{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,31]],"date-time":"2026-07-31T04:58:45Z","timestamp":1785473925695,"version":"3.56.0"},"reference-count":51,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,11,5]],"date-time":"2021-11-05T00:00:00Z","timestamp":1636070400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000199","name":"United States Department of Agriculture","doi-asserted-by":"publisher","award":["6040-32000-009-00D"],"award-info":[{"award-number":["6040-32000-009-00D"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Staphylococcus aureus is an important healthcare-associated bacterium that causes a multitude of infections in humans such as superficial skin and soft tissue infections, necrotizing pneumonia, foodborne illnesses and postsurgical infections. Treatment of S. aureus infections has become more complicated due to the emergence of Methicillin-Resistant Staphylococcus aureus (MRSA), some of which are multidrug resistant. The present study aimed to characterize S. aureus isolates from a tertiary care hospital in the Rawalpindi district of Pakistan. Staphylococci were isolated from 300 clinical samples collected from January 2018 to January 2019 and S. aureus isolates were tested for antimicrobial susceptibility and analyzed using Pulsed-Field Gel Electrophoresis (PFGE), Multi-Locus Sequence Typing (MLST), staphylococcal cassette chromosome mec (SCCmec) and spa typing. Approximately 25.3% (76\/300) of the clinical samples were positive for S. aureus; of those, 88.2% (67\/76) were mecA+ (MRSA). In addition to the \u03b2-lactam antibiotics, high levels of resistance were also found to the fluoroquinolones (ciprofloxacin, gatifloxacin and levofloxacin (73.7% each)). Of the 23 different spa types identified, the majority of isolates belonged to spa type t632 and t657 (9\/66; 13.6% each spa type). ST772-t657 (Bengal Bay clone) was the most commonly identified clone in this study although other clones circulating around different regions of the world were also found indicating the diversity in MRSA isolates from this area of Pakistan. This study emphasizes the need to monitor MRSA in the clinical setting for improved infection control and treatment options.<\/jats:p>","DOI":"10.3390\/microorganisms9112301","type":"journal-article","created":{"date-parts":[[2021,11,7]],"date-time":"2021-11-07T20:41:14Z","timestamp":1636317674000},"page":"2301","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Genetic Diversity of Staphylococcus aureus Strains from a Tertiary Care Hospital in Rawalpindi, Pakistan"],"prefix":"10.3390","volume":"9","author":[{"given":"Muhammad Ali","family":"Syed","sequence":"first","affiliation":[{"name":"Department of Microbiology, The University of Haripur, Haripur 22620, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bushra","family":"Jamil","sequence":"additional","affiliation":[{"name":"BJ Micro Lab (SMC Pvt) Limited, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6687-3758","authenticated-orcid":false,"given":"Hazem","family":"Ramadan","sequence":"additional","affiliation":[{"name":"Hygiene and Zoonoses Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt"},{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, USDA-ARS, US National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Rukan","sequence":"additional","affiliation":[{"name":"Department of Microbiology, The University of Haripur, Haripur 22620, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4281-2659","authenticated-orcid":false,"given":"Shahzad","family":"Ali","sequence":"additional","affiliation":[{"name":"One Health Research Group, Discipline of Zoology, Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shahid Ahmad","family":"Abbasi","sequence":"additional","affiliation":[{"name":"BJ Micro Lab (SMC Pvt) Limited, Islamabad 44000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tiffanie A.","family":"Woodley","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, USDA-ARS, US National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8480-4556","authenticated-orcid":false,"given":"Charlene R.","family":"Jackson","sequence":"additional","affiliation":[{"name":"Bacterial Epidemiology and Antimicrobial Resistance Research Unit, USDA-ARS, US National Poultry Research Center, Athens, GA 30605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1111\/j.1365-2702.1995.tb00004.x","article-title":"Staphylococcus aureus: A review of the literature","volume":"4","author":"Gould","year":"1995","journal-title":"J. Clin. Nurs."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1016\/S1473-3099(05)70295-4","article-title":"The role of nasal carriage in Staphylococcus aureus infections","volume":"5","author":"Wertheim","year":"2005","journal-title":"Lancet Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"658","DOI":"10.1136\/bmj.2.5153.658","article-title":"Nasal staphylococci and sepsis in hospital patients","volume":"2","author":"Williams","year":"1959","journal-title":"Br. Med. J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1186\/s12941-016-0171-z","article-title":"Molecular characterization of Staphylococcus aureus isolates from various healthcare institutions in Nairobi, Kenya: A cross sectional study","volume":"15","author":"Omuse","year":"2016","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"384","DOI":"10.4103\/0255-0857.103756","article-title":"Emergence and dissemination of antibiotic resistance: A global problem","volume":"30","author":"Choudhury","year":"2012","journal-title":"Indian J. Med. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1111\/lam.12735","article-title":"Methicillin-resistant Staphylococcus aureus: A controversial food-borne pathogen","volume":"64","author":"Sergelidis","year":"2017","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_7","first-page":"269","article-title":"Vancomycin resistance in Staphylococcus aureus","volume":"90","author":"McGuinness","year":"2017","journal-title":"Yale J. Biol. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1204","DOI":"10.1086\/520287","article-title":"Genesis of methicillin-resistant Staphylococcus aureus (MRSA), how treatment of MRSA infections has selected for vancomycin-resistant Enterococcus faecium, and the importance of antibiotic management and infection control","volume":"26","author":"Schentag","year":"1998","journal-title":"Clin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1086\/502522","article-title":"The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: Mortality, length of stay, and hospital charges","volume":"26","author":"Cosgrove","year":"2005","journal-title":"Infect. Control. Hosp. Epidemiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1016\/S0140-6736(09)61999-1","article-title":"Community-associated meticillin-resistant Staphylococcus aureus","volume":"375","author":"DeLeo","year":"2010","journal-title":"Lancet"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"57","DOI":"10.3184\/003685002783238870","article-title":"Methicillin resistance in Staphylococcus aureus: Mechanisms and modulation","volume":"85","author":"Stapleton","year":"2002","journal-title":"Sci. Prog."},{"key":"ref_12","first-page":"47","article-title":"Nasal carriage of highly resistant methicillin resistant Staphylococcus aureus (MRSA) strains by hospital staff in Hazara region of Pakistan","volume":"71","author":"Rukan","year":"2021","journal-title":"J. Pak. Med. Assoc."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1016\/j.jiph.2020.05.017","article-title":"First report of mecC gene in clinical methicillin resistant S. aureus (MRSA) from tertiary care hospital Islamabad, Pakistan","volume":"13","author":"Khan","year":"2020","journal-title":"J. Infect. Public Health"},{"key":"ref_14","first-page":"728","article-title":"Current pattern of antibiotic resistance in Staphylococcus aureus clinical isolates and the emergence of vancomycin resistance","volume":"20","author":"Taj","year":"2010","journal-title":"J. Coll. Physicians Surg. Pak."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Monecke, S., Coombs, G., Shore, A.C., Coleman, D.C., Akpaka, P., Borg, M., Chow, H., Ip, M., Jatzwauk, L., and Jonas, D. (2011). A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0017936"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.jhin.2007.06.012","article-title":"Prevalence of meticillin resistance among Staphylococcus aureus isolates in Pakistan and its clinical outcome","volume":"67","author":"Bukhari","year":"2007","journal-title":"J. Hosp. Infect."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1007\/s10096-017-3161-y","article-title":"Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: Molecular characterisation by microarray technology","volume":"37","author":"Jamil","year":"2018","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.1007\/s10096-016-2695-8","article-title":"Molecular characterization of Staphylococcus aureus isolates causing skin and soft tissue infections in patients from Malakand, Pakistan","volume":"35","author":"Madzgalla","year":"2016","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1093\/jac\/dkg084","article-title":"Detection of methicillin resistance in coagulase-negative staphylococci and in staphylococci directly from simulated blood cultures using the EVIGENE MRSA Detection Kit","volume":"51","author":"Poulsen","year":"2003","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_20","unstructured":"CLSI (2020). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [30th ed.]. Volume CLSI Supplement M100."},{"key":"ref_21","unstructured":"CLSI (2007). Performance Standards for Antimicrobial Susceptibility Testing: Seventeenth Informational Supplement, Clinical and Laboratory Standards Institute. [28th ed.]. Volume CLSI Supplement M100-S17 No. 1."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"4089","DOI":"10.1128\/JCM.41.9.4089-4094.2003","article-title":"Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus","volume":"41","author":"Strommenger","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"5113","DOI":"10.1128\/JCM.41.11.5113-5120.2003","article-title":"Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: Establishing a national database","volume":"41","author":"McDougal","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2155","DOI":"10.1128\/AAC.46.7.2155-2161.2002","article-title":"Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus","volume":"46","author":"Oliveira","year":"2002","journal-title":"Antimicrob. Agents. Chemother."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1128\/JCM.01599-07","article-title":"spa Typing of Staphylococcus aureus as a frontline tool in epidemiological typing","volume":"46","author":"Strommenger","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"5442","DOI":"10.1128\/JCM.41.12.5442-5448.2003","article-title":"Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management","volume":"41","author":"Harmsen","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1008","DOI":"10.1128\/JCM.38.3.1008-1015.2000","article-title":"Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus","volume":"38","author":"Enright","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1186\/s40064-016-2277-3","article-title":"High frequency of methicillin-resistant Staphylococcus aureus in Peshawar Region of Pakistan","volume":"5","author":"Ullah","year":"2016","journal-title":"Springerplus"},{"key":"ref_29","first-page":"2417","article-title":"MRSA: Prevalence and susceptibility pattern in health care setups of Karachi","volume":"30","author":"Siddiqui","year":"2017","journal-title":"Pak. J. Pharm. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1186\/s13756-017-0199-7","article-title":"Investigation of antimicrobial use at a tertiary care hospital in Southern Punjab, Pakistan using WHO methodology","volume":"6","author":"Atif","year":"2017","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_31","first-page":"145","article-title":"Self-medication of antibiotics among the students of Hamdard University, Pakistan","volume":"2","author":"Hanif","year":"2016","journal-title":"J. Public Health Dev. Ctries"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/j.sapharm.2019.09.003","article-title":"Factors associated with inappropriate dispensing of antibiotics among non-pharmacist pharmacy workers","volume":"16","author":"Asghar","year":"2020","journal-title":"Res. Social Adm Pharm"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"176","DOI":"10.3402\/ljm.v2i4.4728","article-title":"Vancomycin sensitivity of Staphylococcus aureus isolates from hospital patients in Karachi, Pakistan","volume":"2","author":"Hakim","year":"2007","journal-title":"Libyan J. Med."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"84","DOI":"10.21743\/pjaec\/2017.06.08","article-title":"Frequency of the occurrence of Methicillin-resistant Staphylococcus aureus (MRSA) infections in Hyderabad, Pakistan","volume":"18","author":"Brohi","year":"2017","journal-title":"Pak. J. Anal. Environ. Chem."},{"key":"ref_35","first-page":"139","article-title":"Antimicrobial susceptibility pattern of Staphylococcus aureus on clinical isolates and efficacy of laboratory tests to diagnose MRSA: A multi-centre study","volume":"23","author":"Bukhari","year":"2011","journal-title":"J. Ayub Med. Coll. Abbottabad"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1007\/s42399-019-00131-z","article-title":"Utilization pattern of antibiotics and patient care indicators in the teaching hospitals, Islamabad, Pakistan","volume":"1","author":"Khan","year":"2019","journal-title":"SN Comp. Clin. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1928","DOI":"10.1186\/s40064-016-3615-1","article-title":"WHO\/INRUD prescribing indicators and prescribing trends of antibiotics in the Accident and Emergency Department of Bahawal Victoria Hospital, Pakistan","volume":"5","author":"Atif","year":"2016","journal-title":"Springerplus"},{"key":"ref_38","first-page":"120","article-title":"Inpatient antibiotics pharmacology and physiological use in Hayatabad medical complex, Pakistan","volume":"5","author":"Khan","year":"2013","journal-title":"Int. J. Physiol. Pathophysiol. Pharmacol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1089\/fpd.2017.2336","article-title":"Detection and molecular characterization of methicillin-resistant Staphylococcus aureus from table eggs in Haripur, Pakistan","volume":"15","author":"Syed","year":"2018","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_40","first-page":"568","article-title":"Epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) isolates from Pakistan","volume":"7","author":"Arfat","year":"2013","journal-title":"African J. Microbiol. Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1128\/JCM.06354-11","article-title":"Emergence of hospital- and community-associated panton-valentine leukocidin-positive methicillin-resistant Staphylococcus aureus genotype ST772-MRSA-V in Ireland and detailed investigation of an ST772-MRSA-V cluster in a neonatal intensive care unit","volume":"50","author":"Brennan","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1016\/j.meegid.2015.05.032","article-title":"Genotyping of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA) in a tertiary care centre in Mysore, South India: ST2371-SCCmec IV emerges as the major clone","volume":"34","author":"Rajan","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3727","DOI":"10.1128\/JB.00480-12","article-title":"Draft genome sequence of Staphylococcus aureus 118 (ST772), a major disease clone from India","volume":"194","author":"Prabhakara","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1128\/JCM.01867-09","article-title":"Molecular characterization of methicillin-resistant Staphylococcus aureus with emergence of epidemic clones of sequence type (ST) 22 and ST 772 in Mumbai, India","volume":"48","author":"Rodrigues","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1089\/mdr.2015.0250","article-title":"Predominance of three closely related methicillin-resistant Staphylococcus aureus clones carrying a unique ccrC-positive SCCmec type III and the emergence of spa t304 and t690 SCCmec type IV pvl(+) MRSA isolates in Kinta Valley, Malaysia","volume":"23","author":"Ho","year":"2017","journal-title":"Microb. Drug. Resist."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.jgar.2017.08.016","article-title":"Molecular epidemiology and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolates in Xiangyang, China","volume":"12","author":"Tang","year":"2018","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e01297-20","DOI":"10.1128\/mSphere.01297-20","article-title":"Genomic epidemiology of CC30 methicillin-resistant Staphylococcus aureus strains from Argentina reveals four major clades with distinctive genetic features","volume":"6","author":"Haim","year":"2021","journal-title":"mSphere"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1111\/1348-0421.12128","article-title":"Methicillin-resistant Staphylococcus aureus carriage among veterinary staff and dogs in private veterinary clinics in Hokkaido, Japan","volume":"58","author":"Ishihara","year":"2014","journal-title":"Microbiol. Immunol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/s10096-019-03695-9","article-title":"Genotyping of methicillin-resistant Staphylococcus aureus from sepsis patients in Pakistan and detection of antibodies against staphylococcal virulence factors","volume":"39","author":"Monecke","year":"2020","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1111\/j.1469-0691.2006.01573.x","article-title":"The molecular evolution of methicillin-resistant Staphylococcus aureus","volume":"13","author":"Deurenberg","year":"2007","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1099\/jmm.0.014910-0","article-title":"Epidemiological typing of meticillin-resistant Staphylococcus aureus isolates from Pakistan and India","volume":"59","author":"Shabir","year":"2010","journal-title":"J. Med. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/11\/2301\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:26:41Z","timestamp":1760167601000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/11\/2301"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,5]]},"references-count":51,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["microorganisms9112301"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9112301","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,5]]}}}