Veterinary Research Forum
Vet Res Forum

Genotypic and phenotypic tetracycline-based properties of Trueperella pyogenes isolates from bovine samples

Document Type : Original Article

Authors

Ozlem Şahan Yapicier 1
Dilek Ozturk 2
Mehmet Kaya 2

1 Bacteriological Diagnostic Laboratory, Veterinary Control Central Research Institute, Republic of Turkiye Ministry of Agriculture and Forestry, Ankara, Turkiye

2 Department of Microbiology, Faculty of Veterinary Medicine, Mehmet Akif Ersoy University, Burdur, Turkiye

https://doi.org/10.30466/vrf.2021.138938.3090
Abstract
The purpose of this study was to investigate the tetracycline resistance in Trueperella pyogenes isolates from bovine samples in Burdur, Turkiye, and assess 16 tetracycline-resistance genes distribution among the isolates. Forty-nine T. pyogenes isolates were phenotypically characterized for anti-microbial resistance to doxycycline, oxytetracycline and tetracycline by disc diffusion method. Presence of tetracycline genes of T. pyogenes was investigated by multiplex and singleplex polymerase chain reaction. Our results indicated that 87.80% and 42.86% of the isolates were resistant to tetracycline and oxytetracycline, respectively, and the rate of resistance to doxycycline was 6.12%. Total of 21 (42.85%) were carrying tetracycline-resistance genes and tet(A) was present in 12 (24.49%) isolates; whereas, the tet(W) gene was identified in 9 (18.37%) and 2 (4.08%) of the isolates carried both tet(A) and tet(W), respectively. The study indicated antibiotic resistance patterns of tetracycline agents and links to the tet-genes among T. pyogenes were detected. It makes it worthwhile that this is the first report for detection of tet(A) gene in T. pyogenes.

Keywords

Cattle
Mastitis
Tetracycline resistance genes
Trueperella pyogenes
  1. Billington SJ, Songer JG, Jost BH. Widespread distribution of a tet W determinant among tetracycline-resistant isolates of the animal pathogen Arcanobacterium pyogenes. Antimicrob Agents Chemother 2002; 46(5): 1281-1287.
  2. Wareth G, El-Diasty M, Melzer F, et al. Trueperella pyogenes and Brucella abortus coinfection in a dog and a cat on a dairy farm in Egypt with recurrent cases of mastitis and abortion. Vet Med Int 2018; 2056436. doi: 10.1155/2018/2056436.
  3. Santos TM, Caixeta LS, Machado VS, et al. Antimicrobial resistance and presence of virulence factor genes in Arcanobacterium pyogenes isolated from the uterus of postpartum dairy cows. Vet Microbiol 2010;145(1-2): 84-89.
  4. Zastempowska E, Lassa H. Genotypic characterization and evaluation of an antibiotic resistance of Trueperella pyogenes (Arcanobacterium pyogenes) isolated from milk of dairy cows with clinical mastitis. Vet Microbiol 2012; 161(1-2): 153-158.
  5. Ribeiro MG, Risseti RM, Bolaños CA, et al. Trueperella pyogenes multispecies infections in domestic animals: a retrospective study of 144 cases (2002 to 2012). Vet Q 2015; 35(2): 82-87.
  6. Risseti RM, Zastempowska E, Twarużek M, et al. Virulence markers associated with Trueperella pyogenes infections in livestock and companion animals. Lett App Microbiol 2017; 65(2): 125-132.
  7. Ashrafi Tamai I, Mohammadzadeh A, Zahraei Salehi T, et al. Genomic characterization, detection of genes encoding virulence factors and evaluation of antibiotic resistance of Trueperella pyogenes isolated from cattle with clinical metritis. Antonie Van Leeuwenhoek 2018; 111(12): 2441-2453.
  8. Dong WL, Liu L, Odah KA, et al. Antimicrobial resistance and presence of virulence factor genes in Trueperella pyogenes isolated from pig lungs with pneumonia. Trop Anim Health Prod 2019; 51(7): 2099-2103.
  9. Rzewuska M, Kwiecień E, Chrobak-Chmiel D, et al. Pathogenicity and virulence of Trueperella pyogenes: A review. Int J Mol Sci 2019; 20(11): 2737. doi: 10.3390/ijms20112737.
  10. Gahrn-Hansen B, Frederiksen W. Human infections with Actinomyces pyogenes (Corynebacterium pyogenes). Diagn Microbiol Infect Dis 1992; 15(4): 349-354.
  11. Levy CE, Pedro RJ, Von Nowakonski A, et al. Arcanobacterium pyogenes sepsis in farmer, Brazil. Emerg Infect Dis 2009; 15(7): 1131-1132.
  12. Kavitha K, Latha R, Udayashankar C, et al. Three cases of Arcanobacterium pyogenes-associated soft tissue infection. J Med Microbiol 2010; 59(Pt 6): 736-739.
  13. Rogovskyy AS, Lawhon S, Kuczmanski K, et al. Phenotypic and genotypic characteristics of Trueperella pyogenes isolated from ruminants. J Vet Diagn Invest 2018; 30(3): 348-353.
  14. Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 2001; 65(2): 232-260.
  15. Roberts MC. Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol Rev 1996; 19(1): 1-24.
  16. Roberts MC. Tetracycline therapy: update. Clin Infect Dis 2003; 36(4): 462-467.
  17. Guérin-Faublée V, Flandrois JP, Broue E, et al. Actinomyces pyogenes: susceptibility of 103 clinical isolates to 22 antimicrobial agents. Vet Res 1993; 24(3): 251-259.
  18. Trinh HT, Billington SJ, Field AC, et al. Susceptibility of Arcanobacterium pyogenes from different sources to tetracycline, macrolide and lincosamide antimicrobial agents. Vet Microbiol 2002; 85(4): 353-359.
  19. Griffith M, Postelnick M, Scheetz M. Antimicrobial stewardship programs: methods of operation and suggested outcomes. Expert Rev Anti Infect Ther 2012; 10(1): 63-73.
  20. Liu MC, Wu CM, Liu YC, et al. Identification susceptibility and detection of integron-gene cassettes of Arcanobacterium pyogenes in bovine endometritis. J Dairy Sci 2009; 92(8): 3659-3666.
  21. Tacconelli E. Antimicrobial use: risk driver of multidrug resistant microorganisms in healthcare settings. Curr Opin Infect Dis 2009; 22(4): 352-358.
  22. Yu VL. Guidelines for hospital-acquired pneumonia and health-care-associated pneumonia: a vulnerability, a pitfall, and a fatal flaw. Lancet Infect Dis 2011; 11(3): 248-252.
  23. Zhang D, Zhao J, Wang Q, et al. Trueperella pyogenes isolated from dairy cows with endometritis in Inner Mongolia, China: Tetracycline susceptibility and tetracycline-resistance gene distribution. Microb Pathog 2017; 105: 51-56.
  24. Ozturk D, Turutoglu H, Pehlivanoglu F, et al. Virulence genes, biofilm production and antibiotic susceptibility in Trueperella pyogenes isolated from cattle. Isr J Vet Med 2016 Sep; 71(3): 36-42.
  25. Methods for Antimicrobial susceptibility testing of infrequently isolated or fastidious bacteria isolated from animals. 1st ed. Available at: https://clsi.org/media/ 1524/vet06ed1_sample.pdf Accessed Aug 28, 2022.
  26. Billington SJ, Jost BH. Multiple genetic elements carry the tetracycline resistance gene tet(W) in the animal pathogen Arcanobacterium pyogenes. Antimicrob Agents Chemother 2006; 50(11): 3580-3587.
  27. Mendez B, Tachibana C, Levy SB. Heterogeneity of tetracycline resistance determinants. Plasmid 1980; 31(2): 99-108.
  28. Marshall B, Tachibana C, Levy SB. Frequency of tetracycline resistance determinant classes among lactose-fermenting coliforms. Antimicrob Agents Chemother. 1983; 24(6): 835-840.
  29. Marshall B, Morrissey S, Flynn P, et al. A new tetra-cycline-resistance determinant, class E, isolated from Enterobacteriaceae. Gene 1986; 50(1-3): 111-117.
  30. McMurry LM, Park BH, Burdett V, et al. Energy-dependent efflux mediated by class L (tetL) tetracycline resistance determinant from streptococci. Antimicrob Agents Chemother 1987; 31(10): 1648-1650.
  31. Francois B, Charles M, Courvalin P. Conjugative transfer of tet(S) between strains of Enterococcus faecalis is associated with the exchange of large fragments of chromosomal DNA. Microbiology (Reading) 1997; 143(Pt 7): 2145-2154.
  32. Taylor DE, Hiratsuka K, Ray H, et al. Characterization and expression of a cloned tetracycline resistance determinant from Campylobacter jejuni plasmid pUA466. J Bacteriol 1987; 169(7): 2984-2989.
  33. Zhao J, Aoki T. Nucleotide sequence analysis of the class G tetracycline resistance determinant from Vibrio anguillarum. Microbiol Immunol 1992; 36(10): 1051-1060.
  34. Warsa UC, Nonoyama M, Ida T, et al. Detection of tet(K) and tet(M) in Staphylococcus aureus of Asian countries by the polymerase chain reaction. J Antibiot (Tokyo) 1996; 49(11): 1127-1132.
  35. Burdett V, Inamine J, Rajagopalan S. Heterogeneity of tetracycline resistance determinants in Streptococcus. J Bacteriol 1982; 149(3): 995-1004.
  36. Scott PT, Rood JI. Electroporation-mediated transf-ormation of lysostaphin-treated Clostridium perfringens. Gene 1989; 82(2): 327-333.
  37. Nikolich MP, Shoemaker NB, Salyers AA. A Bacteroides tetracycline resistance gene represents a new class of ribosome protection tetracycline resistance. Anti-microb Agents Chemother 1992; 36(5): 1005-1012.
  38. Speer BS, Salyers AA. Characterization of a novel tetracycline resistance that functions only in aerobically grown Escherichia coli. J Bacteriol 1988; 170(4): 1423-1429.
  39. Ng LK, Martin I, Alfa M, et al. Multiplex PCR for the detection of tetracycline genes. Mol Cell Probes 2001; 15(4): 209-215.
  40. The European agency for the evaluation of medicinal products. Antibiotic resistance in the European Union associated with therapeutic use of veterinary medicines. Report and qualitative risk assessment by the committee for veterinary medicinal products. 1999; 1-79. Available at: https://www.ema.europa.eu/ en/documents/report/antibiotic-resistance european-union-associated-therapeutic-use-veterinary-medicine s-report_en-0.pdf3456789. Accessed Aug 28, 2022.
  41. Michalova E, Novotna P, Schlegelova J. Tetracyclines in veterinary medicine and bacterial resistance to them. Vet Med (Czech) 2004; 49(3): 79-100.
  42. Papich MG. Considerations for using minocycline vs doxycycline for treatment of canine hearthworm disease. Parasit Vectors 2017; 10(Suppl 2): 493. doi: 10.1186/s13071-017-2449-1.
  43. Arabzadeh F, Aeini F, Keshavarzi F, et al. Resistance to tetracycline and vancomycin of Staphylococcus aureus isolates from Sanandaj patients by molecular geno-typing. Ann Clin Lab Res 2018; 6: doi: 10.21767/2386-5180.100260.
  44. Yoshimura H, Kojima A, Ishimaru M. Antimicrobial susceptibility of Arcanobacterium pyogenes isolated from cattle and pigs. J Vet Med B Infect Dis Vet Public Health. 2000; 47(2): 139-143.
  45. Momtaz H, Ghafari A, Sheikh-Samani M, et al. Detecting virulence factors and antibiotic resistance pattern of Trueperella pyogenes isolated from bovine mastitic milk. Int J Med Lab 2016; 3(2): 134-141.
  46. Sheldon IM, Bushnell M, Montgomery J, et al. Minimum inhibitory concentrations of some antimicrobial drugs against bacteria causing uterine infections in cattle. Vet Rec 2004; 155(13): 383-387.
  47. Galán-Relaño Á, Gómez-Gascón L, Luque I, et al. Anti-microbial susceptibility and genetic characterization of Trueperella pyogenes isolates from pigs reared under intensive and extensive farming practices. Vet Microbiol 2019; 232: 89-95.
  48. Roberts MC, Schwarz S, Aarts HJ. Erratum: Acquired antibiotic resistance genes: an overview. Front Microbiol 2012; 16(3): 384. doi: 10.3389/fmicb. 2012.00384.
  49. Rezanejad M, Karimi S, Momtaz H. Phenotypic and molecular characterization of antimicrobial resistance in Trueperella pyogenes strains isolated from bovine mastitis and metritis. BMC Microbiol 2019; 19: 305. doi: 10.1186/s12866-019-1630-4.
Veterinary Research Forum
Volume 13, Issue 4
Autumn 2022
Pages 469-474

  • Receive Date 29 October 2020
  • Revise Date 27 January 2021
  • Accept Date 01 March 2021

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