SALMONELLOSIS, MULTIPLE SEROTYPES - USA (02) : PET TURTLES, MORE STRAINS
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Date: Thu 10 May 2012
Source: CDC, _Salmonella_ Homepage [edited] <http://www.cdc.gov/salmonella/small-turtles-03-12/index.html>
Contact with reptiles (such as turtles, snakes, and lizards) and amphibians (such as frogs and toads) can be a source of human salmonellosis. Small turtles, with a shell length of less than 4 inches [10 cm], are a well-known source of human salmonellosis, especially among young children. Because of this risk, the FDA has banned the sale and distribution of these turtles since 1975.
Amphibians and reptiles can carry salmonellae germs and still appear healthy and clean, shedding organisms in their droppings and can easily contaminate their bodies and anything in areas where these animals live. Reptiles and amphibians that live in tanks or aquariums can contaminate the water with germs, which can spread to people.
CDC continues to collaborate with public health officials in multiple states and the FDA to investigate 5 overlapping, multistate outbreaks of human salmonellosis linked to exposure to turtles or their environments (such as, water from a turtle habitat). Because the majority of ill persons who reported contact with small turtles purchased the turtles from a street vendor, it is difficult to determine the original source of the turtles.
The 5 multistate outbreaks of human salmonellosis linked to small turtles are numbered in the order in which they were identified. The details of each investigation are described below.
Outbreak 1: _S._ Sandiego, strain A
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Case count update:
A total of 55 individuals infected with _S._ Sandiego, strain A have been reported from 13 states. The 5 new cases are from Illinois (1), New Jersey (1), New York (1), Pennsylvania (1), and South Carolina (1). Illnesses began between 3 Aug 2011 and 16 Apr 2012. Ill persons range in age from less than 1 to 86 years, with a median age of 7 years. 62 percent of patients are female. Among 39 persons with available information, 10 (25 percent) reported being hospitalized. No deaths have been reported.
Investigation update:
Among the 41 ill persons for whom information is available, 32 (78
percent) reported contact with turtles before becoming ill. 22 persons who reported contact with turtles also reported the size of the turtle; of these, 21 (95 percent) reported a turtle with a shell length of less than 4 inches. Among those reporting small turtles, 8
(42 percent) of the 19 with information available were exposed to turtles purchased from a street vendor. Of the 9 ill persons who reported the type of turtle they had contact with, 8 (89 percent) reported red-eared slider turtles.
Environmental sampling update:
In March 2012, samples of turtle tank water and turtles from the homes of 2 ill persons in New York yielded the outbreak strain, _S._ Sandiego, strain A.
Outbreak 2: _S._ Pomona, strain A
---------------------------------
Case count update:
No new cases have been reported since the 30 Mar 2012 investigation announcement. Among the 9 cases, 3 (33 percent) have been hospitalized.
Investigation update:
Among the 5 ill persons who reported contact with turtles before becoming ill, 3 (63 percent) described the size of the turtle they had contact with. All 3 (100 percent) identified turtles with shell length of less than 4 inches.
Environmental sampling update:
In March 2012, a sample of turtle tank water from the home of a person in New York who was infected with _S._ Sandiego, strain A yielded 2 outbreak strains. These strains were _S._ Pomona, strain A and _S._ Sandiego, strain A. This suggests that the turtles causing Outbreak 1 and Outbreak 2 may originate from a common source.
Outbreak 3: _S._ Poona
----------------------
Case count update:
A total of 15 individuals infected with the outbreak strain of _S._ Poona have been reported from 8 states. The 3 new cases are from Alabama (1), New York (1), and Texas (1). Among persons for whom information is available, illness onset dates range from 20 Oct 2011 to 6 Apr 2012. Ill persons range in age from less than 1 year to 70 years, with a median age of 3 years. 67 percent of patients are female. Among 11 persons with available information, 3 (27 percent) reported being hospitalized. No deaths have been reported.
Investigation update:
Among the 14 ill persons with available information, 12 (86 percent) reported contact with turtles in the week before becoming ill. 8 persons who reported contact with turtles also reported the size of the turtle; of these, 6 (75 percent) reported a turtle with a shell length of less than 4 inches. 3 (50 percent) of the 6 ill persons who had contact with small turtles reported buying their turtles from a street vendor. Of the 8 ill persons who could recall the type of turtle with which they had contact, 7 (88 percent) reported red-eared slider turtles.
Outbreak 4: _S._ Sandiego, strain B initial investigation announcement
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As of 8 May 2012, a total of 6 individuals infected with _S._ Sandiego, strain B have been reported from 3 states. The number of ill persons identified in each state is as follows: Colorado (3), Nevada (2), and Texas (1). Among the persons who reported the date they became ill, illnesses began between 25 Feb 2012 and 27 Apr 2012.
Infected individuals range in age from less than 1 year old to 65 years old, and the median age is 17 years. 50 percent of patients are female. Among the 6 ill persons, 1 (17 percent) has been hospitalized.
No deaths have been reported.
In interviews, ill persons answered questions about contact with turtles and foods consumed during the week before becoming ill. 4 (67
percent) of 6 ill persons interviewed reported contact with turtles before becoming ill. 4 persons who reported contact with turtles also reported the size of the turtle, all reported a turtle with a shell length of less than 4 inches and all identified red-eared slider turtles. 4 ill persons who reported contact with small turtles also reported where the turtle was purchased. 2 purchased turtles from pet stores, 1 purchased a turtle from a street vendor, and 1 purchased a turtle from a flea market.
In April 2012, a sample of water from a turtle habitat associated with an ill person in Colorado who was infected with _S._ Sandiego, strain B was tested. This sample yielded the outbreak strain, _S._ Sandiego, strain B.
Outbreak 5: _S._ Pomona, strain B initial investigation announcement
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As of 8 May 2012, a total of 39 individuals infected with _S._ Pomona, strain B have been reported from 16 states. The number of ill persons identified in each state is as follows: Alaska (2), Arizona (1), California (9), Colorado (2), Delaware (3), Georgia (2), Michigan (1), Nevada (2), New York (1), Ohio (2), Oregon (1), Pennsylvania (1), South Carolina (2), Texas (7), Virginia (2), and West Virginia (1).
Illness onset dates range from 21 Jun 2011 to 30 Mar 2012. Infected individuals range in age from less than 1 year to 83 years, with a median age of 1 year. 54 percent of patients are male. Among the 20 patients with available information, 2 (10 percent) have been hospitalized. No deaths have been reported.
Among the 19 ill persons with information available, 13 (68 percent) reported exposure to turtles before they became ill. 5 ill persons reported the size of the turtle they had contact with, and all 5 described turtles with a shell length of less than 4 inches. 3 ill persons who had contact with small turtles reported where they purchased the turtles, and all purchased the turtles from a street vendor.
In March 2012, samples from a turtle tank were collected from the home of an ill person in New Mexico infected with _S._ Sandiego, strain A (the Outbreak 1 strain). Samples yielded _S._ Pomona, strain B (the Outbreak 5 strain). This suggests that the turtles causing Outbreak 1 and Outbreak 5 may originate from a common source.
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[In 2008, CDC reported on an ongoing outbreak of _S._ Paratyphi B var.
Java (CDC: _Salmonella_ Infections Associated with Exposure to Turtles
- USA, 2007-2008. Morbid Mortal Weekly Rep 2008; 57(03): 69-72; <http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5703a3.htm>. Some of the discussion of the report is reproduced below:
"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 salmonellosis.
References
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1. Chiodini RJ, Sundberg JP: Salmonellosis in reptiles: a review. Am J Epidemiol 1981; 113(5): 494-9.
2. CDC: Turtle-associated salmonellosis in humans - United States, 2006-2007. MMWR 2007; 56(26): 649-52. Available at <http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5626a1.htm>.
3. CDC: Salmonellosis associated with pet turtles - Wisconsin and Wyoming, 2004. MMWR 2005; 54(09): 223-6. Available at <http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5409a3.htm>.
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(6): 511-7. Abstract available at <http://aje.oxfordjournals.org/cgi/content/abstract/95/6/511>.
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(12): 1247-9. Abstract available at <http://jama.ama-assn.org/content/243/12/1247.abstract>.
6. American Veterinary Medical Association: US pet ownership and demographics sourcebook. Schaumburg, IL: American Veterinary Medical Association; 2007:2. Available at <http://www.avma.org/reference/marketstats/sourcebook.asp>.
7. D'Aoust JY, Daley E, Crozier M, Sewell AM: Pet turtles: a continuing international threat to public health. Am J Epidemiol 1990;
132(2): 233-8. Abstract available at
<http://www.ncbi.nlm.nih.gov/pubmed/2372004>.
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. Abstract available at <http://cat.inist.fr/?aModele=afficheN&cpsidt=18496347>.
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. Abstract available at <http://cid.oxfordjournals.org/content/38/Supplement_3/S253.full.pdf+html>.
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 1997; 99(3): 399-402. Abstract available at <http://pediatrics.aappublications.org/cgi/content/abstract/99/3/399>."
A photograph of the red-eared slider turtle, the small turtle usually involved in this issue, is available at <http://en.wikipedia.org/wiki/Red-eared_slider>. - Mod.LL
A HealthMap/ProMED-mail map can be accessed at:
<http://healthmap.org/r/1hiS>.]
[see also:
Salmonellosis, serotype Paratyphi B - USA (04): (NC), tempeh
20120510.1128989
Salmonellosis, serotype Paratyphi B - USA (03): (NC), tempeh
20120509.1127709
Salmonellosis, serotype Infantis - USA: human, dog food 20120504.1122720 Salmonellosis, serotype Bareilly - USA (09): tuna, 2nd st
20120503.1121817
Salmonellosis, serotype Paratyphi B - USA (02): (NC) tempeh
20120502.1119408
Salmonellosis, serotype Paratyphi B - USA: (NC) 20120428.1116448 Salmonellosis, serotype Bareilly - USA (08): tuna, 2nd st
20120427.1115922
Salmonellosis, serotype Bareilly - USA (07) tuna 20120425.1113957 Salmonellosis, serotype I 4,5,12,i- - USA: feeder rodents
20120419.1107037
Salmonellosis, serotype Bareilly - USA (06): tuna product, more cases
20120418.1105458
Salmonellosis, serotype Bareilly - USA (05): tuna product, recall
20120415.1101361
Salmonellosis, serotype Bareilly - USA (04): possible sushi link
20120412.1098523
Salmonellosis, serotype Bareilly - USA (03): possible sushi link
20120409.1094597
Salmonellosis, serotype Bareilly - USA (02): possible sushi link, CDC report 20120405.1091349 Salmonellosis, serotype Bareilly - USA: possible sushi link
20120404.1090246
Salmonellosis, multiple serotypes - USA: pet turtles 20120331.1086557 Salmonellosis, serotype Paratyphi B - USA: (PA, SC) pet turtles 2011
20120202.1031013
Salmonellosis, serotype Enteritidis - USA: restaurant chain
20120123.1017853
2008
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Salmonellosis, human, pet turtles - USA (05) 20081023.3356 Salmonellosis, human, pet turtles - USA 20080125.0317
2007
----
Salmonellosis, human, pet turtles - USA (multistate): 2006-2007
20070709.2186
Salmonellosis, human, fatal, pet turtles - USA (FL): FDA
20070409.1182
2005
----
Salmonellosis, human, pet turtles, 2004 - USA (WI, WY) 20050311.0715
2004
----
Salmonellosis, human, turtle - USA (WI, KS ex WI) 20040819.2298 2000
----
Salmonellosis, pet reptiles - USA (02) 20000308.0314 Salmonellosis, pet reptiles - USA 20000229.0274 Salmonellosis, pet reptiles - UK: alert 20000227.0267
1999
----
Salmonella, reptile-associated - USA: Summary 19991112.2022
1997
----
Salmonellosis, reptile-associated (02) 19970616.1262 Salmonellosis, reptile-associated, health-regulations: RFI
19970612.1234
1996
----
Reptile-Associated Zoonoses 19960402.0613 Salmonella & reptiles 19960213.0290 Salmonella, fatal, iguana-associated - Indiana (USA) (6)
19960207.0262
Salmonella, fatal, iguana-associated - Indiana 19960202.0245
1995
----
Salmonella & reptiles 19950901.0782]
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