{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T01:12:08Z","timestamp":1789089128821,"version":"build-2803163510"},"reference-count":46,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2024,1,12]],"date-time":"2024-01-12T00:00:00Z","timestamp":1705017600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004152","name":"Macao Polytechnic University","doi-asserted-by":"publisher","award":["RP\/ESS-05\/2017"],"award-info":[{"award-number":["RP\/ESS-05\/2017"]}],"id":[{"id":"10.13039\/501100004152","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Macau, recognized as a global tourism hub and the world\u2019s most densely populated region, provides a unique environment conducive to methicillin-resistant Staphylococcus aureus (MRSA) transmission in healthcare and community settings, posing a significant public health concern both locally and globally. The epidemiology and molecular characteristics of MRSA in the distinct city of Macau remain largely unelucidated. This five-year longitudinal study (2017\u20132022) examined the local prevalence and molecular typing of MRSA in Macau, with future MRSA type distribution predicted through ARIMA modeling. We subsequently analyzed the epidemiological characteristics of MRSA, including specimen source, clinical department, collection year, season, patient age, sex, and the annual number of tourists. Comprehensive antibiotic resistance profiles of the strains were also assessed. Of 504 clinically isolated S. aureus strains, 183 (36.3%) were identified as MRSA by the cefoxitin disk diffusion method and validated through multi-locus sequence typing (MLST). The MRSA detection rate showed an upward trend, increasing from 30.1% in 2017 to 45.7% in 2022. SCCmec type IV was predominant (28.9%), followed by types II (25.4%), III (22.1%), and V (22.1%). The primary sources of MRSA isolates were sputum (39.2%) and secretions (25.6%). Older age emerged as a risk factor for MRSA infection, whereas no significant associations were found with seasonal variations, gender, or the annual number of tourists. Despite displaying universal resistance to cefoxitin, oxacillin, and benzylpenicillin, MRSA isolates in Macau remained fully sensitive to vancomycin, tigecycline, quinupristin, nitrofurantoin, and linezolid. Continuous surveillance and analysis of MRSA distribution in Macau could provide invaluable insights for the effective management of MRSA prevention and control measures within healthcare settings.<\/jats:p>","DOI":"10.3390\/microorganisms12010148","type":"journal-article","created":{"date-parts":[[2024,1,12]],"date-time":"2024-01-12T03:54:34Z","timestamp":1705031674000},"page":"148","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["The Prevalence, Epidemiological, and Molecular Characterization of Methicillin-Resistant Staphylococcus aureus (MRSA) in Macau (2017\u20132022)"],"prefix":"10.3390","volume":"12","author":[{"given":"Abao","family":"Xing","sequence":"first","affiliation":[{"name":"Faculty of Applied Sciences, Macao Polytechnic University, Macau"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hoi Man","family":"Ng","sequence":"additional","affiliation":[{"name":"Clinical Laboratory, Kiang Wu Hospital, Macau"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huining","family":"Jiao","sequence":"additional","affiliation":[{"name":"Faculty of Health Sciences and Sports, Macao Polytechnic University, Macau"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7233-4347","authenticated-orcid":false,"given":"Kefeng","family":"Li","sequence":"additional","affiliation":[{"name":"Faculty of Applied Sciences, Macao Polytechnic University, Macau"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1086-2248","authenticated-orcid":false,"given":"Qianhong","family":"Ye","sequence":"additional","affiliation":[{"name":"Faculty of Health Sciences and Sports, Macao Polytechnic University, Macau"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,1,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1002\/jbm.a.36347","article-title":"Synthesis and characterization of biogenic selenium nanoparticles with antimicrobial properties made by Staphylococcus aureus, methicillin-resistant Staphylococcus aureus (MRSA), Escherichia coli, and Pseudomonas aeruginosa","volume":"106","author":"Mi","year":"2018","journal-title":"J. Biomed. Mater. Res. A"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1038\/s41579-018-0147-4","article-title":"Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research","volume":"17","author":"Turner","year":"2019","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1186\/s13054-017-1801-3","article-title":"Incidence, prevalence, and management of MRSA bacteremia across patient populations","volume":"21","author":"Hassoun","year":"2017","journal-title":"Crit. Care"},{"key":"ref_4","first-page":"1","article-title":"CHINET surveillance of bacterial resistance in China: 2018 report","volume":"20","author":"Hu","year":"2020","journal-title":"Chin. J. Infect. Chemother."},{"key":"ref_5","first-page":"827","article-title":"Inhibitory effects of silybin on the efflux pump of methicillin-resistant Staphylococcus aureus","volume":"18","author":"Wang","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e00020-18","DOI":"10.1128\/CMR.00020-18","article-title":"Methicillin-resistant Staphylococcus aureus: Molecular characterization, evolution, and epidemiology","volume":"31","author":"Lakhundi","year":"2018","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/S1473-3099(18)30605-4","article-title":"Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: A population-level modelling analysis","volume":"19","author":"Cassini","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Hasmukharay, K., Ngoi, S.T., Saedon, N.I., Tan, K.M., Khor, H.M., Chin, A.V., Tan, M.P., Kamarulzaman, A., Idris, N.B., and Niek, W.K. (2023). Evaluation of methicillin-resistant Staphylococcus aureus (MRSA) bacteremia: Epidemiology, clinical characteristics, and outcomes in the older patients in a tertiary teaching hospital in Malaysia. BMC Infect. Dis., 23.","DOI":"10.1186\/s12879-023-08206-y"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"159","DOI":"10.2306\/scienceasia1513-1874.2022.022","article-title":"Prevalence and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus clones: A study at Taksin Hospital, Bangkok, Thailand","volume":"48","author":"Tribuddharata","year":"2022","journal-title":"Sci. Asia"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/s44280-023-00009-9","article-title":"Current status and trends of antimicrobial resistance among clinical isolates in China: A retrospective study of CHINET from 2018 to 2022","volume":"1","author":"Yang","year":"2023","journal-title":"One Health Adv."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1001\/jama.2014.9743","article-title":"Clinical management of Staphylococcus aureus bacteremia: A review","volume":"312","author":"Holland","year":"2014","journal-title":"JAMA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1800680","DOI":"10.2807\/1560-7917.ES.2019.24.42.1800680","article-title":"International travel as source of a hospital outbreak with an unusual meticillin-resistant Staphylococcus aureus clonal complex 398, Denmark, 2016","volume":"24","author":"Moller","year":"2019","journal-title":"Euro Surveill."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"taz036","DOI":"10.1093\/jtm\/taz036","article-title":"Global geographic trends in antimicrobial resistance: The role of international travel","volume":"26","author":"Frost","year":"2019","journal-title":"J. Travel Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3271","DOI":"10.2147\/IDR.S412308","article-title":"Progress in the prevalence, classification and drug resistance mechanisms of methicillin-resistant Staphylococcus aureus","volume":"16","author":"Hou","year":"2023","journal-title":"Infect. Drug Resist."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s13756-023-01210-6","article-title":"The global prevalence of methicillin-resistant Staphylococcus aureus colonization in residents of elderly care centers: A systematic review and meta-analysis","volume":"12","author":"Hasanpour","year":"2023","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1177\/1010539517717365","article-title":"Disease burden, characteristics, and outcomes of methicillin-resistant Staphylococcus aureus bloodstream infection in Hong Kong","volume":"29","author":"You","year":"2017","journal-title":"Asia Pac. J. Public Health"},{"key":"ref_17","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_18","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1128\/AAC.43.6.1449","article-title":"Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315","volume":"43","author":"Ito","year":"1999","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1099\/jmm.0.001013","article-title":"Structures of SCC mec elements in methicillin-resistant Staphylococcus lugdunensis are closely related to those harboured by community-associated methicillin-resistant Staphylococcus aureus","volume":"68","author":"Liu","year":"2019","journal-title":"J. Med. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Uehara, Y. (2022). Current status of Staphylococcal cassette chromosome mec (SCCmec). Antibiotics, 11.","DOI":"10.3390\/antibiotics11010086"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1128\/JCM.01890-09","article-title":"Emergence of SCCmec type IV and SCCmec type V methicillin-resistant Staphylococcus aureus containing the Panton-Valentine leukocidin genes in a large academic teaching hospital in central Switzerland: External invaders or persisting circulators?","volume":"48","author":"Valsesia","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e20200431","DOI":"10.1590\/0037-8682-0431-2020","article-title":"Resistance profile to antimicrobials agents in methicillin-resistant Staphylococcus aureus isolated from hospitals in South Brazil between 2014\u20132019","volume":"53","author":"Rossato","year":"2020","journal-title":"Rev. Soc. Bras. Med. Trop."},{"key":"ref_23","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 SCC mec type III and the emergence of spa t304 and t690 SCC mec type IV pvl+ MRSA Isolates in Kinta Valley, Malaysia","volume":"23","author":"Ho","year":"2017","journal-title":"Microb. Drug Resist."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1007\/s10096-011-1243-9","article-title":"MRSA SCC mec epidemiology in Israel: Development and implementation of an MRSA SCC mec typing strategy","volume":"30","author":"Alon","year":"2011","journal-title":"Eur. J. Clin. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.jiac.2016.11.001","article-title":"Clinical and pathogenic features of SCCmec type II and IV methicillin-resistant Staphylococcus aureus in Japan","volume":"23","author":"Murata","year":"2017","journal-title":"J. Infect. Chemother."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Liu, J., Huang, T., Soteyome, T., Miao, J., Yu, G., Chen, D., Ye, C., Yang, L., and Xu, Z. (2023). Antimicrobial Resistance, SCC mec, Virulence and Genotypes of MRSA in Southern China for 7 Years: Filling the Gap of Molecular Epidemiology. Antibiotics, 12.","DOI":"10.3390\/antibiotics12020368"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1111\/j.1469-0691.2007.01720.x","article-title":"A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I-V","volume":"13","author":"Boye","year":"2007","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_28","unstructured":"Clinical and Laboratory Standards Institute (2017). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.jgar.2022.02.017","article-title":"Is methicillin-susceptible Staphylococcus aureus (MSSA) CC398 a true animal-independent pathogen?","volume":"29","author":"Tegegne","year":"2022","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Pang, R., Wu, S., Zhang, F., Huang, J., Wu, H., Zhang, J., Li, Y., Ding, Y., Zhang, J., and Chen, M. (2020). The genomic context for the evolution and transmission of community-associated Staphylococcus aureus ST59 through the food chain. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.00422"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e02198-20","DOI":"10.1128\/JCM.02198-20","article-title":"Global epidemiology and evolutionary history of Staphylococcus aureus ST45","volume":"59","author":"Effelsberg","year":"2020","journal-title":"J. Clin. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e315","DOI":"10.3346\/jkms.2019.34.e315","article-title":"Molecular epidemiology of Staphylococcus aureus in skin and soft tissue infections and bone and joint infections in Korean children","volume":"34","author":"Park","year":"2019","journal-title":"J. Korean Med. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1111\/1469-0691.12452","article-title":"Population structure analyses of Staphylococcus aureus at Tygerberg Hospital, South Africa, reveals a diverse population, a high prevalence of Panton\u2013Valentine leukocidin genes, and unique local methicillin-resistant S. aureus clones","volume":"20","author":"Oosthuysen","year":"2014","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"7449","DOI":"10.2147\/IDR.S385061","article-title":"Genomic characterization of livestock-associated methicillin-resistant Staphylococcus aureus ST7 Isolates from a case of human bacteremia in China","volume":"15","author":"Xing","year":"2022","journal-title":"Infect. Drug Resist."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1128\/CMR.00134-14","article-title":"Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management","volume":"28","author":"Tong","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Garoy, E.Y., Gebreab, Y.B., Achila, O.O., Tekeste, D.G., Kesete, R., Ghirmay, R., Kiflay, R., and Tesfu, T. (2019). Methicillin-resistant Staphylococcus aureus (MRSA): Prevalence and antimicrobial sensitivity pattern among patients\u2014A multicenter study in Asmara, Eritrea. Can. J. Infect. Dis. Med. Microbiol., 2019.","DOI":"10.1155\/2019\/8321834"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Otarigho, B., and Falade, M.O. (2023). Computational screening of approved drugs for inhibition of the antibiotic resistance gene mecA in methicillin-resistant Staphylococcus aureus (MRSA) strains. BioTech, 12.","DOI":"10.3390\/biotech12020025"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"722","DOI":"10.12688\/f1000research.122225.1","article-title":"Detection of mecA gene and methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and risk factors from farms in Probolinggo, Indonesia","volume":"11","author":"Khairullah","year":"2022","journal-title":"F1000Research"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.ijid.2018.12.002","article-title":"Comparison of molecular epidemiology of bloodstream methicillin-resistant Staphylococcus aureus isolates between a new and an old hospital in central Taiwan","volume":"79","author":"Lee","year":"2019","journal-title":"Int. J. Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1080\/22221751.2022.2032373","article-title":"Methicillin-resistant Staphylococcus aureus in China: A multicentre longitudinal study and whole-genome sequencing","volume":"11","author":"Wang","year":"2022","journal-title":"Emerg. Microbes Infect."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"439","DOI":"10.3122\/jabfm.2021.02.200394","article-title":"Methicillin-resistant Staphylococcus aureus colonization and mortality risk among community adults aged 40\u201385","volume":"34","author":"Mainous","year":"2021","journal-title":"J. Am. Board Fam. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.2147\/IDR.S317670","article-title":"First report of oxacillin susceptible mec A-positive Staphylococcus aureus in a Children\u2019s hospital in kunming, China","volume":"14","author":"Ma","year":"2021","journal-title":"Infect. Drug Resist."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"4","DOI":"10.22270\/ujpr.v3i3.159","article-title":"Prevalence of methicillin resistant staphylococcus aureus (MRSA) and antimicrobial susceptibility patterns at a private hospital in Sana\u2019a, Yemen","volume":"3","author":"Alyahawi","year":"2018","journal-title":"Univers. J. Pharm. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"671428","DOI":"10.3389\/fpubh.2021.671428","article-title":"Seasonal patterns in incidence and antimicrobial resistance of common bacterial pathogens in nursing home patients and their rooms","volume":"9","author":"Cassone","year":"2021","journal-title":"Front. Public Health"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1582","DOI":"10.3201\/eid1510.080877","article-title":"Community-associated methicillin-resistant Staphylococcus aureus, Iowa, USA","volume":"15","author":"Herwaldt","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.nmni.2017.05.009","article-title":"Identification of tigecycline- and vancomycin-resistant Staphylococcus aureus strains among patients with urinary tract infection in Iran","volume":"19","author":"Yousefi","year":"2017","journal-title":"New Microbes New Infect."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/1\/148\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T13:45:05Z","timestamp":1760103905000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/1\/148"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,12]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,1]]}},"alternative-id":["microorganisms12010148"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms12010148","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1,12]]}}}