Salmonellosis

Salmonellosis associated with small pet turtles in the United States was a major public health concern in the 1970s (1). In 1975, the Food and Drug Administration (FDA) banned commercial distribution of small turtles (i.e., those with a carapace of <4 inches) (2). The FDA ban prevents an estimated 100,000 cases of salmonellosis among children each year (3). 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.

Wisconsin

Case 1. While vacationing with her family in Wisconsin in late July 2004, a Kansas girl aged 4 years was taken to an emergency department with diarrhea and fever of 4 days' duration. Her mother was instructed to keep the child on a clear liquid diet until the diarrhea ceased, and the child was released. The next day, the patient was taken to an urgent-care clinic for treatment of bloody diarrhea, cramps, and fever. Stool cultures yielded Salmonella enterica serotype Pomona, a rare serotype. The child was placed on a 3-day course of trimethoprim/sulfamethoxazole, and the illness resolved after 5 days.

Epidemiologic investigation by the Wisconsin Division of Public Health (WDPH) determined that the family had purchased a small turtle at a souvenir shop (store A) in northwest Wisconsin. Warned by the public health nurse of the possible link between the turtle and the child's illness, the family removed the turtle, so the animal was not available for testing.

Cases 2 and 3. In July 2004, a boy aged 2 years was taken to his physician with watery diarrhea and fever of 4 days' duration. Twelve days later, his mother had onset of" diarrhea and fever. The physician counseled the patients; neither patient was treated and both recovered completely.

Cultures of stool samples from both patients yielded S. Pomona. Epidemiologic investigation by WDPH determined that the family had recently purchased small turtles at a souvenir shop (store B) in south-central Wisconsin. The family provided water specimens obtained from the turtle habitat; these were cultured and yielded S. Pomona. The three patient isolates from cases 1, 2, and 3 and water from the turtle habitat were tested by pulsed-field gel electrophoresis (PFGE) at the Wisconsin State Laboratory of Hygiene and produced indistinguishable PFGE patterns with two different restriction enzymes.

Case 4. In August 2004, a boy aged 10 years was taken to an urgent-care clinic with a 3-day history of diarrhea and vomiting. He was hospitalized for 3 days and treated with antibiotics, after which a stool specimen was obtained for culture; no pathogenic organisms could be isolated. He subsequently had no symptoms for several months. In November 2004, he was taken to an urgent-care facility after a 2-day history of diarrhea and vomiting and was hospitalized for 3 days.

Stool specimens for culture yielded S. Pomona, with a PFGE pattern indistinguishable from those of the three patient isolates and turtle water obtained in cases 1,2, and 3 when using one enzyme (XbaI) and with a two-band difference when using a second enzyme (BlnI). Despite negative cultures of stool specimens obtained 1 month after hospital discharge, the child continued to have occasional loose, mucoid stools as of January 2005.

An epidemiologic investigation by WDPH determined that the family had purchased a small turtle from a souvenir shop during a vacation to south-central Wisconsin in late July 2004; the mother could not recall the name of" the store. A week after the first hospitalization, the boy heard media coverage about a link between a pet turtle and an iii child. Consequently, the boy released the turtle into a neighborhood creek. Thus, neither the turtle nor its habitat were available for testing.

Public Health Response. In July 2004, WDPH began receiving reports that small turtles were being sold or given away with purchase in several tourist destinations in Wisconsin. WDPH sent a letter to all local health departments on August 5 to alert them to this potential health threat and asked local public health officials to stop the distribution of turtles in their jurisdictions. Local health officers were also asked to determine whether patients with salmonellosis had any contact with reptiles, specifically turtles, and to provide education for reptile owners. WDPH subsequently learned that at least six souvenir shops in four Wisconsin counties were distributing turtles. The public health alert and subsequent media coverage yielded at least three cases (including case 4) of Salmonella infection reported in young children who had recently purchased small turtles at Wisconsin tourist destinations. The two most recent cases had onset dates in February 2005 and are under investigation.

When PFGE analysis indicated that patterns from the patient and turtle isolates associated with the first three Wisconsin cases were indistinguishable, WDPH issued a press release on August 18, 2004, that identified the link between human cases of disease and contact with pet turtles. The release also provided information on safe handling of these animals and suggested options for surrendering the turtles if owners chose not to keep them.

Once informed of the FDA ban by local health departments, most Wisconsin retailers immediately discontinued selling small turtles, including stores A and B. One retailer refused to comply, stating that his turtles were free of Salmonella and that he was distributing them for educational purposes only, which was permissible under the FDA ban. The retailer produced a report from a private laboratory indicating that cultures of cloacal swabs obtained from 60 of a source batch of 10,000 turtles were negative for Salmonella; the retailer claimed to be distributing turtles that originated solely from this batch. Local health officials informed the retailer that, because of the intermittent nature of bacterial shedding, the results did not ensure that all of the turtles were free of Salmonella and that their distribution was illegal, regardless of their carrier status. The retailer refused to comply with the order from the local health department and continued to distribute the animals. WDPH issued an emergency order on August 19 directing him to terminate any public distribution of small turtles.

The retailer contacted a laboratory that agreed to test the turtles and submitted samples from six of his turtles. Cloacal swabs from one turtle yielded a mixture of S. Pomona and S. enterica serotype IIIb 60:r:z (subspecies diarizonae); only S. IIIb 60:r:z was isolated from the other five turtles. PFGE analysis of the 3". Pomona isolate yielded a one-band difference using the first enzyme (XbaI) and was indistinguishable from the second enzyme (BlnI) pattern of cases 1, 2, and 3. The retailer stopped distributing turtles on August 24 and returned the remaining animals to the supplier.

When specimens from the patient in case 4 were tested in November 2004, the banding pattern of the PFGE supported an epidemiologic link among all four patients. Although slight differences existed in the banding pattern between this last patient and the cloacal sample from the turtle, epidemiologic and laboratory evidence supported the conclusion that the illnesses in all four cases were the result of contact with turtles.

Wyoming

Case 1. In July 2004, a woman aged 80 years from central Wyoming visited her health-care provider with a 5-day history of fever, severe diarrhea, and increased urinary frequency. Cultures of urine, feces, and blood all yielded S. enterica sero-type Typhimurium. The patient was hospitalized for 5 days, then discharged to a transitional care unit for an additional 9 days. She received intravenous (IV) antibiotics for 10 days during her stay in the hospital and transitional care unit. At the time of discharge, her condition had improved.

Investigation by the Casper-Natrona County Health Department (CNCHD) determined that the woman lived with her daughter and the extended family owned a turtle, but the woman had no known direct contact with the turtle. However, the turtle bowl was cleaned in the family kitchen sink. Cultures of environmental samples obtained from the turtle habitat grew S. Typhimurium. PFGE patterns of environmental and patient isolates tested at the Wyoming Public Health Laboratory were indistinguishable.

Case 2. In August 2004, a boy aged 6 years from west-central Wyoming visited his health-care provider with a 3-day history of nausea, diarrhea, and vomiting. On clinical examination, he had a temperature of 102.8[degrees]F (39.3[degrees]C) and pain in the upper right abdominal quadrant. He was admitted to a community hospital, where IV fluids and antibiotics were administered. Blood cultures were negative, but a stool sample yielded S. Typhimurium.

Wyoming Department of Health staff visited the boy's home 7 days after illness onset. His mother reported that the family owned two pet turtles. The boy was allowed to handle the turtles, but his mother fed them and cleaned their aquarium because she was aware of the risk for Salmonella infection.

Specimens for culture were obtained from the turtles and their living environment. All samples yielded S. Typhimurium and were indistinguishable from the patient's sample by PFGE. The samples did not match the patterns of those from case 1.

Both turtles had been purchased from the same pet store (store C), which had been contacted by CNCHD on two previous occasions regarding its illegal sale of turtles. The pet store informed CNCHD that the turtles were being used solely for educational purposes. After investigating the two cases of human salmonellosis, CNCHD confiscated the remaining turtles from store C. CNCHD publicized this event to discourage future sales of small turtles and to inform the public about the risk for salmonellosis. The Wyoming Department of Health plans to mail an informational packet about reptiles and Salmonella to all pet stores in the state in summer 2005.

Editorial Note: Salmonella infections usually result in a mild, self-limiting gastroenteritis but can also lead to severe invasive illness, such as septicemia or meningitis, especially in infants and immunocompromised persons (4). Reptiles are a well-recognized source of human salmonellosis, maintaining fecal carriage rates of Salmonella of >90% (5). Contact with reptiles and amphibians accounts for an estimated 74,000 (6%) of the approximately 1.2 million sporadic human Salmonella infections that occur annually in the United States (6).

These cases highlight the need for local health and environmental officers to be aware that illegal distribution of small turtles might be widespread. Additional sales of small turtles were reported in South Carolina and Texas in recent years. Investigators in both Wisconsin and Wyoming discovered that many retailers were aware of the FDA ban but attempted to circumvent it by giving turtles away with purchase of a turtle habitat or by claiming that turtles were being distributed for educational purposes only. Although the FDA ban does have an exemption for bona fide scientific, educational (i.e., sale to an educational institute or organization, not to a family for a child's educational benefit), or exhibitional purposes, other than use as pets, verifiable documentation of such use must be associated with the sale. Furthermore, the auction or raffle of turtles over the Internet or five distribution of turtles with purchase of a turtle habitat constitute instances of sale, offering for sale, or offering for public distribution. Such practices are banned under 21 CFR 1240.62 (2).

Successful management of turtle-associated salmonellosis requires public health investigations to incorporate laboratory, epidemiologic, environmental health, and policymaking components. When investigating cases of salmonellosis, health officials should consider patient contact with reptiles and take action to ensure that vendors and stores do not distribute small turtles illegally. Additional information about safe ownership of reptiles is available at http://www.cdc.gov/healthypets/animals/reptiles.

Acknowledgments

This report is based, in part, on contributions by C Fallin, MD, R Barnes, MD, Fremont County Pediatric and Allergy Clinic, Lander; J Swederberg, MD, Wyoming Medical Center, Casper, Wyoming.

References

(1.) Lamm SH, Taylor a Jr, Gangarosa EJ, et al. Turtle-associated salmonellosis. I. An estimation of the magnitude of the problem in the United States, 1970-1971. Am J Epidemiol 1972;95:511-7.

(2.) 21 CFR 1240.62. Turtles intrastate and interstate requirements. Available at http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFR Search.cfm? FR=1240.62.

(3.) Cohen ML, Potter M, Pollard R, Feldman RA. Turtle-associated salmonnellosis in the United States: effect of public health action, 1970 to 1976. JAMA 1980;243:1247-9.

(4.) CDC. Reptile-associated salmonellosis--selected states, 1994-1995. MMWR 1995;44:347-50.

(5.) Chiodini RJ, Sundberg JP. Salmonellosis in reptiles: a review. Am J Epidemiol 1981;113:494-9.

(6.) Mermin J, Hoar B, Angulo FJ. Iguanas and Salmonella marina infection in children: a reflection of the increasing incidence of reptile-associated salmonellosis in the United States. Pediatrics 1997:99: 399-402.

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