Flea market finds and global exports: Four multistate outbreaks of human Salmonella infections linked to small turtles, United States-2015.

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. 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. 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. 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.

The sale and distribution of small turtles (shell length <4 inches) as pets has been banned in the United States since 1975 because of the risk of Salmonella transmission, especially to children. Despite this 48-year-old ban, salmonellosis outbreaks continue to be linked to contact with small turtles. During investigations of turtle-associated outbreaks, information regarding the turtle farm of origin is difficult to obtain because turtles are commonly sold by transient vendors. During 2020-2021, public health officials investigated a multistate illness outbreak caused by Salmonella enterica serotype Typhimurium linked to pet small turtles. Cases were defined as a laboratory-confirmed Salmonella Typhimurium infection highly related (within 0-6 allele differences) to the outbreak strain based on whole-genome sequencing analysis by core-genome multilocus sequence typing with illness onset occurring during 27 August 2020-14 May 2021. Forty-three patients were identified from 12 states; of these, 35% (15/43) were children <5 years old. Among patients with available information, 37% (14/38) were hospitalized, and one death was reported. Seventy-four percent (25/34) of patients reported turtle exposure in the week before illness onset, and 84% (16/19) specified exposure to small turtles. The outbreak strain was isolated from samples collected from a Pennsylvania patient's small turtle tank. Two patients reported purchasing their small turtles from pet stores. Salmonella Braenderup was isolated from samples collected from small turtles and their habitat at one of these stores; however, at that time, this strain was not associated with any human illnesses. This investigation was notable because of the documented sale of small turtles from several pet stores combined with the identification of a single small turtle supplier to these pet stores. The high proportion of children involved in this outbreak highlights the continued need to educate the pet industry as well as parents and caregivers about the risk of turtle-associated salmonellosis especially in children. Understanding and addressing the persisting challenges related to the illegal sale and distribution of small turtles could reduce the burden of turtle-associated salmonellosis.

In 2013, the World Health Organization (WHO) reported that small, pet turtles had caused multistate Salmonella outbreaks in the United States, from where small turtles were subsequently exported into the Republic of Korea. We investigated cases of salmonellosis in South Korea associated with domestic small turtles and analysed genetic characteristics of Salmonella isolates in commercially-available small turtles. We traced six Salmonella serovars, known to have caused human infection in the United States (S. Sandiego, S. Pomona, S. Poona, S. Newport, I 4,(5),12:i:-, and S. Typhimurium), in isolates from suspected Salmonella infection cases in Korea from 2006 to 2015. Additionally, we conducted a pilot study of isolates from small turtles being sold in Korean markets, and performed molecular genetic analysis on the identified strains. S. Pomona was identified in one Salmonella infection case, while all strains isolated from small turtles belonged to either subspecies I (enterica, n = 10, 71.4%) or subspecies IIIb (diarizonae, n = 4, 28.6%). Two serovars (S. Pomona and S. Sandiego) that were highly associated with turtle-to-human transmission were identified with 100% homology to human isolates. Previous to this study, turtle-associated human S. Pomona infections were not well reported in Korea. We report Salmonella infection in small turtles in Korea, and confirm that small turtles should be considered the first infectious agent in S. Pomona infection. We therefore suggest quarantine measures for importing small turtles be enhanced in Korea.

Turtles and other reptiles have long been recognized as a source of human Salmonella infections. To prevent turtle-associated Salmonella infections in humans, the sale and distribution of small turtles (i.e., those with a carapace length of less than 4 inches) has been prohibited in the United States since 1975. Despite this prohibition, small turtles remain available to the public from various sources, including pet shops, flea markets, street vendors, and Internet websites. In October 2007, the North Carolina Division of Public Health (NCDPH) notified CDC of human infections caused by Salmonella serotype Paratyphi B L (+) tartrate (+) (Salmonella Paratyphi B var. Java) in several states. Salmonella Paratyphi B var. Java is a nontyphoidal strain of Salmonella that causes gastroenteritis. This report describes the results of the epidemiologic and laboratory investigation conducted by CDC and state and local health departments during October 2007-January 2008. The findings document an ongoing, multistate outbreak of Salmonella Paratyphi B var. Java infections, with the first reported illness onset occurring on May 4, 2007. Many of these infections have occurred in young children and have been associated with exposure to small turtles. Prohibiting the sale and distribution of small turtles likely remains the most effective public health action to prevent turtle-associated salmonellosis.

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.

In the United States (U.S.), pet turtles have been associated with outbreaks of salmonellosis, a serious and sometimes-fatal intestinal illness caused by Salmonella bacteria, with nearly 300,000 people being infected in some years. Children are particularly susceptible because of their propensity to put items, including small turtles, in their mouths. In 1975, a U.S. federal regulation prohibited the sale of turtles <4 inches (101.6 mm) in size, except for the purposes of export, scientific, or educational purposes. This regulation was established to reduce the incidence of salmonellosis, particularly in small children. Previous research has not evaluated the availability of turtles <4 inches in size on websites selling wildlife. We monitored 16 websites in 2021 and quantified listings of small turtles. We determined whether information on Salmonella, the 1975 federal regulation, or related state regulations were provided on the websites and determined legality of sales of small turtles by state regulations. We found that all 16 websites openly advertised and sold turtles <4 inches in size, but only half of these websites provided information about Salmonella and/or the federal regulation. These websites required buyers to confirm that they were not purchasing a turtle as a pet, thereby putting the onus on the consumer to adhere to the regulation. We documented 515 listings of turtles <4 inches in size, including 47 species and one hybrid. Our study has demonstrated that internet sales of small turtles currently represent part of the thriving online pet trade in the U.S. Enforcement of the federal regulation faces jurisdictional challenges in most states. Therefore, we recommend continued public education campaigns by public health agencies in the U.S. to help reduce the risk that pet turtle ownership presents.

In May 2014, a cluster of human Salmonella Poona infections was identified through PulseNet, the national molecular subtyping network for foodborne disease surveillance. Historically, this rare serotype has been identified in multiple Salmonella outbreaks associated with pet turtle exposure and has posed a particular risk to small children. Although the sale and distribution of small turtles (those with carapace [upper shell] lengths <4 inches [<10.2 cm]) is prohibited by federal law, they are still available for legal purchase online for "bona-fide" scientific, educational, or exhibition purposes, other than use as pets. In addition, small turtles are still available for illegal purchase through transient street vendors, at flea markets, and at fairs.

Cryptosporidiosis outbreaks — United States, 2009–2017

Turtle-associated salmonellosis was increasingly recognized in the United States during the 1960s, leading to a federal ban in 1975 on the sale of turtles <4 inches in carapace length (small turtles). Although sporadic reports of turtle-associated Salmonella are frequent, outbreaks are rare. In September 2007, several patients with Salmonella enterica serotype Paratyphi B var Java infections reported recent turtle exposure. We conducted an investigation to determine the source and extent of the infections. Patients with Salmonella Paratyphi B var Java infections with a specific pulsed-field gel electrophoresis pattern (outbreak strain) and illness onset between May 2007 and January 2008, were compared with healthy controls. Reptile exposure and awareness of a Salmonella-reptile link were assessed. Turtle size and purchase information were collected. We identified 107 patients with outbreak-strain infections. The median patient age was 7 years; 33% were hospitalized. Forty-seven (60%) of 78 patients interviewed reported exposure to turtles during the week before illness; 41 (87%) were small turtles, and 16 (34%) were purchased in a retail pet store. In the case-control study, 72% of 25 patients reported turtle exposure during the week before illness compared with 4% of 45 controls (matched odds ratio [mOR]: 40.9 [95% confidence interval (CI): 6.9-unbounded]). Seven (32%) of 22 patients versus 11 (28%) of 39 controls reported knowledge of a link between reptile exposure and Salmonella infection (mOR: 1.3 [95% CI: 0.4-4.6]). We observed a strong association between turtle exposure and Salmonella infections in this outbreak. Small turtles continue to be sold and pose a health risk, especially to children; many people remain unaware of the link between Salmonella infection and reptile contact.

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

Salmonellosis associated with small pet turtles in the United States was a major public health concern in the 1970s. In 1975, the Food and Drug Administration (FDA) banned commercial distribution of small turtles (i.e., those with a carapace of <4 inches). The FDA ban prevents an estimated 100,000 cases of salmonellosis among children each year. However, a recent resurgence in the sale of small turtles has generated concern. In Wisconsin and Wyoming, at least six human cases of salmonellosis have been linked to such turtles. This report describes the investigation into those cases. The findings underscore the need for health and environmental officials to prevent illegal distribution of small turtles and consider patient contact with turtles when investigating salmonellosis cases.

Getting the lead out: Can iron help?

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.

Investigation of Outbreak of Infections Caused by Salmonella Saintpaul

Travel Medicine and Transplant Tourism in Solid Organ Transplantation