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Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması

Year 2020, Volume: 15 Issue: 2, 156 - 166, 27.10.2020
https://doi.org/10.17094/ataunivbd.706993

Abstract

Kedi ve köpeklerden sıklıkla izole edilen Staphylococcus türlerinin metisilin ve çoklu ilaç dirençliliği (MDR) artışı çalışmamızın temelini oluşturdu. Bu amaçla, Yakın Doğu Üniversitesi Hayvan Hastanesi’ne getirilen 100 adet köpek ve 42 adet kediye ait toplamda 142 adet klinik örnek (yara, kulak, göz, burun, deri svapları gibi) çalışıldı. İncelenen örneklerden izole edilen Staphylococcus spp. izolatlarının tür düzeyinde identifikasyonu, VITEK-2 mikrobiyal ID/ADT test sistemi ve API Staph identifikasyon sistemi ile gerçekleştirildi. Staphylococcus izolatlarının antimikrobiyal duyarlılık analizleri VITEK-2 otomatize sistem aracılığı ile gerçekleştirildi. İncelenen numunelerden 78 adet (%54.92) Staphylococcus spp. izole edildi. İzolatların 52’si (%66.67) Koagulaz pozitif Staphylococcus (CoPS) ve 16’sı (%20.51) Koagulaz negatif Staphylococcus (CoNS) olarak identifiye edildi. CoPS’lar arasında en yüksek oranda identifiye edilen türlerin Staphylococcus (S.) pseudintermedius (%38,46) ve S. aureus (%25.64); CoNS’lar arasında ise S. chromogenes (%10.26) olduğu belirlendi. Antimikrobiyal madde duyarlılık analizleri sonucu, 11 (%28.2) izolat metisilin dirençli S. aureus (MRSA), 10 (%25.64) izolat metisilin dirençli S. pseudintermedius (MRSP) ve 10 (%25.64) izolat metisilin dirençli Koagulaz negatif Staphylococcus (MRCoNS) olarak belirlendi. Ayrıca çoklu ilaç direnci tespit edilen türlerin 6’sında (%40.00) MDR-MRSP ve 4’ünde (%26.66) MDR-MRSA pozitifliği belirlendi. Toplamda 23 adet MDR Staphylococcus spp. izolatının 21 adedi köpeklerden ve 2 adedi de kedilerden izole edilmiştir. Çalışmada elde edilen veriler ışığında artan çoklu ilaç direncinin güncel yaklaşımlarını hayvanlardan izole edilen Staphylococcus türlerinde inceleyerek tedavi protokollerinin bu çerçevede uygulanmasına katkı sağlandı.

References

  • 1. Nikaido H., 2009. Multidrug Resistance in Bacteria. Annu Rev Biochem, 78, 119-146.
  • 2. Tanwar J., Das S., Fatima Z., Hameed S., 2014. Multi Resistance: An Emerging Crisis. Interdiscip Perspect on Infect Dis, vol. 2014, Article ID 541340.
  • 3. Magiorakos AP., Srinivasan A., Carey RB., Carmeli Y., Falagas ME., Giske CG., Harbarth S., Hindler JF., Kahlmeter G., Olsson-Liljequist B., Paterson DL., Rice LB., Stelling J., Struelens MJ., Vatopoulos A., Weber JT. and Monnet DL., 2012. Multidrug resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect, 18, 3, 268-281.
  • 4. Weese JS., 2011. Infection control in veterinary practice; the time is now. J Small Anim Pract, 52, 507-508.
  • 5. Walther B., Tedin K., Lübke-Becker A., 2017. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet Microbiol, 200, 71-78.
  • 6. Febler AT., Schuenemann R., Kadlec K., Hensel V., Brombach J., Murugaiyan J., Oechtering G., Burgener IA., Schwarz S., 2018. Methicillinresistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees an in the environment of a small animal hospital. Vet Microbiol, 221, 153-158.
  • 7. Ruple-Czerniak A., Aceto HW., Bender JB., Paradis MR., Shaw SP., Van Metre DC., Weese JS., Wilson DA., Wilson JH., and Morley PS., 2013. Using syndromic surveillance to estimate baseline rates for healthcare-associated infections in critical care units of small animal referral hospitals. J Vet Intern Med, 27, 1392- 1399.
  • 8. Stull JW., Weese JS., 2015. Hospital-associated infections in small animal practice. Vet Clin North Am Small Anim Pract, 45, 217-233.
  • 9. Wieler LH., Walther B., Vincze S., Guenther S., Luebke-Becker A., 2014. In ‘’Zoonoses – Infections Affecting Humans and Animals: Focus on Public Health Aspects’’, Ed., A Sing, 433ff, Springer, Oberschleißheim.
  • 10. Wieler LH., Ewers C., Guenther S., Walther B., Lubke-Becker A., 2011. Methicillin-resistant Staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)- producing Enterobacteriaceae in companion animals: nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. Int J Med Microbiol, 301, 635-641.
  • 11. Pinho MG., de Lencastre H., Tomasz A., 2001. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drugresistant Staphylococci. Proc Natl Acad Sci USA, 98, 1088-10891.
  • 12. Siugzdaite J., Gabinaitiene A., 2017. Methicillinresistant coagulase-negative staphylococci in healthy dogs. Vet Med (Praha), 62, 479-487.
  • 13. Gronthal T., Moodley A., Nykasenoja S., Junnila J., Guardabassi L., Thomson K., Rantala M., 2014. Large outbreak caused by methicillin resistant Staphylococcus pseudintermedius ST71 in a Finnish Veterinary Teaching Hospital–from outbreak control to outbreak prevention. PLoS One 9, 10, e110084.
  • 14. Lee CH., Park YK., Shin S., Park YH., Park KT., 2018. Characterization of methicillin-resistant Staphylococcus pseudintermedius isolated from dogs in veterinary hospitals in Korea. Int J Appl Res Vet Med, 16, 211-220.
  • 15. Rahman MM., Amin KB., Rahman SMM., Khair A., Rahman M., Hossain A., Rahman AKMA., Parvez MS., Miura N. and Alam MM., 2018. Investigation of methicillin-resistant Staphylococcus aureus among clinical isolates from humans and animals by culture methods and multiplex PCR. BMC Vet Res, 14, 300.
  • 16. Guardabassi L., Schwarz S., Lloyd DH., 2004. Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother, 54, 321-332.
  • 17. Lloyd DH., 2007. Reservoirs of antimicrobial resistance in pet animals. Clin Infect Dis, 45, 148-152.
  • 18. Loeffler A., Lloyd DH., 2010. Companion animals: a reservoir for methicillin-resistant Staphylococcus aureus in the community? Epidemiol Infect, 138, 595-605.
  • 19. Tabatabaei S., Najafifarb A., Badouei AM., Salehia TZ., Tamaia IA., Khaksard E., Abbassie MS., Ghazisaeedif F., 2019. Genetic characterization of methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in pets and veterinary personnel in Iran: new insights into emerging methicillin-resistant S. pseudintermedius (MRSP). Journal of Global Antimicrobial Res, 16, 6-10.
  • 20. Weese JS., Dick H., Willey BM., McGeer A., Kreiswirth BN., Innis B., Low DE., 2006. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol, 115, 148-155.
  • 21. Clinical and Laboratory Standards Institute (CLSI) 2017. Performance Standards for Antimicrobial Susceptibility Testing. M02-A12/M07-A10, CLSI Standards and Guidelines, Wayne, PA.
  • 22. Gandolfi-Decristophoris P., Regula G., Petrini O., Zinsstag J., Schelling E., 2013. Prevalence and risk factors for carriage of multidrug resistant staphylococci in healthy cats and dogs. J Vet Sci, 14, 449-456.
  • 23. Detwiler A., Bloom P., Petersen A., Rosser EJ., 2013. Multi-drug and methicillin resistance of staphylococci from canine patients at a veterinary teaching hospital (2006 2011). Vet Quart, 33, 60-67.
  • 24. Kaspar U., von Lützau A., Schlattmann A., Roesler U., Köck R., Becker K., 2018. Zoonotic multidrugresistant microorganisms among small companion animals in Germany. PLoS One 13, 12, e0208364.
  • 25. Bannoehr J., Franco A., Iurescia M., Battisti A., Fitzgerald J., 2009. Molecular diagnostic identification of Staphylococcus pseudintermedius. J Clin Microbiol, 47, 469-471.
  • 26. Qekwana DN., Sebola D., Oguttu JW., Odoi A., 2017. Antimicrobial resistance patterns of Staphylococcus species isolated from cats presented at a veterinary academic hospital in South Africa. BMC Vet Res, 13, 286-292.
  • 27. Saputra S., Jordan D., Worthing KA., Norris JM., Wong HS., Abraham R., Trott DJ., Abraham S., 2017. Antimicrobial resistance in coagulasepositive staphylococci isolated from companion animals in Australia: a one year study. PLoS One 12, 4:e0176379.
  • 28. Loeffler A., Linek M., Moodley A., Guardabassi L., Sung JML., Winkler M., Weiss R. and. Lloyd DH., 2007. First report of multiresistant, mecApositive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Vet Dermatol, 18, 412-421.
  • 29. Fındık A., Çiftci A., Önyay T., Sezener MG., Koçak Y., Gülhan T., 2018. Determination of methicillin resistance and some genotypic characteristics of staphylococci isolated from dogs and their owners. Turk J Vet Anim Sci, 42, 549-555.
  • 30. Vincze S., Stamm I., Kopp PA., Hermes J., Adlhoch C., Semmler T., Wieler LH., Lu¨bke-Becker A., Walther B., 2014. Alarming proportions of methicillin-Resistant Staphylococcus aureus (MRSA) in wound samples from companion animals, Germany 2010-2012. PLoS One 9, 1, e85656.
  • 31. Ludwig C., de Jong A., Moyaert H., El Garch F., Janes R., Klein U., Morrissey I., Thiry J. and Youala M., 2016. Antimicrobial susceptibility monitoring of dermatological bacterial pathogens isolated from diseased dogs and cats across Europe (ComPath results). J Appl Microbiol, 121, 1254-1267.
  • 32. Kizerwetter-Swida M., Chrobak D., Rzewuska M., Binek M., 2009. Antibiotic resistance patterns and occurrence of mecA gene in Staphylococcus intermedius strains of canine origin. Pol J Vet Sci, 12, 9-13.
  • 33. Stegmann R., Burnens A., Maranta CA. Perreten V.,2010. Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J Antimicrob Chemother, 65, 2047-2048.
  • 34. Talan DA., Goldstein EJ., Staatz D., Overturf GD.,1989. Staphylococcus intermedius: clinical presentation of a new human dog bite pathogen. Ann Emerg Med, 18, 410-413.

Investigation of Multidrug Resistance among Staphylococcus Species Isolated from Cats and Dogs

Year 2020, Volume: 15 Issue: 2, 156 - 166, 27.10.2020
https://doi.org/10.17094/ataunivbd.706993

Abstract

The increase in methicillin and multidrug resistance (MDR) of Staphylococcus species, which are frequently isolated from cats and dogs, formed the basis of our study. For this purpose, a total of 142 clinical samples (wound, ear, eye, nasal, skin swabs, etc.) belonging to 100 dogs and 42 cats brought to the Near East University Animal Hospital were studied in our investigation. Species-level identification of Staphylococcus spp. isolated from the samples examined was performed with the VITEK-2 microbial ID/AST test system and API Staph identification system. Antimicrobial susceptibility analyzes of Staphylococcus isolates were carried out through the VITEK-2 automated system. From the samples, 78 (54.92%) Staphylococcus spp. were isolated. 52 (66.67%) of the isolates were identified as Coagulase positive Staphylococcus (CoPS) and 16 (20.51%) as Coagulase negative Staphylococcus (CoNS). Among CoPS, the most frequently identified species were S. pseudintermedius (38.46%) and S. aureus (25.64%); whereas among CoNS, S. chromogenes (10.26%) was determined as the most predominant. According to the results of antimicrobial susceptibility analyzes, 11 (28.2%) isolates were determined as methicillin resistant S. aureus (MRSA), 10 (25.64%) as methicillin resistant S. pseudintermedius (MRSP) and 10 (25.64%) isolate methicillin resistant Coagulase negative Staphylococcus (MRCoNS). Besides, 6 (40.00%) MDR-MRSP and 4 (26.66%) MDRMRSA positivity were determined among the species with multiple drug resistance. Of the 23 MDR Staphylococcus spp. isolates in total, 21 were isolated from dogs and 2 from cats. By analyzing the current approaches of the increased drug resistance with the data obtained in this study in Staphylococcus species isolated from animals, necessary contributions have been implemented to the treatment protocols within this framework.

References

  • 1. Nikaido H., 2009. Multidrug Resistance in Bacteria. Annu Rev Biochem, 78, 119-146.
  • 2. Tanwar J., Das S., Fatima Z., Hameed S., 2014. Multi Resistance: An Emerging Crisis. Interdiscip Perspect on Infect Dis, vol. 2014, Article ID 541340.
  • 3. Magiorakos AP., Srinivasan A., Carey RB., Carmeli Y., Falagas ME., Giske CG., Harbarth S., Hindler JF., Kahlmeter G., Olsson-Liljequist B., Paterson DL., Rice LB., Stelling J., Struelens MJ., Vatopoulos A., Weber JT. and Monnet DL., 2012. Multidrug resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect, 18, 3, 268-281.
  • 4. Weese JS., 2011. Infection control in veterinary practice; the time is now. J Small Anim Pract, 52, 507-508.
  • 5. Walther B., Tedin K., Lübke-Becker A., 2017. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet Microbiol, 200, 71-78.
  • 6. Febler AT., Schuenemann R., Kadlec K., Hensel V., Brombach J., Murugaiyan J., Oechtering G., Burgener IA., Schwarz S., 2018. Methicillinresistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees an in the environment of a small animal hospital. Vet Microbiol, 221, 153-158.
  • 7. Ruple-Czerniak A., Aceto HW., Bender JB., Paradis MR., Shaw SP., Van Metre DC., Weese JS., Wilson DA., Wilson JH., and Morley PS., 2013. Using syndromic surveillance to estimate baseline rates for healthcare-associated infections in critical care units of small animal referral hospitals. J Vet Intern Med, 27, 1392- 1399.
  • 8. Stull JW., Weese JS., 2015. Hospital-associated infections in small animal practice. Vet Clin North Am Small Anim Pract, 45, 217-233.
  • 9. Wieler LH., Walther B., Vincze S., Guenther S., Luebke-Becker A., 2014. In ‘’Zoonoses – Infections Affecting Humans and Animals: Focus on Public Health Aspects’’, Ed., A Sing, 433ff, Springer, Oberschleißheim.
  • 10. Wieler LH., Ewers C., Guenther S., Walther B., Lubke-Becker A., 2011. Methicillin-resistant Staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)- producing Enterobacteriaceae in companion animals: nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. Int J Med Microbiol, 301, 635-641.
  • 11. Pinho MG., de Lencastre H., Tomasz A., 2001. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drugresistant Staphylococci. Proc Natl Acad Sci USA, 98, 1088-10891.
  • 12. Siugzdaite J., Gabinaitiene A., 2017. Methicillinresistant coagulase-negative staphylococci in healthy dogs. Vet Med (Praha), 62, 479-487.
  • 13. Gronthal T., Moodley A., Nykasenoja S., Junnila J., Guardabassi L., Thomson K., Rantala M., 2014. Large outbreak caused by methicillin resistant Staphylococcus pseudintermedius ST71 in a Finnish Veterinary Teaching Hospital–from outbreak control to outbreak prevention. PLoS One 9, 10, e110084.
  • 14. Lee CH., Park YK., Shin S., Park YH., Park KT., 2018. Characterization of methicillin-resistant Staphylococcus pseudintermedius isolated from dogs in veterinary hospitals in Korea. Int J Appl Res Vet Med, 16, 211-220.
  • 15. Rahman MM., Amin KB., Rahman SMM., Khair A., Rahman M., Hossain A., Rahman AKMA., Parvez MS., Miura N. and Alam MM., 2018. Investigation of methicillin-resistant Staphylococcus aureus among clinical isolates from humans and animals by culture methods and multiplex PCR. BMC Vet Res, 14, 300.
  • 16. Guardabassi L., Schwarz S., Lloyd DH., 2004. Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother, 54, 321-332.
  • 17. Lloyd DH., 2007. Reservoirs of antimicrobial resistance in pet animals. Clin Infect Dis, 45, 148-152.
  • 18. Loeffler A., Lloyd DH., 2010. Companion animals: a reservoir for methicillin-resistant Staphylococcus aureus in the community? Epidemiol Infect, 138, 595-605.
  • 19. Tabatabaei S., Najafifarb A., Badouei AM., Salehia TZ., Tamaia IA., Khaksard E., Abbassie MS., Ghazisaeedif F., 2019. Genetic characterization of methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in pets and veterinary personnel in Iran: new insights into emerging methicillin-resistant S. pseudintermedius (MRSP). Journal of Global Antimicrobial Res, 16, 6-10.
  • 20. Weese JS., Dick H., Willey BM., McGeer A., Kreiswirth BN., Innis B., Low DE., 2006. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol, 115, 148-155.
  • 21. Clinical and Laboratory Standards Institute (CLSI) 2017. Performance Standards for Antimicrobial Susceptibility Testing. M02-A12/M07-A10, CLSI Standards and Guidelines, Wayne, PA.
  • 22. Gandolfi-Decristophoris P., Regula G., Petrini O., Zinsstag J., Schelling E., 2013. Prevalence and risk factors for carriage of multidrug resistant staphylococci in healthy cats and dogs. J Vet Sci, 14, 449-456.
  • 23. Detwiler A., Bloom P., Petersen A., Rosser EJ., 2013. Multi-drug and methicillin resistance of staphylococci from canine patients at a veterinary teaching hospital (2006 2011). Vet Quart, 33, 60-67.
  • 24. Kaspar U., von Lützau A., Schlattmann A., Roesler U., Köck R., Becker K., 2018. Zoonotic multidrugresistant microorganisms among small companion animals in Germany. PLoS One 13, 12, e0208364.
  • 25. Bannoehr J., Franco A., Iurescia M., Battisti A., Fitzgerald J., 2009. Molecular diagnostic identification of Staphylococcus pseudintermedius. J Clin Microbiol, 47, 469-471.
  • 26. Qekwana DN., Sebola D., Oguttu JW., Odoi A., 2017. Antimicrobial resistance patterns of Staphylococcus species isolated from cats presented at a veterinary academic hospital in South Africa. BMC Vet Res, 13, 286-292.
  • 27. Saputra S., Jordan D., Worthing KA., Norris JM., Wong HS., Abraham R., Trott DJ., Abraham S., 2017. Antimicrobial resistance in coagulasepositive staphylococci isolated from companion animals in Australia: a one year study. PLoS One 12, 4:e0176379.
  • 28. Loeffler A., Linek M., Moodley A., Guardabassi L., Sung JML., Winkler M., Weiss R. and. Lloyd DH., 2007. First report of multiresistant, mecApositive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Vet Dermatol, 18, 412-421.
  • 29. Fındık A., Çiftci A., Önyay T., Sezener MG., Koçak Y., Gülhan T., 2018. Determination of methicillin resistance and some genotypic characteristics of staphylococci isolated from dogs and their owners. Turk J Vet Anim Sci, 42, 549-555.
  • 30. Vincze S., Stamm I., Kopp PA., Hermes J., Adlhoch C., Semmler T., Wieler LH., Lu¨bke-Becker A., Walther B., 2014. Alarming proportions of methicillin-Resistant Staphylococcus aureus (MRSA) in wound samples from companion animals, Germany 2010-2012. PLoS One 9, 1, e85656.
  • 31. Ludwig C., de Jong A., Moyaert H., El Garch F., Janes R., Klein U., Morrissey I., Thiry J. and Youala M., 2016. Antimicrobial susceptibility monitoring of dermatological bacterial pathogens isolated from diseased dogs and cats across Europe (ComPath results). J Appl Microbiol, 121, 1254-1267.
  • 32. Kizerwetter-Swida M., Chrobak D., Rzewuska M., Binek M., 2009. Antibiotic resistance patterns and occurrence of mecA gene in Staphylococcus intermedius strains of canine origin. Pol J Vet Sci, 12, 9-13.
  • 33. Stegmann R., Burnens A., Maranta CA. Perreten V.,2010. Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J Antimicrob Chemother, 65, 2047-2048.
  • 34. Talan DA., Goldstein EJ., Staatz D., Overturf GD.,1989. Staphylococcus intermedius: clinical presentation of a new human dog bite pathogen. Ann Emerg Med, 18, 410-413.
There are 34 citations in total.

Details

Primary Language Turkish
Subjects Health Care Administration
Journal Section Araştırma Makaleleri
Authors

Hüban Göçmen

Hazel Tamakan

Halit Şükür

Ömer Memduh Esendal

Publication Date October 27, 2020
Published in Issue Year 2020 Volume: 15 Issue: 2

Cite

APA Göçmen, H., Tamakan, H., Şükür, H., Esendal, Ö. M. (2020). Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 15(2), 156-166. https://doi.org/10.17094/ataunivbd.706993
AMA Göçmen H, Tamakan H, Şükür H, Esendal ÖM. Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. October 2020;15(2):156-166. doi:10.17094/ataunivbd.706993
Chicago Göçmen, Hüban, Hazel Tamakan, Halit Şükür, and Ömer Memduh Esendal. “Kedi Ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 15, no. 2 (October 2020): 156-66. https://doi.org/10.17094/ataunivbd.706993.
EndNote Göçmen H, Tamakan H, Şükür H, Esendal ÖM (October 1, 2020) Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 15 2 156–166.
IEEE H. Göçmen, H. Tamakan, H. Şükür, and Ö. M. Esendal, “Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 15, no. 2, pp. 156–166, 2020, doi: 10.17094/ataunivbd.706993.
ISNAD Göçmen, Hüban et al. “Kedi Ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 15/2 (October 2020), 156-166. https://doi.org/10.17094/ataunivbd.706993.
JAMA Göçmen H, Tamakan H, Şükür H, Esendal ÖM. Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2020;15:156–166.
MLA Göçmen, Hüban et al. “Kedi Ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 15, no. 2, 2020, pp. 156-6, doi:10.17094/ataunivbd.706993.
Vancouver Göçmen H, Tamakan H, Şükür H, Esendal ÖM. Kedi ve Köpeklerden İzole Edilen Staphylococcus Türlerinde Çoklu İlaç Dirençliliğinin Araştırılması. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2020;15(2):156-6.