Multistate Outbreak of Human
Salmonella Infections Associated
with Exposure to Turtles --- United States, 2007--2008
Turtles and other reptiles have long been recognized as a source of human
Salmonella infections (
1). To prevent
Salmonella infections in humans, the sale and distribution of small turtles (i.e., those with a carapace length
of less than 4 inches) (Figure 1)
has been prohibited in the United States since 1975.* Despite this
prohibition, small turtles remain available to the public from various
sources, including pet shops, flea markets, street vendors, and
Internet websites (
2,3). In October 2007, the North Carolina Division of Public Health (NCDPH) notified CDC
of human infections caused by
Salmonella serotype Paratyphi B L (+) tartrate (+)
Salmonella Paratyphi B var. Java) in several states.
Salmonella Paratyphi B var. Java is a nontyphoidal strain of
Salmonella Paratyphi B var. Java
infections, with the first reported illness onset occurring on May 4, 2007. Many
of these infections have occurred in young children and have been associated with exposure to small turtles. Prohibiting
the sale and distribution of small turtles likely remains the most effective public health
action to prevent turtle-associated salmonellosis.
that causes gastroenteritis.
This report describes the results of the epidemiologic and laboratory investigation conducted by CDC and state and
local health departments during October 2007--January
2008. The findings document an ongoing, multistate outbreak
Detection of the Outbreak
On August 31, 2007, a girl aged 13 years visited a South Carolina hospital emergency department, where
she reported a 5-day history of bloody diarrhea, abdominal cramps, fever, and vomiting. She was treated with
trimethoprim-sulfamethoxazole and intravenous fluids but was not hospitalized. Her illness resolved in 7 days. A stool
Salmonella Paratyphi B var. Java. Also on August 31, a girl aged 15 years was admitted to a North
Carolina hospital with acute renal failure and a 4-day history of bloody diarrhea, abdominal cramps, fever, and vomiting. She
was hospitalized for 8 days and recovered fully. A joint investigation by NCDPH and the South Carolina Department
of Health and Environmental Control revealed that, on August 24, the two girls had swum in an unchlorinated,
in-ground swimming pool belonging to the family of the older girl. Two pet turtles belonging to the family also were permitted
to swim in the pool. The turtles, both of which had carapace lengths of less than 4 inches, had been purchased
recently from a pet shop in South Carolina. A water
sample collected from the turtle habitat yielded
XbaI pattern indistinguishable by pulsed-field gel electrophoresis (PFGE) from the isolates of the
younger girl. Stool specimens were not collected from the older girl.
Paratyphi B var. Java with an
On October 5, NCDPH informed
PulseNet† that tests of isolates from three other persons revealed
Salmonella Paratyphi B var. Java with an
XbaI pattern indistinguishable from the isolates of the younger girl and the turtle
habitat (defined as the outbreak strain). On October 5, in response to a request issued by NCDPH through PulseNet,
several other state health departments reported human
Salmonella Paratyphi B var. Java isolates with an
XbaI pattern indistinguishable from the outbreak strain. The
Ohio Department of Health provided further evidence of a
turtle-associated outbreak by reporting that isolates indistinguishable
from the outbreak strain had been obtained from a patient with exposure
to a small turtle during the week before illness onset, from that
patient's pet turtle, and from water collected from the turtle's
After NCDPH contacted CDC on October 23 about the possible cluster of
Salmonella Paratyphi B var.
Java infections, CDC and state and local health departments
initiated a multistate investigation to determine
the extent of the outbreak and the sources of infection. A case was defined as a diarrheal illness with onset after May
1, 2007, in a person from whom a clinical specimen yielded
Salmonella Paratyphi B var. Java with a PFGE
XbaI pattern indistinguishable from the outbreak strain; cases were identified by a review of all PFGE-typed isolates in the
As of January 18, 2008, a total of 103 cases with isolates indistinguishable from the outbreak strain had
been reported to CDC from 33 states (Figure 2). Information initially was collected from general enteric
questionnaires administered by state and local health departments. Of the 100 patients for whom age information
was available (median age: 7.5 years; range: <1--87 years), 56 (56%) were aged
<10 years. Fifty-two (51%) of the 101 patients for whom the
sex was known were female. Illness onset dates ranged from May 4, 2007,
to December 15, 2007 (Figure 3). Among the 78 patients for whom clinical information was available, 51 (65%) reported bloody
diarrhea, with a median duration of illness of 7 days; 24 (30%) of the 80 patients for whom hospitalization status was
known were hospitalized for their illnesses, with a median duration of 4 days. Among the 80 patients questioned about
turtle exposure, 47 (59%) reported turtle exposure during the 7 days before illness onset. No deaths were reported.
A case-control study was conducted during November 15--December 5 using age- and
neighborhood-matched controls (age groups: <1 year, 1--9 years, 10--19 years,
years; reverse-digit dialing was used to match cases to controls by
neighborhood). A telephone questionnaire was used to determine whether
the case-patient or control had exposure to turtles, other reptiles, or
aquariums containing tropical fish during a 7-day exposure period (7
days before illness onset in the case-patient, for both cases and
matched controls). Participants who reported exposure to turtles were
asked about the nature of the exposure, including whether the patient
had touched or held the turtle, kissed the turtle or put the turtle in
his or her mouth, or come into contact with the turtle's habitat, such
as by changing the water or cleaning the cage. Participants who
reported exposure to turtles also were asked about turtle size, type,
and source. All participants were asked about their awareness of the
association between contact with reptiles and
Salmonella infection. Seventy case-patients and 45 matched controls were enrolled in the study.
Among the 70 case-patients interviewed, 44 (63%) reported
exposure to a turtle during the 7 days before illness onset, compared
with two (4%) of 45 controls (matched odds ratio [mOR] = 40.9; 95%
confidence interval [CI] = 7.0--unbounded). Two (3%) case-patients and
four (9%) controls reported exposure to a reptile other than a turtle
during the 7 days before illness onset. No other single characteristic
for which data were collected has been implicated in this outbreak.
Twelve (20%) of the 60 case-patients for whom such information was
available and 13 (29%) of the 45 controls reported awareness of the
association between contact with reptiles and
Salmonella infection (mOR = 0.66; CI = 0.27--1.6). Among the
44 case-patients exposed to a turtle, 34 (77%) were exposed at home,
and nine (20%) were exposed at the home of a friend or relative; one
(2%) was exposed outdoors. Of the 43 case-patients exposed at home or
at the home of a friend or relative, three were siblings exposed to
turtles at the home of their babysitter, and two were a husband and
wife exposed to a turtle in their own home; the remaining exposures
occurred in households independent of one another. Of 34 case-patients
exposed to turtles at home, 12 (35%) still owned the turtle at the time
of interview. Of the 42 case-patients for whom the details of the
turtle exposure were known, 28 (67%) reported holding or touching the
turtle, 24 (57%) reported feeding the turtle, and 29 (69%) reported
contact with the turtle's habitat. Four (10%) case-patients reported
kissing the turtle or having put the turtle in his or her mouth.
Thirty-seven (86%) of the 43 case-patients who were exposed to a turtle
and for whom turtle size information was available reported that the
turtle had a carapace length of less than 4 inches; the remaining
turtles involved in these exposures were reported to have carapace
lengths of 4 inches or more.
Forty-two case-patients with turtle exposure reported details about the turtle source. Fifteen (36%) reported that
the turtle was purchased at a pet shop, 10 (24%) reported that the turtle had been a gift, eight (19%) reported that
the turtle was purchased at a flea market, five (12%)
reported that the turtle was purchased from a street vendor, and
one each (2%, respectively) reported that the turtle was purchased on an Internet website, acquired from the wild,
hatched from an egg given by a relative, or purchased at a conference center event.
Salmonella Paratyphi B var. Java matching the outbreak strain
was isolated from six turtles or the water from their habitats in the
homes of case-patients in California, North Carolina, Ohio, and
Wisconsin. Investigations are ongoing to determine whether the turtles
have a common distributor or farm of origin.
D Bergmire-Sweat, MPH, North Carolina Div of Public Health. J Schlegel, MSP, C Marin, South Carolina Dept of Health
and Environmental Control. K Winpisinger, MS, Ohio Dept of Health.
C Perry, M Sotir, PhD, Div of Foodborne, Bacterial, and Mycotic Diseases,
National Center for Zoonotic, Vector-Borne, and Enteric Diseases; J Harris, PhD, EIS Officer, CDC.
This ongoing, multistate outbreak of salmonellosis is associated with small turtles purchased at
pet stores, flea markets, and other outlets, despite a federal prohibition on the sale of turtles with carapace lengths of
less than 4 inches. These turtles are a risk to the public and especially to young children. Other outbreaks of
Salmonella infections have been reported
The prohibition on the sale and distribution of small turtles was enacted in 1975, after public health
investigations demonstrated that small turtles were a major source of human
Salmonella infections, particularly in children. In 1972,
a study in New Jersey indicated that small pet turtles accounted for approximately 23% of
Salmonella infections in children
4). In 1980, the 1975 prohibition was estimated to have prevented 100,000
Salmonella infections in U.S. children each year since going into effect
5). However, this prohibition has an exception: small turtles may be
sold legally for scientific, educational or exhibition
purposes. During 2001--2006, the number of turtles kept as pets in
the United States increased 86% to nearly 2 million
6), suggesting that this exception might provide a
mechanism by which small turtles become household pets.
Turtles, like other reptiles, commonly carry
Salmonella, and fecal carriage rates can be as high as 90%
1). Small turtles sold as pets frequently come from breeding farms, where turtles are housed in crowded ponds and nesting areas
in a way that promotes
7). Attempts to treat turtles, turtle eggs, and turtle breeding ponds
with antibiotics to eliminate
7,8). Other treatments reduce but do not eliminate
8), and the turtles
that continue to shed
Salmonella shedding might be intermittent and stress
related, determining whether turtles are free of the bacteria is difficult
have not been successful and have resulted in a high prevalence of
antibiotic resistance ( shedding from turtles ( might recontaminate other turtles during rearing or shipment. Because
Direct or indirect contact with a reptile is associated with an estimated 6% of human
Salmonella infections in the United States
9). Persons coming into contact with
reptiles, reptile habitats, or surfaces contaminated with reptile
fecal matter risk infection from salmonellae shed by the reptile
(10). Although most reptiles carry
Salmonella, small turtles are likely to be handled differently than other reptiles and thus carry a greater risk of transmitting
Salmonella to children. In contrast to the obvious risk for a
bite or scratch, for example, from a snake or an iguana, a small turtle
is likely to be perceived as safe, and thus might be given directly to
small children to play with. In addition, a young child placed in
charge of caring for a turtle has direct contact with water in the
turtle habitat, where
Salmonella are likely to multiply to high numbers. Although
approximately half of the infections associated with this outbreak
occurred in young children, who are at greater risk for severe illness
2,10), several illnesses occurred in adults with
turtle exposure, demonstrating that turtle-associated
Salmonella infection is not unique to children. Additionally, only 20%
of case-patients interviewed reported awareness of the link between
Salmonella and contact with reptiles, indicating
that measures to educate the public about this link have not been successful. CDC has provided recommendations to
prevent reptile-associated salmonellosis in humans
2). However, because of the particular hazard associated with small
turtles, prohibiting the sale and distribution of small turtles likely remains the most effective public health action to
prevent turtle-associated salmonellosis.
The findings in this report are based, in part, on contributions
from R Reporter, MD, R Bagby, Los Angeles County Dept of Public Health,
A Kao, PhD, San Diego Health and Human Svcs Agency, E Cox, MPH, Long
Beach Dept of Health and Human Svcs, P Cast, San Bernardino County Dept
of Public Health, A Norman, Sacramento Dept of Health and Human Svcs, A
Kimura, MD, California Dept of Health; D Raccasi, T L'Estrange,
Weber-Morgan Health Dept, Utah Dept of Health; Missouri Dept of Health
and Senior Svcs; C Prunty, Summit County Health Dept, P Pflum, Henry
Country Health Dept, Ohio; J Tait, J Baney, CR Cook, CH Sandt, PhD,
Pennsylvania Bur of Laboratories, K Warren, MPH, Pennsylvania Dept of
Health; Y Khachadourian, T Quinlan, Wadsworth Center Laboratory, New
York, T Fitzgerald, New York City Bur of Health, E Villamil, MPH, Perry
Smith, MD, New York State Dept of Health; M Cumming, MS, B Bolstorff,
MPH, Massachussetts Dept of Public Health; S Bidol, MPH, Michigan Dept
of Community Health; and L Schaefer, South Dakota Dept of Health.
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A national molecular subtyping network for foodborne disease surveillance.
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Date last reviewed: 1/24/2008