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Notes from the Field: Four Multistate Outbreaks of Human Salmonella Infections Linked to Small Turtle Exposure — United States, 2015

Weekly / July 1, 2016 / 65(25);655–656


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Kelly Gambino-Shirley, DVM 1,2; Lauren Stevenson, MHS2; Katherine Wargo, MPH2; Laura Burnworth, MPH2; Jonathan Roberts, DVM3; Nancy Garrett2; Susan Van Duyne, MA2; Gillian McAllister2; Megin Nichols, DVM2 (View author affiliations)

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In August 2015, the Food and Drug Administration (FDA) notified CDC of a consumer complaint involving Salmonella Sandiego infection in a child (the index patient), who had acquired a small turtle (shell length <4 inches [<10 cm]) at an Alabama flea market. The subsequent investigation, which included examining data from PulseNet, the national molecular subtyping network for foodborne disease surveillance, identified four multistate Salmonella outbreaks: two involving Salmonella Sandiego and two involving Salmonella Poona. These serotypes have been linked to small turtles in previous outbreaks (1,2). Although selling small turtles as pets in the United States has been banned since 1975 (3), illegal sales still occur at discount stores and flea markets and by street vendors. CDC investigated to determine the extent of the outbreaks and prevent additional infections.

For this investigation, a case was defined as infection with Salmonella serotypes Sandiego or Poona with the pulse-field gel electrophoresis patterns XbaI JL6X01.0104, JL6X01.0544, JL6X01.0055, JLXX01.0030, or JLXX01.0053 in a person with illness onset January 1–December 31, 2015. A total of 124 cases from 22 states were identified. Median patient age was 7 years (range <1–82 years); 51 patients (41%) were aged <5 years, and 59 (49%) were female. Among 108 patients with available information, 36 (33%) were hospitalized. Thirteen (36%) of the 36 hospitalized patients were aged <5 years. No deaths were reported. Fifty-eight (70%) of 83 patients with ethnicity information were Hispanic.

A total of 104 patients or their caregivers were interviewed; 50 patients (48%) had turtle exposure. Among the 50 patients with reported turtle exposure, the median age was 3 years (range <1–77 years), 30 (60%) were aged <5 years, and 25 (50%) were female. Of the 50 patients with turtle exposure, 48 had information on hospitalization; 18 of the 48 (38%) were hospitalized. Nine of those hospitalized were aged <5 years. Twenty-eight (72%) of 39 patients with ethnicity information were Hispanic. Turtle and turtle environment samples were collected from nine patients’ homes. Of these, 21 isolates of Salmonella were culture-positive: 17 matched the outbreak strains, two were Salmonella Paratyphi B var L-tartrate+, and two were Salmonella Pomona (Table).

An FDA consumer safety officer investigating the flea market where the index patient’s turtle was obtained traced the turtle’s origin to farm A (FDA’s Center for Veterinary Medicine did not pursue legal action regarding the sale by farm A of small turtles to the flea market vendor). Pond water samples from farm A yielded cultures of Salmonella (Table). Although the samples from turtle farm A did not yield the 2015 outbreak strains, two of the three Salmonella Pomona isolates from pond water matched isolates from a patient’s pet turtle’s environment.

The high proportion of patients aged <5 years in these outbreaks emphasizes the risk for illness among young children with small turtles as pets. This finding indicates education is needed to address the risk to children for Salmonella infections from small turtles and other reptiles. Many patients in these outbreaks were Hispanic, which highlights the importance of multilingual messages for effective communication. During these outbreaks, the announcement and prevention messages regarding safe handling of pet reptiles and amphibians were translated into Spanish and posted on the “CDC en Español” website. To ensure wider dissemination, information was also provided to a major Spanish-language news agency.

Transient vendors continue to be a source of illegal sales of small turtles. Educational campaigns at schools, child care centers, carnivals, and flea markets regarding the risk for Salmonella from contact with turtles are important to prevent infections among children.

Corresponding author: Kelly Gambino-Shirley, KGambinoShirley@cdc.gov, 404-639-1461.

1Epidemic Intelligence Service, CDC; 2Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, CDC; 3Louisiana Department of Agriculture and Forestry.

References

  1. Basler C, Bottichio L, Higa J, Prado B, Wong M, Bosch S. Notes from the field: multistate outbreak of human Salmonella Poona infections associated with pet turtle exposure—United States, 2014. MMWR Morb Mortal Wkly Rep 2015;64:804. CrossRef PubMed
  2. Walters MS, Simmons L, Anderson TC, et al. Outbreaks of salmonellosis from small turtles. Pediatrics 2016;137: e20151735. CrossRef PubMed
  3. Turtles intrastate and interstate requirements, 21 C.F.R. Sect. 1240.62 (2015). https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/cfrsearch.cfm?fr=1240.62
Return to your place in the textTABLE. Salmonella serotypes and pulsed-field gel electrophoresis (PFGE) XbaI patterns, by source — United States, 2015
Serotype PFGE XbaI pattern Patients with turtle exposure*/total patients No. of isolates cultured positive by source†
Patient Pet turtles and turtle environments Farm A pond water
Sandiego JLXX01.0030 8/13 17 0 0
JLXX01.0053 7/18 21 3 0
Poona JL6X01.0104 27/52 60 11 0
JL6X01.0055 7/20 25 2 0
JL6X01.0544 1/1 1 1 0
Paratyphi B var L-tartrate+ JKXX01.0225 0 0 2 0
Berta JAXX01.0025 0 0 0 1
Braenderup JBPX01.0884 0 0 0 1
Pomona POMX01.0002 0 0 2 2
POMX01.0098 0 0 0 1

* Information obtained from patient interviews.
† Specimens/samples might have more than one isolate from a single source.

Suggested citation for this article: Gambino-Shirley K, Stevenson L, Wargo K, et al. Notes from the Field: Four Multistate Outbreaks of Human Salmonella Infections Linked to Small Turtle Exposure — United States, 2015. MMWR Morb Mortal Wkly Rep 2016;65:655–656. DOI: http://dx.doi.org/10.15585/mmwr.mm6525a3.

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