Customize your JAMA Network experience by selecting one or more topics from the list below.
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
Case 1. While vacationing with her family in
Wisconsin in late July 2004, a Kansas girl aged 4 years was taken to anemergency
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
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 ill 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 S. 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.
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 serotype
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°F (39.3°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.
Reported by: B Salna, MS, Columbia County Div
of Health, Portage; T Monson, MS, T Kurzynski, MS, K Gundlach, Wisconsin State
Laboratory of Hygiene; PE Fox, DVM, J Kazmierczak, DVM, M Wegner, MD, JP Davis,
MD, Wisconsin Dept of Health and Family Svcs. R Harrington, MS, M Dowell,
MD, R Heald, Casper-Natrona County Health Dept, Casper; R Harris, PhD, W Manley,
MS, Wyoming Public Health Laboratory; J Snow, DVM, A Heryford, MS, S Seys,
MPH, Wyoming Dept of Health.
CDC 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 free 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
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.
Salmonellosis Associated With Pet Turtles—Wisconsin and Wyoming,
2004. JAMA. 2005;293(15):1850–1853. doi:10.1001/jama.293.15.1850