Antimicrobial resistance in multistate outbreaks of nontyphoidal Salmonella infections linked to animal contact-United States, 2015-2018.

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.

Multistate nontyphoidal Salmonella and Shiga toxin-producing Escherichia coli outbreaks linked to international travel-United States, 2017-2020.

Enteric bacterial infections are common among people who travel internationally. During 2017-2020, the Centers for Disease Control and Prevention investigated 41 multistate outbreaks of nontyphoidal Salmonella and Shiga toxin-producing Escherichia coli linked to international travel. Resistance to one or more antimicrobial agents was detected in at least 10% of isolates in 16 of 30 (53%) nontyphoidal Salmonella outbreaks and 8 of 11 (73%) Shiga toxin-producing E. coli outbreaks evaluated by the National Antimicrobial Resistance Monitoring System. At least 10% of the isolates in 14 nontyphoidal Salmonella outbreaks conferred resistance to one or more of the clinically significant antimicrobials used in human medicine. This report describes the epidemiology and antimicrobial resistance patterns of these travel-associated multistate outbreaks. Investigating illnesses among returned travellers and collaboration with international partners could result in the implementation of public health interventions to improve hygiene practices and food safety standards and to prevent illness and spread of multidrug-resistant organisms domestically and internationally.

Salmonella Hadar linked to two distinct transmission vehicles highlights challenges to enteric disease outbreak investigations.

In 2020, an outbreak of Salmonella Hadar illnesses was linked to contact with non-commercial, privately owned (backyard) poultry including live chickens, turkeys, and ducks, resulting in 848 illnesses. From late 2020 to 2021, this Salmonella Hadar strain caused an outbreak that was linked to ground turkey consumption. Core genome multilocus sequence typing (cgMLST) analysis determined that the Salmonella Hadar isolates detected during the outbreak linked to backyard poultry and the outbreak linked to ground turkey were closely related genetically (within 0-16 alleles). Epidemiological and traceback investigations were unable to determine how Salmonella Hadar detected in backyard poultry and ground turkey were linked, despite this genetic relatedness. Enhanced molecular characterization methods, such as analysis of the pangenome of Salmonella isolates, might be necessary to understand the relationship between these two outbreaks. Similarly, enhanced data collection during outbreak investigations and further research could potentially aid in determining whether these transmission vehicles are truly linked by a common source and what reservoirs exist across the poultry industries that allow Salmonella Hadar to persist. Further work combining epidemiological data collection, more detailed traceback information, and genomic analysis tools will be important for monitoring and investigating future enteric disease outbreaks.

Human Salmonellosis Outbreak Linked to Salmonella Typhimurium Epidemic in Wild Songbirds, United States, 2020-2021.

Salmonella infection causes epidemic death in wild songbirds, with potential to spread to humans. In February 2021, public health officials in Oregon and Washington, USA, isolated a strain of Salmonella enterica serovar Typhimurium from humans and a wild songbird. Investigation by public health partners ultimately identified 30 illnesses in 12 states linked to an epidemic of Salmonella Typhimurium in songbirds. We report a multistate outbreak of human salmonellosis associated with songbirds, resulting from direct handling of sick and dead birds or indirect contact with contaminated birdfeeders. Companion animals might have contributed to the spread of Salmonella between songbirds and patients; the outbreak strain was detected in 1 ill dog, and a cat became ill after contact with a wild bird. This outbreak highlights a One Health issue where actions like regular cleaning of birdfeeders might reduce the health risk to wildlife, companion animals, and humans.

A Survey of Current Activities and Technologies Used to Detect Carbapenem Resistance in Bacteria Isolated from Companion Animals at Veterinary Diagnostic Laboratories-United States, 2020.

Carbapenems are antimicrobial drugs reserved for the treatment of severe multidrug-resistant Gram-negative bacterial infections. Carbapenem-resistant organisms (CROs) are an urgent public health threat and have been made reportable to public health authorities in many jurisdictions. Recent reports of CROs in companion animals and veterinary settings suggest that CROs are a One Health problem. However, standard practices of U.S. veterinary diagnostic laboratories (VDLs) to detect CROs are unknown. We assessed the capacity of VDLs to characterize carbapenem resistance in isolates from companion animals. Among 74 VDLs surveyed in 42 states, 23 laboratories (31%) from 22 states responded. Most (22/23, 96%) included ≥1 carbapenem on their primary antimicrobial susceptibility testing panel, and approximately one-third (9/23, 39%) performed phenotypic carbapenemase production testing or molecular identification of carbapenemase genes. Overall, 35% (8/23) of VDLs across eight states reported they would notify public health if a CRO was detected. Most (17/21, 81%) VDLs were not aware of CRO reporting mandates, and some expressed uncertainty about whether the scope of known mandates included CROs from veterinary sources. Although nearly all surveyed VDLs tested for carbapenem resistance, fewer had the capacity for mechanism testing or awareness of public health reporting requirements. Addressing these gaps is critical to monitoring CRO incidence and trends in veterinary medicine, preventing spread in veterinary settings, and mounting an effective One Health response. Improved collaboration and communication between public health and veterinary medicine is critical to inform infection control practices in veterinary settings and conduct a public health response when resistant isolates are detected.

Foodborne illness outbreaks linked to unpasteurised milk and relationship to changes in state laws - United States, 1998-2018.

Consumption of unpasteurised milk in the United States has presented a public health challenge for decades because of the increased risk of pathogen transmission causing illness outbreaks. We analysed Foodborne Disease Outbreak Surveillance System data to characterise unpasteurised milk outbreaks. Using Poisson and negative binomial regression, we compared the number of outbreaks and outbreak-associated illnesses between jurisdictions grouped by legal status of unpasteurised milk sale based on a May 2019 survey of state laws. During 2013-2018, 75 outbreaks with 675 illnesses occurred that were linked to unpasteurised milk; of these, 325 illnesses (48%) were among people aged 0-19 years. Of 74 single-state outbreaks, 58 (78%) occurred in states where the sale of unpasteurised milk was expressly allowed. Compared with jurisdictions where retail sales were prohibited (n = 24), those where sales were expressly allowed (n = 27) were estimated to have 3.2 (95% CI 1.4-7.6) times greater number of outbreaks; of these, jurisdictions where sale was allowed in retail stores (n = 14) had 3.6 (95% CI 1.3-9.6) times greater number of outbreaks compared with those where sale was allowed on-farm only (n = 13). This study supports findings of previously published reports indicating that state laws resulting in increased availability of unpasteurised milk are associated with more outbreak-associated illnesses and outbreaks.

Outbreak of Multidrug-Resistant Salmonella Heidelberg Infections Linked to Dairy Calf Exposure, United States, 2015-2018.

In August 2016, the Wisconsin Department of Health Services notified the U.S. Centers for Disease Control and Prevention of multidrug-resistant (MDR) Salmonella enterica serovar Heidelberg infections in people who reported contact with dairy calves. Federal and state partners investigated this to identify the source and scope of the outbreak and to prevent further illnesses. Cases were defined as human Salmonella Heidelberg infection caused by a strain that had one of seven pulsed-field gel electrophoresis (PFGE) patterns or was related by whole genome sequencing (WGS), with illness onset from January 1, 2015, through July 2, 2018. Patient exposure and calf purchase information was collected and analyzed; calves were traced back from the point of purchase. Isolates obtained from animal and environmental samples collected on-farm were supplied by veterinary diagnostic laboratories and compared with patient isolates using PFGE and WGS. Antimicrobial susceptibility testing by standardized broth microdilution was performed. Sixty-eight patients from 17 states were identified. Forty (63%) of 64 patients noted cattle contact before illness. Thirteen (33%) of 40 patients with exposure to calves reported that calves were sick or had died. Seven individuals purchased calves from a single Wisconsin livestock market. One hundred forty cattle from 14 states were infected with the outbreak strain. WGS indicated that human, cattle, and environmental isolates from the livestock market were genetically closely related. Most isolates (88%) had resistance or reduced susceptibility to antibiotics of ≥5 antibiotic classes. This resistance profile included first-line antibiotic treatments for patients with severe salmonellosis, including ampicillin, ceftriaxone, and ciprofloxacin. In this outbreak, MDR Salmonella Heidelberg likely spread from sick calves to humans, emphasizing the importance of illness surveillance in animal populations to prevent future spillover of this zoonotic disease.

Salmonella illness outbreaks linked to backyard poultry purchasing during the COVID-19 pandemic: United States, 2020.

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.

Comparison of Molecular Subtyping and Antimicrobial Resistance Detection Methods Used in a Large Multistate Outbreak of Extensively Drug-Resistant Campylobacter jejuni Infections Linked to Pet Store Puppies.

Campylobacter jejuni is a leading cause of enteric bacterial illness in the United States. Traditional molecular subtyping methods, such as pulsed-field gel electrophoresis (PFGE) and 7-gene multilocus sequence typing (MLST), provided limited resolution to adequately identify C. jejuni outbreaks and separate out sporadic isolates during outbreak investigations. Whole-genome sequencing (WGS) has emerged as a powerful tool for C. jejuni outbreak detection. In this investigation, 45 human and 11 puppy isolates obtained during a 2016-2018 outbreak linked to pet store puppies were sequenced. Core genome multilocus sequence typing (cgMLST) and high-quality single nucleotide polymorphism (hqSNP) analysis of the sequence data separated the isolates into the same two clades containing minor within-clade differences; however, cgMLST analysis does not require selection of an appropriate reference genome, making the method preferable to hqSNP analysis for Campylobacter surveillance and cluster detection. The isolates were classified as sequence type 2109 (ST2109)-a rarely seen MLST sequence type. PFGE was performed on 38 human and 10 puppy isolates; PFGE patterns did not reliably predict clustering by cgMLST analysis. Genetic detection of antimicrobial resistance determinants predicted that all outbreak-associated isolates would be resistant to six drug classes. Traditional antimicrobial susceptibility testing (AST) confirmed a high correlation between genotypic and phenotypic antimicrobial resistance determinations. WGS analysis linked C. jejuni isolates in humans and pet store puppies even when canine exposure information was unknown, aiding the epidemiological investigation during the outbreak. WGS data were also used to quickly identify the highly drug-resistant profile of these outbreak-associated C. jejuni isolates.

Short communication: Multistate outbreak of Listeria monocytogenes infections retrospectively linked to unpasteurized milk using whole-genome sequencing.

Unpasteurized milk can contain harmful bacteria such as Listeria monocytogenes. In 2016, the US Food and Drug Administration notified the Centers for Disease Control and Prevention (Atlanta, GA) that L. monocytogenes isolated from unpasteurized chocolate milk from a Pennsylvania dairy was closely related, by whole-genome sequencing, to L. monocytogenes isolates collected from blood specimens of 2 patients (in California and Florida) in 2014. The California and Florida patients consumed unpasteurized milk from the Pennsylvania dairy. Both were >65 yr old and were hospitalized in 2014; the Florida patient died. Isolates from the 2 patients had indistinguishable pulsed-field gel electrophoresis patterns and were closely related by whole-genome multilocus sequence typing analysis (by 2 alleles) to the isolate from unpasteurized chocolate milk produced by the Pennsylvania dairy in 2015. Together, epidemiologic and laboratory information indicated a common origin. This is the first multistate listeriosis outbreak linked to unpasteurized milk in the United States detected using whole-genome multilocus sequence analysis.

Protracted Outbreak of Salmonella Newport Infections Linked to Ground Beef: Possible Role of Dairy Cows - 21 States, 2016-2017.

In January 2017, CDC identified a cluster of Salmonella enterica serotype Newport infections with isolates sharing an indistinguishable pulsed-field gel electrophoresis (PFGE) pattern, JJPX01.0010 (pattern 10), through PulseNet, the national molecular subtyping network for foodborne disease surveillance. This report summarizes the investigation by CDC, state and local health and agriculture departments, and the U.S. Department of Agriculture's Food Safety and Inspection Service (USDA-FSIS) and discusses the possible role of dairy cows as a reservoir for strains of Salmonella that persistently cause human illness. This investigation combined epidemiologic and whole genome sequencing (WGS) data to link the outbreak to contaminated ground beef; dairy cows were hypothesized to be the ultimate source of Salmonella contamination.

Multidrug-Resistant Campylobacter jejuni Outbreak Linked to Puppy Exposure - United States, 2016-2018.

Campylobacter causes an estimated 1.3 million diarrheal illnesses in the United States annually (1). In August 2017, the Florida Department of Health notified CDC of six Campylobacter jejuni infections linked to company A, a national pet store chain based in Ohio. CDC examined whole-genome sequencing (WGS) data and identified six isolates from company A puppies in Florida that were highly related to an isolate from a company A customer in Ohio. This information prompted a multistate investigation by local and state health and agriculture departments and CDC to identify the outbreak source and prevent additional illness. Health officials from six states visited pet stores to collect puppy fecal samples, antibiotic records, and traceback information. Nationally, 118 persons, including 29 pet store employees, in 18 states were identified with illness onset during January 5, 2016-February 4, 2018. In total, six pet store companies were linked to the outbreak. Outbreak isolates were resistant by antibiotic susceptibility testing to all antibiotics commonly used to treat Campylobacter infections, including macrolides and quinolones. Store record reviews revealed that among 149 investigated puppies, 142 (95%) received one or more courses of antibiotics, raising concern that antibiotic use might have led to development of resistance. Public health authorities issued infection prevention recommendations to affected pet stores and recommendations for testing puppies to veterinarians. This outbreak demonstrates that puppies can be a source of multidrug-resistant Campylobacter infections in humans, warranting a closer look at antimicrobial use in the commercial dog industry.

State Laws Requiring Hand Sanitation Stations at Animal Contact Exhibits-United States, March-April 2016.

In the United States, animal contact exhibits, such as petting zoos and agricultural fairs, have been sources of zoonotic infections, including infections with Escherichia coli, Salmonella, and Cryptosporidium (1-4). The National Association of State Public Health Veterinarians recommends handwashing after contact with animals as an effective prevention measure to disease transmission at these exhibits (4). This report provides a list of states that have used law, specifically statutes and regulations, as public health interventions to increase hand sanitation at animal contact exhibits. The report is based on an assessment conducted by CDC's Public Health Law Program, in collaboration with the Division of Foodborne, Waterborne, and Environmental Diseases in CDC's National Center for Emerging and Zoonotic Infectious Diseases. The assessment found that seven states have used statutes or regulations to require hand sanitation stations at these exhibits (5). Jurisdictions seeking to improve rates of hand sanitation at animal contact exhibits can use this report as a resource in developing their own legal interventions.

Notes from the Field: Four Multistate Outbreaks of Human Salmonella Infections Linked to Small Turtle Exposure - United States, 2015.

In August 2015, the Food and Drug Administration (FDA) notified CDC of a consumer complaint involving Salmonella Sandiego infection in a child (the index patient), who had acquired a small turtle (shell length <4 inches [<10 cm]) at an Alabama flea market. The subsequent investigation, which included examining data from PulseNet, the national molecular subtyping network for foodborne disease surveillance, identified four multistate Salmonella outbreaks: two involving Salmonella Sandiego and two involving Salmonella Poona. These serotypes have been linked to small turtles in previous outbreaks (1,2). Although selling small turtles as pets in the United States has been banned since 1975 (3), illegal sales still occur at discount stores and flea markets and by street vendors. CDC investigated to determine the extent of the outbreaks and prevent additional infections.

Twenty Years of Active Bacterial Core Surveillance.

Active Bacterial Core surveillance (ABCs) was established in 1995 as part of the Centers for Disease Control and Prevention Emerging Infections Program (EIP) network to assess the extent of invasive bacterial infections of public health importance. ABCs is distinctive among surveillance systems because of its large, population-based, geographically diverse catchment area; active laboratory-based identification of cases to ensure complete case capture; detailed collection of epidemiologic information paired with laboratory isolates; infrastructure that allows for more in-depth investigations; and sustained commitment of public health, academic, and clinical partners to maintain the system. ABCs has directly affected public health policies and practices through the development and evaluation of vaccines and other prevention strategies, the monitoring of antimicrobial drug resistance, and the response to public health emergencies and other emerging infections.

Outbreak of Escherichia coli O157:H7 Infections Associated with Dairy Education Event Attendance - Whatcom County, Washington, 2015.

On April 27, 2015, the Whatcom County Health Department (WCHD) in Bellingham, Washington, was notified by a local laboratory regarding three children with presumptive Escherichia coli O157 infection. WCHD interviewed the parents, who indicated that all three children had attended a dairy education event held in a barn April 20­24, 2015, during a school field trip. WCHD, the Washington State Department of Health, and CDC investigated to determine the magnitude of the outbreak, identify risk factors and potential environmental sources of infection, and develop recommendations. A total of 60 cases (25 confirmed and 35 probable) were identified, and 11 patients were hospitalized.

Responding to outbreaks of illness linked to unpasteurized milk: A needs assessment of state health and agriculture departments.

AIMS: Consumption of unpasteurized milk can result in severe illness or death. In the United States, the number of people who regularly consume unpasteurized milk is relatively low, but outbreaks resulting from unpasteurized milk outnumber outbreaks linked to pasteurized milk. The sale of unpasteurized milk for human consumption through interstate commerce is prohibited at the federal level, but laws among states vary considerably with respect to the sale of unpasteurized milk. Each state has a different perspective on responding to and preventing outbreaks of illness linked to consuming unpasteurized milk. METHODS AND RESULTS: We conducted a needs assessment of state health and agriculture departments to gather information on state-level strategies to prevent illnesses linked to consuming unpasteurized milk, characterize challenges states face, and identify areas where partners can support state efforts to prevent illnesses. We deployed a survey from 6 January 2021 to 1 March 2021, using a snowball sampling strategy and had 158 respondents. Of 115 respondents, 46 (40%) believed that state laws were ineffective in preventing illnesses, and 92 (80%) agreed that consumers continue to find ways to get unpasteurized milk despite laws restricting sale. Respondents from 19 states were aware of future legislative or regulatory efforts surrounding unpasteurized milk in their state, with 14 (74%) indicating these efforts would expand consumer access. The most common outbreak prevention strategies respondents mentioned included sharing knowledge and experiences with other public health and agriculture officials, providing information to inform legislative efforts, and communicating to the public about outbreaks. Most respondents (41/50, 91%) were interested in pursuing further efforts to prevent unpasteurized milk-associated illnesses in their state. CONCLUSIONS: The results from this needs assessment can be used to inform future strategies for preventing illness outbreaks associated with unpasteurized milk consumption.

Multistate outbreaks of salmonellosis linked to contact with backyard poultry-United States, 2015-2022.

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.