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.

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.

Large animal veterinarians' knowledge, attitudes, and practices regarding livestock abortion-associated zoonoses in the United States indicate potential occupational health risk.

OBJECTIVE: To understand large animal veterinarians' knowledge of select zoonotic diseases that cause livestock abortions and identify barriers to using personal protective equipment (PPE). SAMPLE: A convenience sample of 469 veterinarians currently working with livestock. PROCEDURES: We sent an electronic survey invitation to large animal veterinarians through various veterinary organizations. Respondents answered questions addressing knowledge and prior experience with select abortion-associated zoonotic diseases, resources available for infection control, attitudes and barriers to PPE use, and demographics. RESULTS: Median participant age was 49 years (range, 22 to 82 years), and 54% (235/438) were male. Half of veterinarians (185/348) were contacted 5 or fewer times per year to consult on livestock abortions. No veterinarians surveyed answered all questions on zoonotic disease transmission correctly. Personal protective equipment access varied, from 99% (289/290) having access to gloves to 20% (59/290) having access to respirators. Concerns for spreading disease to other animals (136/289 [47%]) and to other humans (108/287 [38%]) ranked as the most common reported motivators for PPE use. Reported barriers to PPE use among survey participants were the inconvenience of taking PPE into the field (101/286 [35%]) and the inconvenience of wearing PPE (97/286 [34%]). Access to PPE was not correlated with PPE use. CLINICAL RELEVANCE: Surveyed veterinarians had limited knowledge of transmission of select abortion-associated zoonotic diseases. Incomplete understanding might lead to inappropriate PPE selection, preventable disease exposure, or missed opportunities for client education. Inconvenience was a primary reason PPE was not used.

Agritourism and Kidding Season: A Large Outbreak of Human Shiga Toxin-Producing Escherichia coli O157 (STEC O157) Infections Linked to a Goat Dairy Farm-Connecticut, 2016.

The objective of this study was to determine sources of Shiga toxin-producing Escherichia coli O157 (STEC O157) infection among visitors to Farm X and develop public health recommendations. A case-control study was conducted. Case-patients were defined as the first ill child (aged <18 years) in the household with laboratory-confirmed STEC O157, or physician-diagnosed hemolytic uremic syndrome with laboratory confirmation by serology, who visited Farm X in the 10 days prior to illness. Controls were selected from Farm X visitors aged <18 years, without symptoms during the same time period as case-patients. Environment and animal fecal samples collected from Farm X were cultured; isolates from Farm X were compared with patient isolates using whole genome sequencing (WGS). Case-patients were more likely than controls to have sat on hay bales at the doe barn (adjusted odds ratio: 4.55; 95% confidence interval: 1.41-16.13). No handwashing stations were available; limited hand sanitizer was provided. Overall, 37% (29 of 78) of animal and environmental samples collected were positive for STEC; of these, 62% (18 of 29) yielded STEC O157 highly related by WGS to patient isolates. STEC O157 environmental contamination and fecal shedding by goats at Farm X was extensive. Farms should provide handwashing stations with soap, running water, and disposable towels. Access to animal areas, including animal pens and enclosures, should be limited for young children who are at risk for severe outcomes from STEC O157 infection. National recommendations should be adopted to reduce disease transmission.

Investigations of Possible Multistate Outbreaks of Salmonella, Shiga Toxin-Producing Escherichia coli, and Listeria monocytogenes Infections - United States, 2016.

PROBLEM/CONDITION: Salmonella, Shiga toxin-producing Escherichia coli (STEC), and Listeria monocytogenes are the leading causes of multistate foodborne disease outbreaks in the United States. Responding to multistate outbreaks quickly and effectively and applying lessons learned about outbreak sources, modes of transmission, and risk factors for infection can prevent additional outbreak-associated illnesses and save lives. This report summarizes the investigations of multistate outbreaks and possible outbreaks of Salmonella, STEC, and L. monocytogenes infections coordinated by CDC during the 2016 reporting period. PERIOD COVERED: 2016. An investigation was considered to have occurred in 2016 if it began during 2016 and ended on or before March 31, 2017, or if it began before January 1, 2016, and ended during March 31, 2016-March 31, 2017. DESCRIPTION OF SYSTEM: CDC maintains a database of investigations of possible multistate foodborne and animal-contact outbreaks caused by Salmonella, STEC, and L. monocytogenes. Data were collected by local, state, and federal investigators during the detection, investigation and response, and control phases of the outbreak investigations. Additional data sources used for this report included PulseNet, the national molecular subtyping network based on isolates uploaded by local, state, and federal laboratories, and the Foodborne Disease Outbreak Surveillance System (FDOSS), which collects information from state, local, and territorial health departments and federal agencies about single-state and multistate foodborne disease outbreaks in the United States. Multistate outbreaks reported to FDOSS were linked using a unique outbreak identifier to obtain food category information when a confirmed or suspected food source was identified. Food categories were determined and assigned in FDOSS according to a classification scheme developed by CDC, the Food and Drug Administration (FDA), and the U.S. Department of Agriculture Food Safety and Inspection Service (FSIS) in the Interagency Food Safety Analytics Collaboration. A possible multistate outbreak was determined by expert judgment to be an outbreak if supporting data (e.g., temporal, geographic, demographic, dietary, travel, or food history) suggested a common source. A solved outbreak was an outbreak for which a specific kind of food or animal was implicated (i.e., confirmed or suspected) as the source. Outbreak-level variables included number of illnesses, hospitalizations, cases of hemolytic uremic syndrome (HUS), and deaths; the number of states with illnesses; date of isolation for the earliest and last cases; demographic data describing patients associated with a possible outbreak (e.g., age, sex, and state of residence); the types of data collected (i.e., epidemiologic, traceback, or laboratory); the outbreak source, mode of transmission, and exposure location; the name or brand of the source; whether the source was suspected or confirmed; whether a food was imported into the United States; the types of regulatory agencies involved; whether regulatory action was taken (and what type of action); whether an outbreak was publicly announced by CDC via website posting; beginning and end date of the investigation; and general comments about the investigation. The number of illnesses, hospitalizations, cases of HUS, and deaths were characterized by transmission mode, pathogen, outcome (i.e., unsolved, solved with suspected source, or solved with confirmed source), source, and food or animal category. RESULTS: During the 2016 reporting period, 230 possible multistate outbreaks were detected and 174 were investigated. A median of 24 possible outbreaks was under investigation per week, and investigations were open for a median of 37 days. Of these 174 possible outbreaks investigated, 56 were excluded from this analysis because they occurred in a single state, were linked to international travel, or were pseudo-outbreaks (e.g., a group of similar isolates resulting from laboratory media contamination rather than infection in patients). Of the remaining 118 possible multistate outbreaks, 50 were determined to be outbreaks and 39 were solved (18 with a confirmed food source, 10 with a suspected food source, 10 with a confirmed animal source, and one with a suspected animal source). Sprouts were the most commonly implicated food category in solved multistate foodborne outbreaks (five). Chicken was the source of the most foodborne outbreak-related illnesses (134). Three outbreaks involved novel food-pathogen pairs: flour and STEC, frozen vegetables and L. monocytogenes, and bagged salad and L. monocytogenes. Eleven outbreaks were attributed to contact with animals (10 attributed to contact with backyard poultry and one to small turtles). Thirteen of 18 multistate foodborne disease outbreaks with confirmed sources resulted in product action, including 10 outbreaks with recalls, two with market withdrawals, and one with an FSIS public health alert. Twenty outbreaks, including 11 foodborne and nine animal-contact outbreaks, were announced to the public by CDC via its website, Facebook, and Twitter. These announcements resulted in approximately 910,000 webpage views, 55,000 likes, 66,000 shares, and 5,800 retweets. INTERPRETATION: During the 2016 reporting period, investigations of possible multistate outbreaks occurred frequently, were resource intensive, and required a median of 37 days of investigation. Fewer than half (42%) of the 118 possible outbreaks investigated were determined to have sufficient data to meet the definition of a multistate outbreak. Moreover, of the 50 outbreaks with sufficient data, approximately three fourths were solved. PUBLIC HEALTH ACTION: Close collaboration among CDC, FDA, FSIS and state and local health and agriculture partners is central to successful outbreak investigations. Identification of novel outbreak sources and trends in sources provides insights into gaps in food safety and safe handling of animals, which helps focus prevention strategies. Summarizing investigations of possible multistate outbreaks can provide insights into the investigative process, improve future investigations, and help prevent illnesses. Although identifying and investigating possible multistate outbreaks require substantial resources and investment in public health infrastructure, they are important in determining outbreak sources and implementing prevention and control measures.

Outbreaks of Salmonella enterica infections linked to animal contact: Demographic and outbreak characteristics and comparison to foodborne outbreaks-United States, 2009-2014.

In the United States, multistate Salmonella outbreaks are most commonly linked to a food source; however, contact with live animals can also result in outbreaks of human illness. To characterize Salmonella outbreaks linked to animal contact and examine differences compared to foodborne outbreaks, we analysed data reported to the Centers for Disease Control and Prevention through the National Outbreak Reporting System (NORS) from 2009 to 2014 with a primary mode of transmission listed as "animal contact" or "food." Four hundred and eighty-four outbreaks with animal contact or foodborne transmission were reported through NORS; of these outbreaks, 99 (20.5%) resulted from Salmonella transmission through animal contact and 385 (79.5%) resulted from foodborne transmission, which resulted in 3,604 (19.8%) and 13,568 (80.2%) illnesses, respectively. A higher proportion of illnesses among children aged <1 year and children aged 1-4 years were linked to animal contact outbreaks compared to foodborne outbreaks (15.2% vs. 1.4%, p < 0.01 and 24.5% vs. 5.6%, p < 0.01, respectively). Illnesses resulting in hospitalizations (OR: 1.81, 95% CI: 1.62, 2.02) were more likely to be associated with animal contact compared to food. Animal contact outbreaks reported to NORS were more likely to be multistate compared to foodborne outbreaks (OR: 5.43, 95% CI: 3.37, 8.76) and had a longer median duration (99.0 days vs. 9.0 days, p < 0.01). Characterizing the differences between outbreaks of illness linked to animal contact and outbreaks linked to food provides useful information to investigators to improve public health response.

Whole Genome Sequencing: Bridging One-Health Surveillance of Foodborne Diseases.

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.

Corrigendum: Whole Genome Sequencing: Bridging One-Health Surveillance of Foodborne Diseases.

[This corrects the article DOI: 10.3389/fpubh.2019.00172.].

Onsite investigation at a mail-order hatchery following a multistate Salmonella illness outbreak linked to live poultry-United States, 2018.

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.

Using Hospital Inpatient Discharge Data to Supplement Active Surveillance for Invasive Pneumococcal Disease: Is the Extract Worth the Exertion?

OBJECTIVE: Invasive pneumococcal disease (IPD) surveillance systems monitor morbidity, mortality, and vaccine impact; accurate surveillance is important to detect changes in epidemiology. We evaluated completeness of IPD reporting in New Mexico by comparing data from the Hospital Inpatient Discharge Database (HIDD) and the New Mexico Active Bacterial Core Surveillance (ABCs) program. METHODS: We linked data from the HIDD and the ABCs program. We defined cases of IPD in the HIDD among New Mexico residents with hospitalizations during 2007-2009 as specific (320.1 or 038.2) or nonspecific (481, 320.2, or 041.2) using International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes. To validate if HIDD records that could not be matched to ABCs data were true IPD cases, we reviewed laboratory data and determined if Streptococcus pneumoniae (S. pneumoniae) had been isolated from a sterile body site. RESULTS: We examined 732 HIDD records for cases that were not matched in the ABCs database; of such records, S. pneumoniae was isolated from a sterile body site in 10 HIDD records. CONCLUSION: ABCs data detected the majority of IPD cases in New Mexico. Laboratory and medical record review is essential when using HIDD data because ICD-9-CM coding alone does not ensure data accuracy. The addition of IPD cases to the ABCs program from the HIDD was minimally beneficial to active surveillance and reporting completeness in New Mexico. States that rely exclusively on passive reporting and that have access to HIDD data might use linkages of pneumococcal and IPD-specific ICD-9-CM-coded HIDD data to improve IPD surveillance and case ascertainment.

Failure of total hip arthroplasty secondary to infection caused by Brucella abortus and the risk of transmission to operative staff.

Infection of total knee or hip arthroplasty by Brucella species is a rare complication. We describe the case of a failed hip replacement secondary to infection by Brucella abortus, as well as presentation, treatment course, and 2-year follow-up. In addition, we review the literature for features of periprosthetic Brucella species infections, and we describe the common exposures, clinical presentations, preoperative evaluation, and treatments used in the reported cases. Furthermore, we discuss the risk of transmission to operating room personnel and the appropriate preventative measures to avoid transmission.

Yersinia pestis infection in dogs: 62 cases (2003-2011).

OBJECTIVE: To describe the epidemiology, clinical signs, and treatment practices in dogs with Yersinia pestis infection in New Mexico. DESIGN: Retrospective case series. ANIMALS: 62 dogs with plague in New Mexico. PROCEDURES: Confirmed case animals had isolation of Yersinia pestis from a clinical specimen, a positive direct fluorescent antibody test result, or a minimum 4-fold change between acute and convalescent serum antibody titers with clinically compatible illness. Retrospective review of cases of laboratory-confirmed plague from 2003 to 2011 was performed with a standardized chart abstraction form. Epidemiologic, clinical, and treatment data were evaluated. RESULTS: 62 confirmed cases of canine plague were identified from 2003 to 2011. Most cases (85%) were confirmed by serologic titers alone or in conjunction with other testing methods. Clinical signs included fever (100%), lethargy (97%), anorexia (77%), lymphadenopathy (23%), vomiting (13%), diarrhea (8%), and abscesses (2%). Most case animals (73%) were treated with multiple antimicrobials. Sixty (97%) case animals survived; of the 2 nonsurvivors, one was euthanized and another died. Potential sources of exposure to Y pestis included hunting, rodent or rabbit exposure, and residence in rural areas. CONCLUSIONS AND CLINICAL RELEVANCE: Results indicated that dogs with exposure to Y pestis can develop moderate to severe illness or die as a result of infection. Veterinarians practicing in and examining animals from the western United States need to be familiar with the epidemiology of plague and query owners about potential plague exposures when consistent clinical signs are present. Veterinarians are often the first to recognize signs of plague among sentinel populations and have the opportunity to intervene and prevent zoonotic disease transmission.