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
Seidel ME, Smith HM. Chrysemys, Pseudemys, Trachemys
(Testudines: Emydidae): did Agassiz have it right?
Herpetologica 1986;42:242-8.
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.
21 Code of Federal Regulations S1240.62 (1986).
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.
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.
Chassis G, Gross EM, Greenberg Z, et al. Salmonella in turtles
imported to Israel from Louisiana (Letter). JAMA
1986;256:1003.
42 Code of Federal Regulations S71.52 (1985).
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.
Michael-Marler S, Brown ML, Siebeling RJ. Eradication of
Arizona
hinshawii from artificially infected turtle eggs. Appl Environ
Microbiol 1983;45:748-54.
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.
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.
Harvey S, Greenwood JR. Isolation of Campylobacter fetus from
a
pet turtle. J Clin Microbiol 1985;21:260-1.
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