Sally A. Bidol

Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat.

BACKGROUND Despite a decreasing incidence of listeriosis in the United States, molecular subtyping has increased the number of recognized outbreaks. In September 2000, the New York City Department of Health identified a cluster of infections caused by Listeria monocytogenes isolates with identical molecular subtypes by pulsed-field gel electrophoresis (PFGE) and ribotyping. METHODS To determine the magnitude of the outbreak and identify risk factors for infection, we notified state health departments and conducted a case-control study. A case was defined as a patient or mother-infant pair infected with Listeria monocytogenes whose isolate yielded the outbreak PFGE pattern. Controls were patients infected with Listeria monocytogenes whose isolate yielded a different PFGE pattern. Patients were asked about food and drink consumed during the 30 days before the onset of illness. RESULTS Between May and December 2000, there were 30 clinical isolates of Listeria monocytogenes with identical PFGE patterns identified in 11 US states. Cases of infection caused by these isolates were associated with 4 deaths and 3 miscarriages. A case-control study implicated sliced processed turkey from a delicatessen (Mantel-Haenszel odds ratio, 8.0; 95% confidence interval, 1.2-43.3). A traceback investigation identified a single processing plant as the likely source of the outbreak, and the company voluntarily recalled 16 million pounds of processed meat. The same plant had been identified in a Listeria contamination event that had occurred more than a decade previously. CONCLUSIONS Prevention of persistent L. monocytogenes contamination in food processing plants presents a critical challenge to food safety professionals.

Outbreak of Variant Influenza A(H3N2) Virus in the United States

During an outbreak of H3N2v variant influenza, we identified 306 cases in ten states. Most cases reported agricultural fair attendance and/or contact with swine prior to illness. We found no evidence of efficient or sustained person-to-person transmission of H3N2v.

Multistate Outbreak of Salmonella Typhimurium and Saintpaul Infections Associated with Unpasteurized Orange Juice—United States, 2005

BACKGROUND Infection due to Salmonella species causes an estimated 1.4 million illnesses and 400 deaths annually in the United States. Orange juice is a known vehicle of salmonellosis, for which regulatory controls have recently been implemented. We investigated a nationwide outbreak of Salmonella infection to determine the magnitude of the outbreak and to identify risk factors for infection. METHODS We identified cases through national laboratory-based surveillance. In a case-control study, we defined a case as infection with Salmonella serotype Typhimurium that demonstrated the outbreak pulsed-field gel electrophoresis pattern in a person with illness onset from 1 May through 31 July 2005; control subjects were identified through random digit dialing. RESULTS We identified 152 cases in 23 states. Detailed information was available for 95 cases. The median age of patients was 23 years; 46 (48%) of the 95 patients were female. For 38 patients and 53 age-group matched control subjects in 5 states, illness was associated with consuming orange juice (90% vs. 43%; odds ratio, 22.2; 95% confidence interval, 3.5-927.5). In a conditional logistic regression model, illness was associated with consuming unpasteurized orange juice from company X (53% vs. 0%; odds ratio, 38.0; 95% confidence interval, 6.5-infinity). The US Food and Drug Administration found that company X was noncompliant with the juice Hazard Analysis and Critical Control Point regulation and isolated Salmonella serotype Saintpaul from company Xs orange juice. CONCLUSIONS Unpasteurized orange juice from company X was the vehicle of a widespread outbreak of salmonellosis. Although the route of contamination is unknown, noncompliance with the juice Hazard Analysis and Critical Control Point regulation likely contributed to this outbreak. Pasteurization or other reliable treatment of orange juice could prevent similar outbreaks.

Reptile-Associated Salmonellosis in Preschool-Aged Children in Michigan, January 2001–June 2003

OBJECTIVES Determine the incidence of reptile-associated salmonellosis in preschool-aged children in Michigan. METHODS Cases of reptile-associated salmonellosis in children < or =5 years of age occurring in Michigan January 2001-June 2003 were identified through review of individual patient case-history forms provided by local health departments to the Michigan Department of Community Health and by identification of Michigan Department of Community Health laboratory-confirmed cultures of reptile-associated serotypes, determined by evaluation of the Public Health Laboratory Information Systems Clinical Nonhuman Salmonella data for 1990-2001. RESULTS The incidence of reptile-associated salmonellosis was 11.8% of all Salmonella cases reported in Michigan children aged < or =5 years for the period January 2001 through June 2003. CONCLUSIONS Despite the recommendations of the Centers for Disease Control and Prevention to avoid the exposure of children <5 years old to reptiles, reptile-associated salmonellosis in preschool-aged children continues to be a public health problem in Michigan.

Outbreak of Salmonellosis Linked to Live Poultry from a Mail-Order Hatchery

BACKGROUND Outbreaks of human salmonella infections are increasingly associated with contact with live poultry, but effective control measures are elusive. In 2005, a cluster of human salmonella Montevideo infections with a rare pattern on pulsed-field gel electrophoresis (the outbreak strain) was identified by PulseNet, a national subtyping network. METHODS In cooperation with public health and animal health agencies, we conducted multistate investigations involving patient interviews, trace-back investigations, and environmental testing at a mail-order hatchery linked to the outbreak in order to identify the source of infections and prevent additional illnesses. A case was defined as an infection with the outbreak strain between 2004 and 2011. RESULTS From 2004 through 2011, we identified 316 cases in 43 states. The median age of the patient was 4 years. Interviews were completed with 156 patients (or their caretakers) (49%), and 36 of these patients (23%) were hospitalized. Among the 145 patients for whom information was available, 80 (55%) had bloody diarrhea. Information on contact with live young poultry was available for 159 patients, and 122 of these patients (77%) reported having such contact. A mail-order hatchery in the western United States was identified in 81% of the trace-back investigations, and the outbreak strain was isolated from samples collected at the hatchery. After interventions at the hatchery, the number of human infections declined, but transmission continued. CONCLUSIONS We identified a prolonged multistate outbreak of salmonellosis, predominantly affecting young children and associated with contact with live young poultry from a mail-order hatchery. Interventions performed at the hatchery reduced, but did not eliminate, associated human infections, demonstrating the difficulty of eliminating salmonella transmission from live poultry.

Escherichia coli O157 cluster evaluation.

We investigated a multistate cluster of Escherichia coli O157:H7 isolates; pulsed-field gel electrophoresis subtyping, using a single enzyme, suggested an epidemiologic association. An investigation and additional subtyping, however, did not support the association. Confirmating E. coli O157 clusters with two or more restriction endonucleases is necessary before public health resources are allocated to follow-up investigations.

Nationwide outbreak of multidrug-resistant Salmonella Heidelberg infections associated with ground turkey: United States, 2011

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 patients 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.

Salmonellosis and Meat Purchased at Live-Bird and Animal-Slaughter Markets, United States, 2007–2012

To the Editor: Salmonella spp. cause ≈1.2 million human illnesses annually in the United States (1). Infections are primarily acquired through exposure to contaminated food or infected animals (1,2). Since 2007, state and local health departments and the Centers for Disease Control and Prevention have investigated multiple salmonellosis outbreaks linked to meat purchased at live-bird markets (LBMs) and live-animal markets (LAMs), where poultry and livestock are sold for onsite slaughter. These markets typically operate in large cities and serve populations of diverse ethnic backgrounds (3). In 2007, an outbreak involving 62 case-patients infected with 1 of 3 S. enterica serotype Schwarzengrund strains was investigated in Massachusetts; 61% were children <5 years of age, including 14 (23%) infants <1 year of age, and 96% were Asian (Table). A case-patient was defined as a person infected with S. enterica who had a pulsed-field gel electrophoresis XbaI restriction enzyme pattern indistinguishable from the outbreak strain. Exposure to poultry purchased at LBMs was reported, and environmental sampling at an implicated LBM identified 6 S. enterica serotypes, including 1 outbreak strain. Table Characteristics of outbreaks of human Salmonella enterica serotype Schwarzengrund infections linked to meat purchased at live-bird markets, United States, 2007–2012* Three subsequent investigations of S. enterica serotype Schwarzengrund infections were conducted: a 2009 outbreak of 50 cases in New York, New York; a 2010–2011 multistate outbreak of cases predominantly in New York, New Jersey, and Massachusetts; and a 2012 multistate outbreak of cases mostly in Illinois and Michigan. Most case-patients in these outbreaks were of Asian race or Hispanic ethnicity, but 3/5 case-patients in Michigan reported Arab ethnicity; >50% were infants or children <5 years of age. Among case-patients with available information, exposure to poultry from LBMs was reported by 88% of case-patients in the 2009 New York investigation, 35% in the 2010–2011 multistate investigation, and 50% in the 2012 multistate investigation. In Michigan, the outbreak strain was isolated from chicken purchased at an LBM and collected from households of 2 case-patients. During 2011–2012, the Centers for Disease Control and Prevention investigated a nationwide increase in S. enterica serotype I,4,[5],12:i- infections (pulsed-field gel electrophoresis XbaI restriction enzyme pattern JPXX01.1314). Although no single vehicle was implicated, clusters linked to LAMs were identified. In Minnesota, 14 illnesses were linked to meat from 3 neighboring LAMs. Environmental sampling identified the outbreak strain from an animal-holding pen at 1 of the markets. Seven case-patients were infants <1 year of age, and 10 reported Hmong ethnicity. In California, 10 illnesses likely associated with pork, lamb, and beef purchased at 3 LAMs were identified; case-patients reported Ethiopian and Hmong ethnicity. The outbreak strain was isolated from a pork leg collected from the freezer of a case-patient. LBMs and LAMs appear to be preferred by certain populations for cultural, culinary, or religious reasons. Exposure to meat from these markets is being increasingly recognized as a potential source of salmonellosis. The cause is uncertain, but one factor may be an increased number of markets: in New York, New York, the number of LBMs nearly doubled from 44 to >80 during 1994–2002 (4). Most case-patients in these outbreaks had minimal direct contact with poultry or livestock at these markets; many case-patients were infants or young children who had not visited the markets or consumed meat. Therefore, one risk factor appears to be living in a household where the meat purchased from these markets is handled or consumed. Several factors could make meats from these markets more risky for acquiring salmonellosis. Although LBMs and LAMs must meet sanitation requirements and prevent product adulteration (5–7), most are exempt from Food Safety and Inspection Service pathogen reduction performance standards (8,9) and probably do not require suppliers to use pathogen control measures on the farm or employ them during slaughter. Regulatory oversight by state agencies varies. Investigation findings, including environmental sampling, indicate that these markets could be heavily contaminated with S. enterica. Preliminary results of a Massachusetts study found that fresh-killed chickens from LBMs had higher Salmonella and Campylobacter spp. contamination rates than those for chickens purchased at grocery stores (10; T. Stiles, unpub. data). High-risk cultural preferences identified in these outbreaks included consuming raw or undercooked meat and cooking parts (e.g., feet, intestines) that are more likely to harbor Salmonella spp. Further processing (e.g., de-feathering, butchering) conducted inside homes could lead to cross-contamination in the household environment. Because of language and cultural barriers, existing food safety messages may not have been effective. The number and type of LBMs and LAMs, the populations these markets serve, and regulatory authority vary considerably by state, and many case-patients and market owners have been reluctant to speak with public health authorities. Therefore, illness prevention requires a local, targeted approach. To strengthen regulations, some states have created guidelines and begun regular inspection of these markets. Educational outreach has included distribution of posters, flyers, and magnets with safe food handling messages in multiple languages; collaboration with community groups; and education of market owners and workers. Given the various communities who use LBMs and LAMs, multifaceted interventions, including collaboration between human and animal health agencies, are needed to reduce disease risk among market patrons and their families.

Multistate Outbreak of Human Salmonella Typhimurium Infections Linked to Pet Hedgehogs – United States, 2011–2013

Zoonotic Salmonella infections cause approximately 130 000 illnesses annually in the United States. Of 72.9 million US households owning at least one pet, five million own small mammals; 3000 hedgehogs were documented by USDA in USDA‐licensed breeding facilities and pet stores in 2012. State health department collaborators and PulseNet, the national bacterial subtyping network, identified human infections of a Salmonella Typhimurium outbreak strain, which were investigated by CDC, USDA‐APHIS and state public and animal health officials. A case was defined as an illness in a person infected with the outbreak strain identified between 1 December 2011 and 3 June 2013. Investigators collected information on patient exposures, cultured animal and environmental specimens for Salmonella, and conducted traceback investigations of USDA‐licensed hedgehog facilities. There were 26 cases in 12 states. Illness onset dates ranged from 26 December 2011 to 8 April 2013. The median patient age was 15 years (range = <1–91 years); 58% were female. Among 23 persons with available information, 8 (35%) were hospitalized and one outbreak strain‐associated death was reported. Of 25 patients with available information, 20 (80%) reported pet hedgehog contact in the week before illness onset. The outbreak strain was isolated from animal and environmental samples collected from three ill persons’ homes in three states. Hedgehogs were purchased in geographically distant states from USDA‐licensed breeders (10/17, 59%); a USDA‐licensed pet store (1/17, 6%); unlicensed or unknown status breeders (3/17, 18%); and private individuals (3/17, 18%). Traceback investigations of USDA‐licensed facilities did not reveal a single source of infection. Public and animal health collaboration linked pet hedgehog contact to human infections of Salmonella Typhimurium, highlighting the importance of a One Health investigative approach to zoonotic salmonellosis outbreaks. More efforts are needed to increase awareness among multiple stakeholders on the risk of illness associated with pet hedgehogs.