Outbreaks of Salmonellosis From Small Turtles

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.

Flea market finds and global exports: Four multistate outbreaks of humanSalmonellainfections linked to small turtles, United States—2015

“…Almost half (45%) of the ill people in these outbreaks were children aged <5 years; this high percentage of young children infected with Salmonella is consistent with other published literature on reptile‐associated salmonellosis (Meyer Sauteur, Relly, Hug, Wittenbrink, & Berger, ; Murphy & Oshin, ; Whitten, Bender, Smith, Leano, & Scheftel, ), including recent outbreaks (Harris et al., ; Walters et al., ). This high percentage might be explained by challenges in this age group to enforcing good hygiene practices or preventing the appeal of playing with small turtles or contact with the turtle's habitat, where bacteria grow (Mann & Bjotvedt, ).…”

“…Since 2006, 15 multistate outbreaks of human Salmonella infections linked to small turtles were reported to the Centers for Disease Control and Prevention (CDC), including eight outbreaks in 2012 (Bosch, Tauxe, & Behravesh, ). Several Salmonella serotypes have been repeatedly linked to contact with small turtles, including Poona, Pomona and Sandiego (Basler et al., ; Bosch et al., ; Harris, Neil, Behravesh, Sotir, & Angulo, ; Tauxe, Rigau‐Perez, Wells, & Blake, ; Walters et al., ). In some of these outbreaks, turtle farms in Louisiana were identified as the source of turtles linked to illnesses (Bosch et al., ; Tauxe et al., ; Walters et al., ).…”

Diversified sources for human infections by Salmonella enterica serovar newport

“…Interestingly, the cold-blooded animal strains in ST31 were aquatic animals (fish and shrimp). Thus, Clade-II is mainly populated by certain distinct sources for human infections, such as bovine (ST45), reptile associated cold-blooded animals (ST46), a well-known source for pediatric Salmonella infections (Walters et al, 2016) and seafood animals (ST31), an emerging source for disease outbreaks (Brands et al, 2005). Additionally, the relative number of MDR strains correlated to the number of livestock strains for each Clade-II STs (Figure 2a), confirming that S. Newport MDR phenotype relates to antibiotics usage in livestock production and persistence of MDR strains in the farm-animal source (Havelaar et al, 2015).…”

Detection of multidrug‐resistant Gram‐negative bacteria from imported reptile and amphibian meats

“…Although the sample size was small, the Salmonella serotypes and CTX-M variants identified are not inconsistent with the organisms originating in Asia. Of the Salmonella isolated in this study, Urbana and Poona are reptile-associated serotypes that have been linked to outbreaks in fresh produce and pet reptiles (Jackson et al 2013;Walters et al 2016). Salmonella Weltevreden is the most common serotype associated with imported seafood and aquatic production systems and is a frequent and increasing cause of human infection predominating Southeast Asia (Ponce et al 2007;Makendi et al 2016).…”