Turtle-Associated Salmonellosis in Humans --- United States, 2006--2007

Turtles and other reptiles are reservoirs of Salmonella and have long been a recognized source of Salmonella infection in humans (1). Small turtles have posed a particular danger to young children because these turtles might not be perceived as health hazards and can be handled like toys. Salmonella infections in children can be severe and can result in hospitalization and occasionally in death (2). The association between Salmonella infection in children and exposure to turtles led to a 1975 law prohibiting the sale or distribution of small turtles (i.e., those with a carapace of <4 inches in length) in the United States (3). That prohibition led to a substantial decline in human salmonellosis cases associated with turtles (4). However, because the prohibition is not fully enforced and contains exceptions (e.g., sales for educational purposes), human turtle-associated cases continue to occur. This report describes several recent cases of turtle-associated salmonellosis reported to CDC by state and local health departments since September 2006, including a fatal case in an infant. These cases illustrate that small turtles remain a source of human Salmonella infections. Although ongoing public education measures aimed at preventing reptile-acquired Salmonella infections are helpful, prohibiting the sale of small turtles likely remains the most effective public health action to prevent turtle-associated salmonellosis.

Salmonella Pomona Infections --- Multiple States

On February 20, 2007, a female infant aged 3 weeks with a 1-day history of poor feeding and lethargy was evaluated in an emergency department at a Florida hospital. The patient was transferred immediately to a tertiary-care pediatric hospital; on arrival, she was febrile and in septic shock. Antibiotics were administered. She died on March 1. Cultures of cerebrospinal fluid and blood samples yielded Salmonella serotype Pomona.

The parents of the patient were interviewed by the Florida Department of Health. A family friend had purchased a small turtle with a carapace of 1.25 inches from a flea market in north central Florida in mid-November 2006. The turtle was purchased as a pet and given to the patient's family in late January 2007. After the death of the infant, laboratory testing of the turtle and its environment was performed by the Florida Bureau of Laboratories. A fecal sample from the turtle yielded S. Pomona. The S. Pomona isolates from the patient and the turtle were indistinguishable by pulsed-field gel electrophoresis (PFGE).

A total of 19 other S. Pomona isolates from 19 patients in 11 states (Alabama, Arizona, California, Florida, Massachusetts, Nevada, New Mexico, New York, Pennsylvania, South Carolina, and Texas) with a PFGE pattern closely related to the isolate from the Florida patient and turtle were submitted to PulseNet,* with isolation dates ranging from October 2, 2006 to April 23, 2007. To determine whether these cases of S. Pomona infection were associated with turtle exposure, CDC staff, through OutbreakNet,^† coordinated an investigation with state and city health departments, which conducted interviews with patients or their parents or guardians. The median age of patients was 3 years (range: 2 months--59 years). Illness onsets occurred during September 30, 2006--April 23, 2007. Of the 15 interviewed patients, 12 (80%) had direct or indirect contact with a turtle within 7 days before illness onset. Among those 12 patients, nine (75%) had turtles as household pets. The duration of turtle ownership before illness onset ranged from <1 month to approximately 5 years. Among the six patients for whom purchase information was available, all had purchased small turtles as pets from flea markets or pet shops. Carapace size at time of purchase was not reported. No common vendor was identified.

Salmonella I 4,[5],12:i:- Infections --- Ohio and Tennessee

Ohio. In September 2006, a previously healthy boy aged 8 years had onset of bloody diarrhea with cramping, headache, vomiting, and fever of 101.0^°F (38.3^°C). The Ohio Department of Health Laboratory isolated Salmonella I 4,[5],12:i:- from a stool specimen. The patient recovered at home after 3 days. No family member reported a similar illness while the patient was ill. However, the next month, the patient's brother, aged 12 years, had onset of bloody diarrhea; a stool specimen yielded Salmonella I 4,[5],12:i:-.

Two weeks before the first patient became ill, the family had purchased three red-eared slider turtles as pets, each with a carapace of <4 inches, at a flea market in southeastern Kentucky. The Ohio Department of Agriculture Laboratory isolated Salmonella from the coelomic contents of the turtles and a water sample from the turtles' aquarium. The isolates were serotyped at the U.S. Department of Agriculture's National Veterinary Services Laboratory; the turtle isolates were Salmonella I 4,[5],12:i:-, S. Litchfield, and S. Infantis, and the water sample isolate was S. Infantis. The Salmonella I 4,[5],12:i:- isolates from the patients and turtles were indistinguishable by PFGE performed at the Ohio Department of Health Laboratory.

Tennessee. In September 2006, a previously healthy woman aged 45 years was hospitalized with diarrhea, chills, fever of 102.8^°F (39.3^°C), abdominal cramps, myalgia, fatigue, nausea, and vomiting of 24 hours' duration. The patient was treated with antibiotics and intravenous fluids and released after 3 days. A stool specimen yielded Salmonella I 4,[5],12:i:-. The patient became ill less than 2 weeks after her son, aged 7 years, received two small red-eared slider turtles, both with carapaces of <2 inches, as a gift from family friends who had purchased them in Florida from an unknown vendor. The child also had onset of diarrhea shortly after receiving the turtles, but no specimens were collected during his illness.

County health officials visited the patient's home and collected a stool specimen from the child, an external surface swab from both turtles, and a water sample from the aquarium. Specimens from the child and turtles yielded Salmonella I 4,[5],12:i:- isolates, which were indistinguishable from the mother's isolate based on PFGE performed at the Tennessee Department of Health Laboratory. The aquarium water sample yielded Salmonella Pomona.

Reported by: D Chatfield, MSEH, Clark County Combined Health District; K Winpisinger, MS, Ohio Dept of Health. P Sumner, N Grossman, MD, Marion County Health Dept; R Hammond, PhD, D Windham, P Fiorella, PhD, Florida Dept of Health. ME Ress, Sullivan County Regional Health Dept; H Hardin, MPA, Tennessee Dept of Health Laboratory Svcs; J Dunn, DVM, Tennessee Dept of Health. M Iwamoto, MD, T-A Nguyen, MPH, N Patel, J Lockett, M Sotir, PhD, Div of Foodborne, Bacterial, and Mycotic Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, CDC.

Editorial Note:

Salmonella illness remains a major public health problem in the United States, with an estimated 1.4 million nontyphoidal human Salmonella infections occurring annually, resulting in approximately 15,000 hospitalizations and 400 deaths (5). Reptiles are a well-established source of human salmonellosis; a study conducted during 1996--1997 attributed an estimated 6% of all human, laboratory-confirmed, sporadic Salmonella infections in the United States (and 11% of infections among persons aged <21 years) to contact with reptiles and amphibians (6). The epidemiologic and laboratory findings from the investigations described in this report demonstrate that turtles were the likely source of infection in these human salmonellosis cases. Exposure to turtles was associated with salmonellosis, and identical PFGE Salmonella strains were isolated from samples from patients and their turtles in three separate instances. Nontyphoidal human Salmonella illnesses in the United States are common and usually sporadic; therefore, many cases of turtle-associated human salmonellosis likely occur without detection or without a recognized link to exposure to turtles.

Despite a federal law prohibiting the sale or distribution of small turtles as pets, such sales still occur. Salmonella can be transmitted to humans by direct or indirect contact with a turtle or its feces. No reliable methods are available to guarantee that a turtle is free of Salmonella. Most turtles are colonized with Salmonella and shed the bacteria intermittently in their feces. Certain techniques to eliminate Salmonella from turtles have been unsuccessful and have resulted in Salmonella isolates with increased antibiotic resistance (7). In addition, turtles not shedding Salmonella species under normal circumstances have been shown to actively shed the bacteria when stressed (8). Moreover, water in turtle bowls or aquariums can amplify any Salmonella shed by turtles. For these reasons, all turtles, regardless of carapace size, should be handled as though they are infected with Salmonella.

In 1980, CDC estimated that the 1975 federal prohibition of the sale of small turtles in the United States had prevented an estimated 100,000 cases of turtle-associated salmonellosis in children aged 1--9 years in 1976 (4). These additional cases might have resulted in approximately 1,500 hospitalizations and 40 deaths that year (4--6). Reductions in human illnesses associated with turtle-associated Salmonella strains were observed in other countries when similar small turtle sale prohibitions were enacted (9,10). When Sweden joined the European Union in 1996 and sale prohibitions were repealed, the number of human salmonellosis cases from reptile-associated Salmonella strains increased substantially, with children being most affected (9).

The recent cases of turtle-associated human salmonellosis described in this report emphasize the need for improved prevention measures. Public education aimed at preventing reptile-acquired Salmonella infections is ongoing in the United States (Box). After identification of the cluster of Salmonella Pomona infections and the fatal case in the infant described in this report, the Food and Drug Administration issued a consumer advisory update, available at http://www.fda.gov/consumer/updates/turtles042307.html, emphasizing the risks for salmonellosis associated with small pet turtles. Consumers were reminded of recommendations for reducing the risk for Salmonella infection from all reptiles, which include washing hands with soap and water after handling reptiles or their cages and keeping reptiles out of food-preparation areas. CDC has published similar recommendations, available at http://www.cdc.gov/healthypets/spotlight_an_turtles.htm. Such education measures are helpful, but prohibiting the sale of small turtles likely remains the most effective public health action to prevent turtle-associated salmonellosis.

Acknowledgments

The findings in this report are based, in part, on contributions by C James, MPH, Alabama Dept of Public Health; J Schneider, MPH, California Dept of Health Svcs; E Harvey, Massachusetts Dept of Public Health; C Ewers, New Mexico Dept of Health; L Kidoguchi, MPH, S Slavinski, DVM, Bur of Communicable Diseases, New York City Department of Health and Mental Hygiene, L Kornstein, PhD, L Chicaiza, L Lee, MS, Public Health Laboratory, New York City Dept of Health and Mental Hygiene, G Johnson, D Schoonmaker-Bopp, P Smith, MD, E Villamil, MPH, New York State Dept of Health; A Weltman, MD, S Snyder, M Shaw, C Marriott, MPH, Pennsylvania Dept of Health; J Schlegl, MSP, South Carolina Dept of Health and Environmental Control; and L Gaul, PhD, Texas Dept of State Health Svcs.

References

1. Lamm SH, Taylor A, Gangarosa EJ, et al. Turtle-associated salmonellosis. Am J Epidemiol 1972;95:511--7.
2. Kennedy M, Villar R, Vugia D, et al. Hospitalizations and deaths due to Salmonella infections, FoodNet, 1996--1999. Clin Infect Dis 2004;38(Suppl 3):S142--8.
3. 21 CFR § 240.62. Turtles intrastate and interstate requirements. Available at http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/cfrsearch.cfm?fr=1240.62.
4. Cohen ML, Potter M, Pollard R, Feldman RA. Turtle-associated salmonellosis in the United States: effect of public health action, 1970 to 1976. JAMA 1980;243:1247--9.
5. Voetsch AC, Van Gilder TJ, Angulo FJ, et al. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 2004;38(Suppl 3):S127--34.
6. Mermin J, Hutwagner L, Vugia D, et al. Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. Clin Infect Dis 2004;38(Suppl 3):S253--61.
7. Diaz MA, Cooper RK, Cloeckaert A, Siebeling RJ. Plasmid-mediated high-level gentamicin resistance among enteric bacteria isolated from pet turtles in Louisiana. Appl Environ Microbiol 2006;72:306--12.
8. DuPonte MW, Nakamura RM, Chang EM. Activation of latent Salmonella and Arizona organisms by dehydration in red-eared turtles, Pseudemys scripta-elegans. Am J Vet Res 1978;39:529--30.
9. De Jong B, Anderson Y, Ekdahl K. Effect of regulation and education on reptile-associated salmonellosis. Emerg Infect Dis 2005;11: 398--403.
10. D'Aoust JY, Lior H. Pet turtle regulations and abatement of human salmonellosis. Can J Public Health 1978;69:107--8.

* National Molecular Subtyping Network for Foodborne Disease Surveillance.

^† The network of epidemiologists and other public health officials, facilitated by CDC, that investigates outbreaks of foodborne, waterborne, and other enteric illnesses.

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Date last reviewed: 7/5/2007