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

https://doi.org/10.17221/44/2017-VETMEDCitation:Tomastikova Z., Barazorda Romero S., Knotek Z., Karpiskova R. (2017): Prevalence and characteristics of Salmonella species isolated from captive reptiles in the Czech Republic. Veterinarni Medicina, 62: 456-469.
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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.
References:
Aiken A M, Lane C, Adak G K (2010): Risk of Salmonella infection with exposure to reptiles in England, 2004-2007. Eurosurveillance, 15, -  https://doi.org/10.2807/ese.15.22.19581-en
 
Aleksic S., Heinzerling F., Bockemühl J. (1996): Human Infection Caused by Salmonellae of Subspecies II to VI in Germany, 1977–1992. Zentralblatt für Bakteriologie, 283, 391-398  https://doi.org/10.1016/S0934-8840(96)80074-0
 
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.
 
Romero Silvia Barazorda, Knotek Zdeněk, Čížek Alois, Masaříková Martina, Myšková Petra (2015): The incidence and antibiotic resistance of Salmonella species isolated from cloacae of captive veiled chameleons. Acta Veterinaria Brno, 84, 209-213  https://doi.org/10.2754/avb201584030209
 
Baumler AJ, Tsolis RM, Ficht TA, Adams LG (1998): Evolution in host adaptation in Salmonella enterica. Infection and Immunity 66, 4579–4587.
 
Bauwens L., Vercammen F., Bertrand S., Collard J.-M., De Ceuster S. (2006): Isolation of Salmonella from environmental samples collected in the reptile department of Antwerp Zoo using different selective methods. Journal of Applied Microbiology, 101, 284-289  https://doi.org/10.1111/j.1365-2672.2006.02977.x
 
Bertelloni Fabrizio, Chemaly Marianne, Cerri Domenico, Gall Françoise Le, Ebani Valentina Virginia (2016): Salmonella infection in healthy pet reptiles: Bacteriological isolation and study of some pathogenic characters. Acta Microbiologica et Immunologica Hungarica, 63, 203-216  https://doi.org/10.1556/030.63.2016.2.5
 
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.
 
Briones Victor, Tellez Sonia, Goyache Joaquin, Ballesteros Cristina, del Pilar Lanzarot Maria, Dominguez Lucas, Fernandez-Garayzabal Jose F. (2004): Salmonella diversity associated with wild reptiles and amphibians in Spain. Environmental Microbiology, 6, 868-871  https://doi.org/10.1111/j.1462-2920.2004.00631.x
 
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-puff-cereal-5-13-2008.html (Accessed June 7, 2017).
 
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).
 
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).
 
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).
 
Chambers D. L., Hulse A. C. (): Salmonella Serovars in the Herpetofauna of Indiana County, Pennsylvania. Applied and Environmental Microbiology, 72, 3771-3773  https://doi.org/10.1128/AEM.72.5.3771-3773.2006
 
Chen C.-Y., Chen W.-C., Chin S.-C., Lai Y.-H., Tung K.-C., Chiou C.-S., Hsu Y.-M., Chang C.-C. (2010): Prevalence and Antimicrobial Susceptibility of Salmonellae Isolates from Reptiles in Taiwan. Journal of Veterinary Diagnostic Investigation, 22, 44-50  https://doi.org/10.1177/104063871002200107
 
CHIODINI RODRICK J., SUNDBERG JOHN P. (1981): SALMONELLOSIS IN REPTILES: A REVIEW12. American Journal of Epidemiology, 113, 494-499  https://doi.org/10.1093/oxfordjournals.aje.a113124
 
CLSI – Clinical and Laboratory Standards Institute (2016): Performance standards for antimicrobial susceptibility testing – M100-S26. Twenty-six informational supplement. Wayne, Pensylvania, USA. 296 pp.
 
Freitas Neto OC de, Penha Filho RAC, Barrow P, Berchieri Junior A (2010): Sources of human non-typhoid salmonellosis: a review. Revista Brasileira de Ciência Avícola, 12, 01-11  https://doi.org/10.1590/S1516-635X2010000100001
 
De Sa IVA, Solari CA (2001): Salmonella in Brazilian and imported pet reptiles. Brazilian Journal of Microbiology 32, 293–297.
 
Ebani V.V., 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  https://doi.org/10.1016/j.rvsc.2004.08.002
 
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-trends-sources-EU-summary-report-2014.pdf (Accessed June 7, 2017).
 
Eng Shu-Kee, Pusparajah Priyia, Ab Mutalib Nurul-Syakima, Ser Hooi-Leng, Chan Kok-Gan, Lee Learn-Han (): Salmonella : A review on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Science, 8, 284-293  https://doi.org/10.1080/21553769.2015.1051243
 
EVERARD C.O.R., TOTA BRAJIN, BASSETT DAVID, ALI CAMEILLE (1979): Salmonella IN WILDLIFE FROM TRINIDAD AND GRENADA, W.I.. Journal of Wildlife Diseases, 15, 213-219  https://doi.org/10.7589/0090-3558-15.2.213
 
Gay Noellie, Le Hello Simon, Weill François-Xavier, de Thoisy Benoit, Berger Franck (2014): Salmonella serotypes in reptiles and humans, French Guiana. Veterinary Microbiology, 170, 167-171  https://doi.org/10.1016/j.vetmic.2014.01.024
 
Geue L., Löschner U. (2002): Salmonella enterica in reptiles of German and Austrian origin. Veterinary Microbiology, 84, 79-91  https://doi.org/10.1016/S0378-1135(01)00437-0
 
Giacopello Cristina, Foti Maria, Fisichella Vittorio, Latella Giuseppe, Aleo Aurora, Mammina Caterina (2012): Antibiotic Resistance in Salmonella Isolated from Tegus (Tupinambis spp.). Journal of Exotic Pet Medicine, 21, 328-331  https://doi.org/10.1053/j.jepm.2012.09.008
 
Gopee Neera V., Adesiyun Abiodun A., Caesar Kenneth (2000): RETROSPECTIVE AND LONGITUDINAL STUDY OF SALMONELLOSIS IN CAPTIVE WILDLIFE IN TRINIDAD. Journal of Wildlife Diseases, 36, 284-293  https://doi.org/10.7589/0090-3558-36.2.284
 
Katsuno Shinsuke, Ando Hisami, Seo Takahiko, Shinohara Tsuyoshi, Ochiai Keiko, Ohta Michio (2003): A case of retroperitoneal abscess caused by Salmonella Oranienburg. Journal of Pediatric Surgery, 38, 1693-1695  https://doi.org/10.1016/j.jpedsurg.2003.08.012
 
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.
 
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.
 
Nicewonger C. R., Phillips A. G., Taylor Joan, Lapage S. P. (1966): New serotypes of Salmonella identified before 1964 at the Salmonella Reference Laboratory, Colindale. International Journal of Systematic and Evolutionary Microbiology, 16, 253-298  https://doi.org/10.1099/00207713-16-3-253
 
Lukac Maja, Pedersen Karl, Prukner-Radovcic Estella (2015): PREVALENCE OF SALMONELLA IN CAPTIVE REPTILES FROM CROATIA. Journal of Zoo and Wildlife Medicine, 46, 234-240  https://doi.org/10.1638/2014-0098R1.1
 
Makin Guy, Abu-Harb Majd, Finn Adam, Partridge Susan (1996): Salmonella durban in an infant. The Lancet, 348, 200-  https://doi.org/10.1016/S0140-6736(05)66150-8
 
Münch Sebastian, Braun Peggy, Wernery Ulrich, Kinne Jörg, Pees Michael, Flieger Antje, Tietze Erhard, Rabsch Wolfgang (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  https://doi.org/10.1007/s11250-012-0130-4
 
Murphy Dan, Oshin Femi (): Reptile-associated salmonellosis in children aged under 5 years in South West England: Figure 1. Archives of Disease in Childhood, 100, 364-365  https://doi.org/10.1136/archdischild-2014-306134
 
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.
 
NAKADAI Aya, KUROKI Toshiro, KATO Yukio, SUZUKI Rieko, YAMAI Shiro, YAGINUMA Chiharu, SHIOTANI Ryo, YAMANOUCHI Akira, HAYASHIDANI Hideki (2005): Prevalence of Salmonella spp. in Pet Reptiles in Japan. Journal of Veterinary Medical Science, 67, 97-101  https://doi.org/10.1292/jvms.67.97
 
Onderka DK, Finlayson MC (1985): Salmonella and salmonellosis in captive reptiles. Canadian Journal of Comparative Medicine 49, 268–270.
 
Pedersen K., Lassen-Nielsen A.-M., Nordentoft S., Hammer A. S. (2009): Serovars of Salmonella from captive reptiles. Zoonoses and Public Health, 56, 238-242  https://doi.org/10.1111/j.1863-2378.2008.01196.x
 
Pees M, Rabsch W, Plenz B, Fruth A, Prager R, Simon S, Schmidt V, Münch S, Braun P G (2013): Evidence for the transmission of Salmonella from reptiles to children in Germany, July 2010 to October 2011. Eurosurveillance, 18, -  https://doi.org/10.2807/1560-7917.ES2013.18.46.20634
 
Pfleger Silvia, Benyr Gerald, Sommer Regina, Hassl Andreas (2003): Pattern of Salmonella excretion in amphibians and reptiles in a vivarium. International Journal of Hygiene and Environmental Health, 206, 53-59  https://doi.org/10.1078/1438-4639-00184
 
Piasecki Tomasz, Chrząstek Klaudia, Wieliczko Alina (2014): Salmonella serovar spectrum associated with reptiles in Poland. Acta Veterinaria Brno, 83, 287-294  https://doi.org/10.2754/avb201483040287
 
Sarwari Arif R., Magder Laurence S., Levine Priscilla, McNamara Ann Marie, Knower Susan, Armstrong Gregory L., Etzel Ruth, Hollingsworth Jill, Morris, Jr. J. Glenn (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  https://doi.org/10.1086/319671
 
Schrire L., Crisp S., Bear N., McStay G., Koornhof H. J., Le Minor L. (1987): The prevalence of human isolates of Salmonella subspecies II in southern Africa. Epidemiology and Infection, 98, 25-  https://doi.org/10.1017/S0950268800061689
 
Seepersadsingh N., Adesiyun A. A. (2003): Prevalence and Antimicrobial Resistance of Salmonella spp. in Pet Mammals, Reptiles, Fish Aquarium Water, and Birds in Trinidad. Journal of Veterinary Medicine Series B, 50, 488-493  https://doi.org/10.1046/j.0931-1793.2003.00710.x
 
Stam F., Romkens T. E. H., Hekker T. A. M., Smulders Y. M. (2003): Turtle-Associated Human Salmonellosis. Clinical Infectious Diseases, 37, e167-e169  https://doi.org/10.1086/379612
 
Sylvester W. R. B., Amadi V., Pinckney R., Macpherson C. N. L., McKibben J. S., 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  https://doi.org/10.1111/zph.12093
 
Weiss Bettina, Rabsch Wolfgang, Prager Rita, Tietze Erhard, Koch Judith, Mutschmann Frank, Roggentin Peter, Frank Christina (2011): Babies and Bearded Dragons: Sudden Increase in Reptile-Associated Salmonella enterica Serovar Tennessee Infections, Germany 2008. Vector-Borne and Zoonotic Diseases, 11, 1299-1301  https://doi.org/10.1089/vbz.2010.0239
 
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. https://doi.org/10.1186/1471-2334-5-7
 
Wikström Veronica O, Fernström Lise-Lotte, Melin Lennart, Boqvist Sofia (2014): Salmonella isolated from individual reptiles and environmental samples from terraria in private households in Sweden. Acta Veterinaria Scandinavica, 56, 7-  https://doi.org/10.1186/1751-0147-56-7
 
Woodward DL, Khakhria R, Johnson WM (1997): Human salmonellosis associated with exotic pets. Journal of Clinical Microbiology 35, 2786–2790.
 
Yang Wei-Chiun, Chan Oi-Wa, Wu Tsu-Lan, Chen Chyi-Liang, Su Lin-Hui, Chiu Cheng-Hsun (2016): Development of ceftriaxone resistance in Salmonella enterica serotype Oranienburg during therapy for bacteremia. Journal of Microbiology, Immunology and Infection, 49, 41-45  https://doi.org/10.1016/j.jmii.2014.01.011
 
Zaidi M. B., McDermott P. F., Fedorka-Cray P., Leon V., Canche C., Hubert S. K., 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  https://doi.org/10.1086/498508
 
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