Zoonotic risks: Salmonella and Campylobacter in reptiles

Introduction

Worldwide, reptiles are popular exotic pets. Their popularity can be attributed to a variety of factors including their unique physical characteristics, diversity in species, and reasonably low maintenance. Reptile ownership is highest in the USA and Europe.¹ In Australia, 2.7% of households own at least one reptile representing over 500,000 animals.² The global preference for pet reptiles varies by region, but in Australia, the bearded dragon (Pogona vitticeps) and the blue-tongue skink (Tiliqua scincoides) are among the most popular.³

Reptiles, however, are reservoirs for zoonotic pathogens such as Salmonella and Campylobacter, which are significant contributors to the global burden of human gastroenteritis. These bacteria are often found in the faeces and on the skin of reptiles, and they can easily be transmitted to people through direct animal contact or through contaminated surfaces. The transmission of zoonotic diseases to humans poses an increasingly significant public health challenge, particularly as the practice of keeping reptiles as pets continues to rise globally.^4,5

Salmonella and Campylobacter in reptiles

The genus Salmonella comprises two species, S. enterica and S. bongori. Salmonella enterica has six subspecies: enterica (I), salamae (II), arizonae (IIIa), diarizonae (IIIb), houtenae (IV) and indica (VI). The majority of salmonellae are classified in S. enterica subsp. enterica, which contains over 2600 different serotypes.⁶ Members of Salmonella subsp. enterica (I) are primarily responsible for causing disease in humans.⁷ All other S. enterica subspecies are linked with isolated or sporadic disease in both mammals, reptiles, and birds.⁷

Salmonella is considered a normal part of the reptile gut microbiota, although salmonellosis in reptiles has been reported.⁸ Once infected with Salmonella, reptiles can become asymptomatic carriers, intermittently shedding the bacteria in their faeces. The prevalence of Salmonella in reptiles varies significantly depending on geographical location, as well as whether the reptiles are captive or wild. Studies have shown that the carriage rates of Salmonella in reptiles can range from 30 to 75.8% in captive populations,^9–13 whereas rates are substantially lower for wild populations (8–14%).^11,14 Carriage rates, however, can be affected by seasonal and temporal variation¹⁵ and can vary between species. Snakes and lizards tend to have higher prevalence rates of Salmonella compared to Testudines (turtles and tortoises).^9–11,14,16 The primary modes of Salmonella acquisition in reptiles are through contaminated food, water or environmental exposure. In a captive setting, feeder mice have been reported to carry strains of S. enterica serovar Typhimurium¹⁷ or S. enterica serovar Enteritidis.^18,19 Native rodents²⁰ and insects²¹ have also been shown to carry Salmonella, representing a potential reservoir for wild reptiles.

The genus Campylobacter contains 32 species and 9 subspecies.²² Campylobacter fetus subsp. fetus and C. fetus subsp. testudinum are the most frequently isolated species in reptiles, and they are the predominant causes of human campylobacteriosis linked to reptiles. Additionally, C. jejuni and C. iguaniorum have been commonly isolated from reptiles and are recognised as potential health risks to humans; however, no human infections caused by C. iguaniorum have been reported to date.⁴ Common lizard hosts identified include bearded dragons, the western beaked gecko (Rhynchoedura odura), Philippine sailfin lizard (Hydrosaurus pustulatus), green iguanas (Iguana iguana), Rankin’s dragon (Pogona henrilawsonii), common chuckwalla (Sauromalus ater) and African fat-tailed gecko (Hemitheconyx caudicinctus), as well as the blotched blue-tongued skink (Tiliqua nigrolutea).⁴ Campylobacter infection has also been described for five snake species including western hognose snake (Heterodon nasicus), beauty rat snake (Orthriophis taeniurus), boa constrictor (Boa constrictor), reticulated python (Python reticulatus) and amethystine python (Morelia amethistina).⁴ Research on the prevalence of Campylobacter in reptiles is much more limited compared to studies on Salmonella. The utilisation of polymerase chain reaction (PCR) for detecting Campylobacter species in reptiles yields a higher detection rate compared to culture methods,²³ which poses a challenge when comparing studies that employ different diagnostic approaches. A comprehensive survey conducted in the Netherlands examined the prevalence of Campylobacter species in captive reptiles from three zoos, a diagnostic laboratory, a pathology lab, a veterinary hospital specialising in reptiles and amphibians, and a pet shop. Campylobacter was detected with prevalence of 44.8% and the majority of isolates were C. fetus subsp. fetus.²⁴ In central Australia, 30% of surveyed wild reptiles tested positive for C. jejuni; however, this study did not investigate the prevalence of other reptile associated Campylobacter species.²⁵

Transmission of Campylobacter and Salmonella in reptiles has not been well studied, but similarities with birds are likely to occur. In poultry, Campylobacter colonises the intestinal microbiota and has been found in the oviduct but contamination on eggs or in hatchlings is infrequent. Transmission for poultry primarily occurs by the faecal–oral route. Similarly, Salmonella species also colonise the gut microbiota of poultry. Vertical transmission of Salmonella most commonly is associated with the serotype S. enterica serovar Enteritidis. As with Campylobacter, Salmonella colonises the gastrointestinal tract through faecal–oral transmission.

Reptile–human transmission

Campylobacter and Salmonella species are the two most common causes of food-borne bacterial gastrointestinal disease in humans. Humans commonly become infected with these bacterial species following consumption of contaminated fruit, vegetables, dairy, meat, poultry meat or eggs. Non-food-related risk factors associated with Campylobacter and Salmonella infections include direct or indirect contamination with wildlife and animal faces includes, birds, reptiles, amphibians, livestock and pets.^4,8 In situations where reptiles are kept as pets, transmission may occur through cross contamination or contact with their faeces during terrarium or vivarium cleaning. Indirect transmission of bacteria can also occur. Vacuum cleaners, for example, have previously been identified as a potential source of bacteria and the disturbance of dust can disperse bacteria at concentrations as high as 10⁵ colony forming units per minute.²⁶ In communities where reptiles are raised for food, the consumption of reptilian cuisine also increases the risk of Campylobacter and Salmonella infections.^4,8

One health and exotic reptile trade

The growing demand for exotic pets is coupled with the potential for international importation, which can contribute to the globalisation of diseases. In Australia, it is not legal to import exotic reptiles. However, nearly 30 years ago, Sweden abolished the requirement for a certificate confirming that imported animals were Salmonella free.²⁷ Between 2000 and 2006, the USA imported over 1.4 billion wild reptiles from Asia; a region known for high rates of antibiotic resistance.²⁸ In 2015, 80% of imported wild-caught Indonesian Tokay geckos (Gekko gecko) carried Salmonella and many isolates were found to possess resistance to one or more antibiotics.²⁹ Fluoroquinolones and third-generation cephalosporins are among the most commonly used antibiotics in reptile medicine,³⁰ which poses significant concern. These drugs are classified by the World Health Organization as ‘highest priority critically important antimicrobials’ for human medicine. To date, imported animals for the pet trade have not been systematically surveyed for Campylobacter. However, wild reptiles have been found to be infected with this bacterium, with documented instances in both Europe and Australia.²³

Conclusion

Reptiles are commonly carriers of Campylobacter and Salmonella. Education about the potential health risks associated with reptile ownership is crucial in ensuring prevention of transmission of zoonotic pathogens.⁸ Vulnerable populations, including children, the elderly, the immunocompromised or individuals with chronic illness,^4,5 are particularly at risk for infections linked to reptile handling and consumption of foods containing reptile meat. It is important for reptile owners to practise good hygiene, such as thoroughly washing hands after handling their pets. Regular cleaning and disinfecting of habitats and avoiding free roaming reptiles, particularly in areas where food is prepared or consumed, are also important ways that owners can mitigate Salmonella or Campylobacter. Implementation of proper hygiene and husbandry practices in both captive and wild reptile management will minimise the risk of the zoonotic transmission of Salmonella and Campylobacter.