A Review of the Public Health Challenges of Salmonella and Turtles

Sodagari, Hamid Reza; Habib, Ihab; Shahabi, Majedeh Pakzad; Dybing, Narelle A.; Wang, Penghao; Bruce, Mieghan

doi:10.3390/vetsci7020056

Cited by 26 publications

(29 citation statements)

References 49 publications

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“…Seasonal effects, such as hibernation or season of sampling, have been speculated by previous studies to explain the low isolation rate of Salmonella in chelonians compared to other reptiles ( 31 ). Moreover, the diet may also have an important role ( 43 , 49 ) because, as reported above, a large proportion of the chelonians are fed with food from vegetable origin or processed, and not from animal origin, frequently related with Salmonella outbreaks ( 11 , 31 , 67 ).…”

Section: Discussionmentioning

confidence: 99%

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Pet Reptiles: A Potential Source of Transmission of Multidrug-Resistant Salmonella

et al. 2021

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Salmonella spp. is widely considered one of the most important zoonotic pathogens worldwide. The close contact between reptiles and their owners provides favourable conditions for the transmission of zoonotic pathogen infections, and ~6% of human salmonellosis cases are acquired after direct or indirect contact with reptiles. Moreover, antimicrobial resistance is one of the most important health threats of the twenty-first century and has been reported in Salmonella strains isolated from pet reptiles, which could entail therapeutic consequences for their owners and breeders. The aim of this study was to assess Salmonella carriage by pet reptiles in pet shops and households, and their role in the transmission of antimicrobial resistance, to inform the owners about the possible risks factors. During the period between January 2019 and December 2019, 54 reptiles from pet shops and 69 reptiles from households were sampled in the Valencian Region (Eastern Spain). Three different sample types were collected from each reptile: oral cavity, skin, and cloacal swabs. Salmonella identification was based on ISO 6579-1:2017 (Annex D), serotyped in accordance with Kauffman-White-Le-Minor technique, and antibiotic susceptibility was assessed according to Decision 2013/652. The results of this study showed that 48% of the pet reptiles examined from households and pet shops carry Salmonella spp. All the strains isolated presented resistance to at least one antibiotic, and 72% were multidrug-resistant strains, the most frequently observed resistance patterns being gentamicin-colistin and gentamicin-colistin-ampicillin. The present study demonstrates that pet reptiles could be a source of human multidrug-resistant Salmonella infection. In this context, the most optimal prevention of multidrug-resistant Salmonella infections necessarily involves strict control of the sanitary status of reptile pet shops and hygienic handling by the individual owners at home.

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Section: Discussionmentioning

confidence: 99%

“…Reptiles have been known to be important carriers of Salmonella spp. worldwide, which may pose a health hazard as a source of human infection, particularly in children (4,16,(41)(42)(43). However, there is a lack of consensus regarding the role of reptile shops on MDR Salmonella strains spreading.…”

Section: Discussionmentioning

confidence: 99%

Pet Reptiles: A Potential Source of Transmission of Multidrug-Resistant Salmonella

et al. 2021

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“…was higher in both Ophidians (50%) and Saurians (51.9%), when compared with Chelonians (20.9%) ( p = 0.016). The lower isolation rates in turtles when compared with other reptiles can be associated with seasonal variations, observed when turtles are preparing for hibernation [ 28 ], but also with the diet of these animals [ 12 , 15 , 16 ]. In fact, the sample collection period occurred before the hibernation stage of Chelonians, during the colder months of the year.…”

Section: Discussionmentioning

confidence: 99%

“…Although infrequent when compared with food-borne cases, accounting for 6% of all human salmonellosis cases both in the USA and in Europe [ 10 ], reptile-associated salmonellosis (RAS) seems to be more related with more severe clinical scenarios, such as systemic and severe disease development, especially in children, elderly people, and pregnant women [ 6 ]. In fact, RAS is a growing public health concern worldwide, with different reports pointing out for its role in disease outbreaks [ 11 , 12 ]. Despite the several RAS cases that have been reported in different European countries [ 13 ], there seems to be no available data regarding Portugal.…”

Section: Introductionmentioning

confidence: 99%

Salmonella spp. in Pet Reptiles in Portugal: Prevalence and Chlorhexidine Gluconate Antimicrobial Efficacy

et al. 2021

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A fraction of human Salmonella infections is associated with direct contact with reptiles, yet the number of reptile-associated Salmonellosis cases are believed to be underestimated. Existing data on Salmonella spp. transmission by reptiles in Portugal is extremely scarce. The aim of the present work was to evaluate the prevalence of Salmonella spp. in pet reptiles (snakes, turtles, and lizards), as well as evaluate the isolates’ antimicrobial resistance and virulence profiles, including their ability to form biofilm in the air-liquid interface. Additionally, the antimicrobial effect of chlorhexidine gluconate on the isolates was tested. Salmonella was isolated in 41% of the animals sampled and isolates revealed low levels of antimicrobial resistance. Hemolytic and lypolytic phenotypes were detected in all isolates. The majority (90.63%) of the Salmonella isolates were positive for the formation of pellicle in the air-liquid interface. Results indicate chlorhexidine gluconate is an effective antimicrobial agent, against the isolates in both their planktonic and biofilm forms, demonstrating a bactericidal effect in 84.37% of the Salmonella isolates. This study highlights the possible role of pet reptiles in the transmission of non-typhoidal Salmonella to humans, a serious and increasingly relevant route of exposure in the Salmonella public health framework.

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“…Reptile‐associated salmonellosis cases in the United States comprise 7% of the salmonellosis reported annually to the Centers for Disease Control and Prevention, and excluding unreported cases, approximately 93,000 cases are reported every year (Spicker, 2013). The reptile species involved in RAS occurrence vary from turtles to squamates, such as bearded dragons, corn snakes, iguana and boa (De Jong et al., 2005; Sodagari et al., 2020; Whiley et al., 2017). Furthermore, reported subspecies and serotypes in RAS cases vary (Aiken et al., 2010; Pedersen et al., 2009; Woodward et al., 1997).…”

Section: Introductionmentioning

confidence: 99%

Bacteriophage as an alternative to prevent reptile‐associated Salmonella transmission

Kwon

Kim

et al. 2021

Zoonoses and Public Health

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Salmonellosis is a major global public health issue; its most common infection, gastroenteritis, accounts for approximately 90 million illnesses and 150,000 mortalities per year. Eradicating salmonellosis requires surveillance, prevention and treatment, entailing large expenditures. However, it is difficult to control Salmonella transmission because it occurs via multiple routes; exotic reptiles are a reservoir of Salmonella and comprise one such route. As the popularity of exotic pets and animal exhibition has increased, human encounters with reptiles have also increased. As a result, reptile‐associated salmonellosis (RAS) has been recognized as an emerging disease. The development of antimicrobial resistance in RAS‐causing Salmonella sp. requires alternatives to antibiotics. In this study, bacteriophages have been established as an alternative to antibiotics because only target bacteria are lysed; thus, they are promising biocontrol agents. Here, bacteriophage pSal‐SNUABM‐02, which infects and lyses reptile Salmonella isolates, was isolated and characterized. The morphology, host range, growth traits and stability of the phage were investigated. The phage was assigned to Myoviridae and was stable in the following conditions: pH 5–9, 4–37°C, and ultravioletA/ultravioletB (UVA/UVB) exposure. Salmonella clearance efficacy was tested using planktonic cell lysis activity and biofilm degradation on polystyrene 96‐well plates and reptile skin fragments. The phage exhibited vigorous lysis activity against planktonic cells. In in vitro biofilm degradation tests on reptile skin and polystyrene plates, both low‐ and high‐concentration phage treatments lowered bacterial cell viability by approximately 2.5–3 log colony‐forming units and also decreased biomass. Thus, bacteriophages are a promising alternative to antibiotics for the prevention and eradication of RAS.

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A Review of the Public Health Challenges of Salmonella and Turtles

Cited by 26 publications

References 49 publications

Pet Reptiles: A Potential Source of Transmission of Multidrug-Resistant Salmonella

Pet Reptiles: A Potential Source of Transmission of Multidrug-Resistant Salmonella

Salmonella spp. in Pet Reptiles in Portugal: Prevalence and Chlorhexidine Gluconate Antimicrobial Efficacy

Bacteriophage as an alternative to prevent reptile‐associated Salmonella transmission

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