SALMONELLA AND REPTILES
R. A. Machin. Reviewed June 2020.
KEY POINTS
- Reptiles should be considered carriers of Salmonella
- Salmonella can infect humans and other animals
- Testing is not recommended, generally
- Hygiene measures should be followed
- There are millions of human infections and thousands of deaths every year
Salmonella sp.
is a rod shaped Gran negative bacteria frequently found in reptiles and amphibians and in many cases may be considered part of the normal flora. Salmonella enterica
is the type species and is further divided in to six subspecies with over 2500 serovars.
Due to the high incidence of Salmonella sp.
in reptiles some authorities consider them as asymptomatic carriers, whereas estimates of carriers vary between 36-90%. Veterinary surgeons have an important task of warning owners and general public about precautions that should be taken to prevent infection.
RISK TO HUMANS
This bacteria is able to induce disease in humans and animals and is not only transmitted by reptiles, but may also be transmitted by farm animals through eggs or meat. Every year there are millions of infections worldwide resulting in thousands of deaths. In the United States (US), the Center of Disease Control (CDC) estimates that 7% of he 93.000 human cases are the result of a reptile or amphibian encounter or contact. The same center estimates that 3% of homes have a reptile in the household.
In humans salmonellosis causes fever, abdominal cramps and diarrhoea; this may progress to a more severe form affecting blood, bone marrow and nervous system. Salmonella sp. may be excreted through faeces of reptiles that appear to be healthy. People may become infected upon ingestion of Salmonella sp. after close contact with a reptile (direct faecal-oral transmission) or contaminated objects or fomites.
Although there is a risk of becoming infected with Salmonella there are other more likely sources where a human can be infected. In 2011 an article published in Clinicians Brief authored by an American and European specialist in Herpetology stated that you are more likely to become infected with Salmonella sp. through ingestion of pork meat, eggs or peanut butter than reptiles.
In the US the sale of turtles (equivalent to (aquatic) terrapins in the UK) under 4 inches (10cm) was prohibited due to high numbers of children putting small turtles in their mouths. High numbers of turtles from farms and wild caught specimens were imported from the US to Europe and over a three year period (2002-2005), 3.8 million turtles were exported from the US. In 1975 the Food and drug administration (FDA) banned interstate shipments of turtles under 4 inches due to the fact there were over 280000 cases per year. In 1997 the European Union banned the import of Red Eared Sliders (Trachemys scripta elegans) but following this ban imports of other species continued including yellow Bellied Sliders (Trachemys scripta scripta)
and other North American species.
TESTING - DIAGNOSIS
Salmonella species are a frequent inhabitant of the reptile gut and may be intermittently shed. False negatives are therefore a problem in reptiles making asymptomatic carrier detection a challenge. This means that a reptile may test negative but actually is carrying the bacteria.
Good hygiene practices should be followed with all reptiles and routine testing is not advised (references: Centers of Disease Control (CDC), Association of Reptile and Amphibian Veterinarians (ARAV) - see below).
"A veterinarian will not be able to prevent your reptile or amphibian from shedding Salmonella because Salmonella is a normal bacteria found in healthy reptiles and amphibians."
"All reptiles and amphibians should be considered potential carriers of Salmonella. The organism is shed in feces of reptiles and amphibians and, if ingested by humans, may result in a potentially serious illness. Because Salmonella may be shed intermittently, it is not possible to use diagnostic testing to guarantee that any reptile or amphibian is “free” of Salmonella. Bacterial culture of fecal specimens will not detect Salmonella infection in all reptiles and amphibians.
TREATMENT - NOT INDICATED
Treatment of asymptomatic carriers with antibiotics has proved to be ineffective and sick reptiles with clinical salmonellosis euthanasia should be considered. This may be a challenge for the clinician as the reptile may be positive for Salmonella but may have another disease process undiagnosed. Reptiles with salmonellosis may be septic meaning that the bacteria may be found in other organs including the blood (septic).
In exotics veterinary medicine the use of fluoroquinolones (i.e. Enrofloxacin) is widely criticised and should be seriously considered before treating and exotic pet, as these drugs are used to treat salmonellosis in humans and may also contribute to antimicrobial resistance. Enrofloxacin is a commonly used drug and perhaps should be used as in canine and feline medicine, as a second line antibiotic after culture and sensitivity tests have been performed.
"Attempts to treat asymptomatic reptiles and amphibians with antibiotics to eliminate Salmonella from their intestinal tract have not been demonstrated to be effective. Doing so is not recommended as it may increase the risk of emergence of antimicrobial-resistant Salmonella strains. Attempts to raise “Salmonella-free” reptiles have been equally unsuccessful and colonisation of the intestinal tract can occur at any point in the reptile or amphibian’s lifecycle."
PREVENTION
Optimal husbandry conditions will contribute to a strong immune system and reduce the shedding of Salmonella through the faeces. It is the responsibility of the reptile keeper to provide the optimal conditions in the vivaria for the species in question. These conditions are dependant on the species needs and may include provision of ultraviolet A and B spectrum, thermal gradient, basking area, adequate hides and substrate. Optimal husbandry will ultimately reduce stress and therefore enhance the immune system. In cases where husbandry is deficient there is an increased risk of shedding Salmonella and causing other health problems including overgrowth of parasites or metabolic disease.
The CDC recommends the following:
"Reptiles are not kept in households with children under five years of age. The elderly or immunosuppressed individuals should also avoid exposure to reptiles."
"A veterinarian will not be able to prevent your reptile or amphibian from shedding Salmonella because Salmonella is a normal bacteria found in healthy reptiles and amphibians."
DO
Wash your hands thoroughly with soap and warm water immediately after touching a reptile or amphibian, or anything in the area where they live and roam. Use hand sanitizer if soap and water are not readily available.
Adults should always supervise hand washing for young children.
Keep reptiles and amphibians out of homes with children younger than 5 years old or people with weakened immune systems.
Habitats and their contents should be carefully cleaned outside of the home. Use disposable gloves when cleaning and do not dispose of water in sinks used for food preparation or for obtaining drinking water.
Wash any clothing the reptile or amphibian might have touched.
Use soap or a disinfectant to thoroughly clean any surfaces that have been in contact with reptiles or amphibians.
DON'T
Don't let children younger than 5 years of age, older adults, or people with weak immune systems handle or touch amphibians or reptiles, or anything in the area where they live and roam, including water from containers or aquariums.
Don't keep reptiles and amphibians in child care centers, nursery schools, or other facilities with children younger than 5 years old.
Don't touch your mouth after handling reptiles or amphibians and do not eat or drink around these animals.
Don't let reptiles or amphibians roam freely throughout the house or in areas where food or drink is prepared, served, or stored, such as kitchens, pantries, or outdoor patios.
Don't bathe animals or clean their habitats in your kitchen sink, bathroom sink, or bathtub. To prevent cross-contamination, animals should be bathed in a small plastic tub or bin that is dedicated for animal use only.
If bathtubs must be used for these purposes, they should be thoroughly cleaned afterward. Use bleach to disinfect a sink, bathtub, or other place where reptile or amphibian habitats are cleaned.
References and Further Reading
Association of Reptile and Avian Veterinarians (ARAV) http://www.arav.org
Centers for Disease Control and Prevention (CDC) http://www.cdc.gov/salmonella/
Centers for Disease Control and Prevention (CDC). Take Care with Pet Reptiles and Amphibians: https://www.cdc.gov/Features/SalmonellaFrogTurtle/index.html
CDC Special Advice for People at Extra Risk for Zoonoses http://www.cdc.gov/healthypets/extra_risk.htm
Food and Drug Administration: Pet Turtles Cute But Contaminated With Salmonella http://www.fda.gov/ForConsumers/ConsumerUpdates/ ucm048151.htm
Pathogen Safety Data Sheets and Risk Assessment– Public Health Agency of Canada http://www.phac-aspc.gc.ca/lab-bio/res/psds-ftss/index- eng.php#s
Medical Microbiology http://www.ncbi.nlm.nih.gov/books/NBK7627/
The Merck Manual http://www.merck.com/pubs/mmanual/
Acha PN, Szyfres B (Pan American Health Organization [PAHO]). Zoonoses and communicable diseases common to man and animals. Volume 1. Bacterioses and mycoses. 3rd ed. Washington DC: PAHO; 2003. Scientific and Technical Publication No. 580. Salmonellosis; p. 233-251.
Austin CC, Wilkins MJ. Reptile-associated salmonellosis. JAVMA. 1998 Mar 15;212(6):866-867.
Beers MH, Porter RS, editors. The Merck manual. 18th ed. Whitehouse Station, NJ: Merck and Co.; 2006. Reactive arthritis; p. 292-294.
Boever WJ, Williams J. Arizona septicemia in three boa constrictors. Vet Med Small Anim Clin. 1975;70:1357-1359.
Bradley T, Angulo FJ. Salmonella and reptiles: veterinary guidelines. J Herp Med Surg. 2009; 19:36-37.
Bradley T, Angulo F, Mitchell M. Public health education on Salmonella spp and reptiles. JAVMA. 2001;219(6):754-755.
Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B. Salmonella nomenclature. J Clinical Microbiol. 2000;38:2465-67.
Centers for Disease Control and Prevention [CDC]. Diseases from reptiles [online]. CDC;2004. Available at: http://www.cdc.gov/healthypets/animals/reptiles.htm
Centers for Disease Control and Prevention [CDC]. Iguana- associated salmonellosis -- Indiana, 1990. MMWR Morb Mortal Wkly Rep. 1992;41(03):38-39.
Centers for Disease Control and Prevention [CDC]. Is a turtle the right pet for your family? [online]. CDC;29 Apr 2005. Available at: http://www.cdc.gov/healthypets/spotlight_an_turtles.htm.
Centers for Disease Control and Prevention [CDC]. Notes from the field: Infections with Salmonella I 4,[5],12:i:- linked to exposure to feeder rodents - United States, August 2011- February 2012. MMWR Morb Mortal Wkly Rep. 2012;61(15):277.
Centers for Disease Control and Prevention [CDC]. Reptile- associated salmonellosis--selected states, 1996-1998. MMWR Morb Mortal Wkly Rep. 1999;48(44):1009-1012; Errata 1999;48(45):1051.
Centers for Disease Control and Prevention [CDC]. Reptile- associated salmonellosis--selected states, 1998-2002. Morb Mortal Wkly Rep. 2003;52:1206-9.
Centers for Disease Control and Prevention [CDC]. Salmonella annual summary, 2009. Atlanta, GA:US Department of Health and Human Services; 2009. Available at: http://www.cdc.gov/ncezid/dfwed/PDFs/SalmonellaAnnualSu mmaryTables2009.pdf
Centers for Disease Control and Prevention [CDC]. Salmonellosis associated with pet turtles---Wisconsin and Wyoming, 2004. MMWR Morb Mortal Wkly Rep. 2005 Mar 11;54(09):223-226.
Centers for Disease Control and Prevention [CDC]. Salmonella infection (salmonellosis) and animals [online]. CDC; 2004 Sept. Available at: http://www.cdc.gov/healthypets/diseases/salmonellosis.htm
Centers for Disease Control and Prevention [CDC]. Salmonellosis. Technical information [online]. CDC; 2009 Nov. Available at: http://www.cdc.gov/nczved/divisions/dfbmd/diseases/salmone llosis/technical.html
Cohen ML, Potter M, Pollard R, Feldman RA. Turtle-associated salmonellosis in the United States. Effect of Public Health Action, 1970 to 1976. JAMA. 1980 Mar 28;243(12):1247-9.
Dalton C, Hoffman R, Pape J. Iguana-associated salmonellosis in children. Pediatr Infect Dis J. 1995 Apr;14(4):319-320.
de Jong B, Andersson Y, Ekdahl K. Effect of regulation and education on reptile-associated salmonellosis. Emerg Infect Dis. 2005 ME;11(3): 398-403.
Ebani VV, Cerri D, Fratini F, Meille N, Valentini P, Andreani E. Salmonella enterica isolates from faeces of domestic reptiles and a study of their antimicrobial in vitro sensitivity. Res Vet Sci. 2005 Apr;78(2):117-121.
Food and Drug Administration [FDA]. Pet turtles may be harmful to your children’s health [online]. FDA;2005 Jul. Available at: http://www.fda.gov/downloads/AnimalVeterinary/Resourcesf orYou/UCM064618.pdf
Giannella R. Salmonella [monograph online]. In Baron S, editor. Medical Microbiology. 4th ed. New York: Churchill Livingstone; 1996. Available at: http://www.ncbi.nlm.nih.gov/books/NBK8435/.
Isaza R, Garner M, Jacobson E. Proliferative osteoarthritis and osteoarthrosis in 15 snakes. J Zoo Wildl Med. 2000;31:20-27.
Jacobson ER. Infectious diseases and pathology of reptiles. Boca Raton, FL;CRC/Taylor & Francis; 2007.
Jong B, Andersson Y, Ekdahl K. Effect of regulation and education on reptile-associated salmonellosis. Emerg Infect Dis. 2005 Mar;11(3):398-403.
Kelly J, Hopkin R, Rimsza ME. Rattlesnake meat ingestion and Salmonella arizona infection in childrent: case report and review of the literature. Pediatr Infect Dis J. 1995 Apr;14(4):320-322.
Mader DR. Reptile medicine and surgery, 2nd ed. St Louis, Missouri : Saunders; 2006.
Mermin J, Hoar B, Angulo FJ. Iguanas and Salmonella Marina infection in children: a reflection of the increasing incidence of reptile-associated salmonellosis in the United States. Pediatrics. 1997 Mar;99(3):399-402.
Mermin J, Hutwagner L, Vugia D, Shallow S, Daily P, Bender J, Koehler J, Marcus R, Angulo FJ. Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. CID. 2004;38 (Suppl 3): S253-S261.
Mahajan RK, Khan SA, Chandel DS, Kumar N, Hans C, Chaudhry R. Fatal case of Salmonella enterica subsp. arizonae Gastroenteritis in an infant with microcephaly. J Clin Microbiol. 2003 Dec;41(12):5830-5832.
Nagano N, Oana S, Nagoano Y, Arakawa Y. A severe Salmonella enterica Serotype Paratyphi B infection in a child related to a pet turtle, Tracheyms scripta elegans. Jpn J Infect Dis. 2006;59:132-134.
O’Rourke K. Battling baby turtle sales. JAVMA News. 2004 Nov 15;225(10). Available at: https://www.avma.org/News/JAVMANews/Pages/041115s.as px
O’Rourke K. Reptile owner donates blood, passes on lethal Salmonella infection. JAVMA News. 2002. Available at: https://www.avma.org/News/JAVMANews/Pages/021201b.as px
Olsen SJ, Bishop R, Brenner FW, Roels TH, Bean N, Tauxe RV, Slutsker L. The changing epidemiology of Salmonella: trends in serotypes isolated from humans in the United States, 1987- 1997. J Infect Dis. 2001 Mar 1; 183(5):753-761.
Pasmans F, DeHerdt P, Haesebrouck. Presence of Salmonella infections in freshwater turtles. Vet Rec.2002 Jun 1: 150(22):692-693.
Pasmans F, Martel A, Boyen F, Vandederchove D, Wybo I, Immerseel FV, Heyndrickx M, Collard JM, Ducatelle R, Haesebrouck F. Characterization of Salmonella isolates from captive lizards. Vet Micro. 2005;110:285-291.
Porter RS, Kaplan JL, editors. The Merck manual [monograph online]. 18th ed. Whitehouse Station, NJ: Merck and Co.; 2012. Salmonella infections. Available at: http://www.merckmanuals.com/professional/infectious_diseas es/gram-negative_bacilli/salmonella_infections.html
Public Health Agency of Canada, Office of Laboratory Security. Material Safety Data Sheet – Salmonella spp. (excluding S. typhi, S. choleraesuis, and S. paratyphi). Office of Laboratory Security; 2001 Mar. Available at: http://www.phac- aspc.gc.ca/msds-ftss/msds135e.html
Ramsay EC, Daniel GB, Tryon BW, Merryman JI, Morris PJ, Bemis DA. Osteomyelitis associated with Salmonella enterica SS arizonae in a colony of ridgenose rattlesnakes (Crotalus willardi). J Zoo Wildl Med. 2002;33:301-310.
Schroter M, Roggentin P, Hofmann J, Speicher A, Laufs R, Mack D. Pet snakes as a reservoir for Salmonella enterica subsp. diarizonae (Serogroup IIIb): a prospective study. Appl Environ Microbiol. 2004;70:613-615.
Schroter M, Speicher A, Hogmann J, Roggentin P. Analysis of the transmission of Salmonella spp. through generations of pet snakes. Environ Microbiol. 2006 Mar;8(3):556-9.
Stam F, Romkens EH, Hekker TA, Smulders YM. Turtle- associated human salmonellosis. CID. 2003 Dec 1;37:e167-69.
The Humane Society of the United States [HSUS]. The trade in live reptiles: imports to the United States [online]. HSUS;2001. Available at: http://www.humanesociety.org/assets/pdfs/wildlife/exotics/rep tile_trade_import.pdf
Vora NM, Smith KM, Machalaba CC, Karesh WB. Reptile- and Amphibian-associated Salmonellosis in Childcare Centers, United States [letter]. Emerg Infect Dis [online]. 2012 Dec Available at: http://wwwnc.cdc.gov/eid/article/18/12/12- 0784_article.htm
Ward L. Salmonella perils of pet reptiles. Commun Dis Public Health 2000 Mar;3(1):2-3.
Warwick C, Lambiris AJL, Westwood D, Steedman C. Reptile- related salmonellosis. J R Soc Med. 2001 Mar;94(3):124-126.
Wells EV, Boulton M, Hall W, Bidol SA. Reptile-assoicated salmonellosis in preschool-aged children in Michigan, January 2001-June 2003. CID. 2004 Sep 1;39:687-691.
Weil BJ, Martens PB, Harte JS. Iguana-associated salmonellosis in a young adult. J Adolesc Health. 1995 Aug;17(2):120-122.
Willis C, Wilson T, Greenwood M, Ward L. Pet reptiles associated with a case of salmonellosis in an infant were carrying multiple strains of Salmonella. J Clin Microbiol. 2002;40:4802-3.
Wise JK, Heathcott BL, Gonzalez ML. Results of the AVMA survey on companion animal ownership in U.S. pet-owning households. J Am Vet Med Assoc. 2002;221:1572-1573.
Woodward DL, Khakhria R, Johnson WM. Human salmonellosis associated with exotic pets. J Clin Microbiol. 1997 Nov;35(11):2786-2790.