Research Article
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Determination Of Enterococcus Species And Antibiotic Resistance In Budgerigars

Year 2022, Volume: 11 Issue: 2, 38 - 43, 28.12.2022
https://doi.org/10.53913/aduveterinary.1192214

Abstract

Abstract: In this study, it was aimed to determine the resistance profile by examining the prevalence and species distribution of enterococci in rectal samples of healthy budgerigars and their susceptibility to antibiotics. 100 cloacal swab samples were used in the study. Identification and antibiotic resistance of Enterococcal isolates obtained by classical methods were determined with the automated identification system. As a result of the study, 22 (75.86%) E. faecalis, 2 (6.90%) E. faecium (6.90%) E. hirae (6.90%) and E. casseliflavus/gallinarum and 1 S. uberis (3.44%) was obtained. The presence of Enterococci was detected in 29% of the samples. In general, they were suspectible to Amoxicillin clavunate (96.4%), Ampicillin (100%), Ciproflaxacin (54.2%), Levoflaxacin (60.9%), Gentamicin(Syn) (82.1%), Streptomycin(Syn) (28.6%), Tigecycline (80%), Vancomycin(89.3%), Teicoplanin (96.4%), Linezolide (96.4%) and Nitrofurontion (100%), and they showed 100% resistance to Cefocitin, Amikacin, Gentamicin, Tobramycin, Clindamycin, Erythromycin, TMP-SXT, Fusidic acid and Quinopuristin-Dalfopuristin. The presence of Entrococcal species, which are very important in terms of zoonosis, in healthy budgerigars was revealed. In addition, the different types of antibiotic resistance found in the studies also reveal the necessity of performing antibiotic susceptibility tests in this type of infections. However, it has been demonstrated that which antibiotics will be effective in nosocomial and/or gastrointestinal infections of Enterococcal origin in budgerigars.

Supporting Institution

ADÜ BAP

Project Number

VTF-19023

References

  • Abat, C., Huart, M., Garcia, V., Dubourg, G., & Raoult, D. (2016). Enterococcus faecalis urinary-tract infections: do they have a zoonotic origin. Journal of Infection, 73(4):305-313. DOI: 10.1016/j.jinf.2016.07.012.
  • Akgül, Ö., Gülhan, T., & Güdücüoğlu, H. (2016). Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Veterinary Journal of Ankara University, 63, 235-244.
  • Aktaş, G., & Derbentli, Ş. (2009). The importance and epidemiological characteristics of vancomycin-resistant Enterococci. Turkish Journal Of Infection, 23 (4): 201-209.
  • Bilgehan, H. (1995). “Streptokoklar” Klinik Mikrobiyoloji. Özel Bakteriyoloji ve Bakteri İnfeksiyonları. 9. Basım. İzmir: Şafak Matbaacılık, 248-286.
  • Cabral, B. G., Davies, Y. M., Menao, M. C., Saidenberg, A. B. S., Gomes, V. T. M., Moreno, L. Z., Sato, M. I. Z., Moreno, A. M., & Knöbl, T. (2020). Companion psittacine birds as reservoir of gentamicin and vancomycin-resistant Enterococcus spp. Pesquisa Veterinaria Brasileira, 40(2):129-133. DOI: 10.1590/1678-5150-PVB-6147.
  • Christensen, H., & Bisgaard, M. (2016). Members of Streptococcus and Enterococcus associated with disease in poultry. In A Laboratory Manual for the Isolation, Identification and Characterization of Avian Pathogens. 6th edn. Ed., Williams, S. M., Dufour-Zavala, L., Jackwood, M., Lee, M. W., Lupiani, B., Reed, W. M., Spackman, E. & Woolcock, P. R. 127–137. Jacksonville: American Association of Avian Pathologists.
  • Çetinkaya, Y., Falk, P., & Mayhall, C. G. (2000). Vancomycin resistant enterococci. Clinical Microbiology Reviews, 13, 686-707, 2000. DOI: 10.1128/CMR.13.4.686-707.
  • Devriese L., Baele M., & Butaye P. (2006). The genus Enterococcus. The Procaryotes, New York: Springer, 163–174.
  • Devriese, L. A., Ieven, M., Goossens, H., Vandamme, P., Pot, B., Hommez, J., & Haesebrouck F. (1996). Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrobial Agents and Chemotherapy, 40:2285-2287. DOI: 10.1128/AAC.40.10.2285
  • Franz, C. M., Muscholl-Silberhorn, A. B., Yousıf, N. M., Vancanneyt, M., Swings, J., & Holzapfel, W. H. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Applied and Environmental Microbiology, 67: 4385– 4389. DOI: 10.1128/AEM.67.9.4385-4389.2001.
  • Fisher, K., & Phillips, C. (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology, 155(Pt 6): 1749–1757. DOI: 10.1099/mic.0.026385-0.
  • Freitas, A. A. R., Faria, A. R., Pinto T. C. A., Merquior, V. L. C., Neves, D. M., Costa, R. C. D., & Teixeira, L. M. (2018). Distribution of species and antimicrobial resistance among enterococci isolated from the fecal microbiota of captive blue-fronted parrot (Amazona aestiva) in Rio de Janeiro, Brazil. Science of the Total Environment, 615:1428–1437. DOI: 10.1016/j.scitotenv.2017.09.004.
  • Gaca, A. O., & Lemos, J. A. (2019). Adaptation to adversity: the intermingling of stress tolerance and pathogenesis in Enterococci. Microbiology and Molecular Biology Reviews, 83(3), DOI:10.1128/MMBR.00008-19.
  • Hammerum, A. M., Lester, H., & Heuer, O. E. (2010). Antimicrobial-resistant 205 enterococci in animals and meat: a human health hazard? Foodborne Pathogens and Disease, 7(10):1137-1146. DOI: 10.1089/fpd.2010.0552.
  • Houssem Ben, Y., Sarra, C., Nabil, H., Haythem, G., Rym Ben, S., Sara, C., Carmen., & Karim Ben, S. (2018). Antimicrobial resistance and genetic lineages of faecal enterococci of wild birds: Emergence of vanA and vanB2 harbouring Enterococcus faecalis. International Journal of Antimicrobial Agents, 52, 936-941. DOI: 10.1016/j.ijantimicag.2018.05.005.
  • Huycke, M. M., Sahm, D. F., & Gilmore, M. S. (1998). Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerging Infectious Diseases, 4(2): 239–249. DOI: 10.3201/eid0402.980211.
  • Koneman, E. W., Allen, S. D., Janda, W. M., Schreckenberger, P. C., & Winn, W. C. JR. (1997). “The Gram Positive Cocci Part II Streptococci, Enterococci and The Streptococci Like Bacteria”. In Color Atlas and Textbook of Diagnostic Microbiology. 5 th Ed. Philadelphia: JB Lippincott Company; 577- 629.
  • Larsen, J., Schønheyder, H. C., Lester, C. H., Olsen, S. S., Porsbo, L. J., Garcia-Migura, L., Jensen, L. B., Bisgaard, M. & Hammerum A. M. (2010). Porcine-origin gentamicin resistant Enterococcus faecalis in humans, Denmark. Emerging Infectious Diseases, 16(1):682-684. DOI: 10.3201/eid1604.090500
  • McKinnell, J. A., Kunz, D. F., Chamot, E. , Patel, M., Shirley, R., Moser, S., Baddley, J. W., Pappas, P. G. & Miller, L. G. (2012). Association between vancomycin-resistant enterococci bacteremia and ceftriaxone usage. Infection Control & Hospital Epidemiology, 33(7):718-724. DOI: 10.1086/666331.
  • Murray, P. R., Rosenthal, K. S., & Pfaller, M. A. (2009). Enterococcus and other Gram-positive cocci. Medical Microbiology, (6th Ed), 243–246.
  • Nasiri, M., & Hanifian, S. (2022). Enterococcus faecalis and Enterococcus faecium in pasteurized milk: Prevalence, genotyping, and characterization of virulence traits. Lebensmittel-Wissenschaft & Technologie, 153, art. no. 112452. DOI: 10.1016/j.lwt.2021.112452.
  • Panesso, D., Reyes, J., Rincón, S., Díaz, L., Galloway-Peña, J., Zurita, J., Carrillo, C., Merentes, A., Guzmán, M., Adachi, J. A., Murray, B. E. & Arias, C. A. (2010). Molecular epidemiology of vancomycin-resistant Enterococcus faecium: a prospective, multicenter study in South American hospitals. Journal of Clinical Microbiology, 48(5):1562-1569. DOI: 10.1128/JCM.02526-09
  • Poulsen, L. L., Bisgaard, M., Son, N. T., Trung, N. V., An, H. M. & Dalsgaard, A. (2012). Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam. Emerging Infectious Diseases, 18(1):1096-1100. DOI: 10.3201/eid1807.111754.
  • Soodmand, J., Zeinali, T., Kalidari, G., Hashemitabar, G., & Razmyar, J. (2018). Antimicrobial Susceptibility Profile of Enterococcus Species Isolated from Companion Birds and Poultry in the Northeast of Iran. Archives of Razi Institute, Vol. 73, No. 3, 207-213. DOI: 10.22092/ari.2017.108332.1089.
  • Stępień-Pyśniak, D., Hauschild, T., Kosikowska, U., Dec, M. & Urban-Chmiel, R. (2019) Biofilm formation capacity and presence of virulence factors among commensal Enterococcus spp. from wild birds. Scientific Reports, 9, 1–7. DOI: 10.1038/s41598-019-47602-w
  • Teixeira, L. M., Carvalho, M. G. S., Shewmaker, P. L., & Facklam, R. R. (2011). Manual of Clinical Microbiology. Washington, D.C.: ASM Press, 350–364.
  • Tran, H. T., Vo, N. N., & Truong, Q. T. (2022). Optimization of medium composition for production of a simulated urine sample containing Enterococcus faecalis. Accreditation and Quality Assurance, 27, 119–124 DOI: 10.1007/s00769-022-01493-z.
  • Vu, J., & Carvalho, J. (2011). Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology. Frontiers in Biology, 6(5): 357–366. DOI 10.1007/s11515-011-1167-x.
  • Wada, Y., Ahmad, A. I., Rafidah, H. S., Mustapha, W., Hafeez, A. A., Chan, Y. Y., Azian, H., & Abdul, R. Z. (2022). "Prevalence of Vancomycin-Resistant Enterococcus (VRE) in Poultry in Malaysia: The First Meta-Analysis and Systematic Review" Antibiotics, 11, no. 2: 171.
  • Werner, G., Coque, T. M., Franz, C. M. A. P., Grohmann, E. , Hegstad, K., Jensen, L., van Schaik, W. & Weaver, K. (2013). Antibiotic resistant enterococci-Tales of a drug resistance gene trafficker. International Journal of Medical Microbiology, 303, 360–379. DOI: 10.1016/j.ijmm.2013.03.001.
Year 2022, Volume: 11 Issue: 2, 38 - 43, 28.12.2022
https://doi.org/10.53913/aduveterinary.1192214

Abstract

Project Number

VTF-19023

References

  • Abat, C., Huart, M., Garcia, V., Dubourg, G., & Raoult, D. (2016). Enterococcus faecalis urinary-tract infections: do they have a zoonotic origin. Journal of Infection, 73(4):305-313. DOI: 10.1016/j.jinf.2016.07.012.
  • Akgül, Ö., Gülhan, T., & Güdücüoğlu, H. (2016). Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Veterinary Journal of Ankara University, 63, 235-244.
  • Aktaş, G., & Derbentli, Ş. (2009). The importance and epidemiological characteristics of vancomycin-resistant Enterococci. Turkish Journal Of Infection, 23 (4): 201-209.
  • Bilgehan, H. (1995). “Streptokoklar” Klinik Mikrobiyoloji. Özel Bakteriyoloji ve Bakteri İnfeksiyonları. 9. Basım. İzmir: Şafak Matbaacılık, 248-286.
  • Cabral, B. G., Davies, Y. M., Menao, M. C., Saidenberg, A. B. S., Gomes, V. T. M., Moreno, L. Z., Sato, M. I. Z., Moreno, A. M., & Knöbl, T. (2020). Companion psittacine birds as reservoir of gentamicin and vancomycin-resistant Enterococcus spp. Pesquisa Veterinaria Brasileira, 40(2):129-133. DOI: 10.1590/1678-5150-PVB-6147.
  • Christensen, H., & Bisgaard, M. (2016). Members of Streptococcus and Enterococcus associated with disease in poultry. In A Laboratory Manual for the Isolation, Identification and Characterization of Avian Pathogens. 6th edn. Ed., Williams, S. M., Dufour-Zavala, L., Jackwood, M., Lee, M. W., Lupiani, B., Reed, W. M., Spackman, E. & Woolcock, P. R. 127–137. Jacksonville: American Association of Avian Pathologists.
  • Çetinkaya, Y., Falk, P., & Mayhall, C. G. (2000). Vancomycin resistant enterococci. Clinical Microbiology Reviews, 13, 686-707, 2000. DOI: 10.1128/CMR.13.4.686-707.
  • Devriese L., Baele M., & Butaye P. (2006). The genus Enterococcus. The Procaryotes, New York: Springer, 163–174.
  • Devriese, L. A., Ieven, M., Goossens, H., Vandamme, P., Pot, B., Hommez, J., & Haesebrouck F. (1996). Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrobial Agents and Chemotherapy, 40:2285-2287. DOI: 10.1128/AAC.40.10.2285
  • Franz, C. M., Muscholl-Silberhorn, A. B., Yousıf, N. M., Vancanneyt, M., Swings, J., & Holzapfel, W. H. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Applied and Environmental Microbiology, 67: 4385– 4389. DOI: 10.1128/AEM.67.9.4385-4389.2001.
  • Fisher, K., & Phillips, C. (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology, 155(Pt 6): 1749–1757. DOI: 10.1099/mic.0.026385-0.
  • Freitas, A. A. R., Faria, A. R., Pinto T. C. A., Merquior, V. L. C., Neves, D. M., Costa, R. C. D., & Teixeira, L. M. (2018). Distribution of species and antimicrobial resistance among enterococci isolated from the fecal microbiota of captive blue-fronted parrot (Amazona aestiva) in Rio de Janeiro, Brazil. Science of the Total Environment, 615:1428–1437. DOI: 10.1016/j.scitotenv.2017.09.004.
  • Gaca, A. O., & Lemos, J. A. (2019). Adaptation to adversity: the intermingling of stress tolerance and pathogenesis in Enterococci. Microbiology and Molecular Biology Reviews, 83(3), DOI:10.1128/MMBR.00008-19.
  • Hammerum, A. M., Lester, H., & Heuer, O. E. (2010). Antimicrobial-resistant 205 enterococci in animals and meat: a human health hazard? Foodborne Pathogens and Disease, 7(10):1137-1146. DOI: 10.1089/fpd.2010.0552.
  • Houssem Ben, Y., Sarra, C., Nabil, H., Haythem, G., Rym Ben, S., Sara, C., Carmen., & Karim Ben, S. (2018). Antimicrobial resistance and genetic lineages of faecal enterococci of wild birds: Emergence of vanA and vanB2 harbouring Enterococcus faecalis. International Journal of Antimicrobial Agents, 52, 936-941. DOI: 10.1016/j.ijantimicag.2018.05.005.
  • Huycke, M. M., Sahm, D. F., & Gilmore, M. S. (1998). Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerging Infectious Diseases, 4(2): 239–249. DOI: 10.3201/eid0402.980211.
  • Koneman, E. W., Allen, S. D., Janda, W. M., Schreckenberger, P. C., & Winn, W. C. JR. (1997). “The Gram Positive Cocci Part II Streptococci, Enterococci and The Streptococci Like Bacteria”. In Color Atlas and Textbook of Diagnostic Microbiology. 5 th Ed. Philadelphia: JB Lippincott Company; 577- 629.
  • Larsen, J., Schønheyder, H. C., Lester, C. H., Olsen, S. S., Porsbo, L. J., Garcia-Migura, L., Jensen, L. B., Bisgaard, M. & Hammerum A. M. (2010). Porcine-origin gentamicin resistant Enterococcus faecalis in humans, Denmark. Emerging Infectious Diseases, 16(1):682-684. DOI: 10.3201/eid1604.090500
  • McKinnell, J. A., Kunz, D. F., Chamot, E. , Patel, M., Shirley, R., Moser, S., Baddley, J. W., Pappas, P. G. & Miller, L. G. (2012). Association between vancomycin-resistant enterococci bacteremia and ceftriaxone usage. Infection Control & Hospital Epidemiology, 33(7):718-724. DOI: 10.1086/666331.
  • Murray, P. R., Rosenthal, K. S., & Pfaller, M. A. (2009). Enterococcus and other Gram-positive cocci. Medical Microbiology, (6th Ed), 243–246.
  • Nasiri, M., & Hanifian, S. (2022). Enterococcus faecalis and Enterococcus faecium in pasteurized milk: Prevalence, genotyping, and characterization of virulence traits. Lebensmittel-Wissenschaft & Technologie, 153, art. no. 112452. DOI: 10.1016/j.lwt.2021.112452.
  • Panesso, D., Reyes, J., Rincón, S., Díaz, L., Galloway-Peña, J., Zurita, J., Carrillo, C., Merentes, A., Guzmán, M., Adachi, J. A., Murray, B. E. & Arias, C. A. (2010). Molecular epidemiology of vancomycin-resistant Enterococcus faecium: a prospective, multicenter study in South American hospitals. Journal of Clinical Microbiology, 48(5):1562-1569. DOI: 10.1128/JCM.02526-09
  • Poulsen, L. L., Bisgaard, M., Son, N. T., Trung, N. V., An, H. M. & Dalsgaard, A. (2012). Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam. Emerging Infectious Diseases, 18(1):1096-1100. DOI: 10.3201/eid1807.111754.
  • Soodmand, J., Zeinali, T., Kalidari, G., Hashemitabar, G., & Razmyar, J. (2018). Antimicrobial Susceptibility Profile of Enterococcus Species Isolated from Companion Birds and Poultry in the Northeast of Iran. Archives of Razi Institute, Vol. 73, No. 3, 207-213. DOI: 10.22092/ari.2017.108332.1089.
  • Stępień-Pyśniak, D., Hauschild, T., Kosikowska, U., Dec, M. & Urban-Chmiel, R. (2019) Biofilm formation capacity and presence of virulence factors among commensal Enterococcus spp. from wild birds. Scientific Reports, 9, 1–7. DOI: 10.1038/s41598-019-47602-w
  • Teixeira, L. M., Carvalho, M. G. S., Shewmaker, P. L., & Facklam, R. R. (2011). Manual of Clinical Microbiology. Washington, D.C.: ASM Press, 350–364.
  • Tran, H. T., Vo, N. N., & Truong, Q. T. (2022). Optimization of medium composition for production of a simulated urine sample containing Enterococcus faecalis. Accreditation and Quality Assurance, 27, 119–124 DOI: 10.1007/s00769-022-01493-z.
  • Vu, J., & Carvalho, J. (2011). Enterococcus: review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology. Frontiers in Biology, 6(5): 357–366. DOI 10.1007/s11515-011-1167-x.
  • Wada, Y., Ahmad, A. I., Rafidah, H. S., Mustapha, W., Hafeez, A. A., Chan, Y. Y., Azian, H., & Abdul, R. Z. (2022). "Prevalence of Vancomycin-Resistant Enterococcus (VRE) in Poultry in Malaysia: The First Meta-Analysis and Systematic Review" Antibiotics, 11, no. 2: 171.
  • Werner, G., Coque, T. M., Franz, C. M. A. P., Grohmann, E. , Hegstad, K., Jensen, L., van Schaik, W. & Weaver, K. (2013). Antibiotic resistant enterococci-Tales of a drug resistance gene trafficker. International Journal of Medical Microbiology, 303, 360–379. DOI: 10.1016/j.ijmm.2013.03.001.
There are 30 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Article
Authors

Saniye Dolhan 0000-0003-2855-8332

Göksel Erbaş 0000-0002-1839-754X

Project Number VTF-19023
Publication Date December 28, 2022
Submission Date October 20, 2022
Published in Issue Year 2022 Volume: 11 Issue: 2

Cite

APA Dolhan, S., & Erbaş, G. (2022). Determination Of Enterococcus Species And Antibiotic Resistance In Budgerigars. Animal Health Production and Hygiene, 11(2), 38-43. https://doi.org/10.53913/aduveterinary.1192214