Profile of Multidrug Resistance and Methicillin-Resistant Staphylococcus aureus (MRSA) isolated from cats in Surabaya, Indonesia




Abstract. Afnani DA, Fatih N, Effendi MH, Tyasningsih W, Kairullah AR, Kurniawan SC, Silaen OSM, Ramandianto SC, Widodo A, Hendriana K, Riwu KHP. 2022. Profile of Multidrug Resistance and Methicillin-Resistant Staphylococcus aureus (MRSA) isolated from cats in Surabaya, Indonesia. Biodiversitas 23: 5703-5709. Methicillin-Resistant Staphylococcus aureus (MRSA) is the name given to Staphylococcus aureus that has multidrug-resistance (MDR) characteristics and is resistant to ?-lactam drugs. Compared to other livestock, companion animals have been mentioned as potential MRSA reservoirs more frequently. This study aimed to identify MDR and detects MRSA strains from cats in Surabaya. A total of 150 nasal swab of cats were taken from several clinics and veterinary hospital. Samples were swabbed using Amies Medium Transport then identified using microbiological standard method. Kirby-Bauer diffusion method was performed for S. aureus antibiotic resistance profile on five different antibiotic discs. As a confirmatory test for MRSA, S. aureus isolates that were resistant to cefoxitin continued to grow on Oxacillin Resistance Screening Agar Base (ORSAB). The findings of the isolation and identification and process revealed 18 (12%) S. aureus isolates. The antibiotic resistance test revealed 3 (2%) MDR S. aureus isolates and 4 (2.6%) MDR S. aureus isolates that were ORSAB positive. It has been discovered that there are MDR and MRSA S. aureus isolates. It could be used as an indicator of irrational usage of antibiotics and it explained that cats could be source of infection to public health.


Aarestrup FM, Cavaco L, Hasman H. 2010. Decreased susceptibility to zinc chloride is associated with Methicillin resistant Staphylococcus aureus CC 398 in Danish swine. Vet Microbiol 142 (3-4): 455-457. DOI: 10.1016/j.vetmic.2009.10.021.
Aires-de-Sousa M. 2017. Methicillin-resistant Staphylococcus aureus among animals: current overview. Clin Microbiol Infect 23 (6): 373-380. DOI: 10.1016/j.cmi.2016.11.002.
Algammal AM, Hetta HF, Elkelish A, Alkhalifah DHH, Hozzein WN, Batiha GE, El Nahhas N, Mabrok MA. 2020. Methicillin-Resistant Staphylococcus aureus (MRSA): One Health Perspective Approach to the Bacterium Epidemiology, Virulence Factors, Antibiotic-Resistance, and Zoonotic Impact. Infect Drug Resist 13: 3255-3265. DOI: 10.2147/IDR.S272733.
Asbell PA, Pandit RT, Sanfilippo CM. 2018. Antibiotic Resistance Rates by Geographic Region Among Ocular Pathogens Collected During the ARMOR Surveillance Study. Ophthalmol Ther 7 (2): 417-429. DOI: 10.1007/s40123-018-0141-y.
Bierowiec K, P?oneczka-Janeczko K, Rypu?a K. 2016. Is the Colonisation of Staphylococcus aureus in Pets Associated with Their Close Contact with Owners? PLoS One 11 (5): e0156052. DOI: 10.1371/journal.pone.0156052.
Bloomfield SF, Aiello AE, Cookson B, O'Boyle C, Larson EL. 2007. The effectiveness of hand hygiene procedures in reducing the risks of infections in home and community settings including handwashing and alcohol-based hand sanitizers. Am J Infect Control 35 (10): S27-S64. DOI: 10.1016/j.ajic.2007.07.001.
Bonjean M, Hodille E, Dumitrescu O, Dupieux C, Nkoud Mongo C, Allam C, Beghin M, Paris M, Borrel O, Chardon H, Laurent F, Rasigade JP, Lina G. 2016. Disk Diffusion Testing for Detection of Methicillin-Resistant Staphylococci: Does Moxalactam Improve upon Cefoxitin? J Clin Microbiol 54 (12): 2905-2909. DOI: 10.1128/JCM.01195-16.
Chandrasekaran D, Venkatesan P, Tirumurugaan KG, Gowri B, Subapriya S, Thirunavukkarasu S. 2014. Subacute mastitis associated with Methicillin Resistant Staphylococcus aureus in a cow: A case report. J Adv Vet Anim Res 1 (4): 235-237. DOI: 10.5455/javar.2014.a35.
Clinical and Laboratory Standards Institute. 2020. Performance Standards for Antimicrobial Disk Diffusion Susceptibility Testing; 17th Informational Supplement. Approved Standard M100-17.Clinical and Laboratory Standards Institute.
Cook MA, Wright GD. 2022. The past, present, and future of antibiotics. Sci Transl Med 14 (657): eabo7793. DOI: 10.1126/scitranslmed.abo7793.
Crespo-Piazuelo D, Lawlor PG. 2021. Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) prevalence in humans in close contact with animals and measures to reduce on-farm colonisation. Ir Vet J 74: 21 DOI: 10.1186/s13620-021-00200-7.
Decline V, Effendi MH, Rahmaniar RP, Yanestria SM, Harijani N. 2020. Profile of antibiotic-resistant and presence of methicillin-resistant Staphylococcus aureus from nasal swab of dogs from several animal clinics in Surabaya, Indonesia. Int J One Health 6 (1): 90-94. DOI: 10.14202/ijoh.2020.90-94.
Domon H, Uehara Y, Oda M, Seo H, Kubota N, Terao Y. 2016. Poor survival of Methicillin-resistant Staphylococcus aureus on inanimate objects in the public spaces. Microbiologyopen 5 (1): 39-46. DOI: 10.1002/mbo3.308.
Effendi MH, Hisyam MAM, Hastutiek P, Tyasningsih W. 2019. Detection of coagulase gene in Staphylococcus aureus from several dairy farms in East Java, Indonesia, by polymerase chain reaction. Vet World 12 (1): 68-71. DOI: 10.14202/vetworld.2019.68-71.
Effendi MH, Oktavianto A, Hastutiek P. 2018. Tetracycline resistance gene in Streptococcus agalactiae isolated from bovine subclinical mastitis in Surabaya, Indonesia. Philipp J Vet Med 55 (SI): 115-120.
Fishovitz J, Hermoso JA, Chang M, Mobashery S. 2014. Penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus. IUBMB Life 66 (8): 572-577. DOI: 10.1002/iub.1289.
Gemma CM, Worthing KA,Ward MP, Norris JM. 2020. Commensal Staphylococci Including Methicillin-Resistant Staphylococcus aureus from Dogs and Cats in Remote New South Wales, Australia. Microb Ecol 79 (1): 164-174. DOI: 10.1007/s00248-019-01382-y.
Gulani IA, Geidam YA, Adamu L, Lawal JR, Abadam FA. 2016. Prevalence and phenotypic detection of methicillin resistance Staphylococcus aureus between ruminants butchered for humanoid intake and animal handlers in Maiduguri, Nigeria. J Adv Vet Anim Res 3 (2): 152-159. DOI: 10.5455/javar.2016.c145.
Haag AF, Fitzgerald JR, Penadés JR. 2019. Staphylococcus aureus in Animals. Microbiol Spectr 7 (3): 11. DOI:
Habibullah A, Rahman AMMT, Haydar MR, Nazir KHMNH, Rahman MT. 2017. Prevalence and Molecular Detection of Methicillin Resistant Staphylococcus aureus from Dogs and Cats in Dhaka City. Bangl J Vet Med 15 (1): 51-57. DOI: 10.3329/bvjm.v15i1.34055.
Harkins CP, Pichon B, Doumith M, Parkhill J, Westh H, Tomasz A, de Lencastre H, Bentley SD, Kearns AM, Holden MTG. 2017. Methicillin-resistant Staphylococcus aureus emerged long before the introduction of methicillin into clinical practice. Genome Biol 18 (1): 130. DOI: 10.1186/s13059-017-1252-9.
Harrison EM, Weinert LA, Holden MT, Welch JJ, Wilson K, Morgan FJ, Harris SR, Loeffler A, Boag AK, Peacock SJ, Paterson GK, Waller AS, Parkhill J, Holmes MA. 2014. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. mBio 5 (3): e00985-13. DOI: 10.1128/mBio.00985-13.
Hernandez E, Fawcett A, Brouwer E, Rau J, Turner PV. 2018. Speaking Up: Veterinary Ethical Responsibilities and Animal Welfare Issues in Everyday Practice. Animals (Basel) 8 (1): 15. DOI: 10.3390/ani8010015.
Hiramatsu K, Katayama Y, Matsuo M, Sasaki T, Morimoto Y, Sekiguchi A, Baba T. 2014. Multi-drug-resistant Staphylococcus aureus and future chemotherapy. J Infect Chemother 20 (10): 593-601. DOI: 10.1016/j.jiac.2014.08.001.
Islam A, Nath AD, Islam K, Islam S, Chakma S, Hossain MB, Al-Faruq A, Hassan MM. 2016. Isolation, identification and antimicrobial resistance profile of Staphylococcus aureus in Cockroaches (Periplaneta americana). J Adv Vet Anim Res 3 (3): 221-228. DOI:
János D, Viorel H, Lonica L, Corina P, Tiana F, Roxana D. 2021. Carriage of Multidrug Resistance Staphylococci in Shelter Dogs in Timisoara, Romania. Antibiotics (Basel) 10 (7): 801. DOI: 10.3390/antibiotics10070801.
Jordan D, Simon J, Fury S, Moss S, Giffard P, Maiwald M, Southwell P, Barton MD, Axon JE, Morris SG, Trott DJ. 2011. Carriage of methicillin-resistant Staphylococcus aureus by veterinarians in Australia. Aust Vet J 89 (5): 152-159. DOI: 10.1111/j.1751-0813.2011.00710.x.
Kaspar U, Lützau AV, Svhlattmann A, Roesler U, Köck R, Becker K. 2018. Zoonotic multidrug-resistant microorgranisms among small companion animals in Germany. Plos One 13 (12): 1-15. DOI: 10.1371/journal.pone.0208364.
Khairullah AR, Raharjo D, Rahmahani J, Suwarno, Tyasningsih W, Harijani N. 2019. Antibiotics resistant at Staphylococcus aureus and Streptococcus sp isolated from bovine mastitis in Karangploso, East Java, Indonesia. Indian J Forensic MedToxicol 13(4):439-444. DOI:10.5958/0973-9130.2019.00329.3.
Khairullah AR, Ramandinianto SC, Effendi MH. 2020a. A Review of Livestock-Associated Methicillin-Resistant Staphylococcus aureus (LA-MRSA) on Bovine Mastitis. Syst Rev Pharm 11 (7): 172-183. DOI: 10.31838/srp.2020.7.28.
Khairullah AR, Rehman S, Sudjarwo SA, Effendi MH, Ramandininto SC, Gelolodo MA, Widodo A, Riwu KHP, Kurniawati DA. 2022c. Detection of mecA gene and methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and risk factors from farms in Probolinggo, Indonesia. F1000 Research 11: 722. DOI: 10.12688/f1000research.122225.1.
Khairullah AR, Sudjarwo SA, Effendi MH, Harijani N, Tyasningsih W, Rahmahani J, Permatasari DA, Ramandinianto SC, Widodo A, Riwu KHP. 2020b. A Review of Methicillin-Resistant Staphylococcus aureus (MRSA) on Milk and Milk Products: Public Health Importance. Syst Rev Pharm 11 (8): 59-69. DOI: 10.31838/srp.2020.8.9.
Khairullah AR, Sudjarwo SA, Effendi MH, Ramandininto SC, Gelolodo MA, Widodo A, Riwu KHP, Kurniawati DA, Rehman S. 2022a. Profile of Multidrug Resistance and Methicillin-Resistant Staphylococcus aureus (MRSA) on dairy cows and risk factors from farmer. Biodiversitas 23 (6): 2853-2858. DOI: 10.13057/biodiv/d230610.
Khairullah AR, Sudjarwo SA, Effendi MH, Ramandinianto SC, Widodo A, Riwu KHP. 2022b. A review of horses as a source of spreading livestock-associated methicillin-resistant Staphylococcus aureus to human health. Vet World 15 (8): 1906-1915.
Klaschik S, Lehmann LE, Steinhagen F, Book M, Molitor E, Hoeft A, Stueber F. 2015. Differentiation between Staphylococcus aureus and coagulase-negative Staphylococcus species by real-time PCR including detection of methicillin resistants in comparison to conventional microbiology testing. J Clin Lab Anal 29 (2): 122-128. DOI: 10.1002/jcla.21739.
Lee A, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, Harbarth S. 2018. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers 4: 18033. DOI: 10.1038/nrdp.2018.33.
Lee CS, Montalmont B, O'Hara JA, Syed A, Chaussard C, McGaha TL, Pakstis DL, Lee JH, Shutt KA, Doi Y. 2015. Screening for methicillin-resistant Staphylococcus aureus colonization using sponges. Infect Control Hosp Epidemiol 36 (1): 28-33. DOI: 10.1017/ice.2014.4.
Leung EC, Lee MK, Lai RW. 2013. Admission Screening of Methicillin-Resistant Staphylococcus aureus with Rapid Molecular Detection in Intensive Care Unit: A Three-Year Single-Centre Experience in Hong Kong. ISRN Microbiol 2013: 140294. DOI: 10.1155/2013/140294.
Loeffler A, Pfeiffer DU, Lloyd DH, Smith H, Soares-Magalhaes R, Lindsay JA. 2010. Meticillin-resistant Staphylococcus aureus carriage in UK veterinary staff and owners of infected pets: new risk groups. J Hosp Infect 74 (3): 282-288. DOI: 10.1016/j.jhin.2009.09.020.
López-Alcalde J, Mateos-Mazón M, Guevara M, Conterno LO, Solà I, Cabir Nunes S, Bonfill Cosp X. 2015. Gloves, gowns and masks for reducing the transmission of meticillin-resistant Staphylococcus aureus (MRSA) in the hospital setting. Cochrane Database Syst Rev 2015 (7): CD007087. DOI: 10.1002/14651858.CD007087.pub2.
McClure JA, Conly JM, Obasuyi O, Ward L, Ugarte-Torres A, Louie T, Zhang K. 2020. A Novel Assay for Detection of Methicillin-Resistant Staphylococcus aureus Directly From Clinical Samples. Front Microbiol 11: 1295. DOI: 10.3389/fmicb.2020.01295.
Meng X, Zhang G, Sun B, Liu S, Wang Y, Gao M, Fan Y, Zhang G, Shi G, Kang X. 2020. Rapid Detection of mecA and femA Genes by Loop-Mediated Isothermal Amplification in a Microfluidic System for Discrimination of Different Staphylococcal Species and Prediction of Methicillin Resistance. Front Microbiol 11: 1487. DOI: 10.3389/fmicb.2020.01487.
Miragaia M. 2018. Factors Contributing to the Evolution of mecA-Mediated ?-lactam Resistance in Staphylococci: Update and New Insights From Whole Genome Sequencing (WGS). Front Microbiol 9: 2723. DOI: 10.3389/fmicb.2018.02723
Morris DO, Lautenbach E, Zaoutis T, Leckerman K, Edelstein PH, Rankin SC. 2012. Potential for pet animals to harbour methicillin-resistant Staphylococcus aureus when residing with human MRSA patients. Zoonoses Public Health 59 (4): 286-293. DOI: 10.1111/j.1863-2378.2011.01448.x.
Munita JM, Arias CA. 2016. Mechanisms of Antibiotic Resistance. Microbiol Spectr 4 (2): VMBF-0016-2015. DOI: 10.1128/microbiolspec.
Mustapha M, Kolo YMB, Geidam YA, Gulani IAG. 2014. Review on Methicillin-resistant Staphylococcus aureus (MRSA) in Dogs and Cats. J Anim Vet Adv 6 (2): 61-73. DOI: 10.1111/j.1748-5827.2004.tb00180.x.
Oh JY, Chae JC, Han JI, Song WK, Lee CM, Park HM. 2020. Distribution and epidemiological relatedness of methicillin-resistant Staphylococcus aureus isolated from companion dogs, owners, and environments. J Vet Med Sci 82 (9): 1379-1386. DOI: 10.1292/jvms.19-0523.
Okwu MU, Olley M, Akpoka AO, Izevbuwa OE. 2019. Methicillin-resistant Staphylococcus aureus (MRSA) and anti-MRSA activities of extracts of some medicinal plants: A brief review. AIMS Microbiol 5 (2): 117-1137. DOI: 10.3934/microbiol.2019.2.117.
Overgaauw PAM, Vinke CM, Hagen MAEV, Lipman LJA. 2020. A One Health Perspective on the Human-Companion Animal Relationship with Emphasis on Zoonotic Aspects. Int J Environ Res Public Health 17 (11): 3789. DOI: 10.3390/ijerph17113789.
Pantosti A. 2012. Methicillin-resistant Staphylococcus aureus Associated with animal and its relevance to human. Front Microbiol 3: 127. DOI: 10.3389/fmicb.2012.00127.
Petinaki E, Spiliopoulou I. 2015. Methicillin-resistant Staphylococcus aureus colonization and infection risks from companion animals: current perspectives. Vet Med (Auckl) 6: 373-382. DOI: 10.2147/VMRR.S91313.
Pournajaf A, Ardebili A, Goudarzi L, Khodabandeh M, Narimani T, Abbaszadeh H. 2014. PCR-based identification of methicillin-resistant Staphylococcus aureus strains and their antibiotic resistance profiles. Asian Pac J Trop Biomed 4 (Suppl 1): S293-S297. DOI: 10.12980/APJTB.4.2014C423.
Rahmaniar RP, Yunita MN, Effendi MH, Yanestria SM. 2020. Encoding gene for methicillin-resistant Staphylococcus aureus (MRSA) isolated from nasal swab of dogs. Indian Vet J 97 (2): 37-40.
Ramandinianto SC, Khairullah AR, Effendi MH. 2020a. MecA gene and methicillin resistant Staphylococcus aureus (MRSA) isolated from dairy farms in East Java, Indonesia. Biodiversitas 21 (8): 3562-3568. DOI: 10.13057/biodiv/d210819.
Ramandinianto SC, Khairullah AR, Effendi MH, Hestiana EP. 2020b. Profile of Multidrug Resistance (MDR) and Methicillin Resistant Staphylococcus aureus (MRSA) on Dairy Farms in East Java Province, Indonesia. Indian J Forensic Med Toxicol 14 (4): 3439-3445. DOI: 10.37506/ijfmt.v14i4.12157.
Ruiz-Ripa L, Simón C, Ceballos S, Ortega C, Zarazaga M, Torres C, Gómez-Sanz E. 2021. S. pseudintermedius and S. aureus lineages with transmission ability circulate as causative agents of infections in pets for years. BMC Vet Res 17: 42. DOI: 10.1186/s12917-020-02726-4.
Traverse M, Aceto H. 2015. Environmental cleaning and disinfection. Vet Clin North Am Small Anim Pract 45 (2): 299-330. DOI: 10.1016/j.cvsm.2014.11.011.
Yagüe DP, Mihaljevic J, Mbegbu M, Wood CV, Hepp C, Kyman S, Hornstra H, Trotter R, Cope E, Pearson T. 2021. Survival of Staphylococcus aureus on sampling swabs stored at different temperatures. J Appl Microbiol 131 (3): 1030-1038. DOI: 10.1111/jam.15023.
Vincze S, Stamm I, Kopp PA, Hermes J, Adlhoch C, Semmler T, Wieler LH, Lübke-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. DOI: 10.1371/journal.pone.0085656.
Walther B, Hermes J, Cuny C, Wieler LH, Vincze S, Abou Elnaga Y, Stamm I, Kopp PA, Kohn B, Witte W, Jansen A, Conraths FJ, Semmler T, Eckmanns T, Lu?bke-Becker A. 2012. Sharing more than friendship – nasal colonization with coagulase positive staphylococci (CPS) and co-habitation aspects of dogs and their owners. PloS One 7: e35197. DOI: 10.1371/journal.pone.0035197.

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