Vet Med - Czech, 2017, 62(8):456-469 | DOI: 10.17221/44/2017-VETMED

Prevalence and characteristics of Salmonella species isolated from captive reptiles in the Czech RepublicOriginal Paper

Z. Tomastikova*,1, S. Barazorda Romero2, Z. Knotek2, R. Karpiskova1
1 Veterinary Research Institute, Brno, Czech Republic
2 University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

This study was aimed at determining the prevalence and characterising the strains of Salmonella species in various captive reptiles in the Czech Republic. A total of 211 samples of cloacal swabs from lizards, chelonians and snakes, and 14 swabs from terraria surfaces were collected between November 2014 and July 2015. After isolation according to the reference method (EN ISO), Salmonella spp. isolates were characterised using serotyping and macrorestriction analysis followed by pulsed field gel electrophoresis and antimicrobial susceptibility testing. Altogether, 39 isolates were obtained from 29 (19%) reptiles and from terraria surfaces. Among the different reptilian species, Salmonella spp. were found in 22 (25.6%) lizards, three (17.6%) snakes and four (8%) chelonians with 31 isolates classified as Salmonella enterica subspecies enterica and eight isolates classified as Salmonella enterica subsp. salamae. In total, 14 different serotypes were detected, with the most frequent serotypes being Salmonella Oranienburg, S. Fluntern, S. Tennessee and S. Cotham. Resistance to one antimicrobial agent (ampicillin, tetracycline or streptomycin) was detected in five isolates. The results of the macrorestriction analysis within the serotype groups showed varying level of heterogeneity. This study confirms that reptiles kept as pets can be both carriers and reservoirs of Salmonella spp., and that they can harbour various serotypes with intermittent excretion of the bacteria in faeces. Half of the detected serotypes have been involved in human reptile-associated salmonellosis cases in the past. S. enterica subsp. salamae serotype O:1,13,23;H:z29;H:1,5, monophasic S. enterica subsp. salamae serotype O:40;H:g,t;H:- and its biphasic form (S. enterica subsp. salamae serotype O:40;H:g,t;H:1,5) have apparently been isolated from reptiles for the first time in this study.

Keywords: reptile-associated salmonellosis; serotyping; macrorestriction analysis; antimicrobial susceptibility; reptile species

Published: August 31, 2017  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Tomastikova Z, Barazorda Romero S, Knotek Z, Karpiskova R. Prevalence and characteristics of Salmonella species isolated from captive reptiles in the Czech Republic. Vet Med-Czech. 2017;62(8):456-469. doi: 10.17221/44/2017-VETMED.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aiken AM, Lane C, Adak GK (2010): Risk of Salmonella infection with exposure to reptiles in England, 2004- 2007. Eurosurveillance 15, 11-18. Go to original source...
    2. Aleksic S, Heinzerling F, Bockemuhl J (1996): Human infection caused by salmonellae of subspecies II to VI in Germany, 1977-1992. International Journal of Medical Bacteriology 283, 391-398. Go to original source... Go to PubMed...
    3. Angelo KM, Chu A, Anand M, Nguyen TA, Bottichio L, Wise M, Williams I, Seelman S, Bell R, Fatica M, Lance S, Baldwin D, Shannon K, Lee H, Trees E, Strain E, Gieraltowski L (2015): Outbreak of Salmonella Newport infections linked to cucumbers - United States, 2014. Morbidity and Mortality Weekly Report 64, 144-147.
    4. Barazorda Romero S, Knotek Z, Cizek A, Masarikova M, Myskova P (2015): The incidence and antibiotic resistance of Salmonella species isolated from cloacae of captive veiled chameleons. Acta Veterinaria Brno 84, 209-213. Go to original source...
    5. Baumler AJ, Tsolis RM, Ficht TA, Adams LG (1998): Evolution in host adaptation in Salmonella enterica. Infection and Immunity 66, 4579-4587. Go to original source... Go to PubMed...
    6. Bauwens L, Vercammen F, Bertrand S, Collard JM, De Ceuster S (2006): Isolation of Salmonella from environmental samples collected in reptile department of Antwerp Zoo using different selective methods. Journal of Applied Microbiology 101, 284-289. Go to original source... Go to PubMed...
    7. Bertelloni F, Chemaly M, Cerri D, Le Gall F, Ebani VV (2016): Salmonella infection in healthy pet reptiles: bacteriological isolation and study of some pathogenic characters. Acta Microbiologica and Immunologica Hungarica 63, 203-216. Go to original source... Go to PubMed...
    8. Bertrand S, Rimhanen-Finne R, Weill FX, Rabsch W, Thornton L, Perevoscikovs J, Van Pelt W, Heck M (2008): Salmonella infections associated with reptiles: the current situation in Europe. Eurosurveillance 13, 264-269. Go to original source...
    9. Briones V, Tellez S, Goyache J, Ballesteros C, Del Pilar Lanzarot M, Dominguez L, Fernandez-Garayzabal JF (2004): Salmonella diversity associated with wild reptiles and amphibians in Spain. Environmental Microbiology 6, 868-871. Go to original source... Go to PubMed...
    10. CDC - Centers for Disease Control and Prevention (2008): Multistate outbreak of Salmonella Agona infections linked to rice and wheat puff cereals (final update). Available at www.cdc.gov/salmonella/2008/rice-wheat-puffcereal-5-13-2008.html (Accessed June 7, 2017).
    11. CDC - Centers for Disease Control and Prevention (2011): Multistate outbreak of human Salmonella Agona infections linked to whole, fresh imported papayas (final update). Available at www.cdc.gov/salmonella/2011/ papayas-8-29-2011.html (Accessed June 7, 2017).
    12. CDC - Centers for Disease Control and Prevention (2014): Multistate outbreak of Salmonella Cotham and Salmonella Kisarawe infections linked to contact with pet bearded dragons (final update). Available at www.cdc.gov/salmonella/cotham-04-14/ (Accessed June 7, 2017).
    13. CDC - Centers for Disease Control and Prevention (2016): National enteric disease surveillance: Salmonella annual report, 2013. Available at www.cdc.gov/nationalsurveillance/pdfs/salmonella-annual-report-2013-508c.pdf (Accessed June 7, 2017).
    14. Chambers DL, Hulse AC (2006): Salmonella serovars in herpetofauna of Indiana County, Pennsylvania. Applied and Environmental Microbiology 72, 3771-3773. Go to original source... Go to PubMed...
    15. Chen CY, Chen WC, Chin SC, Lai YH, Tung KC, Chiou CS, Hsu YM, Chang CC (2010): Prevalence and antimicrobial susceptibility of salmonellae isolates from reptiles in Taiwan. Journal of Veterinary Diagnostic Investigation 22, 44-50. Go to original source... Go to PubMed...
    16. Chiodini RJ, Sundberg JP (1981): Salmonellosis in reptiles: a review. American Journal of Epidemiology 113, 494- 499. Go to original source... Go to PubMed...
    17. CLSI - Clinical and Laboratory Standards Institute (2016): Performance standards for antimicrobial susceptibility testing - M100-S26. Twenty-six informational supplement. Wayne, Pensylvania, USA. 296 pp.
    18. De Freitas Neto OC, Penha Filho RAC, Barrow P, Berchieri Junior A (2010): Sources of human non-typhoid salmonellosis: a review. Brazilian Journal of Poultry Science 12, 1-11. Go to original source...
    19. De Sa IVA, Solari CA (2001): Salmonella in Brazilian and imported pet reptiles. Brazilian Journal of Microbiology 32, 293-297. Go to original source...
    20. Ebani VV, Cerri D, Fratini F, Meille N, Valentini P, Andreani E (2005): Salmonella enterica isolates from faeces of domestic reptiles and a study of their antimicrobial in vitro sensitivity. Research in Veterinary Science 78, 117-121. Go to original source... Go to PubMed...
    21. EFSA and ECDC - European Food Safety Authority and European Centre for Disease Prevention and Control (2015): The European Union summary report on trends of zoonoses, zoonotic agents and food - borne outbreaks in 2014. EFSA Journal 13. 191 pp. Available at http://ecdc.europa.eu/en/publications/Publications/zoonoses-trendssources-EU-summary-report-2014.pdf (Accessed June 7, 2017). Go to original source...
    22. Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH (2015): Sallmonella: A review on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Science 8, 284-293. Go to original source...
    23. Everard COR, Tota B, Bassett D, Ali C (1979): Salmonella in wildlife from Trinidad and Grenada. Journal of Wildlife Diseases 15, 213-219. Go to original source... Go to PubMed...
    24. Gay N, Le Hello S, Weill FX, De Thoisy B, Berger F (2014): Salmonella serotypes in reptiles and humans, French Guiana. Veterinary Microbiology 170, 167-171. Go to original source... Go to PubMed...
    25. Geue L, Loschner U (2002): Salmonella enterica in reptiles of German and Austrian origin. Veterinary Microbiology 84, 79-91. Go to original source... Go to PubMed...
    26. Giacopello C, Foti M, Fisichella V, Latella G, Aleo A, Mammina C (2012): Antibiotic resistance in Salmonella isolated from tegus (Tupinambis spp.). Journal of Exotic Pet Medicine 21, 328-331. Go to original source...
    27. Gopee NV, Adesiyun AA, Caesar K (2000): Retrospective and longitudinal study of salmonellosis in captive wildlife in Trinidad. Journal of Wildlife Diseases 36, 284-293. Go to original source... Go to PubMed...
    28. Katsuno S, Ando H, Seo T, Shinohara T, Ochiai K, Ohta M (2003): A case of retroperitoneal abscess caused by Salmonella Oranienburg. Journal of Pediatric Surgery 38, 1693-1695. Go to original source... Go to PubMed...
    29. Kim S, Choi YG, Eom JW, Oh TJ, Lee KS, Kim SH, Lee ET, Park MS, Oh HB, Lee BK (2007): An outbreak of Salmonella enterica serovar Othmarschen at a funeral service in Guri-Si, South Korea. Japanese Journal of Infectious Diseases 60, 412-413. Go to original source...
    30. Landry L, Phan Q, Kelly S, Phillips K, Onofrey S, Daly ER, Talbot EA, Fage M, Deasy M, Spayne M, Lynch M, Olson CK (2007): Salmonella Oranienburg infections associated with fruit salad served in health-care facilities-northeastern United States and Canada 2006. Mobility and Mortality Weekly Reports 56, 1025-1028.
    31. Lapage SP, Taylor J, Nicewonger CR, Phillips AG (1966): New serotypes of Salmonella identified before 1964 at the Salmonella Reference Laboratory, Collindale. International Journal of Systematic Bacteriology 16, 253-297. Go to original source...
    32. Lukac M, Pedersen K, Prukner-Radovcic E (2015): Prevalence of Salmonella in captive reptiles from Croatia. Journal of Zoo and Wildlife Medicine 46, 234-240. Go to original source... Go to PubMed...
    33. Makin G, Abu-Harb M, Finn A, Partridge S (1996): Salmonella Durban in an infant. The Lancet 348, 200. Go to original source... Go to PubMed...
    34. Munch S, Braun P, Wernery U, Kinne J, Pees M, Flieger A, Tietze E, Rabsch W (2012): Prevalence, serovars phage types and antibiotic susceptibilities of Salmonella strains isolated from animals in the United Arab Emirates from 1996 to 2009. Tropical Animal Health and Production 44, 1725-1738. Go to original source... Go to PubMed...
    35. Murphy D, Oshin F (2015): Reptile-associated salmonellosis in children aged under 5 years in South West England. Archives of Disease in Childhood 100, 364-365. Go to original source... Go to PubMed...
    36. Myskova P, Karpiskova R (2014): Diversity of human Salmonella isolates in the South Moravian Region in 2009-2012 (in Czech). Epidemiologie, Mikrobiologie, Imunologie 63, 116-120.
    37. Nakadai A, Kuroki T, Kato Y, Suzuki R, Yamai S, Yaginuma C, Shiotani R, Yamanouchi A, Hayashidani H (2005): Prevalence of Salmonella spp. in pet reptiles in Japan. Journal of Veterinary Medical Science 67, 97-101. Go to original source... Go to PubMed...
    38. Onderka DK, Finlayson MC (1985): Salmonella and salmonellosis in captive reptiles. Canadian Journal of Comparative Medicine 49, 268-270.
    39. Pedersen K, Lassen-Nielsen AM, Nordentoft S, Hammer AS (2009): Serovars of Salmonella from captive reptiles. Zoonoses and Public Health 56, 238-242. Go to original source... Go to PubMed...
    40. Pees M, Rabsch W, Plenz B, Fruth A, Prager R, Simon S, Schmidt V, Munch S, Braun PG (2013): Evidence for the transmission of Salmonella from reptiles to children in Germany, July 2010 to October 2011. Eurosurveillance 18, 12-21. Go to original source... Go to PubMed...
    41. Pfleger S, Benyr G, Sommer R, Hassl A (2003): Pattern of Salmonella excretion in amphibians and reptiles in vivarium. International Journal of Hygiene and Environmental Health 206, 53-59. Go to original source... Go to PubMed...
    42. Piasecki T, Chrzastek K, Wieliczko A (2014): Salmonella serovar spectrum associated with reptiles in Poland. Acta Veterinaria Brno 83, 287-294. Go to original source...
    43. Sarwari AR, Magder LS, Levine P, McNamara AM, Knower S, Armstrong GL, Etzel R, Hollingsworth J, Morris JG (2001): Serotype distribution of Salmonella isolates from food animals after slaughter differs from that of isolates found in humans. The Journal of Infectious Diseases 183, 1295-1299. Go to original source... Go to PubMed...
    44. Schrire L, Crisp S, Bear N, McStay G, Koornhof HJ, Le Minor L (1987): The prevalence of human isolates of Salmonella subspecies II in southern Africa. Epidemiology and Infection 98, 25-31. Go to original source... Go to PubMed...
    45. Seepersadsingh N, Adesiyun AA (2003): Prevalence and antimicrobial resistance of Salmonella spp. in pet mammals, reptiles, fish aquarium water and birds in Trinidad. Journal of Veterinary Medicine B, Infectious Diseases and Veterinary Public Health 50, 488-493. Go to original source... Go to PubMed...
    46. Stam F, Romkens TEH, Hekker TAM, Smulders YM (2003): Turtle-associated human salmonellosis. Clinical Infectious Diseases 37, 167-169. Go to original source... Go to PubMed...
    47. Sylvester WR, Amadi V, Pinckney R, Macpherson CN, McKibben JS, Bruhl-Day R, Johnson R, Hariharan H (2014): Prevalence, serovars and antimicrobial susceptibility of Salmonella spp. from wild and domestic green iguanas (Iguana iguana) in Grenada, West Indies. Zoonoses and Public Health 61, 436-441. Go to original source... Go to PubMed...
    48. Weiss B, Rabsch W, Prager R, Tietze E, Koch J, Mutschmann F, Roggentin P, Frank C (2011): Babies and bearded dragons: Sudden increase in reptile-associated Salmonella enterica serovar Tennessee infections, Germany 2008. Vector-Borne Zoonotic Diseases 11, 1299-1301. Go to original source... Go to PubMed...
    49. Werber D, Dreesman J, Feil F, Van Treeck U, Fell G, Ethelberg S, Hauri A, Roggentin P, Prager R, Fisher I, Behnke S, Bartelt E, Weise E, Ellis A, Siitonen A, Andersson Y, Tschape H, Kramer M, Ammon A (2005): International outbreak of Salmonella Oranienburg due to German chocolate. BMC Infectious Diseases 5, 7. Go to original source... Go to PubMed...
    50. Wikstrom VO, Fernstrom LL, Melin L, Boqvist S (2014): Salmonella isolated from individual reptiles and environmental samples from terraria in private households in Sweden. Acta Veterinaria Scandinavica 56, 7. Go to original source... Go to PubMed...
    51. Woodward DL, Khakhria R, Johnson WM (1997): Human salmonellosis associated with exotic pets. Journal of Clinical Microbiology 35, 2786-2790. Go to original source... Go to PubMed...
    52. Yang WC, Chan OW, Wu TL, Chen CL, Su LH, Chiu CH (2014): Development of ceftriaxone resistence in Salmonella enterica serotype Oranienburg during therapy for bacteremia. Journal of Microbiology, Immunology and Infection 49, 41-45. Go to original source... Go to PubMed...
    53. Zaidi MB, McDermott PF, Fedorka-Cray P, Leon V, Canche C, Hubert SK, Abbott J, Leon M, Zhao S, Headrick M, Tollefson L (2006): Nontyphoidal Salmonella from human clinical cases, asymptomatic children and raw retail meats in Yucatan, Mexico. Clinical Infectious Diseases 42, 21-28. Go to original source... Go to PubMed...

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content