Last data update: Sep 30, 2024. (Total: 47785 publications since 2009)
Records 1-30 (of 32 Records) |
Query Trace: Tolar B[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. |
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 outbreaks of salmonellosis linked to contact with backyard poultry-United States, 2015-2022
Stapleton GS , Habrun C , Nemechek K , Gollarza L , Ellison Z , Tolar B , Koski L , Brandenburg JM , Salah Z , Palacios A , Basler C , Varela K , Nichols M , Benedict K . Zoonoses Public Health 2024 AIMS: Contact with backyard poultry (i.e., privately-owned, non-commercial poultry) was first associated with a multistate outbreak of salmonellosis in 1955. In recent years, backyard poultry-associated salmonellosis outbreaks have caused more illnesses in the United States than salmonellosis outbreaks linked to any other type of animal. Here, we describe the epidemiology of outbreaks from 2015-2022 to inform prevention efforts. METHODS AND RESULTS: During 2015-2022, there were 88 multistate backyard poultry-associated salmonellosis outbreaks and 7866 outbreak-associated illnesses caused by 21 different Salmonella serotypes. Salmonella Enteritidis accounted for the most outbreaks (n = 21) and illnesses (n = 2400) of any serotype. Twenty-four percent (1840/7727) of patients with available information were <5 years of age. In total, 30% (1710/5644) of patients were hospitalized, and nine deaths were attributed to Salmonella infection. Throughout this period, patients reported behaviours that have a higher risk of Salmonella transmission, including kissing or snuggling poultry or allowing poultry inside their home. CONCLUSIONS: Despite ongoing efforts to reduce the burden of salmonellosis associated with backyard poultry, outbreak-associated illnesses have nearly tripled and hospitalizations more than quadrupled compared with those in 1990-2014. Because this public health problem is largely preventable, government officials, human and veterinary healthcare providers, hatcheries, and retailers might improve the prevention of illnesses by widely disseminating health and safety recommendations to the public and by continuing to develop and implement prevention measures to reduce zoonotic transmission of Salmonella by backyard poultry. |
Salmonella Vitkin outbreak associated with bearded dragons, Canada and United States, 2020-2022
Paphitis K , Habrun CA , Stapleton GS , Reid A , Lee C , Majury A , Murphy A , McClinchey H , Corbeil A , Kearney A , Benedict K , Tolar B , Forrest RO . Emerg Infect Dis 2024 30 (2) 225-233 We identified 2 cases of Salmonella enterica serovar Vitkin infection linked by whole-genome sequencing in infants in Ontario, Canada, during 2022. Both households of the infants reported having bearded dragons as pets. The outbreak strain was also isolated from an environmental sample collected from a patient's bearded dragon enclosure. Twelve cases were detected in the United States, and onset dates occurred during March 2021-September 2022 (isolates related to isolates from Canada within 0-9 allele differences by core-genome multilocus sequence typing). Most US patients (66.7%) were <1 year of age, and most (72.7%) had reported bearded dragon exposure. Hospitalization was reported for 5 (38.5%) of 13 patients. Traceback of bearded dragons identified at least 1 potential common supplier in Southeast Asia. Sharing rare serovar information and whole-genome sequencing data between Canada and the United States can assist in timely identification of outbreaks, including those that might not be detected through routine surveillance. |
Multistate nontyphoidal Salmonella and Shiga toxin-producing Escherichia coli outbreaks linked to international travel - United States, 2017-2020
Habrun CA , Birhane MG , François Watkins LK , Benedict K , Bottichio L , Nemechek K , Tolar B , Schroeder MN , Chen JC , Caidi H , Robyn M , Nichols M . Epidemiol Infect 2024 1-33 Enteric bacterial infections are common among people who travel internationally. During 2017– | 23 2020, CDC investigated 41 multistate outbreaks of nontyphoidal Salmonella and Shiga toxin24 producing Escherichia coli (STEC) linked to international travel. Resistance to one or more | 25 antimicrobial agents was detected in at least 10% of isolates in 16 of 30 (53%) nontyphoidal | 26 Salmonella outbreaks and 8 of 11 (73%) STEC outbreaks evaluated by the National | 27 Antimicrobial Resistance Monitoring System. At least 10% of the isolates in 14 nontyphoidal | 28 Salmonella outbreaks conferred resistance to one or more of the clinically significant | 29 antimicrobials used in human medicine. This report describes the epidemiology and | 30 antimicrobial resistance patterns of these travel-associated multistate outbreaks. Investigating | 31 illnesses among returned travelers and collaboration with international partners could result in | 32 implementation of public health interventions to improve hygiene practices and food safety | 33 standards, and to prevent illness and spread of multidrug resistant organisms domestically and | 34 internationally |
Antimicrobial resistance in multistate outbreaks of nontyphoidal Salmonella infections linked to animal contact-United States, 2015-2018
Frey E , Stapleton GS , Nichols MC , Gollarza LM , Birhane M , Chen JC , McCullough A , Carleton HA , Trees E , Hise KB , Tolar B , Francois Watkins L . J Clin Microbiol 2023 e0098123 Animal contact is an established risk factor for nontyphoidal Salmonella infections and outbreaks. During 2015-2018, the U.S. Centers for Disease Control and Prevention (CDC) and other U.S. public health laboratories began implementing whole-genome sequencing (WGS) of Salmonella isolates. WGS was used to supplement the traditional methods of pulsed-field gel electrophoresis for isolate subtyping, outbreak detection, and antimicrobial susceptibility testing (AST) for the detection of resistance. We characterized the epidemiology and antimicrobial resistance (AMR) of multistate salmonellosis outbreaks linked to animal contact during this time period. An isolate was considered resistant if AST yielded a resistant (or intermediate, for ciprofloxacin) interpretation to any antimicrobial tested by the CDC or if WGS showed a resistance determinant in its genome for one of these agents. We identified 31 outbreaks linked to contact with poultry (n = 23), reptiles (n = 6), dairy calves (n = 1), and guinea pigs (n = 1). Of the 26 outbreaks with resistance data available, we identified antimicrobial resistance in at least one isolate from 20 outbreaks (77%). Of 1,309 isolates with resistance information, 247 (19%) were resistant to ≥1 antimicrobial, and 134 (10%) were multidrug-resistant to antimicrobials from ≥3 antimicrobial classes. The use of resistance data predicted from WGS increased the number of isolates with resistance information available fivefold compared with AST, and 28 of 43 total resistance patterns were identified exclusively by WGS; concordance was high (>99%) for resistance determined by AST and WGS. The use of predicted resistance from WGS enhanced the characterization of the resistance profiles of outbreaks linked to animal contact by providing resistance information for more isolates. |
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. |
Evaluation of whole and core genome multilocus sequence typing allele schemes for Salmonella enterica outbreak detection in a national surveillance network, PulseNet USA
Leeper MM , Tolar BM , Griswold T , Vidyaprakash E , Hise KB , Williams GM , Im SB , Chen JC , Pouseele H , Carleton HA . Front Microbiol 2023 14 1254777 Salmonella enterica is a leading cause of bacterial foodborne and zoonotic illnesses in the United States. For this study, we applied four different whole genome sequencing (WGS)-based subtyping methods: high quality single-nucleotide polymorphism (hqSNP) analysis, whole genome multilocus sequence typing using either all loci [wgMLST (all loci)] and only chromosome-associated loci [wgMLST (chrom)], and core genome multilocus sequence typing (cgMLST) to a dataset of isolate sequences from 9 well-characterized Salmonella outbreaks. For each outbreak, we evaluated the genomic and epidemiologic concordance between hqSNP and allele-based methods. We first compared pairwise genomic differences using all four methods. We observed discrepancies in allele difference ranges when using wgMLST (all loci), likely caused by inflated genetic variation due to loci found on plasmids and/or other mobile genetic elements in the accessory genome. Therefore, we excluded wgMLST (all loci) results from any further comparisons in the study. Then, we created linear regression models and phylogenetic tanglegrams using the remaining three methods. K-means analysis using the silhouette method was applied to compare the ability of the three methods to partition outbreak and sporadic isolate sequences. Our results showed that pairwise hqSNP differences had high concordance with cgMLST and wgMLST (chrom) allele differences. The slopes of the regressions for hqSNP vs. allele pairwise differences were 0.58 (cgMLST) and 0.74 [wgMLST (chrom)], and the slope of the regression was 0.77 for cgMLST vs. wgMLST (chrom) pairwise differences. Tanglegrams showed high clustering concordance between methods using two statistical measures, the Baker's gamma index (BGI) and cophenetic correlation coefficient (CCC), where 9/9 (100%) of outbreaks yielded BGI values ≥ 0.60 and CCCs were ≥ 0.97 across all nine outbreaks and all three methods. K-means analysis showed separation of outbreak and sporadic isolate groups with average silhouette widths ≥ 0.87 for outbreak groups and ≥ 0.16 for sporadic groups. This study demonstrates that Salmonella isolates clustered in concordance with epidemiologic data using three WGS-based subtyping methods and supports using cgMLST as the primary method for national surveillance of Salmonella outbreak clusters. |
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. |
Detecting national human enteric disease outbreaks linked to animal contact in the United States of America.
Nichols M , Stevenson L , Koski L , Basler C , Wise M , Whitlock L , Francois Watkins L , Friedman CR , Chen J , Tagg K , Joseph L , Caidi H , Patel K , Tolar B , Hise K , Classon A , Ceric O , Reimschuessel R , Williams IT . Rev Sci Tech 2020 39 (2) 471-480 Enteric pathogens, such as non-typhoidal Salmonella, Campylobacter and Escherichia coli, can reside in the intestinal tract of many animals, including livestock, companion animals, small mammals and reptiles. Often, these animals can appear healthy; nonetheless, humans can become infected after direct or indirect contact, resulting in a substantial illness burden. An estimated 14% of the 3.2 million illnesses that occur in the United States of America (USA) each year from such enteric pathogens are attributable to animal contact. Surveillance for enteric pathogens in the USA includes the compilation and interpretation of both laboratory and epidemiologic data. However, the authors feel that a collaborative, multisectoral and transdisciplinary - or One Health - approach is needed for data collection and analysis, at every level. In addition, they suggest that the future of enteric illness surveillance lies in the development of improved technologies for pathogen detection and characterisation, such as genomic sequencing and metagenomics. In particular, using whole-genome sequencing to compare genetic sequences of enteric pathogens from humans, food, animals and the environment, can help to predict antimicrobial resistance among these pathogens, determine their genetic relatedness and identify outbreaks linked to a common source. In this paper, the authors describe three recent, multi-state human enteric illness outbreaks linked to animal contact in the USA and discuss how integrated disease surveillance was essential to outbreak detection and response. Additional datasharing between public health and animal health laboratories and epidemiologists at the local, national, regional and international level may help to improve surveillance for emerging animal and human health threats and lead to new opportunities for prevention. |
Increased Multidrug-Resistant Salmonella enterica I Serotype 4,[5],12:i:- Infections Associated with Pork, United States, 2009-2018.
Plumb ID , Brown AC , Stokes EK , Chen JC , Carleton H , Tolar B , Sundararaman P , Saupe A , Payne DC , Shah HJ , Folster JP , Friedman CR . Emerg Infect Dis 2023 29 (2) 314-22 Reports of Salmonella enterica I serotype 4,[5],12:i:- infections resistant to ampicillin, streptomycin, sulphamethoxazole, and tetracycline (ASSuT) have been increasing. We analyzed data from 5 national surveillance systems to describe the epidemiology, resistance traits, and genetics of infections with this Salmonella strain in the United States. We found ASSuT-resistant Salmonella 4,[5],12:i:- increased from 1.1% of Salmonella infections during 2009-2013 to 2.6% during 2014-2018; the proportion of Salmonella 4,[5],12:i:- isolates without this resistance pattern declined from 3.1% to 2.4% during the same timeframe. Among isolates sequenced during 2015-2018, a total of 69% were in the same phylogenetic clade. Within that clade, 77% of isolates had genetic determinants of ASSuT resistance, and 16% had genetic determinants of decreased susceptibility to ciprofloxacin, ceftriaxone, or azithromycin. Among outbreaks related to the multidrug-resistant clade, 63% were associated with pork consumption or contact with swine. Preventing Salmonella 4,[5],12:i:- carriage in swine would likely avert human infections with this strain. |
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. |
Multistate reptile- and amphibian-associated salmonellosis outbreaks in humans, United States, 20092018
Waltenburg MA , Perez A , Salah Z , Karp BE , Whichard J , Tolar B , Gollarza L , Koski L , Blackstock A , Basler C , Nichols M . Zoonoses Public Health 2022 69 (8) 925-937 Non-typhoidal Salmonella cause an estimated 1.4 million human illnesses, 26,000 hospitalizations and 400 deaths annually in the United States. Approximately 11% of these infections are attributed to animal contact. Reptiles and amphibians are known sources of salmonellosis; young children (aged <5 years) are disproportionately affected by reptile- and amphibian-associated salmonellosis (RAAS) outbreaks. We describe multistate RAAS outbreaks to characterize illnesses and inform prevention efforts. RAAS outbreaks were defined as ≥2 culture-confirmed human Salmonella infections with similar pulsed-field gel electrophoresis patterns and epidemiologic, laboratory or traceback evidence linking them to a common reptile/amphibian exposure. Data sources included the Animal Contact Outbreak Surveillance System; CDC Outbreak Response and Prevention Branch's outbreak management database; PulseNet, the national molecular subtyping network for foodborne disease surveillance in the United States; and the National Antimicrobial Resistance Monitoring System. Twenty-six RAAS outbreaks were reported during 2009–2018, resulting in 1465 illnesses and 306 hospitalizations. The outbreaks were associated with turtles (19), lizards (5), snakes (1) and frogs (1). Sixteen (61.5%) outbreaks were linked to small turtles (<4 inches), resulting in 914 illnesses. Forty-nine percent of outbreak-associated patients were aged <5 years. Of 362 patients/caregivers interviewed, 111 (30.7%) were aware that reptiles/amphibians can carry Salmonella. Among 267 patient isolates with antimicrobial susceptibility information, 20 (7.5%) were non-susceptible to ≥1 antibiotic used to treat human salmonellosis. RAAS outbreaks result in considerable morbidity, particularly among young children. Illnesses linked to small turtles are preventable through education, targeted outreach to caregivers and paediatricians, and when appropriate, enforcement. Historically, individual states and jurisdictions have enforced existing or promulgated new authorities to address outbreaks. Preventing future RAAS outbreaks requires addressing challenges related to the illegal sale/distribution of small turtles; and for legal reptile sales, providing information on RAAS risk to consumers at point of sale to support informed pet ownership decisions. Published 2022. This article is a U.S. Government work and is in the public domain in the USA. Zoonoses and Public Health published by Wiley-VCH GmbH. |
Salmonella Illness Outbreaks linked to Backyard Poultry Purchasing during the COVID-19 Pandemic - United States, 2020.
Nichols M , Gollarza L , Palacios A , Stapleton GS , Basler C , Hoff C , Low M , McFadden K , Koski L , Leeper M , Brandenburg J , Tolar B . Epidemiol Infect 2021 149 1-10 Poultry contact is a risk factor for zoonotic transmission of non-typhoidal Salmonella spp. Salmonella illness outbreaks in the United States are identified by PulseNet, the national laboratory network for enteric disease surveillance. During 2020, PulseNet observed a 25% decline in the number of Salmonella clinical isolates uploaded by state and local health departments. However, 1722 outbreak-associated Salmonella illnesses resulting from 12 Salmonella serotypes were linked to contact with privately owned poultry, an increase from all previous years. This report highlights the need for continued efforts to prevent backyard poultry-associated outbreaks of Salmonella as ownership increases in the United States. |
Onsite investigation at a mail-order hatchery following a multistate Salmonella illness outbreak linked to live poultry-United States, 2018.
Robertson SA , Sidge JL , Koski L , Hardy MC , Stevenson L , Signs K , Stobierski MG , Bidol S , Donovan D , Soehnlen M , Jones K , Robeson S , Hambley A , Stefanovsky L , Brandenburg J , Hise K , Tolar B , Nichols MC , Basler C . Poult Sci 2019 98 (12) 6964-6972 Centers for Disease Control and Prevention (CDC), health departments, and other state and federal partners have linked contact with live poultry to 70 human Salmonella outbreaks in the United States from 2000 to 2017, which resulted in a total of 4,794 illnesses, 894 hospitalizations, and 7 deaths. During human salmonellosis outbreaks environmental sampling is rarely conducted as part of the outbreak investigation. CDC was contacted by state health officials on June 12, 2018, to provide support during an investigation of risk factors for Salmonella infections linked to live poultry originating at a mail-order hatchery. From January 1, 2018, to June 15, 2018, 13 human Salmonella infections in multiple states were attributed to exposure to live poultry from a single hatchery. Two serotypes of Salmonella were associated with these infections, Salmonella Enteritidis and Salmonella Litchfield. Molecular subtyping of the S. Enteritidis clinical isolates revealed they were closely related genetically (within 0 to 9 alleles) by core genome multi-locus sequence typing (cgMLST) to isolates obtained from environmental samples taken from hatchery shipping containers received at retail outlets. Environmental sampling and onsite investigation of practices was conducted at the mail-order hatchery during an investigation on June 19, 2018. A total of 45 environmental samples were collected, and 4 (9%) grew Salmonella. A chick box liner from a box in the pre-shipping area yielded an isolate closely related to the S. Enteritidis outbreak strain (within 1 to 9 alleles by cgMLST). The onsite investigation revealed lapses in biosecurity, sanitation, quality assurance, and education of consumers. Review of Salmonella serotype testing performed by the hatchery revealed that the number of samples and type of samples collected monthly varied. Also, S. Enteritidis was identified at the hatchery every year since testing began in 2016. Recommendations to the hatchery for biosecurity, testing, and sanitation measures were made to help reduce burden of Salmonella in the hatchery and breeding flocks, thereby reducing the occurrence of human illness. |
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. |
An Overview of PulseNet USA Databases.
Tolar B , Joseph LA , Schroeder MN , Stroika S , Ribot EM , Hise KB , Gerner-Smidt P . Foodborne Pathog Dis 2019 16 (7) 457-462 PulseNet USA is the molecular surveillance network for foodborne disease in the United States. The network consists of state and local public health laboratories, as well as food regulatory agencies, that follow PulseNet's standardized protocols to perform pulsed-field gel electrophoresis (PFGE) and whole genome sequencing (WGS) and analyze the results using standardized software. The raw sequences are uploaded to the GenomeTrakr or PulseNet bioprojects at the National Center for Biotechnology Information. The PFGE patterns and analyzed sequence data are uploaded in real time with associated demographic data to the PulseNet national databases managed at the Centers for Disease Control and Prevention. The PulseNet databases are organism specific and provide a central storage location for molecular and demographic data related to an isolate. Sequences are compared in the databases, thereby facilitating the rapid detection of clusters of foodborne diseases that may represent widespread outbreaks. WGS genotyping data, for example, antibiotic resistance and virulence profiles, are also uploaded in real time to the PulseNet databases to improve food safety surveillance activities. |
Notes from the Field: Recurrence of a multistate outbreak of Salmonella enteritidis infections linked to contact with guinea pigs - eight states, 2015-2017
Robertson S , Burakoff A , Stevenson L , Tompkins B , Patel K , Tolar B , Whitlock L , House J , Schlater L , Mackie T , Morningstar-Shaw B , Nichols M , Basler C . MMWR Morb Mortal Wkly Rep 2018 67 (42) 1195-1196 In December 2017, the Colorado Department of Public Health and Environment reported two human Salmonella Enteritidis infections in persons with exposure to pet guinea pigs. The guinea pigs had been purchased from two separate pet stores, belonging to a single chain, and supplied by a common distributor located in California. Clinical isolates were indistinguishable by pulsed-field gel electrophoresis (PFGE), suggesting the infections were related. This PFGE pattern was previously seen in a 2010 multistate outbreak linked to contact with pet guinea pigs (1). An investigation was initiated to determine the number of patients affected and to identify the source of human illnesses. |
Multistate outbreak of Salmonella Paratyphi B variant L(+) tartrate(+) and Salmonella Weltevreden infections linked to imported frozen raw tuna: USA, March-July 2015.
Hassan R , Tecle S , Adcock B , Kellis M , Weiss J , Saupe A , Sorenson A , Klos R , Blankenship J , Blessington T , Whitlock L , Carleton HA , Concepcion-Acevedo J , Tolar B , Wise M , Neil KP . Epidemiol Infect 2018 146 (11) 1-7 Foodborne non-typhoidal salmonellosis causes approximately 1 million illnesses annually in the USA. In April 2015, we investigated a multistate outbreak of 65 Salmonella Paratyphi B variant L(+) tartrate(+) infections associated with frozen raw tuna imported from Indonesia, which was consumed raw in sushi. Forty-six (92%) of 50 case-patients interviewed ate sushi during the week before illness onset, and 44 (98%) of 45 who specified ate sushi containing raw tuna. Two outbreak strains were isolated from the samples of frozen raw tuna. Traceback identified a single importer as a common source of tuna consumed by case-patients; this importer issued three voluntary recalls of tuna sourced from one Indonesian processor. Four Salmonella Weltevreden infections were also linked to this outbreak. Whole-genome sequencing was useful in establishing a link between Salmonella isolated from ill people and tuna. This outbreak highlights the continuing foodborne illness risk associated with raw seafood consumption, the importance of processing seafood in a manner that minimises contamination with pathogenic microorganisms and the continuing need to ensure imported foods are safe to eat. People at higher risk for foodborne illness should not consume undercooked animal products, such as raw seafood. |
Notes from the Field: Salmonella Oranienburg Infection Linked to Consumption of Rattlesnake Pills - Kansas and Texas, 2017.
Bottichio L , Webb LM , Leos G , Tolar B , Dowell N , Basler C . MMWR Morb Mortal Wkly Rep 2018 67 (17) 502-503 In November 2017, as part of a salmonellosis illness investigation, the Texas Department of State Health Services collected a bottle of rattlesnake pills from a patient’s home. The Texas Department of State Health Services then contacted CDC to report that a sample of these rattlesnake pills yielded Salmonella Oranienburg. The Salmonella serotype isolated from the patient was not related by pulsed-field gel electrophoresis (PFGE) to that isolated from the rattlesnake pills. PulseNet, the national molecular subtyping network for foodborne disease surveillance, identified numerous isolates with a PFGE pattern indistinguishable from that of the rattlesnake pill isolate.* Whole genome sequencing (WGS) indicated that the Salmonella found in the sample of rattlesnake pills was closely related genetically to an isolate from a patient in Kansas.† This close genetic relationship makes it likely that the Kansas patient became ill from consumption of rattlesnake pills. Because the Salmonella serotype isolated from the patient was not related by PFGE to that isolated from the rattlesnake pills, the definitive cause of the Texas patient’s illness was not ascertained; this patient was unable to be reinterviewed, and no additional samples were able to be collected. |
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. |
Unusually high illness severity and short incubation periods in two foodborne outbreaks of Salmonella Heidelberg infections with potential coincident Staphylococcus aureus intoxication
Nakao JH , Talkington D , Bopp CA , Besser J , Sanchez ML , Guarisco J , Davidson SL , Warner C , Mc Intyre Mg , Group JP , Comstock N , Xavier K , Pinsent TS , Brown J , Douglas JM , Gomez GA , Garrett NM , Carleton HA , Tolar B , Wise ME . Epidemiol Infect 2017 146 (1) 1-9 We describe the investigation of two temporally coincident illness clusters involving salmonella and Staphylococcus aureus in two states. Cases were defined as gastrointestinal illness following two meal events. Investigators interviewed ill persons. Stool, food and environmental samples underwent pathogen testing. Alabama: Eighty cases were identified. Median time from meal to illness was 5.8 h. Salmonella Heidelberg was identified from 27 of 28 stool specimens tested, and coagulase-positive S. aureus was isolated from three of 16 ill persons. Environmental investigation indicated that food handling deficiencies occurred. Colorado: Seven cases were identified. Median time from meal to illness was 4.5 h. Five persons were hospitalised, four of whom were admitted to the intensive care unit. Salmonella Heidelberg was identified in six of seven stool specimens and coagulase-positive S. aureus in three of six tested. No single food item was implicated in either outbreak. These two outbreaks were linked to infection with Salmonella Heidelberg, but additional factors, such as dual aetiology that included S. aureus or the dose of salmonella ingested may have contributed to the short incubation periods and high illness severity. The outbreaks underscore the importance of measures to prevent foodborne illness through appropriate washing, handling, preparation and storage of food. |
Epidemiology of Salmonella enterica serotype Dublin infections among humans, United States, 1968-2013
Harvey RR , Friedman CR , Crim SM , Judd M , Barrett KA , Tolar B , Folster JP , Griffin PM , Brown AC . Emerg Infect Dis 2017 23 (9) 1493-501 Salmonella enterica serotype Dublin is a cattle-adapted bacterium that typically causes bloodstream infections in humans. To summarize demographic, clinical, and antimicrobial drug resistance characteristics of human infections with this organism in the United States, we analyzed data for 1968-2013 from 5 US surveillance systems. During this period, the incidence rate for infection with Salmonella Dublin increased more than that for infection with other Salmonella. Data from 1 system (FoodNet) showed that a higher percentage of persons with Salmonella Dublin infection were hospitalized and died during 2005-2013 (78% hospitalized, 4.2% died) than during 1996-2004 (68% hospitalized, 2.7% died). Susceptibility data showed that a higher percentage of isolates were resistant to >7 classes of antimicrobial drugs during 2005-2013 (50.8%) than during 1996-2004 (2.4%). |
Utility of Combining Whole Genome Sequencing with Traditional Investigational Methods To Solve Foodborne Outbreaks of Salmonella Infections Associated with Chicken: A New Tool for Tackling This Challenging Food Vehicle.
Crowe SJ , Green A , Hernandez K , Peralta V , Bottichio L , Defibaugh-Chavez S , Douris A , Gieraltowski L , Hise K , La-Pham K , Neil KP , Simmons M , Tillman G , Tolar B , Wagner D , Wasilenko J , Holt K , Trees E , Wise ME . J Food Prot 2017 80 (4) 654-660 High consumption rates and a multitude of brands make multistate foodborne outbreaks of Salmonella infections associated with chicken challenging to investigate, but whole genome sequencing is a powerful tool that can be used to assist investigators. Whole genome sequencing of pathogens isolated from clinical, environmental, and food samples is increasingly being used in multistate foodborne outbreak investigations to determine with unprecedented resolution how closely related these isolates are to one another genetically. In 2014, federal and state health officials investigated an outbreak of 146 Salmonella Heidelberg infections in 24 states. A follow-up analysis was conducted after the conclusion of the investigation in which 27 clinical and 24 food isolates from the outbreak underwent whole genome sequencing. These isolates formed seven clades, the largest of which contained clinical isolates from a subcluster of case patients who attended a catered party. One isolate from a chicken processed by a large producer was closely related genetically (zero to three single-nucleotide polymorphism differences) to the clinical isolates from these subcluster case patients. Chicken from this large producer was also present in the kitchen of the caterer on the day before the event, thus providing additional evidence that the chicken from this producer was the outbreak source. This investigation highlights how whole genome sequencing can be used with epidemiologic and traceback evidence to identify chicken sources of foodborne outbreaks. |
Outbreak of Salmonella Oslo Infections Linked to Persian Cucumbers - United States, 2016.
Bottichio L , Medus C , Sorenson A , Donovan D , Sharma R , Dowell N , Williams I , Wellman A , Jackson A , Tolar B , Griswold T , Basler C . MMWR Morb Mortal Wkly Rep 2016 65 (5051) 1430-1433 In April 2016, PulseNet, the national molecular subtyping network for foodborne disease surveillance, detected a multistate cluster of Salmonella enterica serotype Oslo infections with an indistinguishable pulsed-field gel electrophoresis (PFGE) pattern (XbaI PFGE pattern OSLX01.0090).* This PFGE pattern was new in the database; no previous infections or outbreaks have been identified. CDC, state and local health and agriculture departments and laboratories, and the Food and Drug Administration (FDA) conducted epidemiologic, traceback, and laboratory investigations to identify the source of this outbreak. A total of 14 patients in eight states were identified, with illness onsets occurring during March 21-April 9, 2016. Whole genome sequencing, a highly discriminating subtyping method, was used to further characterize PFGE pattern OSLX01.0090 isolates. Epidemiologic evidence indicates Persian cucumbers as the source of Salmonella Oslo infections in this outbreak. This is the fourth identified multistate outbreak of salmonellosis associated with cucumbers since 2013. Further research is needed to understand the mechanism and factors that contribute to contamination of cucumbers during growth, harvesting, and processing to prevent future outbreaks. |
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. |
Outbreaks of salmonellosis from small turtles
Walters MS , Simmons L , Anderson TC , DeMent J , Van Zile K , Matthias LP , Etheridge S , Baker R , Healan C , Bagby R , Reporter R , Kimura A , Harrison C , Ajileye K , Borders J , Crocker K , Smee A , Adams-Cameron M , Joseph LA , Tolar B , Trees E , Sabol A , Garrett N , Bopp C , Bosch S , Behravesh CB . Pediatrics 2015 137 (1) OBJECTIVE: Turtle-associated salmonellosis (TAS), especially in children, is a reemerging public health issue. In 1975, small pet turtles (shell length <4 inches) sales were banned by federal law; reductions in pediatric TAS followed. Since 2006, the number of multistate TAS outbreaks has increased. We describe 8 multistate outbreaks with illness-onset dates occurring in 2011-2013. METHODS: We conducted epidemiologic, environmental, and traceback investigations. Cases were defined as infection with ≥1 of 10 molecular subtypes of Salmonella Sandiego, Pomona, Poona, Typhimurium, and I 4,[5],12:i:-. Water samples from turtle habitats linked to human illnesses were cultured for Salmonella. RESULTS: We identified 8 outbreaks totaling 473 cases from 41 states, Washington DC, and Puerto Rico with illness onsets during May 2011-September 2013. The median patient age was 4 years (range: 1 month-94 years); 45% percent were Hispanic; and 28% were hospitalized. In the week preceding illness, 68% (187 of 273) of case-patients reported turtle exposure; among these, 88% (124 of 141) described small turtles. Outbreak strains were isolated from turtle habitats linked to human illnesses in seven outbreaks. Traceback investigations identified 2 Louisiana turtle farms as the source of small turtles linked to 1 outbreak; 1 outbreak strain was isolated from turtle pond water from 1 turtle farm. CONCLUSIONS: Eight multistate outbreaks associated with small turtles were investigated during 2011-2013. Children <5 years and Hispanics were disproportionately affected. Prevention efforts should focus on patient education targeting families with young children and Hispanics and enactment of state and local regulations to complement federal sales restrictions. |
Nationwide outbreak of multidrug-resistant Salmonella Heidelberg infections associated with ground turkey: United States, 2011
Routh JA , Pringle J , Mohr M , Bidol S , Arends K , Adams-Cameron M , Hancock WT , Kissler B , Rickert R , Folster J , Tolar B , Bosch S , Barton Behravesh C , Williams IT , Gieraltowski L . Epidemiol Infect 2015 143 (15) 1-8 On 23 May 2011, CDC identified a multistate cluster of Salmonella Heidelberg infections and two multidrug-resistant (MDR) isolates from ground turkey retail samples with indistinguishable pulsed-field gel electrophoresis patterns. We defined cases as isolation of outbreak strains in persons with illness onset between 27 February 2011 and 10 November 2011. Investigators collected hypothesis-generating questionnaires and shopper-card information. Food samples from homes and retail outlets were collected and cultured. We identified 136 cases of S. Heidelberg infection in 34 states. Shopper-card information, leftover ground turkey from a patient's home containing the outbreak strain and identical antimicrobial resistance profiles of clinical and retail samples pointed to plant A as the source. On 3 August, plant A recalled 36 million pounds of ground turkey. This outbreak increased consumer interest in MDR Salmonella infections acquired through United States-produced poultry and played a vital role in strengthening food safety policies related to Salmonella and raw ground poultry. |
Identification and characterization of multidrug-resistant Salmonella enterica serotype Albert isolates in the United States.
Folster JP , Campbell D , Grass J , Brown AC , Bicknese A , Tolar B , Joseph LA , Plumblee JR , Walker C , Fedorka-Cray PJ , Whichard JM . Antimicrob Agents Chemother 2015 59 (5) 2774-9 Salmonella enterica is one of the most common causes of bacterial foodborne illness in the United States. Although most Salmonella infections are self-limiting, antimicrobial treatment is critical for invasive salmonellosis. Primary antimicrobial treatment options include fluoroquinolones or extended-spectrum cephalosporins and antimicrobial resistance to these drugs may complicate treatment. At present, Salmonella enterica is composed of more than 2,600 unique serotypes, which vary greatly in geographic prevalence, ecological niche, and ability to cause human disease and it is important to understand and mitigate the source of human infection, particularly when antimicrobial resistance is found. In this study, we identified and characterized 19 Salmonella enterica serotype Albert isolates from food animals, retail meat, and humans collected in the United States during 2005-2013. All 5 isolates from non-human sources were obtained from turkeys or ground turkey and epidemiologic data suggest poultry consumption or live poultry exposure as the probable source of infection. Salmonella ser. Albert also appears to be geographically localized to the Midwestern states of the U.S. All 19 isolates displayed multidrug resistance (MDR), including decreased susceptibility to fluoroquinolones and resistance to extended-spectrum cephalosporins. Turkeys are a likely source of multidrug resistant Salmonella Albert, and circulation of resistance plasmids, as opposed to expansion of a single resistant strain, is playing a role. More work is needed to understand why these resistance plasmids spread and how their presence and the serotype they reside in contribute to human disease. |
Comparative analysis of subtyping methods against a whole-genome-sequencing standard for Salmonella enterica serotype Enteritidis.
Deng X , Shariat N , Driebe EM , Roe CC , Tolar B , Trees E , Keim P , Zhang W , Dudley EG , Fields PI , Engelthaler DM . J Clin Microbiol 2014 53 (1) 212-8 A retrospective investigation was performed to evaluate whole genome sequencing as a benchmark for comparing molecular subtyping methods for Salmonella enterica serotype Enteritidis (SE) and survey the population structure of commonly encountered SE outbreak isolates in the United States. A total of 52 SE isolates representing 16 major outbreaks and three sporadic cases between 2001 and 2012 were sequenced and subjected to subtyping by four different methods: 1) whole genome single nucleotide polymorphism typing (WGST), 2) multiple loci VNTR (variable-number tandem repeat) analysis (MLVA), 3) clustered regularly interspaced short palindromic repeats combined with multi-virulence-locus sequence typing (CRISPR-MVLST) and 4) pulsed-field gel electrophoresis (PFGE). WGST resolved all outbreak clusters and provided useful robust phylogenetic inference with high epidemiological correlation. While both MLVA and CRISPR-MVLST yielded higher discriminatory power than PFGE, MLVA outperformed in delineating outbreak clusters whereas CRISPR-MVLST showed the potential to trace major lineages and ecological origins of SE. Our results suggested that whole genome sequencing makes a viable platform for the evaluation and benchmarking molecular subtyping methods. |
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