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Turtle-Associated Salmonellosis -- Ohio

On June 6, 1986, two cases of turtle-associated salmonellosis were reported in Columbus, Ohio. A 2-year-old boy became ill with fever, abdominal pain, and bloody diarrhea 4 days after his mother had purchased a pet turtle from a local pet store. His 4-year-old brother developed similar symptoms the next day.

Stool cultures from both boys yielded Salmonella typhimurium. Following investigation by the Ohio Department of Health, S. typhimurium was isolated from the turtle and from a water sample taken from the turtle bowl in the children's home. All four isolates of S. typhimurium had the same plasmid profile. The turtle was a red-eared slider, Trachemys scripta elegans (formerly Pseudemys scripta elegans (1)), with a carapace diameter of 2 inches.

When investigators from the Food and Drug Administration and the Ohio Department of Health visited the pet store, no more turtles were available. The store owner had purchased the turtles from a local distributor who sells reptiles primarily to local universities and other institutions for scientific purposes. The invoice for the sale of the turtles to the pet store stated that the turtles were to be used for scientific purposes only.

Local health departments in Ohio were notified that turtles might be for sale illegally in their jurisdictions. No other cases of turtle-associated salmonellosis have been reported in Ohio. Reported by LK Giljahn, MPH, Infectious Disease Epidemiology Unit, TJ Halpin, MD, MPH, State Epidemiologist, Ohio Dept of Health; Food and Drug Administration; Enteric Diseases Br, Div of Bacterial Diseases, Center for Infectious Diseases, CDC.

Editorial Note

Editorial Note: Pet turtles are estimated to have caused 14% of reported cases of salmonellosis in humans in the early 1970s (2). Consequently, the interstate and intrastate commercial distribution of turtles 4 inches in carapace diameter was banned in 1975, except for bonafide scientific, educational, or exhibitional purposes (3). After this ban went into effect, turtle-associated salmonellosis in the United States became rare (4). However, pet turtles exported from the United States have been associated with human salmonellosis in the United Kingdom (5), Japan (6), and Yugoslavia (7). Recently, in Israel, aquarium cultures of pet turtles imported from the United States yielded Salmonella, and that country has temporarily banned the importation of these turtles (8). Diversion of these turtles into U.S. markets has been associated with human illness in Puerto Rico and, sporadically, in the continental United States (7). Since the importation of small turtles into the United States has long been restricted, turtles for sale in pet stores in the United States are likely to be of U.S. origin (9).

Turtles are easily infected with Salmonella from the environment and can acquire the organism in ovo or after hatching (10). Treating turtle eggs with gentamicin has been proposed as a means of producing Salmonella-free turtles (11). However, only one evaluation of this technique has been published, and the efficacy of the technique in practice has not been established. The technique may promote gentamicin resistance in Salmonella, as a similar technique has when used in treating turkey eggs (12). Furthermore, uninfected baby turtles can easily acquire Salmonella from other turtles or from the environment after hatching. Turtles also harbor Campylobacter, Aeromonas, and other potential pathogens (13,14). They are not appropriate pets for small children.

Prompt investigation of turtle-associated salmonellosis can prevent further illness. It is particularly important to determine the origin and distribution of the turtles, whether they were hatched from gentamicin-treated eggs, and whether they carry Salmonella. Clinicians who encounter cases of turtle-associated salmonellosis are encouraged to report them to local and state public health officials, who, along with Food and Drug Administration officials, can investigate the cases and enforce the law.

References

  1. Seidel ME, Smith HM. Chrysemys, Pseudemys, Trachemys (Testudines: Emydidae): did Agassiz have it right? Herpetologica 1986;42:242-8.

  2. 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.

  3. 21 Code of Federal Regulations S1240.62 (1986).

  4. Cohen ML, Potter M, Pollard R, Feldman RA. Turtle-associated salmonellosis in the United States: effect of Public Health Action. JAMA 1980;243:1247-9.

  5. Anonymous. Reptilian salmonellosis . Lancet 1981;2:120-31.

  6. Fujita K, Murono K, Yoshioka H. Pet-linked salmonellosis (Letter). Lancet 1981;2:525.

  7. Tauxe RV, Rigau-Perez JG, Wells JG, Blake PA. Turtle-associated salmonellosis in Puerto Rico: hazards of the global turtle trade. JAMA 1985;254:237-9.

  8. Chassis G, Gross EM, Greenberg Z, et al. Salmonella in turtles imported to Israel from Louisiana (Letter). JAMA 1986;256:1003.

  9. 42 Code of Federal Regulations S71.52 (1985).

  10. Kaufmann AF, Fox MD, Morris GK, et al. Turtle-associated salmonellosis: 3. the effects of environmental Salmonellae in commercial turtle breeding ponds. Am J Epidemiol 1972;95:521-8.

  11. Michael-Marler S, Brown ML, Siebeling RJ. Eradication of Arizona hinshawii from artificially infected turtle eggs. Appl Environ Microbiol 1983;45:748-54.

  12. Hirsh DC, Ikeda JS, Martin LD, Kelly BJ, Ghazikhanian GY. R Plasmid-mediated gentamicin resistance in Salmonellae isolated from turkeys and their environment. Avian Dis 1983;27:766-72.

  13. McCoy RH, Siedler RJ. Potential pathogens in the environment: isolation, enumeration, and identification of seven genera of intestinal bacteria associated with small green pet turtles. Appl Microbiol 1973;25:534-8.

  14. Harvey S, Greenwood JR. Isolation of Campylobacter fetus from a pet turtle. J Clin Microbiol 1985;21:260-1.

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