Published Date: 2008-01-25 13:00:14
Subject: PRO/AH/EDR> Salmonellosis, human, pet turtles - USA
Archive Number: 20080125.0317
SALMONELLOSIS, HUMAN, PET TURTLES - USA
A ProMED-mail post
ProMED-mail is a program of the
International Society for Infectious Diseases
 Outbreak of turtles-associated serotype Paratyphi var Java
 Domestic Pet Turtle Equality Act
 Outbreak of turtles-associated serotype Paratyphi var Java
Date: Thu 24 Jan 2008
Source: Morbid Mortal Weekly Rep 2008;57: 69-72 [edited]
Salmonella Infections Associated with Exposure to Turtles - USA, 2007-2008
Turtles and other reptiles have long been recognized as a source of
human _Salmonella_ infections (1). To prevent turtle-associated
_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 [the figures can be seen on the original URL - Mod.LL]) 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 the Centers for Disease Control and Prevention (CDC) of
human infections caused by _Salmonella [enterica_] serotype Paratyphi
B L (+) tartrate (+) (_Salmonella_ Paratyphi B var. Java) in several
states. Serotype Paratyphi B var. Java is a nontyphoidal strain of
_Salmonella_ that causes gastroenteritis. This report describes the
results of the epidemiologic and laboratory investigation conducted
by the CDC and state and local health departments during October
2007-January 2008. The findings document an ongoing, multistate
outbreak of _S._ Paratyphi B var. Java infections, with the 1st
reported illness onset occurring on 4 May 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.
Detection of the outbreak
On 31 Aug 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
specimen yielded _S._ Paratyphi B var. Java. Also on 31 Aug 2007, 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 24 Aug 2007, the 2 girls had swum in an unchlorinated,
in-ground swimming pool belonging to the family of the older girl. 2
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
_S._ Paratyphi B var. Java with an _Xba_I pattern indistinguishable
by pulsed-field gel electrophoresis (PFGE) from the isolates of the
younger girl. Stool specimens were not collected from the older girl.
On 5 Oct 2007, NCDPH informed PulseNet (a national molecular
subtyping network for foodborne disease surveillance) that tests of
isolates from 3 other persons revealed _S._ Paratyphi B var. Java
with an _Xba_I pattern indistinguishable from the isolates of the
younger girl and the turtle habitat (defined as the outbreak strain).
On 5 Oct 2007, in response to a request issued by NCDPH through
PulseNet, several other state health departments reported human _S._
Paratyphi B var. Java isolates with an _Xba_I 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 habitat.
After NCDPH contacted CDC on 23 Oct 2007 about the possible cluster
of turtle-associated _S._ 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 1 May 2007, in a person from whom a clinical specimen yielded
_S._ Paratyphi B var. Java with a PFGE _Xba_I pattern
indistinguishable from the outbreak strain; cases were identified by
a review of all PFGE-typed isolates in the PulseNet database.
As of 18 Jan 2008, a total of 103 cases with isolates
indistinguishable from the outbreak strain had been reported to CDC
from 33 states (Figure 2 [for the figure, see the orginal URL -
Mod.LL]). Information initially was collected from general enteric
disease questionnaires administered by state and local health
departments. Of the 100 patients for whom age information was
available (median age: 7.5 years; range: less than 1-87 years), 56
(56 percent) were aged less than 10 years. 52 (51 percent) of the 101
patients for whom the sex was known were female. Illness onset dates
ranged from 4 May 2007, to 15 Dec 2007 (Figure 3 [for figure, see
original URL - Mod.LL]). Among the 78 patients for whom clinical
information was available, 51 (65 percent) reported bloody diarrhea,
with a median duration of illness of 7 days; 24 (30 percent) 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
percent) reported turtle exposure during the 7 days before illness
onset. No deaths were reported.
A case-control study was conducted during 15 Nov 2007 Nov-5 Dec 2007
using age- and neighborhood-matched controls (age groups: less than 1
year, 1-9 years, 10-19 years, 20-49 years, 50 years or older;
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
A total of 70 case-patients and 45 matched controls were enrolled in
the study. Among the 70 case-patients interviewed, 44 (63 percent)
reported exposure to a turtle during the 7 days before illness onset,
compared with 2 (4 percent) of 45 controls (matched odds ratio (mOR)
= 40.9; 95 percent confidence interval (CI) = 7.0 unbounded). 2 (3
percent) case-patients and 4 (9 percent) 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. 12 (20 percent) of the 60
case-patients for whom such information was available and 13 (29
percent) 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 percent) were exposed at home, and 9 (20 percent) were exposed at
the home of a friend or relative; 1 (2 percent) was exposed outdoors.
Of the 43 case-patients exposed at home or at the home of a friend or
relative, 3 were siblings exposed to turtles at the home of their
babysitter, and 2 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 percent) 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 percent) reported holding or touching the
turtle, 24 (57 percent) reported feeding the turtle, and 29 (69
percent) reported contact with the turtle's habitat. 4 (10 percent)
case-patients reported kissing the turtle or having put the turtle in
his or her mouth. 37 (86 percent) 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.
42 case-patients with turtle exposure reported details about the
turtle source. 15 (36 percent) reported that the turtle was purchased
at a pet shop, 10 (24 percent) reported that the turtle had been a
gift, 8 (19 percent) reported that the turtle was purchased at a flea
market, 5 (12 percent) reported that the turtle was purchased from a
street vendor, and 1 each (2 percent, 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. _S._ Paratyphi B var. Java matching the outbreak strain
was isolated from 6 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.
[Byline: Bergmire-Sweat D, Schlegel J, Marin C, et al.]
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
turtle-associated salmonellosis have been reported (2,3).
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 percent of
_Salmonella_ infections in children (4). In 1980, the 1975
prohibition was estimated to have prevented 100 000 Salmonella
infections in American 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 USA
increased 86 percent to nearly 2 million turtles (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 percent (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
_Salmonella_ transmission (7). Attempts to treat turtles, turtle
eggs, and turtle breeding ponds with antibiotics to eliminate
_Salmonella_ have not been successful and have resulted in a high
prevalence of antibiotic resistance (7,8). Other treatments reduce
but do not eliminate shedding from turtles (8), and the turtles that
continue to shed might recontaminate other turtles during rearing or
shipment. Because shedding might be intermittent and stress related,
determining whether turtles are free of the bacteria is difficult (1).
Direct or indirect contact with a reptile is associated with an
estimated 6 percent of human salmonellosis in the USA (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 salmonellae 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 from salmonellosis (2,10), several illnesses
occurred in adults with turtle exposure, demonstrating that
turtle-associated salmonellosis is not unique to children.
Additionally, only 20 percent of case-patients interviewed reported
awareness of the link between salmonellosis 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
1. Chiodini RJ, Sundberg JP: Salmonellosis in reptiles: a review. Am
J Epidemiol 1981;113: 494-99.
2. CDC: Turtle-associated salmonellosis in humans--United States,
2006--2007. MMWR 2007;56: 649-52.
3. CDC: Salmonellosis associated with pet turtles--Wisconsin and
Wyoming, 2004. MMWR 2005;54: 223-26.
4. Lamm S, Taylor A, Gangarosa E, 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: 511-17.
5. Cohen ML, Potter M, Pollard R, Feldman RA: Turtle-associated
salmonellosis in the United States: effect of public health action,
1970 to 1976. JAMA 1980;243: 1247-79.
6. American Veterinary Medical Association: U.S. pet ownership and
demographics sourcebook. Schaumburg, IL: American Veterinary Medical
7. D'Aoust JY, Daley E, Crozier M, Sewell AM: Pet turtles: a
continuing international threat to public health. Am J Epidemiol
8. Mitchell MA, Adamson T, Singleton C, et al: Evaluation of a
combination of sodium hypochlorite and polyhexamethylene biguanide as
an egg wash for red-eared slider turtles (Trachemys scripta elegans)
to suppress or eliminate Salmonella organisms on egg surfaces and in
hatchlings. Am J Vet Res 2007;68: 158-64.
9. Mermin J, Hutwagner L, Vugia D, et al: Reptiles, amphibians, and
human Salmonella infection: a population-based, case-control study.
Clin Infect Dis 2004;38: S253-61.
10. 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
[From a recent post on a foodborne outbreak of the organism
originating in Eurosurvelliance (Salmonellosis, serotype Paratyphi
var Java - Europe 20071221.4100):
"_Salmonella_ Paratyphi B and Java are biovars of common serotype
1,4,, 12:b:1,2 which respectively cause human paratyphoid fever
and gastroenteritis. The d-tartrate fermenting variant _S. enterica_
subspecies _enterica_ serovar Paratyphi B dT+ (formerly called _S._
Java) is thought to be less virulent to humans than the non
d-tartrate fermenting variant, although cases of invasive infection
have been reported. _S._ Java is a complex organism with a range of
genetically distinct clonal lineages. Unlike 'classical' _S._
Paratyphi B, _S._ Java has an animal reservoir and has caused
substantive outbreaks as a result of the contamination of food products."
As a reminder regarding nomenclature, _Salmonella_ as a genus has 2
species, _enterica_ and _bongori_. _S. enterica_ is divided into 6
subspecies: _enterica_, _salamae_, _arizonae_, _diarizonae_,
_houtenae_ and _indica_. _S. enterica_ subspecies _enterica_ (or
subspecies I) strains are the ones usually isolated from humans or
warm-blooded animals and represent a majority of the salmonellas that
are clinically important.
The designation _Salmonella_ I 1,4,, 12:b:1,2 means:
- the "I" reflects subspecies _enterica_;
- the "1, 4, " are the O (or somatic) antigens associated with
- the nomenclature after the colon, in this case b:1,2, reflect the
flagellar or H antigens. It is these H antigens that define the
serotype identity within an individual group of salmonellae.
Given the continuing risk of human salmonellosis directly linked to
these small turtles as reflected in this CDC-originated posting, it
seems odd that the following posting about a potential repeal of the
ban appeared recently. No mention of this is found in the CDC report. - Mod.LL]
 Domestic Pet Turtle Equality Act
Date: Mon 7 Jan 2008
Source: Natchez (MS) Democrat [edited]
For the first time since 1975, selling small pet turtles is legal.
The transmission of turtles smaller than 10.2 centimeters in
diameter, whether by sale or donation, has been illegal for the last
31 years because of the risk they might transfer _Salmonella_, a
bacterium the turtles transfer to humans that causes illness. But
since then farmers have developed ways to ensure the reptiles are
salmonella free, and the U.S. Farm Bill passed in December 2007 had
an amendment that repealed the tiny turtle ban.
American Senator David Vitter and Representative Rodney Alexander
sponsored the turtle amendment. The Farm, Nutrition and Bioenergy Act
of 2007 (H.R. 2419) that included the amendment passed 79-14.
The farming process begins when the turtles come out of hibernation
in the spring. Once the turtles start to lay their eggs on the levees
around the turtle ponds, the eggs are gathered daily, and all dirt is
removed from the eggs before they are soaked for 10 minutes in a
water and Clorox solution. After that, they are cleaned in a commercial washer.
Once washed, the eggs are placed in a special vacuum tank to
eradicate any _Salmonella_. After that, they are placed in incubation
trays until they hatch, at which time a state veterinarian certifies
they are salmonella free.
[The portion of the bill (H.R. 2419, Food and Energy Security Act of
2007 (<http://www.opencongress.org/bill/110-h2419/show>) dealing with
the turtle issue is displayed below. The wording does not immediately
prohibit the ban but rather seems to try establish more current
prevalence rates of salmonellosis in turtles as well as other
reptiles and amphibians as a way of prohibiting the ban. Neither does
the amendment reflect the issues of difficulty in maintaining
_Salmonella_-free turtles nor does it look to understand that the
increased risk of salmonellosis associated with small turtles in
children exists because the turtles can be more easily handled. This
moderator does not wish to discriminate against little turtles but
hopefully, more rational heads will prevail and the ban despite
difficulties in enforcement will remain. - Mod.LL]
"Subtitle C--DOMESTIC PET TURTLE MARKET ACCESS
SEC. 11101. SHORT TITLE.
This title may be cited as the 'Domestic Pet Turtle Equality Act'.
SEC. 11102. FINDINGS.
Congress makes the following findings:
(1) Pet turtles less than 10.2 centimeters in diameter have been
banned for sale in the United States by the Food and Drug
Administration since 1975 due to health concerns.
(2) The Food and Drug Administration does not ban the sale of
iguanas or other lizards, snakes, frogs, or other amphibians or
reptiles that are sold as pets in the United States that carry
salmonella bacteria. The Food and Drug Administration also does not
require that these animals be treated for salmonella bacteria before
being sold as pets.
(3) The technology to treat turtles for salmonella, and make them
safe for sale, has greatly advanced since 1975. Treatments exist that
can eradicate salmonella from turtles up until the point of sale, and
individuals are more aware of the causes of salmonella, how to treat
salmonella poisoning, and the seriousness associated with salmonella poisoning.
(4) University research has shown that these turtles can be treated
in such a way that they can be raised, shipped, and distributed
without having a recolonization of salmonella.
(5) University research has also shown that pet owners can be
equipped with a treatment regimen that allows the turtle to be
maintained safe from salmonella.
(6) The Food and Drug Administration and the Department of
Agriculture should allow the sale of turtles less than 10.2
centimeters in diameter as pets as long as the sellers are required
to use proven methods to treat these turtles for salmonella.
SEC. 11103. REVIEW, REPORT, AND ACTION ON THE SALE OF BABY TURTLES.
(a) Pet Turtle- In this section, the term 'pet turtle' means a
turtle that is less than 10.2 centimeters in diameter.
(b) Prevalence of Salmonella -- Not later than 60 days after the
date of enactment of this title, the Secretary of Health and Human
Services, acting through the Commissioner of Food and Drugs, shall
determine the prevalence of salmonella in each species of reptile and
amphibian sold legally as a pet in the United States in order to
determine whether the prevalence of salmonella in reptiles and
amphibians sold legally as pets in the United States on average is
not more than 10 percent less than the percentage of salmonella in pet turtles.
(c) Action if Prevalence Is Similar -- If the prevalence of
salmonella in reptiles and amphibians sold legally as pets in the
United States on average is not more than 10 percent less than the
percentage of salmonella in pet turtles --
(1) the Secretary of Agriculture shall --
(A) conduct a study to determine how pet turtles can be sold safely
as pets in the United States and provide recommendations to Congress
not later than 150 days after the date of such determination;
(B) in conducting such study, consult with all relevant
stakeholders, such as the Centers for Disease Control and Prevention,
the turtle farming industry, academia, and the American Academy of
(C) examine the safety measures taken to protect individuals from
salmonella-related dangers involved with reptiles and amphibians sold
legally in the United States that contain a similar or greater
presence of salmonella than that of pet turtles; and
(2) the Secretary of Agriculture --
(A) may not prohibit the sale of pet turtles in the United States; or
(B) shall prohibit the sale in the United States of any reptile or
amphibian that contains a similar or greater prevalence of salmonella
than that of pet turtles."