SALMONELLOSIS, SEROTYPE TYPHIMURIUM - USA: FROGS, 2009
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International Society for Infectious Diseases
Date: Thu 7 Jan 2010
Source: Morbidity Mortality Weekly Report 2010;58: 1433-1436 [edited]
During April-July 2009, the Utah Department of Health identified 5
cases of _Salmonella [enterica_ serotype] Typhimurium infection with
indistinguishable pulsed-field gel electrophoresis (PFGE) patterns,
predominantly among children. In August 2009, the Centers for Disease
Control and Infection (CDC) began a multistate outbreak investigation
to determine the source of the infections. This report summarizes the
results of this ongoing investigation, which, as of 30 Dec 2009, had
identified 85 _S._ Typhimurium human isolates with the outbreak
strain from 31 states.
In a multistate case-control study, exposure to frogs was found to be
significantly associated with illness (63 percent of cases versus 3
percent of controls; matched odds ratio = 24.4). Among 14
case-patients who knew the type of frog, all had exposure to an
exclusively aquatic frog species, the African dwarf frog.
Environmental samples from aquariums containing aquatic frogs in 4
homes of case-patients yielded _S._ Typhimurium isolates matching the
outbreak strain. Preliminary traceback information has indicated
these frogs likely came from the same breeder in California. Reptiles
(e.g., turtles) and amphibians (e.g., frogs) have long been
recognized as Salmonella carriers (1,2), and 3 multistate outbreaks
of human Salmonella infections associated with turtle contact have
occurred since 2006 (3,4). However, this is the 1st reported
multistate outbreak of Salmonella infections associated with
amphibians. Educational materials aimed at preventing salmonellosis
from contact with reptiles should be expanded to include amphibians,
such as aquatic frogs.
The 5 cases identified in July 2009 by the Utah Department of Health
all had isolates indistinguishable by pulsed field gel
electrophoresis and were identified with XbaI pattern JPXX01.0177.
The cases had occurred during April-July 2009. On 29 Sep 2009,
PulseNet, the national molecular subtyping network for foodborne
disease surveillance, identified a national increase of isolates with
this PFGE pattern (37 isolates from 19 states in 60 days).
Multiple-locus variable-number tandem repeat analysis (MLVA) provided
additional discrimination of the outbreak strain. For this
investigation, a case was defined as _S._ Typhimurium infection with
illness onset on or after 1 Apr 2009, with 1) PFGE pattern
indistinguishable from the cluster-defining pattern and 2) MLVA
pattern either matching that of the main outbreak strain, or MLVA unknown.
The multistate investigation began with in-depth, open-ended
interviews of salmonellosis patients regarding exposures in the week
before illness onset. A total of 11 interviews with patients were
conducted through November 2009. All 11 persons reported consumption
of cheese-flavored crackers; 8 reported exposure to aquatic animals,
including fish and aquatic frogs.
As of 30 Dec 2009, _S._ Typhimurium isolates with the outbreak strain
had been identified in 85 patients from 31 states, extending from
Massachusetts to California, with week of illness onset ranging from
22 Mar to 29 Nov 2009 (Figure 1 [for figures, use original URL -
Mod.LL]). Among the patients, 52 percent were male; median age was 5
years (range: 3 weeks-54 years), and 79 percent were aged less than
10 years. Among 47 patients with outcome information available, 16
(34 percent) had been hospitalized; no deaths were reported.
To examine possible associations between illness and consumption of
cheese crackers and exposure to aquatic pets, the CDC conducted a
nationwide case-control study during 30 Nov-7 Dec 2009. Patients
infected with _S._ Typhimurium with the outbreak strain who had
specimen collection dates after 15 Jul 2009 were enrolled. Controls
were persons with recent infection of Salmonella strains other than
the outbreak strain and matched to case-patients by age and county of
residence. Exposure histories were collected for 7 days before
illness onset for case-patients and for 7 days before interview for controls.
Investigators sought to match each case-patient with 2 controls. A
total of 19 case-patients (18 with stool specimens and one with a
urine specimen) and 31 matching controls were enrolled from 15
states. Case-patients were found to be significantly more likely than
controls to have had exposure to an aquatic pet, including fish and
frogs (74 percent of case-patients versus 35 percent of controls; mOR
= 4.7 and 95 percent confidence interval (CI) = 1.2-27.0). More
specifically, illness was found to be associated with exposure to
frogs (63 percent of case-patients versus 3 percent of controls; mOR
= 24.4 and CI = 4.0-infinity]). Exposure to fish was not
statistically significant (58 percent of case-patients versus 29
percent of controls, mOR = 3.1 and CI = 0.8--14.2). No association
was found between illness and consumption of any food item, including
Among 39 patients interviewed as of 9 Dec 2009, including some of the
19 case-patients enrolled in the case-control study, 14 knew the type
of frog involved in their exposure, and all 14 identified the frog as
an African dwarf frog (Figure 2). When asked about potential for
Salmonella infection, 19 of 36 (53 percent) patients reported
awareness of association between contact with reptiles and Salmonella
infection, but only 11 of 36 (31 percent) reported awareness of
association with amphibians. Among 20 patients from whom the
information was available, the frog's aquarium was cleaned in the
kitchen sink in the homes of 6 persons (30 percent) and in the
bathroom sink in the homes of 7 others (35 percent).
Environmental Testing and Traceback
Environmental samples taken from patient homes in 4 states yielded
the outbreak strain of _S._ Typhimurium. The Colorado Department of
Public Health obtained matched isolates from 2 African dwarf frogs,
and from a rock and water in the aquarium containing the 2 frogs. The
New Mexico Department of Health matched the outbreak strain with
isolates from the filtration system, gravel, and water from an
aquarium in a patient's home containing fish and a small water frog.
The Ohio Department of Health matched the outbreak strain with
isolates from a patient's deceased African dwarf frog, its water, and
the lid and edge of its aquarium. The Utah Department of Health
obtained matched isolates from a container used to clean African
dwarf frogs in a patient's home.
Traceback investigations of frogs associated with positive
environmental isolates have been completed. African dwarf frogs from
the homes of the Colorado patient and the Utah patient were prizes
from games at 2 different carnivals. The vendor who distributed the
frogs to both carnivals was from Utah and identified the source as a
breeder in California. Environmental sampling from the vendor's home
(of aquarium filters and skin previously shed from African dwarf
frogs) yielded multiple isolates matching the outbreak strain. The
aquatic frog from the home of the New Mexico patient was purchased
from a pet store chain, whose distributor identified the same breeder
as the source for all of its aquatic frogs. The family of the Ohio
patient purchased its African dwarf frog from a department store,
whose distributor identified the breeder as the ultimate source of its frogs.
Environmental sampling from the breeder's California facility yielded
_S._ Typhimurium isolates matching the outbreak strain. Positive
samples were collected from multiple locations in the facility,
including water tanks that contained African dwarf frogs and gravel
in the water filtration system.
[Byline: Hall J, Poulson M, Fawcett L, et al]
Salmonella illness remains a major public health problem in the USA,
with an estimated 1.4 million human Salmonella infections, 15 000
hospitalizations, and 400 deaths annually (5). Although most
Salmonella infections are foodborne, animal contact is an important
source of human salmonellosis (6). Studies conducted during 1996-1997
determined that approximately 74 000 Salmonella infections each year
in the USA resulted from reptile and amphibian exposure (1). The
ongoing investigation described in this report documents the 1st
multistate outbreak of Salmonella infections associated with amphibians.
A case-control study described here found an association between
infections and exposure to aquatic pet frogs such as African dwarf
frogs. In addition, the outbreak strain was isolated from African
dwarf frogs in 2 patient homes, from a container used to clean
African dwarf frogs in a 3rd home, and from water in an aquarium
containing a small frog in a 4th home. Traceback investigations
converged on a breeder in California; environmental sampling of the
breeder's facility yielded the outbreak strain.
The most likely source of transmission in this outbreak was contact
with water from the frogs' aquariums. Because African dwarf frogs are
small and tend to rest at the bottom of aquariums where children have
difficulty reaching them, direct handling as the source of
transmission is less likely. Amphibians are known carriers of
Salmonella (2). African dwarf frogs are purely aquatic animals,
typically less than 2 inches long from nose to tail stub, and sold as
ornamental aquarium pets. In one study, 21 percent of aquarium frogs
tested from 16 retailers were positive for Salmonella (2).
Furthermore, Salmonella bacteria shed from frogs are readily
recoverable from aquarium water where frogs are housed (2).
Salmonella can survive for an extended period in the environment, and
indirect transmission through environmental contamination might occur (1).
Although 53 percent of case-patients described in this report knew
that Salmonella infection could be acquired from reptiles, including
turtles, only 31 percent knew that Salmonella could be acquired from
amphibians. These findings are consistent with anecdotal reports of
persons buying frogs as pets as an alternative to pet turtles because
of concern over salmonellosis. Human exposure to Salmonella from
aquariums can occur in homes, but also in pet stores, retail stores,
schools, or child care centers (7). Public education regarding the
risk for illness associated with turtles and other reptiles should be
expanded to include the risk for salmonellosis from aquatic pet frogs
and other amphibians. Most notably, because children aged less than 5
years might be less likely to consistently practice proper hand
hygiene, prevention and control measures should be emphasized for
this age group.
Water contained in aquariums where frogs and other amphibians are
housed is an ideal environment for Salmonella growth (1,2,8).
Aquarium water should be changed regularly and aquariums should be
cleaned frequently. However, in this investigation, in 30 percent of
patient households, aquariums were cleaned in the kitchen sink,
posing a risk for cross-contamination with food preparation areas
(2). The CDC has published guidelines for consumers on how to reduce
the risk for Salmonella infection from amphibians and reptiles (available at
measures include washing hands thoroughly with soap and water after
touching animals or cleaning aquariums. No regulations prohibit the
sale of small frogs, but education measures might help reduce the
risk for Salmonella transmission.
1. 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(Suppl 3): S253-261.
2. Bartlett KH, Trust TJ, Lior H: Small pet aquarium frogs as a
source of Salmonella. Appl Environ Microbiol 1977;33: 1026-1029.
3. CDC: Multistate outbreak of human Salmonella infections associated
with exposure to turtles---United States, 2007--2008. MMWR 2008;57: 69-72.
4. CDC: Turtle-associated salmonellosis in humans---United States,
2006--2007. MMWR 2007;56: 649-652.
5. Voetsch AC, Van Gilder TJ, Angulo FJ, et al: FoodNet estimate of
the burden of illness caused by nontyphoidal Salmonella infections in
the United States. Clin Infect Dis 2004;38(Suppl 3): S127-134.
6. CDC: Compendium of measures to prevent disease associated with
animals in public settings, 2009: National Association of State
Public Health Veterinarians, Inc. (NASPHV). MMWR 2009;58(No. RR-5).
7. Trust TJ, Bartlett KH, Lior H: Importation of salmonellae with
aquarium species. Can J Microbiol 1981;27: 500-504.
8. Mann PH, Bjotvedt G: Salmonella organisms isolated from water used
for storage of pet turtles. Can J Comp Med Vet Sci 1967;31:43-45.
[The formal CDC report on this outbreak of ornamental frog-associated
salmonellosis previously reported on ProMED. A picture of the African
dwarf frog can be found at:
Salmonellosis, serotype Typhimurium - USA (13): frogs 20091208.4178
Salmonellosis, serotype Typhimurium - USA (12): poss. lettuce source
Salmonellosis, serotype Newport - USA: ground beef, alert, recall 20090806.2779
Salmonellosis, serotype Saintpaul - USA (03): sprouts, geo. spread
Salmonellosis, serotype Saintpaul - USA (02): sprouts recall 20090306.0929
Salmonellosis, serotype Saintpaul - USA: (NE) 20090303.0873
Salmonellosis, serotype Typhimurium - USA (11): peanut butter 20090210.0606
Salmonellosis, serotype Typhimurium - USA: RFI 20090108.0077
Salmonellosis, human, pet turtles - USA (05) 20081023.3356
Salmonellosis, human, pet turtles - USA 20080125.0317
Salmonellosis, human, pet turtles - USA (multistate): 2006-2007 20070709.2186
Salmonellosis, human, fatal, pet turtles - USA (FL): FDA 20070409.1182
Salmonellosis, human, pet turtles, 2004 - USA (WI, WY) 20050311.0715]
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