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Quinolone susceptibility and genetic characterization of Salmonella enterica subsp. enterica isolated from pet turtles


Turtle-borne Salmonella enterica owns significance as a leading cause in human salmonellosis. The current study aimed to determine the quinolone susceptibility and the genetic characteristics of 21 strains of S. enterica subsp. enterica isolated from pet turtles. Susceptibility of four antimicrobials including nalidixic acid, ciprofloxacin, ofloxacin, and levofloxacin was examined in disk diffusion and MIC tests where the majority of the isolates were susceptible to all tested quinolones. In genetic characterization, none of the isolates were positive for qnr or aac(6’)-Ib genes and no any target site mutations could be detected in gyrA, gyrB, and parC quinolone resistance determining regions (QRDR). In addition, neighbor-joining phylogenetic tree derived using gyrA gene sequences exhibited two distinct clads comprising; first, current study isolates, and second, quinolone-resistant isolates of human and animal origin. All results suggest that studied strains of S. enterica subsp. enterica isolated from pet turtles are susceptible to quinolones and genetically more conserved with regards to gyrA gene region.


  1. 1.

    Hui YH, Gorham JR, Murrell KD. Foodborne Disease Handbook; Vol. 1; Diseases Caused by Bacteria, Marcel Dekker Inc., New York, 1994; pp 97–131.

    Google Scholar 

  2. 2.

    Barrow PA, Methner U. Salmonella in Domestic Animals. 2nd ed, CABI, UK, 2013. pp 136–351.

    Book  Google Scholar 

  3. 3.

    Marcus R. New information about pediatric foodborne infections: the view from FoodNet. Curr Opin Pediatr 2008; 20(1): 79–84.

    PubMed  Article  Google Scholar 

  4. 4.

    Bennett SD, Manikonda K, Mungai E, Dewey-Mattia D, Gould LH. Surveillance. 2014 [cited 2016 Dec 31]; Available from:

    Google Scholar 

  5. 5.

    Kruse H, kirkemo AM, Handeland K. Wildlife as source of zoonotic infections. Emerg Infect Dis 2004; 10(12): 2067–2072.

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Eng S-K, Pusparajah P, Ab Mutalib N-S, Ser H-L, Chan K-G, Lee L-H. Salmonella: A review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci 2015; 8(3): 284–293.

    CAS  Article  Google Scholar 

  7. 7.

    Kownhar H, Shankar EM, Rajan R, Rao UA. Emergence of nalidixic acid-resistant Salmonella enterica serovar Typhi resistant to ciprofloxacin in India. J Med Microbiol 2007; 56(1):136-137.

    Google Scholar 

  8. 8.

    Souza RB, Ferrari RG, Magnani M, Kottwitz LB, Alcocer I, Tognim MC, Oliveira TC. Ciprofloxacin susceptibility reduction of Salmonella strains isolated from outbreaks. Braz J Microbiol 2010; 41(2): 497–500.

    PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Carrique-Mas JJ, Papadopoulou C, Evans SJ, Wales A, Teale CJ, Davies RH. Trends in phage types and antimicrobial resistance of Salmonella enterica serovar Enteritidis isolated from animals in Great Britain from 1990 to 2005. Vet Rec 2008; 162(17): 541–546.

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Meakins S, Fisher IS, Berghold C, Gerner-Smidt P, Tschäpe H, Cormican M, Luzzi I, Schneider F, Wannett W, Coia J, Echeita A, Threlfall EJ; Enter-net participants. Antimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000-2004: a report from the Enter-net International Surveillance Network. Microb Drug Resist 2008; 14(1): 31–35.

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Eaves DJ, Randall L, Gray DT, Buckley A, Woodward MJ, White AP, Piddock LJ. Prevalence of mutations within the quinolone resistance-determining region of gyrA, gyrB, parC, and parE and association with antibiotic resistance in quinolone-resistant Salmonella enterica. Antimicrob Agents Chemother 2004; 48(10): 4012–4015.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Avsaroglu MD, Helmuth R, Junker E, Hertwig S, Schroeter A, Akcelik M, Bozoglu F, Guerra B. Plasmid-mediated quinolone resistance conferred by qnrS1 in Salmonella enterica serovar Virchow isolated from Turkish food of avian origin. J Antimicrob Chemother 2007; 60(5): 1146–1150.

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A. Plasmid-mediated quinolone resistance: an update. J Infect Chemother 2011; 17(2): 149–182.

    PubMed  Article  Google Scholar 

  14. 14.

    Warwick C, Arena PC, Steedman C. Health implications associated with exposure to farmed and wild sea turtles. JRSM Short Rep 2013; 4(1): 8.

    PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Warwick C, Arena PC, Steedman C, Jessop M. A review of captive exotic animal-linked zoonoses. J Environ Health Res 2012; 12(1): 9–24.

    Google Scholar 

  16. 16.

    Shin D-M, Hossain S, Wimalasena S, Heo G-J. Antimicrobial resistance and virulence factors of Edwardsiella tarda isolated from pet turtles. Pak Vet J 2016; 37(1): 85–89.

    Google Scholar 

  17. 17.

    Wendt M, Heo GJ. Multilocus sequence typing analysis of Pseudomonas aeruginosa isolated from pet Chinese stripe-necked turtles (Ocadia sinensis). Lab Anim Res 2016; 32(4): 208–216.

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Hossain S, Wimalasena SHMP, Heo G-J. Virulence factors and antimicrobial resistance pattern of Citrobacter freundii isolated from healthy pet turtles and their environment. Asian J Anim Vet Adv 2017; 12(1): 10–16.

    CAS  Article  Google Scholar 

  19. 19.

    Bosch S, Tauxe RV, Behravesh CB. Turtle-Associated Salmonellosis, United States, 2006–2014. Emerg Infect Dis 2016; 22(7): 1149–1155.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    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; 243(12): 1247–1249.

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Díaz MA, Cooper RK, Cloeckaert A, Siebeling RJ. Plasmid-mediated high-level gentamicin resistance among enteric bacteria isolated from pet turtles in Louisiana. Appl Environ Microbiol 2006; 72(1): 306–312.

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Nowakiewicz A, Ziółkowska G, Zięba P, Stępniewska K, Tokarzewski S. Russian tortoises (Agrionemys horsfieldi) as a potential reservoir for Salmonella spp. Res Vet Sci 2012; 92(2): 187–190.

    PubMed  Article  Google Scholar 

  23. 23.

    Giacopello C, Foti M, Passantino A, Fisichella V, Aleo A, Mammina C. Serotypes and antibiotic susceptibility patterns of Salmonella spp. isolates from spur-thighed tortoise, Testudo graeca illegally introduced in Italy. HVM Bioflux 2012; 4(2): 76–81.

    Google Scholar 

  24. 24.

    Bertelloni F, Chemaly M, Cerri D, Gall FL, Ebani V. V. Salmonella infection in healthy pet reptiles: Bacteriological isolation and study of some pathogenic characters. Acta Microbiol Immunol Hung 2016; 63(2): 203–216.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Back DS, Shin GW, Wendt M, Heo GJ. Prevalence of Salmonella spp. in pet turtles and their environment. Lab Anim Res 2016; 32(3): 166–170.

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Bluvias JE, Eckert KL. Marine Turtle Trauma Response Procedures: A Husbandry Manual, Wider Caribbean Sea Turtle Conservation Network (WIDECAST), 2008; pp 11–46.

    Google Scholar 

  27. 27.

    CLSI. Performance standards for antimicrobial susceptibility testing: Twenty-fourth informational supplement: CLSI M100S24, Clinical and Laboratory Standards Institute (CLSI), Wayne, USA, 2014.

    Google Scholar 

  28. 28.

    Giacopello C, Foti M, Fisichella V, Latella G, Aleo A, Mammina C. Antibiotic resistance in Salmonella isolated from tegus (Tupinambis spp.). J Exot Pet Med 2012; 21(4): 328–331.

    Article  Google Scholar 

  29. 29.

    Corrente M, Madio A, Friedrich KG, Greco G, Desario C, Tagliabue S, D’Incau M, Campolo M, Buonavoglia C. Isolation of Salmonella strains from reptile faeces and comparison of different culture media. J Appl Microbiol 2004; 96(4): 709–715.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Ferrari R, Galiana A, Cremades R, Rodríguez JC, Magnani M, Tognim MC, Oliveira TC, Royo G. Plasmid-mediated quinolone resistance (PMQR) and mutations in the topoisomerase genes of Salmonella enterica strains from Brazil. Braz J Microbiol 2013; 44(2): 651–656.

    PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Gay K, Robicsek A, Strahilevitz J, Park CH, Jacoby G, Barrett TJ, Medalla F, Chiller TM, Hooper DC. Plasmid-mediated quinolone resistance in non-Typhi serotypes of Salmonella enterica. Clin Infect Dis 2006; 43(3): 297–304.

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Nordmann P, Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 2005; 56(3): 463–469.

    CAS  PubMed  Article  Google Scholar 

  33. 33.

    Kim JH, Cho JK, Kim KS. Prevalence and characterization of plasmid-mediated quinolone resistance genes in Salmonella isolated from poultry in Korea. Avian Pathol 2013; 42(3): 221–229.

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Asai T, Sato C, Masani K, Usui M, Ozawa M, Ogino T, Aoki H, Sawada T, Izumiya H, Watanabe H. Epidemiology of plasmid-mediated quinolone resistance in salmonella enterica serovar typhimurium isolates from food-producing animals in Japan. Gut Pathog 2010; 2(1): 17.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    García-Fernández A, Gallina S, Owczarek S, Dionisi AM, Benedetti I, Decastelli L, Luzzi I. Emergence of Ciprofloxacin-Resistant Salmonella enterica Serovar Typhi in Italy. PLoS One 2015; 10(6): e0132065.

    Google Scholar 

  36. 36.

    Kim SY, Lee SK, Park MS, Na HT. Analysis of the Fluoroquinolone Antibiotic Resistance Mechanism of Salmonella enterica Isolates. J Microbiol Biotechnol 2016; 26(9): 1605–1612.

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Dimitrov T, Dashti AA, Albaksami O, Udo EE, Jadaon MM, Albert MJ. Ciprofloxacin-resistant Salmonella enterica serovar typhi from Kuwait with novel mutations in gyrA and parC genes. J Clin Microbiol 2009; 47(1): 208–211.

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Amarantini C, Satwika D. Molecular phylogeny of Salmonellae: Relationships among Salmonella species determined from gyrA, gyrB, parC, and parE genes. Microbiol Indones 2015; 9(1): 1–8.

    Article  Google Scholar 

  39. 39.

    Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC. Prevalence in the United States of aac(6’)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 2006; 50(11): 3953–3955.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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This study was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A1A01060638).

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Correspondence to Gang-Joon Heo.

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De Silva, B.C.J., Hossain, S., Wimalasena, S.H.M.P. et al. Quinolone susceptibility and genetic characterization of Salmonella enterica subsp. enterica isolated from pet turtles. Lab Anim Res 33, 49–56 (2017).

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  • Salmonella enterica subsp. enterica
  • quinolone susceptibility
  • pet turtles
  • qnr genes
  • QRDR