Research Article
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The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates

Year 2024, Volume: 71 Issue: 2, 183 - 194, 01.04.2024
https://doi.org/10.33988/auvfd.1113432

Abstract

The assessment of antibiotic resistance and related genes of foodborne Acinetobacter spp. and the analysis of whether they are genetically related to clinical infection-agent strains are crucial in terms of sustainability of food safety. The study at hand investigated antibiotic resistance, aminoglycoside-modifying enzyme (AME), and colistin resistance (PmrA) genes, clonal relationships while evaluating a possible correlation between antibiotic resistance and related genes between 27 foodborne and 50 clinical Acinetobacter spp. in Turkey. Antimicrobial susceptibilities, AME, PmrA genes, and clonal relatedness of the strains were performed by disc diffusion, PCR, and Pulsed Field gel Electrophoresis (PFGE) methods, respectively. The aph-AI, aph-6, anth(3’’)-I, aadA1, aadB, and PmrA genes were found as 48%(n=24), 22%(n=11), 14%(n=7), 2%(n=1), 4%(n=2), and 92%(n=46) respectively, in clinical strains. This rate was found as 51.9%(n=14),59.3%(n=16), 70.4%(n=19), 7.4%(n=2), 0%(n=0), and 100%(n=27), respectively in foodborne isolates. A positive correlation existed between the number of aph-AI gene positivity and trimethoprim-sulfamethoxazole and gentamycin resistance; anth (3’’)-I gene positivity, and colistin resistance; PmrA gene positivity and piperacillin-tazobactam, ceftazidime, meropenem, amikacin, and imipenem resistance in clinical strains (P<0.05). A positive correlation between trimethoprim-sulfamethoxazole resistance and aadAI gene positivity was found in foodborne strains (P<0.05). Clonal relations were absent between foodborne and clinical A. baumanni species. Finally, AME genes rise parallel to multidrug-resistance in the clinical isolates, and foods may be potential reservoirs for disseminating multi-AME and PmrA genes while being susceptible to several antibiotics.

Ethical Statement

This study was carried out after the clinical samples were approved by Çukurova University Local Ethics Committee (Decision number: 14.06.2019-89).

Supporting Institution

This research has been supported within the content of the project no 2020-PT 2-001 by Osmaniye Korkut Ata University Scientific Research Project Unit.

Project Number

OKUBAP-2020-PT 2-001

References

  • Adams MD, Nickel GC, Bajaksouzian S, et al (2009): Resistance to colistin in Acinetobacter baumannii associated with mutations in the PmrAB two-component system. Antimicrob Agent and Chemot, 53, 3628-3634.
  • Ahmadi A, Salimizand H (2017): Delayed identification of Acinetobacter baumannii during an outbreak owing to disrupted blaOXA-51-like by ISAba19. Int J Antimicrob Agents, 50, 119-122.
  • Askari N, Momtaz H, Tajbakhsh E (2019): Acinetobacter baumannii in sheep, goat, and camel raw meat: virulence and antibiotic resistance pattern. AIMS Microbiol, 5, 272.
  • Brigante G, Migliavacca R, Bramati S, et al (2012): Emergence and spread of a multidrug-resistant Acinetobacter baumannii clone producing both the carbapenemase OXA-23 and the 16S rRNA methylase ArmA. J Med Microbiol, 61, 653-661.
  • Carvalheira A, Silva J, Teixeira P (2017):Lettuce and fruits as a source of multidrug resistant Acinetobacter spp. Food Microbiol, 64, 119-125.
  • Choi M-J, Ko KS (2014): Mutant prevention concentrations of colistin for Acinetobacter baumannii, Pseudomonas aeruginosaand Klebsiella pneumoniaclinical isolates. J Antimic Chemo, 69, 275-277.
  • CLSI (2021): Performance standards for antimicrobial susceptibility testing, 31st ed.; CLSI: Annapolis Junction, M100-A22. Wayne, PA: Clinical and Laboratory Standards Institute.
  • Durmaz R, Otlu B, Koksal F, et al (2009): The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis, 62, 372-377.
  • Elisha BG, Steyn LM (1994): High level kanamycin resistance associated with the hyperproduction of AAC (3) II and a generalised reduction in the accumulation of aminoglycosides in Acinetobacter spp. J Antimicrob Chemot, 34, 457-464.
  • Espinal P, Seifert H, Dijkshoorn L, et al (2012): Rapid and accurate identification of genomic species from the Acinetobacter baumannii (Ab) group by MALDI-TOF MS. Clin Microbiol Infect, 18, 1097-1103.
  • Espinal P, Poirel L, Carmeli Y, et al (2013): Spread of NDM-2-producing Acinetobacter baumannii in the Middle East. J Antimicrob Chemot, 68, 1928-1930.
  • EUCAST (2014): Breakpoint tables for interpretation of MICS and zone diameters, versions 3.1 Available: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Break-point_tables/Breakpointtable_v_3.1.pdf. (Accessed July 23, 2020).
  • Franco MR, Caiaffa-Filho HH, Burattini MN, et al (2010): Metallo-beta-lactamases among imipenem resistant Pseudomonas aeruginosain a Brazilian university hospital. Clinics (Sao Paulo), 65, 825-829.
  • Garneau-Tsodikova S, Labby KJ (2016): Mechanisms of resistance to aminoglycoside antibiotics: Overview and perspectives. Med Chem Comm, 7, 11–27.
  • Gholami M, Haghshenas M, Moshiri M, et al (2017): Frequency of 16S rRNA Methylase and Aminoglycoside-Modifying Enzyme Genes among Clinical Isolates of Acinetobacter baumanniiin Iran. Iran J Path, 12, 329–338.
  • Hujer KM, Hujer AM, Hulten EA, et al (2006): Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Agent and Chemo, 50, 4114-4123.
  • Kanaan MHG, Al-Shadeedi SM, Al-Massody AJ, et al (2020): Drug resistance and virulence traits of Acinetobacter baumannii from Turkey and chicken raw meat. Comp Immun Microbiol Infect Dis, 70, 101451.
  • Khoshnood S, Savari M, Montazeri EA, et al (2020): Survey on genetic diversity, biofilm formation, and detection of colistin resistance genes in clinical isolates of Acinetobacter baumannii. Infect and Drug Res, 13, 1547.
  • Khurshid M, Rasool MH, Siddique MH, et al (2019): Molecular mechanisms of antibiotic co-resistance among carbapenem resistant Acinetobacter baumannii. The J Infect in Develop Count, 13, 899-905.
  • Kim YJ, Kim SI, Hong KW, et al (2012): Risk factors for mortality in patients with carbapenem-resistant Acinetobacter baumannii bacteremia: impact of appropriate antimicrobial therapy. J Kor Med Sci, 27, 471-475.
  • Li S, Duan X, Peng Y, et al (2019): Molecular characteristics of carbapenem-resistant Acinetobacter spp. from clinical infection samples and fecal survey samples in Southern China. BMC Infect Dis, 19, 1-12.
  • Lin MF, Lan CY (2014): Antimicrobial resistance in Acinetobacter baumannii: From bench to bedside. World J Clin Cases, 2, 787-814.
  • Lupo A, Vogt D, Seiffert SN, et al (2014): Antibiotic resistance and phylogenetic characterization of Acinetobacter baumannii strains isolated from commercial raw meat in Switzerland. J Food Prot, 77, 1976-1981.
  • Moniri R, Farahani RK, Shajari G, et al (2010): Molecular epidemiology of aminoglycosides resistance in Acinetobacter spp. with emergence of multidrug-resistant strains. Iran J Pub Health, 39, 63.
  • Mortazavi SM, Farshadzadeh Z, Janabadi S, et al (2020): Evaluating the frequency of carbapenem and aminoglycoside resistance genes among clinical isolates of Acinetobacter baumannii from Ahvaz, south-west Iran. New Microbes and New Infect, 38, 100779.
  • Park YK, Choi JY, Shin D, et al (2011): Correlation between overexpression and amino acid substitution of the PmrAB locus and colistin resistance in Acinetobacter baumannii. Int J Antimicrob Agents, 37, 525-530.
  • Pournaras S, Poulou A, Dafopoulou K, et al (2014): Growth retardation, reduced invasiveness, and ımpaired colistinmediated cell death associated with colistin resistance development in Acinetobacter baumannii. Antimicrob Agent and Chemo, 58, 828-832.
  • Ramirez MS, Tolmasky ME (2010): Aminoglycoside modifying enzymes. Drug Resist Upda, 13, 151–171.
  • Rose M, Landman D, Quale J (2014): Are community environmental surfaces near hospitals reservoirs for gram-negative nosocomial pathogens? Am J Infect Control, 42, 346–348.
  • Sepahvand S, Doudi M, Davarpanah MA, et al (2016): Analyzing pmrA and pmrB genes in Acinetobacter baumannii resistant to colistin in Shahid Rajai Shiraz, Iran Hospital by PCR: First report in Iran. Pakistan J of Pharm Sci, 29, 1401-1406.
  • Shamim S, Abbas M, Qazi MH (2015): Prevalence of multidrug resistant Acinetobacter baumannii in hospitalized patients in Lahore, Pakistan. Pakistan J Mol Med, 2, 23-28.
  • Sheikhalizadeh V, Hasani A, Rezaee MA, et al (2017): Comprehensive study to investigate the role of various aminoglycoside resistance mechanisms in clinical isolates of Acinetobacter baumannii. J Infect and Chemot, 23, 74-79.
  • Skov RL, Monnet DL (2016): Plasmid-mediated colistin resistance (mcr-1 gene): three months later, the story unfolds. Euro Surveil, 21, 30155.
  • Tutun H, Karagöz A, Altıntaş L, et al (2019): Determination of antibiotic susceptibility, ESBL genes and pulsed-field gel electrophoresis profiles of extended-spectrum β-lactamase-containing Escherichia coli isolates. Ankara Univ Vet Fak Derg, 66, 407-416.
  • Voets GM, Fluit AC, Scharringa J, et al (2011): A set of multiplex pcrs for genotypic detection of extended-spectrum β628 lactamases, carbapenemases, plasmid-mediated ampc β-lactamases and oxa β629 lactamases. Int J Antimicrob Agents, 37, 356-359.
  • Wareth G, Linde J, Hammer P, et al (2020): Phenotypic and WGS-derived antimicrobial resistance profiles of clinical and non-clinical Acinetobacter baumannii isolates from Germany and Vietnam. Int J Antimicrob Agents, 56, 106127.
  • Wen J, Zhou Y, Yang L (2014): Multidrug-resistant genes of aminoglycoside-modifying enzymes and 16S rRNA methylases in Acinetobacter baumannii strains. Genet Mol Res, 13, 3842-3849.
  • Wen Y, Ouyang Z, Yu Y, et al (2017): Mechanistic insight into how multidrug resistant Acinetobacter baumannii response regulator AdeR recognizes an intercistronic region. Nuc Acids Res, 45, 9773-9787.
  • Wisplinghoff H, Paulus T, Lugenheim M, et al (2012): Nosocomial bloodstream infections due to Acinetobacter baumannii, Acinetobacter pittii and Acinetobacter nosocomialis in the United States. J Infect, 64, 282-290.
  • Xiao-Min X, You-Fen F, Wei-Yun F, et al (2014): Antibiotic resistance determinants of a group of multidrug-resistant Acinetobacter baumannii in China. J Antibiot, 67, 439-444.
Year 2024, Volume: 71 Issue: 2, 183 - 194, 01.04.2024
https://doi.org/10.33988/auvfd.1113432

Abstract

Supporting Institution

Osmaniye Korkut Ata Üniversitesi

Project Number

OKUBAP-2020-PT 2-001

References

  • Adams MD, Nickel GC, Bajaksouzian S, et al (2009): Resistance to colistin in Acinetobacter baumannii associated with mutations in the PmrAB two-component system. Antimicrob Agent and Chemot, 53, 3628-3634.
  • Ahmadi A, Salimizand H (2017): Delayed identification of Acinetobacter baumannii during an outbreak owing to disrupted blaOXA-51-like by ISAba19. Int J Antimicrob Agents, 50, 119-122.
  • Askari N, Momtaz H, Tajbakhsh E (2019): Acinetobacter baumannii in sheep, goat, and camel raw meat: virulence and antibiotic resistance pattern. AIMS Microbiol, 5, 272.
  • Brigante G, Migliavacca R, Bramati S, et al (2012): Emergence and spread of a multidrug-resistant Acinetobacter baumannii clone producing both the carbapenemase OXA-23 and the 16S rRNA methylase ArmA. J Med Microbiol, 61, 653-661.
  • Carvalheira A, Silva J, Teixeira P (2017):Lettuce and fruits as a source of multidrug resistant Acinetobacter spp. Food Microbiol, 64, 119-125.
  • Choi M-J, Ko KS (2014): Mutant prevention concentrations of colistin for Acinetobacter baumannii, Pseudomonas aeruginosaand Klebsiella pneumoniaclinical isolates. J Antimic Chemo, 69, 275-277.
  • CLSI (2021): Performance standards for antimicrobial susceptibility testing, 31st ed.; CLSI: Annapolis Junction, M100-A22. Wayne, PA: Clinical and Laboratory Standards Institute.
  • Durmaz R, Otlu B, Koksal F, et al (2009): The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis, 62, 372-377.
  • Elisha BG, Steyn LM (1994): High level kanamycin resistance associated with the hyperproduction of AAC (3) II and a generalised reduction in the accumulation of aminoglycosides in Acinetobacter spp. J Antimicrob Chemot, 34, 457-464.
  • Espinal P, Seifert H, Dijkshoorn L, et al (2012): Rapid and accurate identification of genomic species from the Acinetobacter baumannii (Ab) group by MALDI-TOF MS. Clin Microbiol Infect, 18, 1097-1103.
  • Espinal P, Poirel L, Carmeli Y, et al (2013): Spread of NDM-2-producing Acinetobacter baumannii in the Middle East. J Antimicrob Chemot, 68, 1928-1930.
  • EUCAST (2014): Breakpoint tables for interpretation of MICS and zone diameters, versions 3.1 Available: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Break-point_tables/Breakpointtable_v_3.1.pdf. (Accessed July 23, 2020).
  • Franco MR, Caiaffa-Filho HH, Burattini MN, et al (2010): Metallo-beta-lactamases among imipenem resistant Pseudomonas aeruginosain a Brazilian university hospital. Clinics (Sao Paulo), 65, 825-829.
  • Garneau-Tsodikova S, Labby KJ (2016): Mechanisms of resistance to aminoglycoside antibiotics: Overview and perspectives. Med Chem Comm, 7, 11–27.
  • Gholami M, Haghshenas M, Moshiri M, et al (2017): Frequency of 16S rRNA Methylase and Aminoglycoside-Modifying Enzyme Genes among Clinical Isolates of Acinetobacter baumanniiin Iran. Iran J Path, 12, 329–338.
  • Hujer KM, Hujer AM, Hulten EA, et al (2006): Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Agent and Chemo, 50, 4114-4123.
  • Kanaan MHG, Al-Shadeedi SM, Al-Massody AJ, et al (2020): Drug resistance and virulence traits of Acinetobacter baumannii from Turkey and chicken raw meat. Comp Immun Microbiol Infect Dis, 70, 101451.
  • Khoshnood S, Savari M, Montazeri EA, et al (2020): Survey on genetic diversity, biofilm formation, and detection of colistin resistance genes in clinical isolates of Acinetobacter baumannii. Infect and Drug Res, 13, 1547.
  • Khurshid M, Rasool MH, Siddique MH, et al (2019): Molecular mechanisms of antibiotic co-resistance among carbapenem resistant Acinetobacter baumannii. The J Infect in Develop Count, 13, 899-905.
  • Kim YJ, Kim SI, Hong KW, et al (2012): Risk factors for mortality in patients with carbapenem-resistant Acinetobacter baumannii bacteremia: impact of appropriate antimicrobial therapy. J Kor Med Sci, 27, 471-475.
  • Li S, Duan X, Peng Y, et al (2019): Molecular characteristics of carbapenem-resistant Acinetobacter spp. from clinical infection samples and fecal survey samples in Southern China. BMC Infect Dis, 19, 1-12.
  • Lin MF, Lan CY (2014): Antimicrobial resistance in Acinetobacter baumannii: From bench to bedside. World J Clin Cases, 2, 787-814.
  • Lupo A, Vogt D, Seiffert SN, et al (2014): Antibiotic resistance and phylogenetic characterization of Acinetobacter baumannii strains isolated from commercial raw meat in Switzerland. J Food Prot, 77, 1976-1981.
  • Moniri R, Farahani RK, Shajari G, et al (2010): Molecular epidemiology of aminoglycosides resistance in Acinetobacter spp. with emergence of multidrug-resistant strains. Iran J Pub Health, 39, 63.
  • Mortazavi SM, Farshadzadeh Z, Janabadi S, et al (2020): Evaluating the frequency of carbapenem and aminoglycoside resistance genes among clinical isolates of Acinetobacter baumannii from Ahvaz, south-west Iran. New Microbes and New Infect, 38, 100779.
  • Park YK, Choi JY, Shin D, et al (2011): Correlation between overexpression and amino acid substitution of the PmrAB locus and colistin resistance in Acinetobacter baumannii. Int J Antimicrob Agents, 37, 525-530.
  • Pournaras S, Poulou A, Dafopoulou K, et al (2014): Growth retardation, reduced invasiveness, and ımpaired colistinmediated cell death associated with colistin resistance development in Acinetobacter baumannii. Antimicrob Agent and Chemo, 58, 828-832.
  • Ramirez MS, Tolmasky ME (2010): Aminoglycoside modifying enzymes. Drug Resist Upda, 13, 151–171.
  • Rose M, Landman D, Quale J (2014): Are community environmental surfaces near hospitals reservoirs for gram-negative nosocomial pathogens? Am J Infect Control, 42, 346–348.
  • Sepahvand S, Doudi M, Davarpanah MA, et al (2016): Analyzing pmrA and pmrB genes in Acinetobacter baumannii resistant to colistin in Shahid Rajai Shiraz, Iran Hospital by PCR: First report in Iran. Pakistan J of Pharm Sci, 29, 1401-1406.
  • Shamim S, Abbas M, Qazi MH (2015): Prevalence of multidrug resistant Acinetobacter baumannii in hospitalized patients in Lahore, Pakistan. Pakistan J Mol Med, 2, 23-28.
  • Sheikhalizadeh V, Hasani A, Rezaee MA, et al (2017): Comprehensive study to investigate the role of various aminoglycoside resistance mechanisms in clinical isolates of Acinetobacter baumannii. J Infect and Chemot, 23, 74-79.
  • Skov RL, Monnet DL (2016): Plasmid-mediated colistin resistance (mcr-1 gene): three months later, the story unfolds. Euro Surveil, 21, 30155.
  • Tutun H, Karagöz A, Altıntaş L, et al (2019): Determination of antibiotic susceptibility, ESBL genes and pulsed-field gel electrophoresis profiles of extended-spectrum β-lactamase-containing Escherichia coli isolates. Ankara Univ Vet Fak Derg, 66, 407-416.
  • Voets GM, Fluit AC, Scharringa J, et al (2011): A set of multiplex pcrs for genotypic detection of extended-spectrum β628 lactamases, carbapenemases, plasmid-mediated ampc β-lactamases and oxa β629 lactamases. Int J Antimicrob Agents, 37, 356-359.
  • Wareth G, Linde J, Hammer P, et al (2020): Phenotypic and WGS-derived antimicrobial resistance profiles of clinical and non-clinical Acinetobacter baumannii isolates from Germany and Vietnam. Int J Antimicrob Agents, 56, 106127.
  • Wen J, Zhou Y, Yang L (2014): Multidrug-resistant genes of aminoglycoside-modifying enzymes and 16S rRNA methylases in Acinetobacter baumannii strains. Genet Mol Res, 13, 3842-3849.
  • Wen Y, Ouyang Z, Yu Y, et al (2017): Mechanistic insight into how multidrug resistant Acinetobacter baumannii response regulator AdeR recognizes an intercistronic region. Nuc Acids Res, 45, 9773-9787.
  • Wisplinghoff H, Paulus T, Lugenheim M, et al (2012): Nosocomial bloodstream infections due to Acinetobacter baumannii, Acinetobacter pittii and Acinetobacter nosocomialis in the United States. J Infect, 64, 282-290.
  • Xiao-Min X, You-Fen F, Wei-Yun F, et al (2014): Antibiotic resistance determinants of a group of multidrug-resistant Acinetobacter baumannii in China. J Antibiot, 67, 439-444.
There are 40 citations in total.

Details

Primary Language English
Subjects Veterinary Food Hygiene and Technology, Veterinary Microbiology
Journal Section Research Article
Authors

Mevhibe Terkuran 0000-0002-3150-459X

Zerrin Erginkaya 0000-0001-6208-2927

Fatih Köksal 0000-0003-0790-1525

Project Number OKUBAP-2020-PT 2-001
Early Pub Date September 21, 2023
Publication Date April 1, 2024
Published in Issue Year 2024Volume: 71 Issue: 2

Cite

APA Terkuran, M., Erginkaya, Z., & Köksal, F. (2024). The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 71(2), 183-194. https://doi.org/10.33988/auvfd.1113432
AMA Terkuran M, Erginkaya Z, Köksal F. The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates. Ankara Univ Vet Fak Derg. April 2024;71(2):183-194. doi:10.33988/auvfd.1113432
Chicago Terkuran, Mevhibe, Zerrin Erginkaya, and Fatih Köksal. “The Presence of Antibiotic Resistance and Molecular Characterization of Aminoglycoside and PmrA Genes Among Food- and Clinical-Acquired Acinetobacter Isolates”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71, no. 2 (April 2024): 183-94. https://doi.org/10.33988/auvfd.1113432.
EndNote Terkuran M, Erginkaya Z, Köksal F (April 1, 2024) The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71 2 183–194.
IEEE M. Terkuran, Z. Erginkaya, and F. Köksal, “The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates”, Ankara Univ Vet Fak Derg, vol. 71, no. 2, pp. 183–194, 2024, doi: 10.33988/auvfd.1113432.
ISNAD Terkuran, Mevhibe et al. “The Presence of Antibiotic Resistance and Molecular Characterization of Aminoglycoside and PmrA Genes Among Food- and Clinical-Acquired Acinetobacter Isolates”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71/2 (April 2024), 183-194. https://doi.org/10.33988/auvfd.1113432.
JAMA Terkuran M, Erginkaya Z, Köksal F. The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates. Ankara Univ Vet Fak Derg. 2024;71:183–194.
MLA Terkuran, Mevhibe et al. “The Presence of Antibiotic Resistance and Molecular Characterization of Aminoglycoside and PmrA Genes Among Food- and Clinical-Acquired Acinetobacter Isolates”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 71, no. 2, 2024, pp. 183-94, doi:10.33988/auvfd.1113432.
Vancouver Terkuran M, Erginkaya Z, Köksal F. The presence of antibiotic resistance and molecular characterization of aminoglycoside and PmrA genes among food- and clinical-acquired Acinetobacter isolates. Ankara Univ Vet Fak Derg. 2024;71(2):183-94.