Abstract
Reptile-associated human salmonellosis cases have increased recently in the United States. It is not uncommon to find healthy chelonians shedding Salmonella enterica. The rate and frequency of bacterial shedding are not fully understood, and most studies have focused on captive vs. free-living chelonians and often in relation to an outbreak. Their ecology and significance as sentinels are important to understanding Salmonella transmission. In 2012–2013, Salmonella prevalence was determined for free-living aquatic turtles in man-made ponds in Clarke and Oconee Counties, in northern Georgia (USA) and the correlation between species, basking ecology, demographics (age/sex), season, or landcover with prevalence was assessed. The genetic relatedness between turtle and archived, human isolates, as well as, other archived animal and water isolates reported from this study area was examined. Salmonella was isolated from 45 of 194 turtles (23.2%, range 14–100%) across six species. Prevalence was higher in juveniles (36%) than adults (20%), higher in females (33%) than males (18%), and higher in bottom-dwelling species (31%; common and loggerhead musk turtles, common snapping turtles) than basking species (15%; sliders, painted turtles). Salmonella prevalence decreased as forest cover, canopy cover, and distance from roads increased. Prevalence was also higher in low-density, residential areas that have 20–49% impervious surface. A total of 9 different serovars of two subspecies were isolated including 3 S. enterica subsp. arizonae and 44 S. enterica subsp. enterica (two turtles had two serotypes isolated from each). Among the S. enterica serovars, Montevideo (n = 13) and Rubislaw (n = 11) were predominant. Salmonella serovars Muenchen, Newport, Mississippi, Inverness, Brazil, and Paratyphi B. var L(+) tartrate positive (Java) were also isolated. Importantly, 85% of the turtle isolates matched pulsed-field gel electrophoresis patterns of human isolates, including those reported from Georgia. Collectively, these results suggest that turtles accumulate Salmonella present in water bodies, and they may be effective sentinels of environmental contamination. Ultimately, the Salmonella prevalence rates in wild aquatic turtles, especially those strains shared with humans, highlight a significant public health concern.
Highlights
Salmonella enterica infections are a significant public health threat, responsible for over 93 million annual illnesses worldwide [1]
There is a link between human cases and the Little River watershed in South Georgia, where 46% of Salmonella isolated from the Little River matched human isolates by pulsedfield gel electrophoresis (PFGE) [21]
Compared to studies in other countries [7, 34, 39, 40, 43, 45, 47, 70,71,72,73], there is a paucity of information about Salmonella prevalence in wild turtles, in the United States (41, FIGURE 3 | Salmonella prevalence of aquatic turtle species varied based on their basking behavior (2012–2013)
Summary
Salmonella enterica infections are a significant public health threat, responsible for over 93 million annual illnesses worldwide [1]. In the United States alone, over 1 million cases of salmonellosis and 600 deaths are reported annually [2]. Most cases of human salmonellosis are caused by food-borne Salmonella strains associated with contaminated meat, eggs, or produce. Produce has become a significant source of foodborne outbreaks associated with Salmonella [3,4,5], accounting for half the outbreaks and one quarter of the illnesses reported for the U.S in 2016 alone [4]. Wildlife captured in the Little River watershed harbor some of the same Salmonella strains present in the river. Only half of the raccoons and opossums sampled in this region possess the same Salmonella strains present in the CDC PulseNet database of human isolates [21]. Might an aquatic species prove a better sentinel for monitoring pathogenic Salmonella strains in watersheds or irrigation ponds?
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