Outbreaks of Salmonellosis From Small Turtles

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Maroya Spalding Walters, Latoya Simmons, Tara C. Anderson, Jamie DeMent, Kathleen Van Zile, Laura P. Matthias, Sonia Etheridge, Ronald Baker, Cheryl Healan, Rita Bagby, Roshan Reporter, Akiko Kimura, Cassandra Harrison, Kadri Ajileye, Julie Borders, Kia Crocker, Aaron Smee, Meg Adams-Cameron, Lavin A. Joseph, Beth Tolar, Eija Trees, Ashley Sabol, Nancy Garrett, Cheryl Bopp, Stacey Bosch, Casey Barton Behravesh

Pediatrics, January 2016

Author Information

Maroya Spalding Walters, PhD, ScMa,b,
Latoya Simmons, BAa,
Tara C. Anderson, DVM, MPH, PhDa,b,
Jamie DeMent, MNSc,
Kathleen Van Zile, RS, MSEHc,
Laura P. Matthias, MPHc,
Sonia Etheridge, AAc,
Ronald Baker, MS, MT, ASCPc,
Cheryl Healan, MT-P (AAB)c,
Rita Bagby, RN, MSNd,
Roshan Reporter, MDd,
Akiko Kimura, MDe,
Cassandra Harrison, MSPHf,
Kadri Ajileye, MDg,
Julie Borders, MSHPh,
Kia Crocker, MPHi,
Aaron Smee, MPHj,
Meg Adams-Cameron, MPHk,
Lavin A. Joseph, MSa,
Beth Tolar, MSa,
Eija Trees, PhD, DVMa,
Ashley Sabol, MSa,
Nancy Garrett, BSa,
Cheryl Bopp, MSa,
Stacey Bosch, DVM, MPHa, and
Casey Barton Behravesh, MS, DVM, DrPHa

a-Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Atlanta, Georgia;
2--Epidemic Intelligence Service, Scientific Education and Professional Development Program Office, Centers for Disease Control and Prevention, Atlanta, Georgia;
c-cFlorida Department of Health, Jacksonville, Florida;
d-Los Angeles County Department of Health, Los Angeles, California;
e-California Department of Public Health, Gardena, California;
f-New York City Department of Health and Mental Hygiene, New York, New York;
g-New York State Health Department, Albany, New York;
h-Texas Department of State Health Services, Austin, Texas;
i-Maryland Department of Health and Mental Hygiene, Baltimore, Maryland;
j-Pennsylvania Department of Health, Reading, Pennsylvania;
k-New Mexico Department of Health, Albuquerque, New Mexico


Dr Walters developed the data collection instruments, coordinated the data collection, conducted the analysis, and drafted and revised the manuscript; Ms Simmons and Dr Anderson reviewed and revised data collection instruments, helped coordinate data collection, and critically reviewed and revised the manuscript; Drs Reporter, Kimura, and Ajileye and Ms Bagby, Ms DeMent, Ms Van Zile, Ms Harrison, Ms Borders, Ms Crocker, Ms Adams-Cameron, and Mr Smee collected data through patient interviews, interpreted epidemiologic data, coordinated environmental sampling, and critically reviewed and revised the manuscript; Ms Matthias, Ms Etheridge, Mr Baker, Ms Healan, Mr Joseph, Ms Tolar, Dr Trees, Ms Sabol, Ms Garrett, and Ms Bopp conducted laboratory analyses, interpreted laboratory data, and critically reviewed and revised the manuscript; Drs Bosch and Behravesh reviewed and revised data collection instruments, supervised coordination of collection of patient and environmental data, and critically reviewed and revised the manuscript; and all authors approved the final manuscript as submitted.


Abstract

OBJECTIVE: Turtle-associated salmonellosis (TAS), especially in children, is a reemerging public health issue. In 1975, small pet turtles (shell length <4 inches) sales were banned by federal law; reductions in pediatric TAS followed. Since 2006, the number of multistate TAS outbreaks has increased. We describe 8 multistate outbreaks with illness-onset dates occurring in 2011–2013.

METHODS: We conducted epidemiologic, environmental, and traceback investigations. Cases were defined as infection with ≥1 of 10 molecular subtypes of Salmonella Sandiego, Pomona, Poona, Typhimurium, and I 4,[5],12:i:-. Water samples from turtle habitats linked to human illnesses were cultured for Salmonella.

RESULTS: We identified 8 outbreaks totaling 473 cases from 41 states, Washington DC, and Puerto Rico with illness onsets during May 2011–September 2013. The median patient age was 4 years (range: 1 month–94 years); 45% percent were Hispanic; and 28% were hospitalized. In the week preceding illness, 68% (187 of 273) of case-patients reported turtle exposure; among these, 88% (124 of 141) described small turtles. Outbreak strains were isolated from turtle habitats linked to human illnesses in seven outbreaks. Traceback investigations identified 2 Louisiana turtle farms as the source of small turtles linked to 1 outbreak; 1 outbreak strain was isolated from turtle pond water from 1 turtle farm.

CONCLUSIONS: Eight multistate outbreaks associated with small turtles were investigated during 2011–2013. Children <5 years and Hispanics were disproportionately affected. Prevention efforts should focus on patient education targeting families with young children and Hispanics and enactment of state and local regulations to complement federal sales restrictions.
 

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