Last data update: Nov 04, 2024. (Total: 48056 publications since 2009)
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Query Trace: Schwensohn C[original query] |
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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 |
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 |
Strain of multidrug-resistant salmonella newport remains linked to travel to Mexico and U.S. beef products - United States, 2021-2022
Ford L , Ellison Z , Schwensohn C , Griffin I , Birhane MG , Cote A , Fortenberry GZ , Tecle S , Higa J , Spencer S , Patton B , Patel J , Dow J , Maroufi A , Robbins A , Donovan D , Fitzgerald C , Burrell S , Tolar B , Folster JP , Cooley LA , Francois Watkins LK . MMWR Morb Mortal Wkly Rep 2023 72 (45) 1225-1229 In 2016, CDC identified a multidrug-resistant (MDR) strain of Salmonella enterica serotype Newport that is now monitored as a persisting strain (REPJJP01). Isolates have been obtained from U.S. residents in all 50 states and the District of Columbia, linked to travel to Mexico, consumption of beef products obtained in the United States, or cheese obtained in Mexico. In 2021, the number of isolates of this strain approximately doubled compared with the 2018-2020 baseline and remained high in 2022. During January 1, 2021- December 31, 2022, a total of 1,308 isolates were obtained from patients, cattle, and sheep; 86% were MDR, most with decreased susceptibility to azithromycin. Approximately one half of patients were Hispanic or Latino; nearly one half reported travel to Mexico during the month preceding illness, and one third were hospitalized. Two multistate outbreak investigations implicated beef products obtained in the United States. This highly resistant strain might spread through travelers, animals, imported foods, domestic foods, or other sources. Isolates from domestic and imported cattle slaughtered in the United States suggests a possible source of contamination. Safe food and drink consumption practices while traveling and interventions across the food production chain to ensure beef safety are necessary in preventing illness. |
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 |
Multistate outbreak of salmonella thompson infections linked to seafood exposure - United States, 2021
Shen AQ , Dalen A , Bankers L , Matzinger SR , Schwensohn C , Patel K , Hise KB , Pereira E , Cripe J , Jervis RH . MMWR Morb Mortal Wkly Rep 2023 72 (19) 513-516 In July 2021, the Colorado Department of Public Health and Environment (CDPHE) laboratory identified a cluster of five Salmonella enterica serotype Thompson isolates related to one another within one allele difference, using whole genome multilocus sequence typing (wgMLST). These five isolates, submitted to the public health laboratory as is routine process for confirmatory testing of Salmonella, were highly related to those identified in a 2020 multistate investigation, during which traceback was conducted for sushi-grade tuna and salmon; a common supplier was not identified. The 2021 investigation commenced on August 5, 2021, with five patients living in Colorado, and one each in Missouri, Washington, and Wisconsin. During August-December 2021, CDC, CDPHE, public health and regulatory officials in several states, and the Food and Drug Administration (FDA) conducted epidemiologic, environmental, and laboratory investigations of this multistate outbreak of Salmonella Thompson. Isolates were genetically related to one another and to 2020 isolates within zero to one allele difference. Implicated seafood products were traced to a single seafood distributor, in which the outbreak strain was identified through environmental sampling, and in which inspection identified inadequate sanitization and opportunities for cross-contamination of raw fish. The distributor issued a voluntary recall of 16 seafood items with high potential for contamination and completed remediation actions. This outbreak illustrated the importance of effective cleaning and sanitizing procedures and implementation of controls. When multiple products are recalled during an outbreak investigation, collaboration between public health agencies and implicated facilities can help provide food safety information to restaurants, retailers, and consumers, and to ensure disposal of all recalled products. |
Corrigendum: Whole Genome Sequencing: Bridging One-Health Surveillance of Foodborne Diseases.
Gerner-Smidt P , Besser J , Concepción-Acevedo J , Folster JP , Huffman J , Joseph LA , Kucerova Z , Nichols MC , Schwensohn CA , Tolar B . Front Public Health 2019 7 365 In the original article, there was a mistake in Figure 1 and Figure 2 as published. The graphics used are different than those originally submitted. |
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. |
Genome Sequences of 18 Salmonella enterica Serotype Hadar Strains Collected from Patients in the United States.
Webb HE , Kim JY , Tagg KA , de la Cruz F , Peñil-Celis A , Tolar B , Ellison Z , Schwensohn C , Brandenburg J , Nichols M , Folster JP . Microbiol Resour Announc 2022 11 (10) e0052222 Despite being linked to a number of recent poultry-associated outbreaks in the United States, few reference genomes are available for Salmonella enterica serotype Hadar. Here, we address this need by reporting 18 Salmonella Hadar genomes from samples collected from patients in the United States between 2014 and 2020. |
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. |
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 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. |
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. |
Ability of whole-genome sequencing to refine a salmonella i 4,[5],12:I:-cluster in New York state and detect a multistate outbreak linked to raw poultry
Huth P , Wirth SE , Baker D , Nicholas DC , Douris A , Freiman J , Kline KE , Devinney K , Glsker S , Schwensohn C . Food Prot Trends 2021 41 (2) 239-245 Whole-genome sequencing (WGS) has proven to be a more powerful tool than pulsed-field gel electrophoresis for foodborne illness cluster definition because of improved resolution. Between November 2017 and May 2018, the New York State (NYS) Dept. of Health investigated 10 cases of Salmonella I 4,[5],12:i:-with pulsed-field gel electrophoresis pattern JPXX01.0621; comparison of case exposures did not identify a common source of infection. In June 2018, the NYS Dept. of Healths Wadsworth Center analyzed the isolates using WGS and defined a subcluster of five isolates related within zero to six single-nucleotide polymorphisms. The National Center for Biotechnology Information Pathogen Detection browser advanced this investigation by identifying additional clinical and food (chicken) isolates related within zero to eight single-nucleotide polymorphisms to the original subcluster. Comparison of WGS-related isolates would support the hypothesis that illness was associated with exposure to a kosher poultry product. This outbreak ultimately consisted of 25 cases from six states. Of 20 cases interviewed, all reported chicken consumption, and of those able to recall brand information, 83% cited a brand produced at a facility linked to the WGS-related chicken isolates. This paper demonstrates how WGS was able to refine a Salmonella I 4,[5],12:i:-cluster in NYS to uncover a multistate outbreak linked to raw poultry. 2021, International Association for Food Protection 2900 100th Street, Suite 309, Des Moines, IA 50322-3855. |
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. |
Outbreak of Salmonella Newport Infections with Decreased Susceptibility to Azithromycin Linked to Beef Obtained in the United States and Soft Cheese Obtained in Mexico - United States, 2018-2019.
Plumb ID , Schwensohn CA , Gieraltowski L , Tecle S , Schneider ZD , Freiman J , Cote A , Noveroske D , Kolsin J , Brandenburg J , Chen JC , Tagg KA , White PB , Shah HJ , Francois Watkins LK , Wise ME , Friedman CR . MMWR Morb Mortal Wkly Rep 2019 68 (33) 713-717 In September 2018, CDC identified Salmonella enterica serotype Newport (Newport) infections that were multidrug resistant (MDR), with decreased susceptibility to azithromycin, a recommended oral treatment agent. Until 2017, decreased susceptibility to azithromycin had occurred in fewer than 0.5% of Salmonella isolates from U.S. residents. This report summarizes the investigation of a multistate MDR Salmonella outbreak conducted by CDC, state and local health departments, and the U.S. Department of Agriculture's Food Safety and Inspection Service. During June 2018-March 2019, 255 cases of infection with the outbreak strain were identified in 32 states; 43% of patients (89 of 206 with information on travel) reported recent travel to Mexico. Infections were linked to consumption of soft cheese obtained in Mexico and beef obtained in the United States. Consumers should avoid eating soft cheese that could be made from unpasteurized milk, regardless of the source of the cheese. When preparing beef, a food thermometer should be used to ensure that appropriate cooking temperatures are reached. When antibiotic treatment is needed for a patient, clinicians should choose antibiotics based on susceptibility testing wherever possible. |
Whole Genome Sequencing: Bridging One-Health Surveillance of Foodborne Diseases.
Gerner-Smidt P , Besser J , Concepcion-Acevedo J , Folster JP , Huffman J , Joseph LA , Kucerova Z , Nichols MC , Schwensohn CA , Tolar B . Front Public Health 2019 7 172 Infections caused by pathogens commonly acquired from consumption of food are not always transmitted by that route. They may also be transmitted through contact to animals, other humans or the environment. Additionally, many outbreaks are associated with food contaminated from these non-food sources. For this reason, such presumed foodborne outbreaks are best investigated through a One Health approach working across human, animal and environmental sectors and disciplines. Outbreak strains or clones that have propagated and continue to evolve in non-human sources and environments often show more sequence variation than observed in typical monoclonal point-source outbreaks. This represents a challenge when using whole genome sequencing (WGS), the new gold standard for molecular surveillance of foodborne pathogens, for outbreak detection and investigation. In this review, using recent examples from outbreaks investigated in the United States (US) some aspects of One Health approaches that have been used successfully to solve such outbreaks are presented. These include using different combinations of flexible WGS based case definition, efficient epidemiological follow-up, traceback, surveillance, and testing of potential food and environmental sources and animal hosts. |
Intensified sampling in response to a Salmonella Heidelberg outbreak associated with multiple establishments within a single poultry corporation
Green A , Defibaugh-Chavez S , Douris A , Vetter D , Atkinson R , Kissler B , Khroustalev A , Robertson K , Sharma Y , Becker K , Dessai U , Antoine N , Allen L , Holt K , Gieraltowski L , Wise M , Schwensohn C . Foodborne Pathog Dis 2018 15 (3) 153-160 On June 28, 2013, the Food Safety and Inspection Service (FSIS) was notified by the Centers for Disease Control and Prevention (CDC) of an investigation of a multistate cluster of illnesses of Salmonella enterica serovar Heidelberg. Since case-patients in the cluster reported consumption of a variety of chicken products, FSIS used a simple likelihood-based approach using traceback information to focus on intensified sampling efforts. This article describes the multiphased product sampling approach taken by FSIS when epidemiologic evidence implicated chicken products from multiple establishments operating under one corporation. The objectives of sampling were to (1) assess process control of chicken slaughter and further processing and (2) determine whether outbreak strains were present in products from these implicated establishments. As part of the sample collection process, data collected by FSIS personnel to characterize product included category (whole chicken and type of chicken parts), brand, organic or conventional product, injection with salt solutions or flavorings, and whether product was skinless or skin-on. From the period September 9, 2013, through October 31, 2014, 3164 samples were taken as part of this effort. Salmonella percent positive declined from 19.7% to 5.3% during this timeframe as a result of regulatory and company efforts. The results of intensified sampling for this outbreak investigation informed an FSIS regulatory response and corrective actions taken by the implicated establishments. The company noted that a multihurdle approach to reduce Salmonella in products was taken, including on-farm efforts such as environmental testing, depopulation of affected flocks, disinfection of affected houses, vaccination, and use of various interventions within the establishments over the course of several months. |
Multistate Outbreak of Salmonella Virchow Infections Linked to a Powdered Meal Replacement Product - United States, 2015-2016.
Gambino-Shirley KJ , Tesfai A , Schwensohn CA , Burnett C , Smith L , Wagner JM , Eikmeier D , Smith K , Stone JP , Updike D , Hines J , Shade LN , Tolar B , Fu TJ , Viazis S , Seelman SL , Blackshear K , Wise ME , Neil KP . Clin Infect Dis 2018 67 (6) 890-896 Background: Nontyphoidal Salmonella is the leading cause of bacterial gastroenteritis in the United States. Meal replacement products containing raw and 'superfood' ingredients have gained increasing popularity among consumers in recent years. In January 2016, we investigated a multistate outbreak of infections with a novel strain of Salmonella Virchow. Methods: Cases were defined using molecular subtyping procedures. Commonly reported exposures were compared with responses from healthy people interviewed in the 2006-2007 FoodNet Population Survey. Firm inspections and product traceback and testing were performed. Results: Thirty-five cases from 24 states were identified; 6 hospitalizations and no deaths were reported. Thirty-one (94%) of 33 ill people interviewed reported consuming a powdered supplement in the week before illness; of these, 30 (97%) reported consuming Product A, a raw organic powdered shake product consumed as a meal replacement. Laboratory testing isolated the outbreak strain of Salmonella Virchow from: leftover Product A collected from ill people's homes, organic moringa leaf powder (an ingredient in Product A), and finished product retained by the firm. Firm inspections at three facilities linked to Product A production did not reveal contamination at the facilities. Traceback identified that the contaminated moringa leaf powder was imported from South Africa. Conclusions: This investigation identified a novel outbreak vehicle and highlighted the potential risk with similar products not intended to be cooked by consumers before consuming. The company issued a voluntary recall of all implicated products. As this product has a long shelf-life, the recall likely prevented additional illnesses. |
Notes from the field: Multistate outbreak of Escherichia coli O157:H7 infections linked to dough mix - United States, 2016
Gieraltowski L , Schwensohn C , Meyer S , Eikmeier D , Medus C , Sorenson A , Forstner M , Madad A , Blankenship J , Feng P , Williams I . MMWR Morb Mortal Wkly Rep 2017 66 (3) 88-89 On January 4, 2016, CDC PulseNet, the molecular subtyping network for foodborne disease surveillance, identified a cluster of 10 Shiga toxin-producing Escherichia coli (STEC) O157:H7 infections with indistinguishable pulsed-field gel electrophoresis (PFGE) pattern combinations. STEC infections with the identified outbreak PFGE pattern are commonly reported to PulseNet, with an average of 40–50 illnesses reported annually. Because this was a relatively common strain of STEC, multiple locus variable-number tandem repeat analysis (MLVA), another subtyping technique used to characterize the genetic relatedness of bacteria, was used to help define cases in the cluster. CDC collaborated with state and local health and agricultural agencies and the Food and Drug Administration (FDA) to investigate the outbreak. A case was defined as STEC O157:H7 infection with an isolate having PFGE and MLVA patterns indistinguishable from the outbreak strain in a person with diarrheal illness onset during December 6, 2015–February 9, 2016. | Thirteen STEC O157:H7 outbreak-associated cases were identified in nine states: Iowa (one case), Illinois (one), Kansas (one), Minnesota (five), North Carolina (one), Nebraska (one), New Jersey (one), South Dakota (one), and Wisconsin (one). The median age of patients was 17 years (range = 7–71 years); 53% were female. Among 12 patients with available information, eight were hospitalized, including two who developed hemolytic uremic syndrome; no deaths were reported. |
National outbreak of multidrug resistant Salmonella Heidelberg infections linked to a single poultry company
Gieraltowski L , Higa J , Peralta V , Green A , Schwensohn C , Rosen H , Libby T , Kissler B , Marsden-Haug N , Booth H , Kimura A , Grass J , Bicknese A , Tolar B , Defibaugh-Chavez S , Williams I , Wise M . PLoS One 2016 11 (9) e0162369 IMPORTANCE: This large outbreak of foodborne salmonellosis demonstrated the complexity of investigating outbreaks linked to poultry products. The outbreak also highlighted the importance of efforts to strengthen food safety policies related to Salmonella in chicken parts and has implications for future changes within the poultry industry. OBJECTIVE: To investigate a large multistate outbreak of multidrug resistant Salmonella Heidelberg infections. DESIGN: Epidemiologic and laboratory investigations of patients infected with the outbreak strains of Salmonella Heidelberg and traceback of possible food exposures. SETTING: United States. Outbreak period was March 1, 2013 through July 11, 2014. PATIENTS: A case was defined as illness in a person infected with a laboratory-confirmed Salmonella Heidelberg with 1 of 7 outbreak pulsed-field gel electrophoresis (PFGE) XbaI patterns with illness onset from March 1, 2013 through July 11, 2014. A total of 634 case-patients were identified through passive surveillance; 200/528 (38%) were hospitalized, none died. RESULTS: Interviews were conducted with 435 case-patients: 371 (85%) reported eating any chicken in the 7 days before becoming ill. Of 273 case-patients interviewed with a focused questionnaire, 201 (74%) reported eating chicken prepared at home. Among case-patients with available brand information, 152 (87%) of 175 patients reported consuming Company A brand chicken. Antimicrobial susceptibility testing was completed on 69 clinical isolates collected from case-patients; 67% were drug resistant, including 24 isolates (35%) that were multidrug resistant. The source of Company A brand chicken consumed by case-patients was traced back to 3 California production establishments from which 6 of 7 outbreak strains were isolated. CONCLUSIONS: Epidemiologic, laboratory, traceback, and environmental investigations conducted by local, state, and federal public health and regulatory officials indicated that consumption of Company A chicken was the cause of this outbreak. The outbreak involved multiple PFGE patterns, a variety of chicken products, and 3 production establishments, suggesting a reservoir for contamination upstream from the production establishments. Sources of bacteria and genes responsible for resistance, such as farms providing birds for slaughter or environmental reservoir on farms that raise chickens, might explain how multiple PFGE patterns were linked to chicken from 3 separate production establishments and many different poultry products. |
Outbreak of Salmonella enterica serotype Infantis infection in humans linked to dry dog food in the United States and Canada, 2012
Imanishi M , Rotstein DS , Reimschuessel R , Schwensohn CA , Woody DH Jr , Davis SW , Hunt AD , Arends KD , Achen M , Cui J , Zhang Y , Denny LF , Phan QN , Joseph LA , Tuite CC , Tataryn JR , Behravesh CB . J Am Vet Med Assoc 2014 244 (5) 545-53 CASE DESCRIPTION: In April 2012, Salmonella enterica serotype Infantis was detected in an unopened bag of dry dog food collected during routine retail surveillance. PulseNet, a national bacterial subtyping network, identified humans with Salmonella Infantis infection with the same genetic fingerprint as the dog food sample. CLINICAL FINDINGS: An outbreak investigation identified 53 ill humans infected with the outbreak strain during January 1 to July 5, 2012, in 21 states and 2 provinces in Canada; 20 (38%) were children ≤ 2 years old, and 12 of 37 (32%) were hospitalized. Of 21 ill people who remembered the dog food brand, 12 (57%) reported a brand produced at a plant in Gaston, SC. Traceback investigations also identified that plant. The outbreak strain was isolated from bags of dry dog food and fecal specimens obtained from dogs that lived with ill people and that ate the implicated dry dog food. TREATMENT AND OUTCOME: The plant was closed temporarily for cleaning and disinfection. Sixteen brands involving > 27,000 metric tons (> 30,000 tons) of dry dog and cat food were recalled. Thirty-one ill dogs linked to recalled products were reported through the FDA consumer complaint system. CLINICAL RELEVANCE: A one-health collaborative effort on epidemiological, laboratory, and traceback investigations linked dry dog foods produced at a plant to illnesses in dogs and humans. More efforts are needed to increase awareness among pet owners, health-care professionals, and the pet food industry on the risk of illness in pets and their owners associated with dry pet foods and treats. |
Outbreak of Shiga toxin-producing Escherichia coli (STEC) O157:H7 associated with romaine lettuce consumption, 2011
Slayton RB , Turabelidze G , Bennett SD , Schwensohn CA , Yaffee AQ , Khan F , Butler C , Trees E , Ayers TL , Davis ML , Laufer AS , Gladbach S , Williams I , Gieraltowski LB . PLoS One 2013 8 (2) e55300 BACKGROUND: Shiga toxin-producing Escherichia coli (STEC) O157:H7 is the causal agent for more than 96,000 cases of diarrheal illness and 3,200 infection-attributable hospitalizations annually in the United States. MATERIALS AND METHODS: We defined a confirmed case as a compatible illness in a person with the outbreak strain during 10/07/2011-11/30/2011. Investigation included hypothesis generation, a case-control study utilizing geographically-matched controls, and a case series investigation. Environmental inspections and tracebacks were conducted. RESULTS: We identified 58 cases in 10 states; 67% were hospitalized and 6.4% developed hemolytic uremic syndrome. Any romaine consumption was significantly associated with illness (matched Odds Ratio (mOR) = 10.0, 95% Confidence Interval (CI) = 2.1-97.0). Grocery Store Chain A salad bar was significantly associated with illness (mOR = 18.9, 95% CI = 4.5-176.8). Two separate traceback investigations for romaine lettuce converged on Farm A. Case series results indicate that cases (64.9%) were more likely than the FoodNet population (47%) to eat romaine lettuce (p-value = 0.013); 61.3% of cases reported consuming romaine lettuce from the Grocery Store Chain A salad bar. CONCLUSIONS: This multistate outbreak of STEC O157:H7 infections was associated with consumption of romaine lettuce. Traceback analysis determined that a single common lot of romaine lettuce harvested from Farm A was used to supply Grocery Store Chain A and a university campus linked to a case with the outbreak strain. An investigation at Farm A did not identify the source of contamination. Improved ability to trace produce from the growing fields to the point of consumption will allow more timely prevention and control measures to be implemented. |
Outbreak of human Salmonella Typhimurium infections linked to contact with baby poultry from a single agricultural feed store chain and mail-order hatchery, 2009
Loharikar A , Vawter S , Warren K , Deasy M 3rd , Moll M , Sandt C , Gilhousen R , Villamil E , Rhorer A , Briere E , Schwensohn C , Trees E , Lafon P , Adams JK , Le B , Behravesh CB . Pediatr Infect Dis J 2012 32 (1) 8-12 BACKGROUND: Over thirty outbreaks of human salmonellosis linked to contact with live poultry from mail-order hatcheries were reported to CDC between 1990-2010. In May 2009, we investigated an outbreak of human Salmonella Typhimurium infections, primarily affecting children. METHODS: A case was defined as a person with the outbreak strain of Salmonella Typhimurium, as determined by pulsed-field gel electrophoresis (PFGE) and multiple-locus variable-number tandem repeat analysis (MLVA), in a Pennsylvania or New York resident with illness onset between May 1- September 1, 2009. We conducted a case-control study to examine the relationship between illness and live poultry contact. Controls were age- and geographically-matched. Traceback and environmental investigations were conducted. RESULTS: We identified 36 case-patients in Pennsylvania and New York; 36% were children aged ≤5 years. Case-patients were more likely than controls to report live baby poultry contact (matched odds ratio [mOR]: 17.0; 95% Confidence Interval [CI]:2.7-710.5), contact with chicks (mOR:14.0; 95% CI:2.1-592.0), ducklings (mOR:8.0; 95% CI:1.1-355.0), and visiting agricultural feed stores (mOR:6.0; 95% CI:1.3-55.2). Most (83%) visited agricultural Feed Store Chain Y, a national agricultural feed store chain, which received poultry from Hatchery C, which is supplied by multiple egg sources. Salmonella Typhimurium was isolated from a source duck flock, but had a different PFGE pattern than the outbreak strain. CONCLUSION: Live baby poultry remain an important source of human salmonellosis, particularly among children. Preventing these infections requires comprehensive interventions at hatcheries and agricultural feed stores; pediatricians should inform patients of risks associated with live poultry contact. |
Four multistate outbreaks of human Salmonella infections associated with live poultry contact, United States, 2009
Loharikar A , Briere E , Schwensohn C , Weninger S , Wagendorf J , Scheftel J , Garvey A , Warren K , Villamil E , Rudroff JA , Kurkjian K , Levine S , Colby K , Morrison B , May A , Anderson S , Daly E , Marsden-Haug N , Erdman MM , Gomez T , Rhorer A , Castleman J , Adams JK , Theobald L , Lafon P , Trees E , Mitchell J , Sotir MJ , Behravesh CB . Zoonoses Public Health 2012 59 (5) 347-54 Outbreaks of human salmonellosis associated with live poultry contact have been reported since 1955. Multiple Salmonella serotypes have been associated with these outbreaks, and specific outbreak strains have been repeatedly linked to single hatcheries over multiple years. During 2009, four multistate outbreaks of human Salmonella infections associated with direct and indirect exposure to live poultry purchased from mail-order hatcheries and agricultural feed stores were identified, resulting in 165 culture-confirmed cases in 30 states. This report describes the epidemiologic, environmental and laboratory investigations conducted by state and local health departments, state departments of agriculture, the U.S. Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS), National Poultry Improvement Plan (NPIP) and National Veterinary Services Laboratories (NVSL), and the Centers for Disease Control and Prevention (CDC). Case-patients were identified through PulseNet, the national molecular subtyping network for foodborne disease surveillance, and interviewed using the CDC standard live poultry contact questionnaire that asks about poultry-related exposures during the 7 days before illness onset. These outbreaks highlight the need to focus efforts on strategies to decrease and prevent human illness associated with live poultry contact through comprehensive interventions at the mail-order hatchery, agricultural feed store and consumer levels. Additional consumer education and interventions at mail-order hatcheries and venues where live poultry are sold, including agricultural feed stores, are necessary to prevent transmission of Salmonella from poultry to humans. |
Salmonella typhimurium infections associated with peanut products
Cavallaro E , Date K , Medus C , Meyer S , Miller B , Kim C , Nowicki S , Cosgrove S , Sweat D , Phan Q , Flint J , Daly ER , Adams J , Hyytia-Trees E , Gerner-Smidt P , Hoekstra RM , Schwensohn C , Langer A , Sodha SV , Rogers MC , Angulo FJ , Tauxe RV , Williams IT , Behravesh CB . N Engl J Med 2011 365 (7) 601-10 BACKGROUND: Contaminated food ingredients can affect multiple products, each distributed through various channels and consumed in multiple settings. Beginning in November 2008, we investigated a nationwide outbreak of salmonella infections. METHODS: A case was defined as laboratory-confirmed infection with the outbreak strain of Salmonella Typhimurium occurring between September 1, 2008, and April 20, 2009. We conducted two case-control studies, product "trace-back," and environmental investigations. RESULTS: Among 714 case patients identified in 46 states, 166 (23%) were hospitalized and 9 (1%) died. In study 1, illness was associated with eating any peanut butter (matched odds ratio, 2.5; 95% confidence interval [CI], 1.3 to 5.3), peanut butter-containing products (matched odds ratio, 2.2; 95% CI, 1.1 to 4.7), and frozen chicken products (matched odds ratio, 4.6; 95% CI, 1.7 to 14.7). Investigations of focal clusters and single cases associated with nine institutions identified a single institutional brand of peanut butter (here called brand X) distributed to all facilities. In study 2, illness was associated with eating peanut butter outside the home (matched odds ratio, 3.9; 95% CI, 1.6 to 10.0) and two brands of peanut butter crackers (brand A: matched odds ratio, 17.2; 95% CI, 6.9 to 51.5; brand B: matched odds ratio, 3.6; 95% CI, 1.3 to 9.8). Both cracker brands were made from brand X peanut paste. The outbreak strain was isolated from brand X peanut butter, brand A crackers, and 15 other products. A total of 3918 peanut butter-containing products were recalled between January 10 and April 29, 2009. CONCLUSIONS: Contaminated peanut butter and peanut products caused a nationwide salmonellosis outbreak. Ingredient-driven outbreaks are challenging to detect and may lead to widespread contamination of numerous food products. |
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