Vet Med - Czech, 2017, 62(3):169-177 | DOI: 10.17221/65/2016-VETMED
Identification and antibiotic resistance profiling of bacterial isolates from septicaemic soft-shelled turtles (Pelodiscus sinensis)Original Paper
- 1 Department of Animal Science, Joongbu University, Chungnam, Republic of Korea
- 2 Bio-safety Research Institute and College of Veterinary Medicine, Chonbuk National University, Jeonju, Republic of Korea
The present study sought to identify pathogens associated with septicaemia in the Chinese soft-shelled turtle (Pelodiscus sinensis) and to characterise antibiotic resistance in these pathogens. Twenty-three isolates recovered from the livers of diseased soft-shelled turtles were genetically identified as Aeromonas hydrophila (n = 8), A. veronii (n = 3), Citrobacter freundii (n = 4), Morganella morganii (n = 3), Edwardsiella tarda (n = 2), Wohlfahrtiimonas chitiniclastica (n = 1), Chryseobacterium sp. (n = 1), and Comamonas sp. (n = 1). Most isolates (n = 21) were resistant to ampicillin whereas a low percentage of isolates was susceptible to aminoglycosides (amikacin, gentamicin, and tobramycin). PCR assays and sequence analysis revealed the presence of the qnrS2 and blaTEM antibiotic resistance genes in all isolates. The blaDHA-1, blaCTX-M-14 and blaCMY-2 genes were harboured by 17.4% (n = 4), 13.5% (n = 3) and 8.7% (n = 2) of the strains, respectively. One or more tetracycline resistance genes were detected in 60.9% (n = 14) of the isolates. Four isolates (17.4%) harboured single or multiple class 1 integron cassettes. Collectively, a variety of bacterial pathogens were involved in the occurrence of septicaemia in Chinese soft-shelled turtles and most of the isolates had multi-antibiotic resistant phenotypes. To our knowledge, the present report is the first to identify W. chitiniclastica and Comamonas sp. as causes of septicaemia in soft-shelled turtles and the first to identify Aeromonas spp. with blaCTX-M-14 and blaDHA-1 resistance genes.
Keywords: pet; ulcer disease; liver; lesions; septicaemia; antibiotic resistance
Published: March 31, 2017 Show citation
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References
- Akinbowale OL, Peng H, Barton MD (2007): Diversity of tetracycline resistance genes in bacteria from aquaculture sources in Australia. Journal of Applied Microbiology 103, 2016-2025.
Go to original source...
Go to PubMed...
- Al-Bahry S, Mahmoud I, Elshafie A, Al-Harthy A, Al-Ghafri S, Al-Amri I, Alkindi A (2009): Bacterial flora and antibiotic resistance from eggs of green turtles Chelonia mydas: An indication of polluted effluents. Marine Pollution Bulletin 58, 720-725.
Go to original source...
Go to PubMed...
- Al-Bahry SN, Mahmoud IY, Al-Zadjali M, Elshafie A, AlHarthy A, Al-Alawi W (2011): Antibiotic resistant bacteria as bio-indicator of polluted effluent in the green turtles, Chelonia mydas in Oman. Marine Environmental Research 71, 139-144.
Go to original source...
Go to PubMed...
- Al-Bahry SN, Al-Zadjali MA, Mahmoud IY, Elshafie AE (2012): Biomonitoring marine habitats in reference to antibiotic resistant bacteria and ampicillin resistance determinants from oviductal fluid of the nesting green sea turtle, Chelonia mydas. Chemosphere 87, 1308-1315.
Go to original source...
Go to PubMed...
- Almuzara MN, Palombarani S, Tuduri A, Figueroa S, Gianecini A, Sabater L, Ramirez MS, Vay CA (2011): First case of fulminant sepsis due to Wohlfahrtiimonas chitiniclastica. Journal of Clinical Microbiology 49, 2333-2335.
Go to original source...
Go to PubMed...
- Aravena-Roman M, Inglis TJJ, Henderson B, Riley TV, Chang BJ (2012): Antimicrobial susceptibilities of Aeromonas strains isolated from clinical and environmental sources to 26 antimicrobial agents. Antimicrobial Agents Chemotherapy 56, 1110-1112.
Go to original source...
Go to PubMed...
- Barnaud G, Arlet G, Verdet C, Gaillot O, Lagrange PH, Philippon A (1998): Salmonella enteritidis: AmpC plasmid-mediated inducible beta-lactamase (DHA-1) with an ampR gene from Morganella morganii. Antimicrobial Agents Chemotherapy 42, 2352-2358.
Go to original source...
Go to PubMed...
- Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P (2007): Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. Journal of Antimicrobial Chemotherapy 60, 394-397.
Go to original source...
Go to PubMed...
- 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...
- Chen JS, Ding XY, Zhu NY, Kong L, He ZY (2013a): Prevalence and antimicrobial susceptibility of Aeromonas species from diseased Chinese soft-shelled turtles (Trionyx sinens). Aquaculture Research 46, 1527-1536.
Go to original source...
- Chen JS, Zhu NY, Kong L, Bei YJ, Zheng TL, Ding XY, He ZY (2013b): First case of soft shell disease in Chinese softshelled turtle (Trionyx sinens) associated with Aeromonas sobria-A. veronii complex. Aquaculture 406, 62-67.
Go to original source...
- Dallenne C, Da Costa A, Decre D, Favier C, Arlet G (2010): Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy 65, 490-495.
Go to original source...
Go to PubMed...
- Davies J, Davies D (2010): Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews 74, 417-433.
Go to original source...
Go to PubMed...
- Diaz MA, Cooper RK, Cloeckaert A, Siebeling RJ (2006): Plasmid-mediated high-level gentamicin resistance among enteric bacteria isolated from pet turtles in Louisiana. Applied and Environmental Microbiology 72, 306-312.
Go to original source...
Go to PubMed...
- Farshad S, Norouzi F, Aminshahidi M, Heidari B, Alborzi A (2012): Two cases of bacteremia due to an unusual pathogen, Comamonas testosteroni in Iran and a review literature. Journal of Infection in Developing Countries 6, 521-525.
Go to original source...
Go to PubMed...
- Feng H, Yamazaki M, Matsuki N, Saito H (1996): Anti-tumor effects of orally administered soft-shelled turtle powder in mice. Biological and Pharmaceutical Bulletin 19, 367-368.
Go to original source...
Go to PubMed...
- Foti M, Giacopello C, Bottari T, Fisichella V, Rinaldo D, Mammina C (2009): Antibiotic resistance of Gram negatives isolates from loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea. Marine Pollution Bulletin 58, 1363-1366.
Go to original source...
Go to PubMed...
- Guerra B, Helmuth R, Thomas K, Beutlich J, Jahn S, Schroeter A (2010): Plasmid-mediated quinolone resistance determinants in Salmonella spp. isolates from reptiles in Germany. Journal of Antimicrobial Chemotherapy 65, 2043-2045.
Go to original source...
Go to PubMed...
- Hernandez-Divers SJ, Hensel P, Gladden J, HernandezDivers SM, Buhlmann KA, Hagen C, Sanchez S, Latimer KS, Ard M, Camus AC (2009): Investigation of shell disease in map turtles (Graptemys Spp.). Journal of Wildlife Diseases 45, 637-652.
Go to original source...
Go to PubMed...
- Hu G, Li D, Li T, Su X (2010): Isolation and identification of bacteria from soft-shelled turtle (Trionyx sinensis) associated with fulminant septicaemia. Journal of Fishery Sciences of China 17, 859-868.
- Jacoby GA (2009): AmpC beta-Lactamases. Clinical Microbiology Reviews 22, 161-182.
Go to original source...
Go to PubMed...
- Jang J, Suh YS, Di DYW, Unno T, Sadowsky MJ, Hur HG (2013): Pathogenic Escherichia coli strains producing extended-spectrum β-Lactamases in the Yeongsan river basin of South Korea. Environmental Science and Technology 47, 1128-1136.
Go to original source...
Go to PubMed...
- Kim J, Lim YM, Jeong YS, Seol SY (2005): Occurrence of CTX-M-3, CTX-M-15, CTX-M-14, and CTX-M-9 extended-spectrum beta-lactamases in Enterobacteriaceae clinical isolates in Korea. Antimicrobial Agents Chemotherapy 49, 1572-1575.
Go to original source...
Go to PubMed...
- Kohler G (ed.) (2006): Diseases of Amphibians and Reptiles. Krieger Publishing Co., Malabar. 184 pp.
- Lazar V, Nagy I, Spohn R, Csorgo B, Gyorkei A, Nyerges A, Horvath B, Voros A, Busa-Fekete R, Hrtyan M, Bogos B, Mehi O, Fekete G, Szappanos B, Kegl B, Papp B, Pal C (2014): Genome-wide analysis captures the determinants of the antibiotic cross-resistance interaction network. Nature Communications 5, 4352.
Go to original source...
Go to PubMed...
- Lee MF, Peng CF, Lin YH, Lin SR, Chen YH (2008): Molecular diversity of class 1 integrons in human isolates of Aeromonas spp. from southern Taiwan. Japanese Journal of Infectious Diseases 61, 343-349.
Go to original source...
- Livermore DM (1995): β-Lactamases in laboratory and clinical resistance. Clinical Microbiology Reviews 8, 557-584.
Go to original source...
Go to PubMed...
- Marti E, Variatza E, Balcazar JL (2014): The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends in Microbiology 22, 36-41.
Go to original source...
Go to PubMed...
- Martinez-Murcia AJ, Monera A, Saavedra MJ, Oncina R, Lopez-Alvarez M, Lara E, Figueras MJ (2011): Multilocus phylogenetic analysis of the genus Aeromonas. Systematic and Applied Microbiology 34, 189-199.
Go to original source...
Go to PubMed...
- Nseir W, Khateeb J, Awawdeh M, Ghali M (2011): Catheterrelated bacteremia caused by Comamonas testosteroni in a hemodialysis patient. Hemodialysis International 15, 293-296.
Go to original source...
Go to PubMed...
- Oros J, Torrent A, Calabuig P, Deniz S (2005): Diseases and causes of mortality among sea turtles stranded in the Canary Islands, Spain (1998-2001). Diseases of Aquatic Organisms 63, 13-24.
Go to original source...
Go to PubMed...
- Rebaudet S, Genot S, Renvoise A, Fournier PE, Stein A (2009): Wohlfahrtiimonas chitiniclastica bacteremia in homeless woman. Emerging Infectious Diseases 15, 985-987.
Go to original source...
Go to PubMed...
- 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 50, 488-493.
Go to original source...
Go to PubMed...
- Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP (2013): The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. The Lancet Infectious Diseases 13, 155-165.
Go to original source...
Go to PubMed...
- Wheeler E, Hong PY, Bedon LC, Mackie RI (2012): Carriage of antibiotic-resistant enteric bacteria varies among sites in Galapagos reptiles. Journal of Wildlife Diseases 48, 56-67.
Go to original source...
Go to PubMed...
- Wu PJ, Shannon K, Phillips I (1994): Effect of hyperproduction of tem-1 beta-lactamase on in vitro susceptibility of Escherichia coli to beta-lactam antibiotics. Antimicrobial Agents Chemotherapy 38, 494-498.
Go to original source...
Go to PubMed...
- Yanez MA, Catalan V, Apraiz D, Figueras MJ, MartinezMurcia AJ (2003): Phylogenetic analysis of members of the genus Aeromonas based on gyrB gene sequences. International of Journal of Systematic and Evolutionary Microbiology 53, 875-883.
Go to original source...
Go to PubMed...
- Yi SW, You MJ, Cho HS, Lee CS, Kwon JK, Shin GW (2013): Molecular characterization of Aeromonas species isolated from farmed eels (Anguilla japonica). Veterinary Microbiology 164, 195-200.
Go to original source...
Go to PubMed...
- Yin J, Tezuka Y, Shi L, Ueda JY, Matsushige K, Kadota S (2005): A combination of soft-shell turtle powder and essential oil of a unicellular chlorophyte prevents bone loss and decreased bone strength in ovariectomized rats.
- Biological Pharmaceutical Bulletin 28, 275-279.
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