Last data update: Oct 07, 2024. (Total: 47845 publications since 2009)
Records 1-30 (of 49 Records) |
Query Trace: Gieraltowski L[original query] |
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Genetic diversity in Salmonella enterica in outbreaks of foodborne and zoonotic origin in the USA in 2006-2017
Trees E , Carleton HA , Folster JP , Gieraltowski L , Hise K , Leeper M , Nguyen TA , Poates A , Sabol A , Tagg KA , Tolar B , Vasser M , Webb HE , Wise M , Lindsey RL . Microorganisms 2024 12 (8) Whole genome sequencing is replacing traditional laboratory surveillance methods as the primary tool to track and characterize clusters and outbreaks of the foodborne and zoonotic pathogen Salmonella enterica (S. enterica). In this study, 438 S. enterica isolates representing 35 serovars and 13 broad vehicle categories from one hundred epidemiologically confirmed outbreaks were evaluated for genetic variation to develop epidemiologically relevant interpretation guidelines for Salmonella disease cluster detection. The Illumina sequences were analyzed by core genome multi-locus sequence typing (cgMLST) and screened for antimicrobial resistance (AR) determinants and plasmids. Ninety-three of the one hundred outbreaks exhibited a close allele range (less than 10 allele differences with a subset closer than 5). The remaining seven outbreaks showed increased variation, of which three were considered polyclonal. A total of 16 and 28 outbreaks, respectively, showed variations in the AR and plasmid profiles. The serovars Newport and I 4,[5],12:i:-, as well as the zoonotic and poultry product vehicles, were overrepresented among the outbreaks, showing increased variation. A close allele range in cgMLST profiles can be considered a reliable proxy for epidemiological relatedness for the vast majority of S. enterica outbreak investigations. Variations associated with mobile elements happen relatively frequently during outbreaks and could be reflective of changing selective pressures. |
An investigation of an outbreak of Salmonella Typhimurium infections linked to cantaloupe – United States, 2022
Seelman Federman S , Jenkins E , Wilson C , DeLaGarza A , Schwensohn C , Schneider B , Nsubuga J , Literman R , Wellman A , Whitney BM , Bell RL , Harris-Garner K , McKenna C , Brillhart D , Cross M , Rueber K , Schlichte T , Oni K , Adams J , Crosby AJ , Bazaco MC , Gieraltowski L , Nolte K , Viazis S . Food Control 2024 166 In 2022, the Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state health and regulatory partners investigated an outbreak of Salmonella enterica serovar Typhimurium infections linked to cantaloupes from southwest Indiana, resulting in 87 ill persons and 32 hospitalizations reported in 11 states. Epidemiologic and traceback evidence confirmed cantaloupe as the vehicle for these infections. Based on records collected by FDA, traceback of cantaloupe exposures for 14 ill people converged on a packing house in southwest Indiana, which supplied cantaloupe to eight of the 11 points of service where ill people purchased cantaloupe. Salmonella isolates were recovered from environmental samples collected by FDA from three growers and a packing house in southwest Indiana. Whole genome sequencing analyses of these isolates found that isolates collected from one grower matched the Salmonella Typhimurium outbreak strain, and samples collected from the other two growers and the packing house matched a 2020 Salmonella Newport outbreak strain. State and federal public health and agricultural partners identified potential conditions and practices that could have possibly resulted in the contamination of cantaloupe, including the presence of Salmonella spp. in on-farm, post-harvest, and off-farm environments. This is the third outbreak of salmonellosis confirmed to be linked to melons, sourced from southwest Indiana in the last decade. The 2012, 2020, and 2022 outbreaks of reoccurring and persisting strains of Salmonella illustrate the need for additional efforts to determine the source and extent of environmental contamination in the melon growing region of southwest Indiana and for outreach and education to help promote practices to reduce contamination of melons. © 2024 |
Salmonella Hadar linked to two distinct transmission vehicles highlights challenges to enteric disease outbreak investigations
Brandenburg JM , Stapleton GS , Kline KE , Khoury J , Mallory K , Machesky KD , Ladd-Wilson SG , Scholz R , Freiman J , Schwensohn C , Palacios A , Gieraltowski L , Ellison Z , Tolar B , Webb HE , Tagg KA , Salah Z , Nichols M . Epidemiol Infect 2024 1-27 |
Multistate outbreak of Salmonella Oranienburg infections linked to bulb onions imported from Mexico – United States, 2021
Mitchell MR , Kirchner M , Schneider B , McClure M , Neil KP , Madad A , Jemaneh T , Tijerina M , Nolte K , Wellman A , Neises D , Pightling A , Swinford A , Piontkowski A , Sexton R , McKenna C , Cornell J , Sandoval AL , Wang H , Bell RL , Stager C , Zamora Nava MC , Lara de la Cruz JL , Sánchez Córdova LI , Galván PR , Ortiz JA , Flowers S , Grisamore A , Gieraltowski L , Bazaco M , Viazis S . Food Control 2024 160 In 2021, the U.S. Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state and local health and regulatory partners investigated an outbreak of Salmonella enterica serovar Oranienburg infections linked to bulb onions from Mexico, resulting in 1040 illnesses and 260 hospitalizations across 39 states, the District of Columbia, and Puerto Rico. The Kansas Department of Agriculture recovered the outbreak strain of Salmonella Oranienburg from a sample of condiment collected from an ill person's home. The condiment was made with cilantro, lime, and onions, but, at the time of collection, there were no onions remaining in it. FDA conducted traceback investigations for white, yellow, and red bulb onions, cilantro, limes, tomatoes, and jalapeño peppers. Growers in the state of Chihuahua, Mexico, were identified as supplying the implicated onions that could account for exposure to onions for all illnesses included in the traceback investigation, but investigators could not determine a single source or route of contamination. FDA collected product and environmental samples across the domestic supply chain but did not recover the outbreak strain of Salmonella. Binational collaboration and information sharing supported Mexican authorities in collecting environmental samples from two packing plants and onion, water, and environmental samples from 15 farms and firms in Chihuahua, Mexico identified through FDA's traceback investigation, but did not recover the outbreak strain. Distributors of the implicated onions issued voluntary recalls of red, yellow, and white whole, fresh onions imported from the state of Chihuahua, Mexico. This outbreak showcased how investigators overcame significant traceback and epidemiologic challenges, the need for strengthening the ongoing collaboration between U.S. and Mexican authorities and highlighted the need for identifying practices across the supply chain that can help improve the safety of onions. © 2024 |
Notes from the field: Rapidly linking an outbreak of salmonella typhimurium infections to domestically grown cantaloupes through early collaboration - United States, 2022
Schwensohn C , Schneider B , Jenkins E , Wellman A , Federman SS , Oni O , Stone N , Adams J , Gieraltowski L . MMWR Morb Mortal Wkly Rep 2024 73 (5) 114-115 |
Notes from the field: Multistate outbreak of Escherichia coli O157:H7 infections linked to a national fast-food chain - United States, 2022
Stager C , Donovan D , Edwards L , Pereira E , Williams L , Freiman J , Schwensohn C , Gieraltowski L . MMWR Morb Mortal Wkly Rep 2023 72 (26) 732-733 In August 2022, the Michigan Department of Health and Human Services alerted CDC to an approximately fivefold increase in regional cases of Escherichia coli O157:H7 infection. Whole genome sequencing was used to characterize isolates from laboratory-confirmed infections in ill persons. Initial patient interviews indicated that many had consumed meals from the same national fast-food chain. Federal, state, and local officials initiated an investigation to identify the outbreak source and prevent additional cases. This activity was reviewed by CDC and was conducted consistent with applicable federal law and CDC policy.* | | CDC defined a case as an E. coli O157:H7 infection with an isolate highly related to the outbreak strain (within 0–2 alleles) by core genome multilocus sequence typing, with illness onset during July 26–August 24, 2022. PulseNet, CDC’s national molecular subtyping network for enteric disease surveillance, detected 109 cases from six states, including Michigan (67; 61%), Ohio (24; 22%), Indiana (11; 10%), Pennsylvania (four; 4%), Kentucky (two; 2%) and New York (one; 1%). The median patient age was 22 years (range = 1–94 years), and 49 (45%) were female. Fifty-two (48%) patients were hospitalized, and 13 (12%) developed hemolytic-uremic syndrome, a recognized complication of E. coli O157:H7 infection; no deaths occurred. |
An investigation of an outbreak of Salmonella Newport infections linked to melons United States, 2020
Jenkins E , Gardenhire I , Whitney BM , Martin KB , Schwensohn C , Gieraltowski L , Leeper MM , McCurdy V , McClure M , Wellman A , Pightling A , Smith M , Swinford A , Hainstock L , Crosby AJ , Bazaco MC , Viazis S . Food Control 2023 152 The United States are one of the world's leading consumers of melons. In 2020, the Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state health and regulatory partners investigated an outbreak of Salmonella Newport infections linked to melons from southwest Indiana, resulting in 80 ill persons and 18 hospitalizations reported across 15 states. Epidemiologic and traceback data indicated melons as the vehicle for these infections, but the collinearity of melon varieties purchased and consumed together in combination with the traceback investigation that could not rule out either melon type, did not allow investigators to delineate whether the vehicle was cantaloupe alone or, both cantaloupe and watermelons. Analysis of traceback records for cantaloupe and/or watermelon exposures for 12 ill people indicated convergence on a grower in southwest Indiana which supplied cantaloupe to the nine of eleven points of service where ill people purchased cantaloupe; similar convergence was not observed for watermelon. While Salmonella isolates were recovered from environmental samples collected by FDA throughout the growing operation, they were not highly genetically related to the outbreak strain by whole genome sequencing analyses, i.e. greater than a 20 high quality single nucleotide polymorphisms difference. This outbreak illustrates the need for additional efforts to determine the source and extent of environmental contamination in the melon growing region of southwest Indiana and emphasizes the need for outreach and education efforts to help promote farm practices to reduce pathogen contamination of melons. 2023 |
Salmonella Outbreaks Linked to Beef, United States, 2012-2019.
Canning M , Birhane MG , Dewey-Mattia D , Lawinger H , Cote A , Gieraltowski L , Schwensohn C , Tagg KA , Francois Watkins LK , Park Robyn M , Marshall KE . J Food Prot 2023 86 (5) 100071 The Centers for Disease Control and Prevention (CDC) has identified nontyphoidal Salmonella as one of the top five pathogens contributing to foodborne illnesses in the United States. Beef continues to be a common source of Salmonella outbreaks, despite the implementation of interventions at slaughter and processing facilities to reduce contamination of beef. We described Salmonella outbreaks linked to beef in the United States during 2012-2019, examined trends, and identified potential targets for intervention and prevention strategies. We queried CDC's Foodborne Disease Outbreak Surveillance System (FDOSS) for all foodborne nontyphoidal Salmonella outbreaks linked to beef as the single contaminated ingredient or implicated food, with the date of first illness onset from 2012 to 2019. Information on antimicrobial resistance (AR) for outbreak-related isolates was obtained from CDC's National Antimicrobial Resistance Monitoring System (NARMS). We calculated the number of outbreaks, outbreak-related illnesses, hospitalizations, and deaths overall, by beef processing category and Salmonella serotype. During 2012-2019, 27 Salmonella outbreaks were linked to beef consumption, resulting in 1103 illnesses, 254 hospitalizations, and two deaths. The most common category of beef implicated was nonintact raw, ground beef (12 outbreaks, 44%), followed by intact raw (six outbreaks, 22%). Ground beef was responsible for the most illnesses (800, 73%), both of the reported deaths, and was the source of the largest outbreak. AR data were available for 717 isolates from 25 (93%) outbreaks. Nine (36%) of these outbreaks had isolates resistant to one or more of the antibiotics tested by NARMS, of which eight (89%) contained multidrug-resistant isolates. Several outbreaks reported highlight challenges faced during investigations, areas where further research may be warranted, and opportunities to prevent future outbreaks along the farm-to-fork continuum. |
An Overview of Foodborne Sample-Initiated Retrospective Outbreak Investigations and Interagency Collaboration in the United States.
Wellman A , Bazaco M , Blessington T , Pightling A , Dwarka A , Hintz L , Wise ME , Gieraltowski L , Conrad A , Nguyen TA , Hise K , Viazis S , Beal J . J Food Prot 2023 86 (6) 100089 Foodborne outbreak investigations have traditionally included the detection of a cluster of illnesses first, followed by an epidemiologic investigation to identify a food of interest. The increasing use of whole genome sequencing (WGS) subtyping technology for clinical, environmental, and food isolates of foodborne pathogens, and the ability to share and compare the data on public platforms, present new opportunities to identify earlier links between illnesses and their potential sources. We describe a process called sample-initiated retrospective outbreak investigations (SIROI) used by federal public health and regulatory partners in the United States. SIROIs begin with an evaluation of the genomic similarity between bacterial isolates recovered from food or environmental samples and clusters of clinical isolates while subsequent and parallel epidemiologic and traceback investigations are initiated to corroborate their connection. SIROIs allow for earlier hypothesis generation, followed by targeted collection of information about food exposures and the foods and manufacturer of interest, to confirm a link between the illnesses and their source. This often leads to earlier action that could reduce the breadth and burden of foodborne illness outbreaks. We describe two case studies of recent SIROIs and present the benefits and challenges. Benefits include insight into foodborne illness attribution, international collaboration, and opportunities for enhanced food safety efforts in the food industry. Challenges include resource intensiveness, variability of epidemiologic and traceback data, and an increasingly complex food supply chain. SIROIs are valuable in identifying connections among small numbers of illnesses that may span significant time periods; detecting early signals for larger outbreaks or food safety issues associated with manufacturers; improving our understanding of the scope of contamination of foods; and identifying novel pathogen/commodity pairs. |
An outbreak investigation of Salmonella typhimurium illnesses in the United States linked to packaged leafy greens produced at a controlled environment agriculture indoor hydroponic operation - 2021
McClure M , Whitney B , Gardenhire I , Crosby A , Wellman A , Patel K , McCormic ZD , Gieraltowski L , Gollarza L , Low MSF , Adams J , Pightling A , Bell RL , Nolte K , Tijerina M , Frost JT , Beix JA , Boegler KA , Dow J , Altman S , Wise ME , Bazaco MC , Viazis S . J Food Prot 2023 86 (5) 100079 In 2021, the U.S. Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and state partners investigated a multistate outbreak of Salmonella Typhimurium illnesses linked to packaged leafy greens from a controlled environment agriculture (CEA) operation in Illinois. Thirty-one illnesses and four hospitalizations were reported in four states, with a significant epidemiologic signal for packaged leafy greens from Farm A. A traceback investigation for leafy greens included seven points of service (POS) with food exposure data from eight ill people. Each POS was supplied leafy greens by Farm A. FDA investigators observed operations at Farm A and noted that 1) the firm did not consider their indoor hydroponic pond water as agricultural water, 2) condensate dripping from the chiller water supply line inside the building, and 3) unprotected outdoor storage of packaged soilless growth media and pallets used for finished product. FDA collected 25 product, water, and environmental samples from Farm A. The outbreak strain was recovered from a water sample collected from a stormwater drainage basin located on the property adjacent to Farm A. In addition, an isolate of Salmonella Liverpool was recovered from two indoor growing ponds within the same growing house, but no illnesses were linked to the isolate. Farm A voluntarily recalled all implicated products and provided their root cause analysis (RCA) and return-to-market plan to FDA. While the source and route of the contamination were not determined by the RCA, epidemiologic and traceback evidence confirmed the packaged salads consumed by ill persons were produced by Farm A. This was the first investigation of a multistate foodborne illness outbreak associated with leafy greens grown in a CEA operation. This outbreak demonstrated the need for growers using hydroponic methods to review their practices for potential sources and routes of contamination and to reduce food safety risks when identified. |
Bi-national Outbreak of Salmonella Newport Infections Linked to Onions: the United States Experience.
McCormic ZD , Patel K , Higa J , Bancroft J , Donovan D , Edwards L , Cheng J , Adcock B , Bond C , Pereira E , Doyle M , Wise ME , Gieraltowski L . Epidemiol Infect 2022 150 1-23 From 2016-2019, dry bulb onions were the suspected cause of three multistate outbreaks in the United States. We investigated a large multistate outbreak of Salmonella Newport infections that caused illnesses in both the United States and Canada in 2020. Epidemiologic, laboratory and traceback investigations were conducted to determine the source of the infections, and data were shared among U.S. and Canadian public health officials. We identified 1127 U.S. illnesses from 48 states with illness onset dates ranging from 19 June to 11 September 2020. Sixty-six per cent of ill people reported consuming red onions in the week before illness onset. Thirty-five illness sub-clusters were identified during the investigation and seventy-four per cent of sub-clusters served red onions to customers during the exposure period. Traceback for the source of onions in illness sub-clusters identified a common onion grower in Bakersfield, CA as the source of red onions, and onions were recalled at this time. Although other strains of Salmonella Newport were identified in environmental samples collected at the Bakersfield, CA grower, extensive environmental and product testing did not yield the outbreak strain. This was the third largest U.S. foodborne Salmonella outbreak in the last 30 years. It is the first U.S. multistate outbreak with a confirmed link to dry bulb onions, and it was nearly 10-fold larger than prior outbreaks with a suspected link to onions. This outbreak is notable for its size and scope, as well as the international data sharing that led to implication of red onions as the primary cause of the outbreak. Although an environmental assessment at the grower identified several factors that likely contributed to the outbreak, no main reason was identified. The expedient identification of the outbreak vehicle and response of multiple public health agencies allowed for recall and removal of product from the marketplace, and rapid messaging to both the public and industry on actions to protect consumers; these features contributed to a decrease in cases and expeditious conclusion of the outbreak. |
A multiple-serotype outbreak of Salmonella infections linked to kratom, United States, 2017-2018
Schwensohn C , Nsubuga J , Cronquist L , Jose G , Mastel L , McCullough L , Smith L , Powell M , Booth H , Allen K , Classon A , Gieraltowski L . Foodborne Pathog Dis 2022 19 (9) 648-653 In early 2018, we investigated a large national multiple-serotype Salmonella outbreak linked to contaminated kratom, a raw minimally processed botanical substance. Kratom is a plant consumed for its stimulant effects and as an opioid substitute. A case was defined as a laboratory-confirmed Salmonella infection with one of the outbreak strains (serotypes I 4,[5],12:b:-, Heidelberg, Javiana, Okatie, Weltevreden, or Thompson) with illnesses onset during January 11, 2017-May 8, 2018. State and local officials collected detailed information on product consumption and sources. Suspected products were tested for Salmonella and traceback was conducted to determine product distribution chains and suppliers. We identified 199 cases from 41 states; 54 patients were hospitalized. Early interviews indicated kratom was an exposure of interest. Seventy-six (74%) of 103 people interviewed reported consuming kratom in pills, powders, or teas. Multiple serotypes of Salmonella were detected in samples of kratom collected from the homes of the patients and from retail locations. Several companies issued recalls of kratom products due to Salmonella contamination. To the authors' knowledge, this investigation is the first to establish kratom as a vehicle for Salmonella infection. Our findings underscore the serious safety concerns regarding minimally processed botanical substances intended for oral consumption and the challenges in investigating outbreaks linked to novel outbreak vehicles. |
A 2019 Outbreak Investigation of Hepatitis A Virus Infections in the United States Linked to Imported Fresh Blackberries.
McClure M , Nsubuga J , Montgomery MP , Jenkins E , Crosby A , Schoelen D , Basler C , Ramachandran S , Lin Y , Xia GL , Khudaykov Y , Suktankar V , Wagley A , Thomas V , Woods J , Hintz L , Oliveira J , Sandoval AL , Frederick J , Hendrickson B , Gieraltowski L , Viazis S . Food Environ Virol 2022 14 (3) 236-245 Globally, hepatitis A virus (HAV) is one of the most common agents of acute viral hepatitis and causes approximately 1.4 million cases and 90,000 deaths annually despite the existence of an effective vaccine. In 2019, federal, state, and local partners investigated a multi-state outbreak of HAV infections linked to fresh blackberries sourced from multiple suppliers in Michoacn, Mexico. A total of 20 individuals with outbreak-related HAV infection were reported in seven states, including 11 hospitalizations, and no deaths. The Food and Drug Administration (FDA), the Centers for Disease Control and Prevention (CDC), and Nebraska State and Douglas County Health Departments conducted a traceback investigation for fresh blackberries reportedly purchased by 16 ill persons. These individuals reported purchasing fresh blackberries from 11 points of service from September 16 through 29, 2019 and their clinical isolates assessed through next-generation sequencing and phylogenetic analysis were genetically similar. The traceback investigation did not reveal convergence on a common grower or packing house within Mexico, but all of the blackberries were harvested from growers in Michoacn, Mexico. FDA did not detect the pathogen after analyzing fresh blackberry samples from four distributors, one consumer, and from nine importers at the port of entry as a result of increased screening. Challenges included gaps in traceability practices and the inability to recover the pathogen from sample testing, which prohibited investigators from determining the source of the implicated blackberries. This multi-state outbreak illustrated the importance of food safety practices for fresh produce that may contribute to foodborne illness outbreaks. |
Multistate outbreak of Salmonella mbandaka infections linked to sweetened puffed wheat cereal-United States, 2018
Keaton AA , Schwensohn CA , Brandenburg JM , Pereira E , Adcock B , Tecle S , Hinnenkamp R , Havens J , Bailey K , Applegate B , Whitney P , Gibson D , Manion K , Griffin M , Ritter J , Biskupiak C , Ajileye K , Golwalkar M , Gosciminski M , Viveiros B , Caron G , McCullough L , Smith L , Vidyaprakash E , Doyle M , Hardy C , Elliot EL , Gieraltowski LB . Epidemiol Infect 2022 150 1-14 In May of 2018, PulseNet, the national molecular subtyping network for enteric pathogens, detected a multistate cluster of illnesses caused by an uncommon molecular subtype of Salmonella serovar Mbandaka. A case was defined as an illness in a person infected with the outbreak strain of Salmonella Mbandaka with illness onset on or after 3 March 2018 and before 1 September 2018. One-hundred thirty-six cases from 36 states were identified; 35 hospitalisations and no deaths were reported. Ill people ranged in age from <1 year to 95 years (median: 57 years). When standardised questionnaires did not generate a strong hypothesis, opened-ended interviews were performed. Sixty-three of 84 (75%) ultimately reported consuming or possibly consuming a specific sweetened puffed wheat cereal in the week before illness onset. Environmental sampling performed at the cereal manufacturing facility yielded the outbreak strain. The outbreak strain was also isolated from open cereal samples from ill people's homes and from a sealed retail sample. Due to these findings, the brand owner of the product issued a voluntary recall of the cereal on 14 June 2018. Additional investigation of the manufacturing facility identified persistent environmental contamination with Salmonella Mbandaka that was closely genetically related to other isolates in the outbreak. This investigation highlights the ability of Salmonella to survive in low-moisture environments, and the potential for prolonged outbreaks linked to products with long shelf lives and large distribution areas. |
Multistate Outbreak of Listeria monocytogenes Infections Linked to Fresh, Soft Hispanic-Style Cheese - United States, 2021.
Palacios A , Otto M , Flaherty E , Boyle MM , Malec L , Holloman K , Low M , Wellman A , Newhart C , Gollarza L , Weeks T , Muyombwe A , Lozinak K , Kafka E , O'Halloran D , Rozza T , Nicholas D , Ivory S , Kreil K , Huffman J , Gieraltowski L , Conrad A . MMWR Morb Mortal Wkly Rep 2022 71 (21) 709-712 Listeriosis is a serious infection usually caused by eating food contaminated with the bacterium Listeria monocytogenes. An estimated 1,600 persons become ill with listeriosis each year, among whom approximately 260 die. Persons at higher risk for listeriosis include pregnant persons and their newborns, adults aged ≥65 years, and persons with weakened immune systems. Persons with invasive listeriosis usually report symptoms starting 1-4 weeks after eating food contaminated with L. monocytogenes; however, some persons who become infected have reported symptoms starting as late as 70 days after exposure or as early as the same day of exposure (1). On January 29, 2021, PulseNet, the national molecular subtyping surveillance network coordinated by CDC, identified a multistate cluster of three L. monocytogenes infections: two from Maryland and one from Connecticut (2). CDC, the Food and Drug Administration (FDA), and state and local partners began an investigation on February 1, 2021. A total of 13 outbreak-related cases were eventually identified from four states. All patients reported Hispanic ethnicity; 12 patients were hospitalized, and one died. Rapid food testing and record collection by regulatory agencies enabled investigators to identify a brand of queso fresco made with pasteurized milk as the likely source of the outbreak, leading to an initial product recall on February 19, 2021. Fresh, soft Hispanic-style cheeses made with pasteurized milk are a well-documented source of listeriosis outbreaks. These cheeses can be contaminated with L. monocytogenes unless stringent hygienic controls are implemented, and the processing environment is monitored for contamination (3). U.S. public health agencies should establish or improve communications, including new methods of disseminating information that also effectively reach Hispanic populations, to emphasize the risk from eating fresh, soft Hispanic-style cheeses, even those made with pasteurized milk. |
Multistate Outbreak Investigation of Salmonella Infections Linked to Kratom: A Focus on Traceback, Laboratory, and Regulatory Activities.
Nsubuga J , Baugher J , Dahl E , Schwensohn C , Blessington T , Aguillon R , Whitney B , Goldman S , Brewster M , Humbert J , Crosby A , Gieraltowski L , Shade Singleton L , Hilgendorf J . J Food Prot 2022 85 (5) 747-754 During the spring of 2018, the U.S. Food and Drug Administration (FDA), U.S. Centers for Disease Control and Prevention (CDC), states and local public health agencies responded to a multistate outbreak of gastrointestinal illnesses caused by multiple Salmonella serovars and associated with consumption of kratom, a product harvested from a tropical tree native to Southeast Asia. The outbreak included 199 case-patients reported by 41 U.S. states, with illness onset dates ranging from January 11, 2017 to May 8, 2018, leading to 54 hospitalizations, and no deaths. Case-patients reported purchasing kratom products from physical and online retail points of service (POS). Products distributed to 16 POS where 24 case-patients from 17 states purchased kratom were selected for traceback investigation. Traceback revealed that the kratom was imported from several countries, the most common being Indonesia. Local and state officials collected product samples from case-patients and retail POS. The FDA collected 76 product samples from POS and distributors, of which 42 (55%) tested positive for Salmonella . The positive samples exhibited a wide range of pulsed field gel electrophoresis (PFGE) patterns and whole genome sequence (WGS) genetic heterogeneity, and a total 25 of 42 (60%) yielded at least one isolate indistinguishable from one or more outbreak-related clinical isolates. While it does not exclude a possibility of a single contamination source, the extent of genetic diversity exhibited by the Salmonella isolates recovered from product samples and a lack of traceback convergence, suggested that kratom was widely contaminated across multiple sites from which it was grown, harvested, and packaged. As a result of the contamination, kratom products were recalled by numerous firms (both voluntarily and mandatory). Epidemiologic, traceback, and laboratory evidence supported the conclusion that kratom products were associated with illnesses. |
Decisions to attend holiday gatherings during COVID-19 and engagement in key prevention strategies - United States, January 2021.
Pomeroy MA , Hoover ER , Dumas BL , Kennedy KS , Wittry B , Laughlin ME , Harris DM , Gieraltowski L , Yellman MA , Garcia-Williams AG , Marshall KE . Epidemiol Infect 2022 150 1-29 Gatherings where people are eating and drinking can increase the risk of getting and spreading SARS-CoV-2 among people who are not fully vaccinated; prevention strategies like wearing masks and physical distancing continue to be important for some groups. We conducted an online survey to characterise fall/winter 2020-2021 holiday gatherings, decisions to attend and prevention strategies employed during and before gatherings. We determined associations between practicing prevention strategies, demographics and COVID-19 experience. Among 502 respondents, one-third attended in person holiday gatherings; 73% wore masks and 84% practiced physical distancing, but less did so always (29% and 23%, respectively). Younger adults were 44% more likely to attend gatherings than adults >/=35 years. Younger adults (adjusted prevalence ratio (aPR) 1.53, 95% CI 1.19-1.97), persons who did not experience COVID-19 themselves or have relatives/close friends experience severe COVID-19 (aPR 1.56, 95% CI 1.18-2.07), and non-Hispanic White persons (aPR 1.57, 95% CI 1.13-2.18) were more likely to not always wear masks in public during the 2 weeks before gatherings. Public health messaging emphasizing consistent application of COVID-19 prevention strategies is important to slow the spread of COVID-19. |
Two multistate outbreaks of a reoccurring Shiga toxin-producing Escherichia coli strain associated with romaine lettuce - United States, 2018-2019
Waltenburg MA , Schwensohn C , Madad A , Seelman SL , Peralta V , Koske SE , Boyle MM , Arends K , Patel K , Mattioli M , Gieraltowski L , Neil KP . Epidemiol Infect 2021 150 e16 Leafy green vegetables are a common source of Shiga toxin-producing Escherichia coli O157:H7 (STEC O157) foodborne illness outbreaks. Ruminant animals, primarily cattle, are the major reservoir of STEC O157. Epidemiological, traceback, and field investigations were conducted to identify potential outbreak sources. Product and environmental samples were tested for STEC. A reoccurring strain of STEC O157 caused two multistate outbreaks linked to romaine lettuce in 2018 and 2019, resulting in 234 illnesses in 33 states. Over 80% of patients interviewed consumed romaine lettuce before illness. The romaine lettuce was sourced from two California growing regions: Santa Maria and Salinas Valley in 2018 and Salinas Valley in 2019. The outbreak strain was isolated from environmental samples collected at sites >90 miles apart across growing regions, as well as from romaine-containing products in 2019. Although the definitive route of romaine contamination was undetermined, use of a contaminated agricultural water reservoir in 2018 and contamination from cattle grazing on adjacent land in 2019 were suspected as possible factors. Preventing lettuce contamination from growth to consumption is imperative to preventing illness. These outbreaks highlight the need to further understand mechanisms of romaine contamination, including the role of environmental or animal reservoirs for STEC O157. © 2021 Cambridge University Press. All rights reserved. |
A Series of Papaya-Associated Salmonella Illness Outbreak Investigations in 2017 and 2019: A Focus on Traceback, Laboratory, and Collaborative Efforts.
Whitney BM , McClure M , Hassan R , Pomeroy M , Seelman SL , Singleton LN , Blessington T , Hardy C , Blankenship J , Pereira E , Davidson CN , Luo Y , Pettengill J , Curry P , McConnell T , Gieraltowski L , Schwensohn C , Basler C , Fritz K , McKenna C , Nieves K , Oliveira J , Sandoval AL , Crosby A , Williams D , Crocker K , Thomas D , Fulton T , Muetter L , Li L , Omoregie E , Holloman K , Brennan C , Thomas N , Barnes A , Viazis S . J Food Prot 2021 84 (11) 2002-2019 In 2017 and 2019, five outbreaks of infections from multiple strains of Salmonella linked to the consumption of whole, fresh Maradol papayas were reported in the United States, resulting in 325 ill persons. Traceback, laboratory, and epidemiologic evidence indicated papayas as the likely vehicle for each of these outbreaks and identified the source of papayas. State and U.S. Food and Drug Administration (FDA) laboratories recovered Salmonella from papaya samples from various points of distribution, including at import entry, and conducted serotyping, pulsed-field gel electrophoresis, and phylogenetic analyses of whole genome sequencing data. Federal and state partners led traceback investigations to determine the source of papayas. Four different suppliers of papayas were linked by traceback and laboratory results to five separate outbreaks of Salmonella infections associated with papayas. In 2017, multiple states tested papaya samples collected at retail, and Maryland and Virginia investigators recovered strains of Salmonella associated with one outbreak. FDA collected 183 papaya samples in 2017, and 11 samples yielded 62 isolates of Salmonella. Eleven serotypes of Salmonella were recovered from FDA papaya samples, and nine serotypes were closely related genetically by pulsed-field gel electrophoresis and whole genome sequencing to clinical isolates of four outbreaks, including the outbreak associated with positive state sample results. Four farms in Mexico were identified, and their names were released to the general public, retailers, and foreign authorities. In 2019, FDA collected 119 papaya samples, three of which yielded Salmonella; none yielded the 2019 outbreak strain. Investigators determined that papayas of interest had been sourced from a single farm in Campeche, Mexico, through traceback. This information was used to protect public health through public guidance, recalls, and import alerts and helped FDA collaborate with Mexican regulatory partners to enhance the food safety requirements for papayas imported from Mexico. |
Notes from the Field: An Outbreak of Escherichia coli O157:H7 Infections Linked to Romaine Lettuce Exposure - United States, 2019
Hoff C , Higa J , Patel K , Gee E , Wellman A , Vidanes J , Holland A , Kozyreva V , Zhu J , Mattioli M , Roundtree A , McFadden K , Whitlock L , Wise M , Gieraltowski L , Schwensohn C . MMWR Morb Mortal Wkly Rep 2021 70 (18) 689-690 On September 16, 2019, PulseNet, the national molecular subtyping network for foodborne disease surveillance, reported a multistate cluster of seven Escherichia coli O157:H7 infections from California (five), Oregon (one), and Pennsylvania (one). Isolates from cases of human illness were sequenced and then analyzed using core-genome multilocus sequence typing (cgMLST); the isolates were closely related within three allele differences (1). Federal, state, and local officials initiated a multistate outbreak investigation to identify the source and prevent additional illnesses. |
Hypothesis Generation during Foodborne Illness Outbreak Investigations
White AE , Smith KE , Booth H , Medus C , Tauxe RV , Gieraltowski L , Walter ES . Am J Epidemiol 2021 190 (10) 2188-2197 Hypothesis generation is a critical, but challenging, step in a foodborne outbreak investigation. The pathogens that contaminate food have many diverse reservoirs, resulting in seemingly limitless potential vehicles. Identifying a vehicle is particularly challenging for clusters detected through national pathogen-specific surveillance, as cases can be geographically dispersed and lack an obvious epidemiological link. Moreover, state and local health departments may have limited resources to dedicate to cluster and outbreak investigations. These challenges underscore the importance of hypothesis generation during an outbreak investigation. In this review, we present a framework for hypothesis generation focusing on three primary sources of information, typically used in combination: (1) known sources of the pathogen causing illness; (2) person, place, and time characteristics of cases associated with the outbreak (descriptive data); and (3) case exposure assessment. Hypothesis generation can narrow the list of potential food vehicles and focus subsequent epidemiologic, laboratory, environmental, and traceback efforts, ensuring that time and resources are used more efficiently and increasing the likelihood of rapidly and conclusively implicating the contaminated food vehicle. |
An Overview of Traceback Investigations and Three Case Studies of Recent Outbreaks ofEscherichia coliO157:H7 Infections Linked to Romaine Lettuce
Irvin K , Viazis S , Fields A , Seelman S , Blickenstaff K , Gee E , Wise M , Marshall K , Gieraltowski L , Harris S . J Food Prot 2021 84 (8) 1340-1356 Leafy greens contaminated with Shiga toxin-producing Escherichia coli (STEC) have continued to cause foodborne illness outbreaks in recent years and present a threat to public health. An important component of foodborne illness outbreak investigations is determining the source of the outbreak vehicle through traceback investigations. The Food and Drug Administration is home to traceback investigation experts that employ a standardized process to initiate, execute, and interpret the results of traceback investigations in collaboration with the Centers for Disease Control and Prevention and state and local partners. Traceback investigations of three outbreaks of STEC infections linked to romaine lettuce in 2018 and 2019 were examined to demonstrate challenges, limitations, and opportunities for improvement. The three outbreaks resulted in a total of 474 illnesses, 215 hospitalizations, and five deaths. These illnesses were linked to the consumption of romaine lettuce from three distinct growing regions in Arizona and California. Some of the challenges encountered included the time it took to initiate a traceback, limited product-identifying information throughout the supply chain, lack of interoperability in record keeping systems, and co-mingling of product from multiple suppliers. These challenges led to time delays in the identification of the farm source of the leafy greens and the inability to identify the root cause of contamination. Implementation of technology enabled traceability systems, testing of these systems, and future regulations to incentivize adoption of traceability systems are some of the initiatives that will help address these challenges by improving traceback investigations and ultimately preventing foodborne illnesses and future outbreaks from occurring. |
Lessons learned from a decade of investigations of shiga toxin-producing Escherichia coli outbreaks linked to leafy greens, United States and Canada
Marshall KE , Hexemer A , Seelman SL , Fatica MK , Blessington T , Hajmeer M , Kisselburgh H , Atkinson R , Hill K , Sharma D , Needham M , Peralta V , Higa J , Blickenstaff K , Williams IT , Jhung MA , Wise M , Gieraltowski L . Emerg Infect Dis 2020 26 (10) 2319-2328 Shiga toxin-producing Escherichia coli (STEC) cause substantial and costly illnesses. Leafy greens are the second most common source of foodborne STEC O157 outbreaks. We examined STEC outbreaks linked to leafy greens during 2009-2018 in the United States and Canada. We identified 40 outbreaks, 1,212 illnesses, 77 cases of hemolytic uremic syndrome, and 8 deaths. More outbreaks were linked to romaine lettuce (54%) than to any other type of leafy green. More outbreaks occurred in the fall (45%) and spring (28%) than in other seasons. Barriers in epidemiologic and traceback investigations complicated identification of the ultimate outbreak source. Research on the seasonality of leafy green outbreaks and vulnerability to STEC contamination and bacterial survival dynamics by leafy green type are warranted. Improvements in traceability of leafy greens are also needed. Federal and state health partners, researchers, the leafy green industry, and retailers can work together on interventions to reduce STEC contamination. |
Estimating the incubation period of Salmonella urinary tract infections using foodborne outbreak data
Jacobs Slifka KM , Blackstock A , Nguyen V , Schwensohn C , Gieraltowski L , Mahon BE . Foodborne Pathog Dis 2020 17 (10) 628-630 Urinary tract infections (UTIs) are common and may occur in foodborne Salmonella outbreaks. Using data from PulseNet, the U.S. national molecular subtyping network for foodborne disease surveillance, we analyzed the 9781 Salmonella isolates associated with the 110 outbreaks from 2004 to 2013 that included at least one urine isolate. Within each outbreak, we calculated standardized isolation dates, using these dates in a linear mixed model to estimate the difference in incubation period for infections yielding stool versus urine isolates. We estimate that the incubation period for Salmonella UTIs is on average 10.6 (95% confidence interval 6.0-15.2) days longer than for gastrointestinal illness, suggesting that outbreak investigators should interview UTI patients about a longer time period before illness onset to identify sources of infection. |
Estimated Community Seroprevalence of SARS-CoV-2 Antibodies - Two Georgia Counties, April 28-May 3, 2020.
Biggs HM , Harris JB , Breakwell L , Dahlgren FS , Abedi GR , Szablewski CM , Drobeniuc J , Bustamante ND , Almendares O , Schnall AH , Gilani Z , Smith T , Gieraltowski L , Johnson JA , Bajema KL , McDavid K , Schafer IJ , Sullivan V , Punkova L , Tejada-Strop A , Amiling R , Mattison CP , Cortese MM , Ford SE , Paxton LA , Drenzek C , Tate JE , CDC Field Surveyor Team , Brown Nicole , Chang Karen T , Deputy Nicholas P , Desamu-Thorpe Rodel , Gorishek Chase , Hanchey Arianna , Melgar Michael , Monroe Benjamin P , Nielsen Carrie F , Pellegrini Gerald JJr , Shamout Mays , Tison Laura I , Vagi Sara , Zacks Rachael . MMWR Morb Mortal Wkly Rep 2020 69 (29) 965-970 Transmission of SARS-CoV-2, the virus that causes coronavirus disease 2019 (COVID-19), is ongoing in many communities throughout the United States. Although case-based and syndromic surveillance are critical for monitoring the pandemic, these systems rely on persons obtaining testing or reporting a COVID-19-like illness. Using serologic tests to detect the presence of SARS-CoV-2 antibodies is an adjunctive strategy that estimates the prevalence of past infection in a population. During April 28-May 3, 2020, coinciding with the end of a statewide shelter-in-place order, CDC and the Georgia Department of Public Health conducted a serologic survey in DeKalb and Fulton counties in metropolitan Atlanta to estimate SARS-CoV-2 seroprevalence in the population. A two-stage cluster sampling design was used to randomly select 30 census blocks in each county, with a target of seven participating households per census block. Weighted estimates were calculated to account for the probability of selection and adjusted for age group, sex, and race/ethnicity. A total of 394 households and 696 persons participated and had a serology result; 19 (2.7%) of 696 persons had SARS-CoV-2 antibodies detected. The estimated weighted seroprevalence across these two metropolitan Atlanta counties was 2.5% (95% confidence interval [CI] = 1.4-4.5). Non-Hispanic black participants more commonly had SARS-CoV-2 antibodies than did participants of other racial/ethnic groups (p<0.01). Among persons with SARS-CoV-2 antibodies, 13 (weighted % = 49.9; 95% CI = 24.4-75.5) reported a COVID-19-compatible illness,* six (weighted % = 28.2; 95% CI = 11.9-53.3) sought medical care for a COVID-19-compatible illness, and five (weighted % = 15.7; 95% CI = 5.1-39.4) had been tested for SARS-CoV-2 infection, demonstrating that many of these infections would not have been identified through case-based or syndromic surveillance. The relatively low seroprevalence estimate in this report indicates that most persons in the catchment area had not been infected with SARS-CoV-2 at the time of the survey. Continued preventive measures, including social distancing, consistent and correct use of face coverings, and hand hygiene, remain critical in controlling community spread of SARS-CoV-2. |
Use, acceptability, performance, and health impact of hollow fiber ultrafilters for water treatment in rural Kenyan households, 2009-2011
Fagerli K , Gieraltowski L , Nygren B , Foote E , Gaines J , Oremo J , Odhiambo A , Kim S , Quick R . Am J Trop Med Hyg 2020 103 (1) 465-471 Diarrheal illness remains a leading cause of morbidity and mortality in children < 5 years in developing countries, and contaminated water contributes to diarrhea risk. To address this problem, a novel hollow fiber ultrafilter (HFU) was developed for household water treatment. To test its impact on water quality and infant health, we conducted a cluster-randomized longitudinal evaluation in 10 intervention and 10 comparison villages in Kenya, attempting to enroll all households with infants (< 12 months old). We conducted a baseline survey, distributed HFUs to intervention households, made biweekly home visits for 1 year to assess water treatment practices and diarrhea in infants, and tested water samples from both groups every 2 months for Escherichia coli. We enrolled 92 infants from intervention households and 74 from comparison households. During the 1-year study period, 45.7% of intervention households and 97.3% of comparison households had at least one stored water sample test positive for E. coli. Compared with comparison households, the odds of E. coli contamination in stored water was lower for intervention households (OR: 0.42, 95% CI: 0.24, 0.74), but there was no difference in the odds of reported diarrhea in infants, adjusting for covariates (OR: 1.19, 95% CI: 0.74, 1.90). Although nearly all water samples obtained from unprotected sources and filtered by the HFU were free of E. coli contamination, HFUs alone were not effective at reducing diarrhea in infants. |
Cyclosporiasis epidemiologically linked to consumption of green onions: Houston Metropolitan Area, August 2017
Hall NB , Chancey RJ , Keaton AA , Heines V , Cantu V , Vakil V , Long S , Short K , Franciscus E , Wahab N , Gieraltowski L , Straily A . J Food Prot 2020 83 (2) 326-330 During July 2017, Texas public health officials noted an increase in the number of reported cyclosporiasis cases. They detected a cluster in the Houston metropolitan area that involved four locations of a Mediterranean restaurant chain, restaurant A. A case-control study was conducted among patrons of restaurant A to identify a common food vehicle among items containing fresh produce. In matched case-control ingredient-level analyses that included both probable and confirmed cases, consumption of green onions, red onions, tomatoes, and cabbage was significantly associated with illness. A substantial percentage of case patients reported consumption of green onions, and only green onions remained statistically significantly associated with illness, whether probable and confirmed cases were included in analyses (matched odds ratio: 11.3; 95% confidence interval: 2.5 to 104.7), or only confirmed cases were included in analyses (matched odds ratio: 17.6; 95% confidence interval: 2.5 to 775.7). These results provide evidence that green onions were the likely vehicle of infection. It was not possible to trace the green onions to their source due to the need to redirect public health resources to Hurricane Harvey response efforts in Texas. |
Shiga Toxin-Producing E. coli Infections Associated with Romaine Lettuce - United States, 2018.
Bottichio L , Keaton A , Thomas D , Fulton T , Tiffany A , Frick A , Mattioli M , Kahler A , Murphy J , Otto M , Tesfai A , Fields A , Kline K , Fiddner J , Higa J , Barnes A , Arroyo F , Salvatierra A , Holland A , Taylor W , Nash J , Morawski BM , Correll S , Hinnenkamp R , Havens J , Patel K , Schroeder MN , Gladney L , Martin H , Whitlock L , Dowell N , Newhart C , Watkins LF , Hill V , Lance S , Harris S , Wise M , Williams I , Basler C , Gieraltowski L . Clin Infect Dis 2019 71 (8) e323-e330 BACKGROUND: Produce-associated outbreaks of Shiga toxin-producing Escherichia coli (STEC) were first identified in 1991. In April 2018, New Jersey and Pennsylvania officials reported a cluster of STEC O157 infections associated with multiple locations of a restaurant chain. CDC queried PulseNet, the national laboratory network for foodborne disease surveillance, for additional cases and began a national investigation. METHODS: A case was defined as an infection between March 13 and August 22, 2018 with one of the 22 identified outbreak-associated E. coli O157:H7 or E. coli O61 pulsed-field gel electrophoresis pattern combinations, or with a strain STEC O157 that was closely related to the main outbreak strain by whole genome sequencing. We conducted epidemiologic and traceback investigations to identify illness sub-clusters and common sources. An FDA-led environmental assessment, which tested water, soil, manure, compost, and scat samples, was conducted to evaluate potential sources of STEC contamination. RESULTS: We identified 240 case-patients from 37 states; 104 were hospitalized, 28 developed hemolytic uremic syndrome, and five died. Of 179 people who were interviewed, 152 (85%) reported consuming romaine lettuce in the week before illness onset. Twenty sub-clusters were identified. Product traceback from sub-cluster restaurants identified numerous romaine lettuce distributors and growers; all lettuce originated from the Yuma growing region. Water samples collected from an irrigation canal in the region yielded the outbreak strain of STEC O157. CONCLUSION: We report on the largest multistate leafy green-linked STEC O157 outbreak in several decades. The investigation highlights the complexities associated with investigating outbreaks involving widespread environmental contamination. |
Multistate outbreak of Salmonella infections linked to raw turkey products - United States, 2017-2019
Hassan R , Buuck S , Noveroske D , Medus C , Sorenson A , Laurent J , Rotstein D , Schlater L , Freiman J , Douris A , Simmons M , Donovan D , Henderson J , Tewell M , Snyder K , Oni O , Von Stein D , Dassie K , Leeper M , Adediran A , Dowell N , Gieraltowski L , Basler C . MMWR Morb Mortal Wkly Rep 2019 68 (46) 1045-1049 During 2018–2019, CDC, local and state public health partners, the U.S. Department of Agriculture (USDA), and the Food and Drug Administration (FDA) investigated a multistate outbreak of 356 Salmonella Reading infections from 42 states and the District of Columbia (DC) linked to turkey. The outbreak strain was isolated from raw turkey products, raw turkey pet food, and live turkeys. In July 2018, CDC and USDA’s Food Safety and Inspection Service (FSIS) shared outbreak investigation results with representatives from the U.S. turkey industry, engaging with an industry group rather than a specific company for the first time during an outbreak, and CDC issued a public investigation notice. During the investigation, four recalls of turkey products were issued. Evidence suggested that the outbreak strain of Salmonella was widespread in the turkey industry, and therefore, interventions should target all parts of the supply chain, including slaughter and processing facilities and upstream farm sources. |
Multistate outbreak of Salmonella Poona infections associated with imported cucumbers, 2015-2016.
Laughlin M , Bottichio L , Weiss J , Higa J , McDonald E , Sowadsky R , Fejes D , Saupe A , Provo G , Seelman S , Concepcion-Acevedo J , Gieraltowski L . Epidemiol Infect 2019 147 e270 We investigated a large multistate outbreak that occurred in the United States in 2015-2016. Epidemiologic, laboratory, and traceback studies were conducted to determine the source of the infections. We identified 907 case-patients from 40 states with illness onset dates ranging from July 3, 2015 to March 2, 2016. Sixty-three percent of case-patients reported consuming cucumbers in the week before illness onset. Ten illness sub-clusters linked to events or purchase locations were identified. All sub-clusters investigated received cucumbers from a single distributor which were sourced from a single grower in Mexico. Seventy-five cucumber samples were collected, 19 of which yielded the outbreak strain. Whole genome sequencing performed on 154 clinical isolates and 19 cucumber samples indicated that the sequenced isolates were closely related genetically to one another. This was the largest US foodborne disease outbreak in the last ten years and the third largest in the past 20 years. This was at least the fifth multistate outbreak caused by contaminated cucumbers since 2010. The outbreak is noteworthy because a recall was issued only 17 days after the outbreak was identified, which allowed for the removal of the contaminated cucumbers still available in commerce, unlike previous cucumber associated outbreaks. The rapid identification and response of multiple public health agencies resulted in preventing this from becoming an even larger outbreak. |
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