Laura Kornstein

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 Agricultures 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.

Microbiological Aspects of the Investigation That Traced the 1998 Outbreak of Listeriosis in the United States to Contaminated Hot Dogs and Establishment of Molecular Subtyping-Based Surveillance for Listeria monocytogenes in the PulseNet Network

ABSTRACT A multistate outbreak of listeriosis occurred in the United States in 1998 with illness onset dates between August and December. The outbreak caused illness in 108 persons residing in 24 states and caused 14 deaths and four miscarriages or stillbirths. This outbreak was detected by public health officials in Tennessee and New York who observed significant increases over expected listeriosis cases in their states. Subsequently, the Centers for Disease Control and Prevention (CDC) began laboratory characterization of clinical isolates of Listeria monocytogenes by serotyping and restriction fragment length polymorphism analysis using pulsed-field gel electrophoresis (PFGE). For the purpose of this investigation, outbreak-related isolates were defined as those that had a specific AscI-PFGE pattern and indistinguishable or highly similar (no more than 2 band difference in 26 bands) ApaI-PFGE patterns when their DNA was restricted by AscI and ApaI restriction enzymes. Timely availability of molecular subtyping results enabled epidemiologists to separate outbreak cases from temporally associated sporadic cases in the same geographic areas and facilitated the identification of contaminated hot dogs manufactured at a single commercial facility as the source of the outbreak. During the investigation of this outbreak, a standardized protocol for subtyping L. monocytogenes by PFGE was developed and disseminated to public health laboratories participating with CDCs PulseNet network; these laboratories were requested to begin routine PFGE subtyping of L. monocytogenes.

A Whole-Genome Single Nucleotide Polymorphism-Based Approach To Trace and Identify Outbreaks Linked to a Common Salmonella enterica subsp. enterica Serovar Montevideo Pulsed-Field Gel Electrophoresis Type

ABSTRACT In this study, we report a whole-genome single nucleotide polymorphism (SNP)-based evolutionary approach to study the epidemiology of a multistate outbreak of Salmonella enterica subsp. enterica serovar Montevideo. This outbreak included 272 cases that occurred in 44 states between July 2009 and April 2010. A case-control study linked the consumption of salami made with contaminated black and red pepper to the outbreak. We sequenced, on the SOLiD System, 47 isolates with XbaI PFGE pattern JIXX01.0011, a common pulsed-field gel electrophoresis (PFGE) pattern associated with isolates from the outbreak. These isolates represented 20 isolates collected from human sources during the period of the outbreak and 27 control isolates collected from human, food, animal, and environmental sources before the outbreak. Based on 253 high-confidence SNPs, we were able to reconstruct a tip-dated molecular clock phylogeny of the isolates and to assign four human isolates to the actual outbreak. We developed an SNP typing assay to rapidly discriminate between outbreak-related cases and non-outbreak-related cases and tested this assay on an extended panel of 112 isolates. These results suggest that only a very small percentage of the human isolates with the outbreak PFGE pattern and obtained during the outbreak period could be attributed to the actual pepper-related outbreak (20%), while the majority (80%) of the putative cases represented background cases. This study demonstrates that next-generation-based SNP typing provides the resolution and accuracy needed for outbreak investigations of food-borne pathogens that cannot be distinguished by currently used subtyping methods.

Distribution of Listeria monocytogenes Molecular Subtypes among Human and Food Isolates from New York State Shows Persistence of Human Disease-Associated Listeria monocytogenes Strains in Retail Environments

While there is considerable information available regarding Listeria monocytogenes contamination patterns in food processing plants, our understanding of L. monocytogenes contamination and transmission in retail operations is limited. We characterized 125 food, 40 environmental, and 342 human clinical L. monocytogenes isolates collected in New York State from 1997 to 2002 using automated ribotyping and hly allelic variation. All environmental isolates were obtained from retail establishments and the majority of food isolates (98 isolates) were obtained from foods that were prepared or handled at retail. Overall, food and/or environmental isolates from 50 different retail establishments were characterized. The 125 food and 40 environmental isolates were differentiated into 29 and 10 ribotypes, respectively. For 16 retail establishments, we found evidence for persistence of one or more specific L. monocytogenes strains as indicated by isolation of the same EcoRI ribotype from food or environmental samples collected in a given establishment on different days. The human isolates were differentiated into 48 ribotypes. Statistical analyses showed that two ribotypes were significantly (P < 0.0001) more common among food isolates as compared with human isolates. However, a total of 17 ribotypes found among the human clinical isolates were also found among the food and environmental isolates. We conclude that L. monocytogenes, including subtypes that have been linked to human disease, can persist in retail environments. Implementation of Listeria control procedures in retail operations, which process and handle products that permit the growth of L. monocytogenes, are thus a critical component of a farm-to-table L. monocytogenes control program.

Comparative Phenotypic, Molecular, and Virulence Characterization of Vibrio parahaemolyticus O3:K6 Isolates

ABSTRACT Historically, Vibrio parahaemolyticus infections have been characterized by sporadic cases caused by multiple, diverse serotypes. However, since 1996, V. parahaemolyticus serotype O3:K6 strains have been associated with several large-scale outbreaks of illness, suggesting the emergence of a “new” group of organisms with enhanced virulence. We have applied three different molecular subtyping techniques to identify an appropriate method for differentiating O3:K6 isolates from other serotypes. Pulsed-field gel electrophoresis (PFGE) following NotI digestion differentiated seven closely related subtypes among O3:K6 and related strains, which were distinct from PFGE patterns for non-O3:K6 isolates. Ribotyping and tdh sequencing were less discriminatory than PFGE, but further confirmed close genetic relationships among recent O3:K6 isolates. In vitro adherence and cytotoxicity studies with human epithelial cells showed that O3:K6 isolates exhibited statistically higher levels of adherence and cytotoxicity to host cells than non-O3:K6 isolates. Epithelial cell cytotoxicity patterns were determined with a lactate dehydrogenase release assay. At 3 h postinfection, high relative cytotoxicities (>50% maximum lactate dehydrogenase activity) were found among a greater proportion of recently isolated O3:K6 and closely related strains (75%) than among the non-O3:K6 isolates (23%). A statistically significant relationship between adherence and cytotoxicity suggests that the pathogenic potential of some isolates may be associated with increased adherence to epithelial cells. Our findings suggest that enhanced adherence and cytotoxicity may contribute to the apparent unique pathogenic potential of V. parahaemolyticus O3:K6 strains.

A recurring outbreak of Shigella sonnei among traditionally observant Jewish children in New York City: the risks of daycare and household transmission

Dispersed community outbreaks of Shigella sonnei have occurred cyclically among traditionally observant Jews in the United States. In February 2000, we investigated a S. sonnei outbreak in one Jewish community in New York City. To determine risk factors for introduction of infection into households, we conducted a cohort study of households to compare risk factors for illness among primary subjects within households and age-matched well siblings. Isolates were subtyped by pulsed-field gel electrophoresis (PFGE). We used a random effects model to assess extra-household vs. intra-household transmission in households with multiple ill household members. Daycare or pre-school attendance [matched odds ratio (mOR) 16.1, P<0.001] and age <60 months (mOR 6.3, P<0.001) were independently associated with index subject illness. Outbreak isolates were closely related by PFGE analysis to the strain previously observed in Jewish community outbreaks. The random effects model strongly indicated that multiple illnesses in a single household are due to secondary transmission. Disease containment efforts should focus on reducing Shigella transmission in childcare settings and within homes.

Molecular Epidemiology and Cluster Analysis of Human Listeriosis Cases in Three U.S. States

To better understand the transmission and epidemiology of human listeriosis, 647 Listeria monocytogenes isolates obtained from human listeriosis cases in four U.S. locations (Michigan, Ohio, New York State, and New York City) over 61 months (1998 to 2003) were characterized by automated EcoRI ribotyping. A total of 65 ribotypes were differentiated among the characterized isolates; 393, 227, and 24 isolates were classified into lineages I, II, and III, respectively, and 3 isolates were not classified to lineage. The three most common ribotypes (responsible for 39% of all cases) represented L. monocytogenes epidemic clones, each of which had previously been linked to at least two human listeriosis outbreaks. Categorical analyses revealed that ribotypes and lineages were nonrandomly distributed among the four locations. Temporal cluster analysis of cases identified 13 statistically significant temporal subtype clusters, which represented 26% of all cases. Three of these clusters matched previously described human listeriosis outbreaks. Isolates involved in clusters belonged to nine ribotypes. Four, eight, and one cluster were caused by lineages I, II, and III, respectively. The two largest clusters were both caused by the epidemic clone representing ribotype DUP-1044A. Categorical analyses revealed no significant associations between lineage or ribotype and clinical manifestation (central nervous system infection, septicemia, fetal infection, or other infection) or disease outcome (fatal or not fatal). Although human listeriosis cases are caused by isolates belonging to a diversity of EcoRI ribotypes, specific lineage I epidemic clones cause a large number of human listeriosis cases. Many human listeriosis cases can be grouped into statistically significant temporal clusters, including widely distributed and region-specific clusters associated with isolates of various ribotypes. L. monocytogenes lineages and EcoRI ribotypes do not appear to differ in their likelihood of causing different clinical manifestations or mortality.

Serving High-Risk Foods in a High-Risk Setting: Survey of Hospital Food Service Practices after an Outbreak of Listeriosis in a Hospital

BACKGROUND AND OBJECTIVES Prepared ready-to-eat salads and ready-to-eat delicatessen-style meats present a high risk for Listeria contamination. Because no foodborne illness risk management guidelines exist specifically for US hospitals, a survey of New York City (NYC) hospitals was conducted to characterize policies and practices after a listeriosis outbreak occurred in a NYC hospital. METHODS From August through October 2008, a listeriosis outbreak in a NYC hospital was investigated. From February through April 2009, NYCs 61 acute-care hospitals were asked to participate in a telephone survey regarding food safety practices and policies, specifically service of high-risk foods to patients at increased risk for listeriosis. RESULTS Five patients with medical conditions that put them at high risk for listeriosis had laboratory-confirmed Listeria monocytogenes infection. The Listeria outbreak strain was isolated from tuna salad prepared in the hospital. Fifty-four (89%) of 61 hospitals responded to the survey. Overall, 81% of respondents reported serving ready-to-eat deli meats to patients, and 100% reported serving prepared ready-to-eat salads. Pregnant women, patients receiving immunosuppressive drugs, and patients undergoing chemotherapy were served ready-to-eat deli meats at 77%, 59%, and 49% of hospitals, respectively, and were served prepared ready-to-eat salads at 94%, 89%, and 73% of hospitals, respectively. Only 4 (25%) of 16 respondents reported having a policy that ready-to-eat deli meats must be heated until steaming hot before serving. CONCLUSIONS Despite the potential for severe outcomes of Listeria infection among hospitalized patients, the majority of NYC hospitals had no food preparation policies to minimize risk. Hospitals should implement policies to avoid serving high-risk foods to patients at risk for listeriosis.

Child Care-associated Outbreak Of escherichia Coli O157:h7 And Hemolytic Uremic Syndrome

We present an outbreak of E. coli O157:H7 diarrhea in an urban child care center. Eleven of 45 attendees with diarrhea had positive tests (stool culture or shiga-like toxin assay) for E. coli O157:H7. Two of these 11 (18%) progressed to hemolytic uremic syndrome. Diarrheal illness in child care centers should be considered a public health risk. Staff education, hand washing, and cohorting or exclusion of attendees with diarrhea must be performed to help control infectious outbreaks.

Salmonella enterica Serotype Uganda Infection in New York City and Chicago

Outbreaks associated with distinct strains of Salmonella enterica serotype Uganda, a rare serotype, occurred in New York City and Chicago during the summer of 2001. Both outbreaks were linked to eating ready-to-eat pork products. This serotype may emerge as a more frequent cause of human infections.