LTBI. These data support the use of QFT over TST in this population.

Association between intensive handwashing promotion and child development in Karachi, Pakistan: a cluster randomized controlled trial.

OBJECTIVE: To evaluate associations between handwashing promotion and child growth and development. DESIGN: Cluster randomized controlled trial. SETTING: Informal settlements in Karachi, Pakistan. PARTICIPANTS: A total of 461 children who were enrolled in a trial of household-level handwashing promotion in 2003 and were younger than 8 years at reassessment in 2009. INTERVENTIONS: In 2003, neighborhoods were randomized to control (n = 9), handwashing promotion (n = 9), or handwashing promotion and drinking water treatment (n = 10); intervention households received free soap and weekly handwashing promotion for 9 months. MAIN OUTCOME MEASURES: Anthropometrics and developmental quotients measured with the Battelle Developmental Inventory II at 5 to 7 years of age. RESULTS: Overall, 24.9% (95% CI, 20.0%-30.6%) and 22.1% (95% CI, 18.0%-26.8%) of children had z scores that were more than 2 SDs below the expected z scores for height and body mass index for age, respectively; anthropometrics did not differ significantly across study groups. Global developmental quotients averaged 104.4 (95% CI, 101.9-107.0) among intervention children and 98.3 (95% CI, 93.1-103.4) among control children (P = .04). Differences of similar magnitude were measured across adaptive, personal-social, communication, cognitive, and motor domains. CONCLUSIONS: Although growth was similar across groups, children randomized to the handwashing promotion during their first 30 months of age attained global developmental quotients 0.4 SDs greater than those of control children at 5 to 7 years of age. These gains are comparable to those of at-risk children enrolled in publicly funded preschools in the United States and suggest that handwashing promotion could improve child well-being and societal productivity. TRIAL REGISTRATION: clinicaltrials.gov Identifier: NCT01538953.

Human Salmonella infections linked to contaminated dry dog and cat food, 2006-2008.

OBJECTIVE: Human Salmonella infections associated with dry pet food have not been previously reported. We investigated such an outbreak of Salmonella Schwarzengrund and primarily affecting young children. PATIENTS AND METHODS: Two multistate case-control studies were conducted to determine the source and mode of infections among case-patients with the outbreak strain. Study 1 evaluated household exposures to animals and pet foods, and study 2 examined risk factors for transmission among infant case-patients. Environmental investigations were conducted. RESULTS: Seventy-nine case-patients in 21 states were identified; 48% were children aged 2 years or younger. Case-households were significantly more likely than control households to report dog contact (matched odds ratio [mOR]: 3.6) and to have recently purchased manufacturer X brands of dry pet food (mOR: 6.9). Illness among infant case-patients was significantly associated with feeding pets in the kitchen (OR: 4.4). The outbreak strain was isolated from opened bags of dry dog food produced at plant X, fecal specimens from dogs that ate manufacturer X dry dog food, and an environmental sample and unopened bags of dog and cat foods from plant X. More than 23 000 tons of pet foods were recalled. After additional outbreak-linked illnesses were identified during 2008, the company recalled 105 brands of dry pet food and permanently closed plant X. CONCLUSIONS: Dry dog and cat foods manufactured at plant X were linked to human illness for a 3-year period. This outbreak highlights the importance of proper handling and storage of pet foods in the home to prevent human illness, especially among young children.

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.

Usefulness of the hydrogen sulfide test for assessment of water quality in Bangladesh.

AIM: To evaluate the usefulness of the hydrogen sulfide (H(2)S) test for assessing water quality in Bangladesh. METHODS AND RESULTS: We tested 382 water samples from a variety of sources using locally produced H(2)S test kits and laboratory-based membrane filtration for the detection of Escherichia coli. Compared with membrane filtration, H(2)S tests, when incubated for 24 h, had both a sensitivity and positive predictive value (PPV) of <40% when analysis was restricted to water samples with E. coli levels below 100 colony forming units (CFU) per 100 ml. In contrast, for E. coli levels from 1000 to 9999 CFU per 100 ml, sensitivity was 94% and PPV 88%; specificity was 97% and negative predictive value was 99%. CONCLUSIONS: The hydrogen sulfide test, when incubated at 24 h, is a promising alternative for assessing water quality where E. coli levels may be high. An improved understanding of the incremental impact of contamination level on health is needed to better determine its usefulness. SIGNIFICANCE AND IMPACT OF THE STUDY: The hydrogen sulfide test is inexpensive, easy to use and portable. Its use may allow rapid assessment of water quality in situations where cost or logistics prevent use of other testing methods, such as in remote areas or during flood and other natural disasters.

Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005.

Salmonella Newport causes more than an estimated 100,000 infections annually in the United States. In 2002, tomatoes grown and packed on the eastern shore of Virginia contaminated with a pan-susceptible S. Newport strain caused illness in 510 patients in 26 states. In July-November 2005, the same strain caused illness in at least 72 patients in 16 states. We conducted a case-control study during the 2005 outbreak, enrolling 29 cases and 140 matched neighbourhood controls. Infection was associated with eating tomatoes (matched odds ratio 9.7, 95% confidence interval 3.3-34.9). Tomatoes were traced back to the eastern shore of Virginia, where the outbreak strain was isolated from pond water used to irrigate tomato fields. Two multistate outbreaks caused by one rare strain, and identification of that strain in irrigation ponds 2 years apart, suggest persistent contamination of tomato fields. Further efforts are needed to prevent produce contamination on farms and throughout the food supply chain.

The impact of a school-based safe water and hygiene programme on knowledge and practices of students and their parents: Nyanza Province, western Kenya, 2006.

Safe drinking water and hygiene are essential to reducing Kenya's diarrhoeal disease burden. A school-based safe water and hygiene intervention in Kenya was evaluated to assess its impact on students' knowledge and parents' adoption of safe water and hygiene practices. We surveyed 390 students from nine schools and their parents at baseline and conducted a final evaluation of 363 students and their parents. From baseline to final evaluation, improvement was seen in students' knowledge of correct water treatment procedure (21-65%, P<0.01) and knowing when to wash their hands. At final evaluation, 14% of parents reported currently treating their water, compared with 6% at baseline (P<0.01). From 2004 to 2005, school absenteeism in the September-November term decreased in nine project schools by 35% and increased in nine neighbouring comparison schools by 5%. This novel programme shows promise for reducing school absenteeism and promoting water and hygiene interventions in the home.

Outbreak of Salmonella Braenderup infections associated with Roma tomatoes, northeastern United States, 2004: a useful method for subtyping exposures in field investigations.

Salmonella Braenderup is an uncommon serotype in the United States. In July 2004, a multistate outbreak of Salmonella Braenderup diarrhoeal infections occurred, with 125 clinical isolates identified. To investigate, we conducted a case-control study, enrolling 32 cases and 63 matched controls. Cheese, lettuce and tomato eaten at restaurants all appeared to be associated with illness. To further define specific exposures, we conducted a second study and asked managers of restaurants patronized by patients and controls about cheese, lettuce and tomato varieties used in dishes their patrons reported consuming. This information was obtained for 27 cases and 29 controls. Roma tomatoes were the only exposure significantly associated with illness (odds ratio 4.3, 95% confidence interval 1.2-15.9). Roma tomatoes from two restaurants were traced back to a single tomato packing house. The methods used in this field investigation to define specific exposures may be useful for other foodborne outbreaks.

Evaluation of community-based serologic screening for identification of chronic Salmonella typhi carriers in Vietnam.

OBJECTIVES: To determine the utility of screening anti-Vi antibodies to detect chronic Salmonella Typhi carriers in an endemic community. METHODS: We conducted a community-based serologic survey for anti-Vi antibodies to identify chronic Salmonella Typhi carriers in a typhoid endemic region in Vietnam. RESULTS: We tested sera from 3209 (67.2%) of 4772 eligible adults. The median age was 37 years (range 20-92), 57.3% were female, 4.6% reported a history of typhoid fever and 0.3% reported typhoid vaccination. Anti-Vi antibody titers tested in Vietnam were < 1:40 in 2759 (86.0%), 1:40 in 194 (6.0%), 1:80 in 168 (5.2%), 1:160 in 57 (1.8%), and > or = 1:320 in 31 (1.0%). On re-testing in the USA, an additional 19 sera with titers > or = 1:160 were identified. We collected 589 rectal swabs from 103 (96.3%) of 107 persons with Vi antibody titers > or = 1:160 and 183 swabs from 33 persons with antibody titers < 1:80. No Salmonella Typhi was isolated. CONCLUSIONS: Community-based serologic screening is a feasible, but impractical method for identifying chronic Salmonella Typhi carriers. Background levels of anti-Vi antibody titers in this endemic area may be high despite a low prevalence of chronic carriers.

Web-based investigation of multistate salmonellosis outbreak.

We investigated a large outbreak of Salmonella enterica serotype Javiana among attendees of the 2002 U.S. Transplant Games, including 1,500 organ transplant recipients. Web-based survey methods identified pre-diced tomatoes as the source of this outbreak, which highlights the utility of such investigative tools to cope with the changing epidemiology of foodborne diseases.

Salmonella bacteriuria: an increasing entity in elderly women in the United States.

Salmonellosis is a major cause of gastroenteritis in the United States and can lead to septicaemia, and other extra-intestinal illness including urinary tract infections (UTIs). To examine trends in Salmonella bacteriuria in the United States, surveillance data from the National Salmonella Surveillance System from 1980 to the end of 1999 were reviewed. Overall, 17442 urinary Salmonella isolates were reported, representing 2% of all Salmonella isolates from a known source. This proportion increased from 2% during 1980--1984 to 4% during 1995--1999. The median age of persons from whom these isolates came was 51 years; 12,176 (70 %) were women. Compared to the last national survey conducted between 1968 and 1979, the rate of Salmonella bacteriuria increased among women, from 2.0 per million persons in 1980 to 3.7 in 1999; the highest rate occurring in women > or = 70 years. National reporting of Salmonella bacteriuria increased in absolute incidence and as a proportion of all Salmonella, especially in elderly women and may represent an increase in the incidence of Salmonella UTIs. Better understanding of the uropathogenicity of Salmonella serotypes may further clarify the mechanisms of Salmonella UTIs.

Typhoid fever in travelers: who should be targeted for prevention?

To clarify indications for typhoid vaccination, we reviewed laboratory-confirmed cases of typhoid fever reported to the United States Centers for Disease Control and Prevention between 1994 and 1999. To estimate the risk of adverse events associated with typhoid vaccination, we reviewed reports to the Vaccine Adverse Event Reporting System for the same period. Acute Salmonella enterica serotype Typhi infection was reported for 1393 patients. Of these patients, recent travel was reported by 1027 (74%), only 36 (4%) of whom reported having received a vaccination. Six countries accounted for 76% of travel-associated cases (India [30%], Pakistan [13%], Mexico [12%], Bangladesh [8%], The Philippines [8%], and Haiti [5%]). For 626 travelers who traveled to a single country, the length of stay was

Microbiologic effectiveness of hand washing with soap in an urban squatter settlement, Karachi, Pakistan.

We conducted a study in a squatter settlement in Karachi, Pakistan where residents report commonly washing their hands to determine if providing soap, encouraging hand washing, and improving wash-water quality would improve hand cleanliness. We allocated interventions to 75 mothers and collected hand-rinse samples on unannounced visits. In the final model compared with mothers who received no hand-washing intervention, mothers who received soap would be expected to have 65% fewer thermotolerant coliform bacteria on their hands (95% CI 40%, 79%) and mothers who received soap, a safe water storage vessel, hypochlorite for water treatment, and instructions to wash their hands with soap and chlorinated water would be expected to have 74% fewer (95% CI 57%, 84%). The difference between those who received soap alone, and those who received soap plus the safe water vessel was not significant (P = 0.26). Providing soap and promoting hand washing measurably improved mothers' hand cleanliness even when used with contaminated water.