Genetic Diversity, Antibiotic Resistance, and Virulence Gene Features of Methicillin-Resistant Staphylococcus aureus Epidemics in Guiyang, Southwest China

References

• Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12:547–569. doi:10.1080/21505594.2021.1878688
   PubMed Web of Science ®Google Scholar
• Siddiqui AH, Koirala J. Methicillin Resistant Staphylococcus Aureus. Treasure Island (FL): StatPearls; 2022.
   Google Scholar
• Palavecino EL. Clinical, epidemiologic, and laboratory aspects of methicillin-resistant Staphylococcus aureus infections. Methods Mol Biol. 2020;2069:1–28.
   PubMedGoogle Scholar
• Jin Y, Zhou W, Yin Z, et al. The genetic feature and virulence determinant of highly virulent community-associated MRSA ST338-SCCmec Vb in China. Emerg Microbes Infect. 2021;10:1052–1064. doi:10.1080/22221751.2021.1914516
   PubMed Web of Science ®Google Scholar
• Mousavi SF, Mirzaei B, Shaghaghi B, et al. Phenotypic and genotypic features of first biofilm forming nasopharyngeal colonized Streptococcus pneumoniae isolates. Iran J Microbiol. 2017;9:200–207.
   Web of Science ®Google Scholar
• Lu L, Hu W, Tian Z, et al. Developing natural products as potential anti-biofilm agents. Chin Med. 2019;14:11. doi:10.1186/s13020-019-0232-2
   PubMed Web of Science ®Google Scholar
• Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev. 2020;2020:84.
   Google Scholar
• Wang C, Wei PW, Song CR, et al. Evaluation of the antimicrobial function of Ginkgo biloba exocarp extract against clinical bacteria and its effect on Staphylococcus haemolyticus by disrupting biofilms. J Ethnopharmacol. 2022;298:115602. doi:10.1016/j.jep.2022.115602
   Web of Science ®Google Scholar
• Wang B, Wei PW, Yao Y, et al. Functional and expression characteristics identification of Phormicins, novel AMPs from Musca domestica with anti-MRSA biofilm activity, in response to different stimuli. Int J Biol Macromol. 2022;209:299–314. doi:10.1016/j.ijbiomac.2022.03.204
   Web of Science ®Google Scholar
• Wang B, Song CR, Zhang QY, et al. The fusaric acid derivative qy17 inhibits Staphylococcus haemolyticus by disrupting biofilm formation and the stress response via altered gene expression. Front Microbiol. 2022;13:822148. doi:10.3389/fmicb.2022.822148
   PubMed Web of Science ®Google Scholar
• Peng-Wei W, Chao-Rong S, Xu W, et al. A potential milk preservative----Phormicin C-NS, sorbic acid-modified housefly antimicrobial peptide, inhibits Candida albicans hypha and biofilm formation. Lwt. 2022;168:113883. doi:10.1016/j.lwt.2022.113883
   Web of Science ®Google Scholar
• Wang B, Yao Y, Wei P, et al. Housefly Phormicin inhibits Staphylococcus aureus and MRSA by disrupting biofilm formation and altering gene expression in vitro and in vivo. Int J Biol Macromol. 2021;167:1424–1434. doi:10.1016/j.ijbiomac.2020.11.096
   Web of Science ®Google Scholar
• Wang B, Wei PW, Wan S, et al. Ginkgo biloba exocarp extracts inhibit S. aureus and MRSA by disrupting biofilms and affecting gene expression. J Ethnopharmacol. 2021;271:113895. doi:10.1016/j.jep.2021.113895
   PubMed Web of Science ®Google Scholar
• Naimi HM, Rasekh H, Noori AZ, et al. Determination of antimicrobial susceptibility patterns in Staphylococcus aureus strains recovered from patients at two main health facilities in Kabul, Afghanistan. BMC Infect Dis. 2017;17:737. doi:10.1186/s12879-017-2844-4
   Web of Science ®Google Scholar
• Shahmoradi M, Faridifar P, Shapouri R, et al. Determining the biofilm forming gene profile of Staphylococcus aureus clinical isolates via multiplex colony PCR method. Rep Biochem Mol Biol. 2019;7:181–188.
   PubMed Web of Science ®Google Scholar
• Mirzaei B, Moosavi SF, Babaei R, et al. Purification and evaluation of Polysaccharide Intercellular Adhesion (PIA) antigen from Staphylococcus epidermidis. Curr Microbiol. 2016;73:611–617. doi:10.1007/s00284-016-1098-5
   Web of Science ®Google Scholar
• Mirzaei B, Babaei R, Valinejad S. Staphylococcal vaccine antigens related to biofilm formation. Hum Vaccin Immunother. 2021;17:293–303. doi:10.1080/21645515.2020.1767449
   PubMed Web of Science ®Google Scholar
• Mirzaei B, Babaei R, Zeighami H, et al. Staphylococcus aureus putative vaccines based on the virulence factors: a mini-review. Front Microbiol. 2021;12:704247. doi:10.3389/fmicb.2021.704247
   Web of Science ®Google Scholar
• Mirzaei B, Mousavi SF, Babaei R, et al. Synthesis of conjugated PIA-rSesC and immunological evaluation against biofilm-forming Staphylococcus epidermidis. J Med Microbiol. 2019;68:791–802. doi:10.1099/jmm.0.000910
   PubMed Web of Science ®Google Scholar
• O’Hara FP, Suaya JA, Ray GT, et al. spa typing and multilocus sequence typing show comparable performance in a macroepidemiologic study of Staphylococcus aureus in the United States. Microb Drug Resist. 2016;22:88–96. doi:10.1089/mdr.2014.0238
   Web of Science ®Google Scholar
• Bai X, Wang H, Xin Y, et al. Prevalence and characteristics of Shiga toxin-producing Escherichia coli isolated from retail raw meats in China. Int J Food Microbiol. 2015;200:31–38. doi:10.1016/j.ijfoodmicro.2015.01.018
   Web of Science ®Google Scholar
• Chao G, Bao G, Cao Y, et al. Prevalence and diversity of enterotoxin genes with genetic background of Staphylococcus aureus isolates from different origins in China. Int J Food Microbiol. 2015;211:142–147. doi:10.1016/j.ijfoodmicro.2015.07.018
   PubMed Web of Science ®Google Scholar
• Chizimu JY, Solo ES, Bwalya P, et al. Genetic diversity and transmission of multidrug-resistant Mycobacterium tuberculosis strains in Lusaka, Zambia. Int J Infect Dis. 2022;114:142–150. doi:10.1016/j.ijid.2021.10.044
   Web of Science ®Google Scholar
• Bhowmik D, Das BJ, Pandey P, et al. An array of multiplex PCR assays for detection of Staphylococcal chromosomal cassette mec (SCCmec) types among staphylococcal isolates. J Microbiol Methods. 2019;166:105733. doi:10.1016/j.mimet.2019.105733
   PubMed Web of Science ®Google Scholar
• Urushibara N, Aung MS, Kawaguchiya M, et al. Novel staphylococcal cassette chromosome mec (SCCmec) type XIV (5A) and a truncated SCCmec element in SCC composite islands carrying speG in ST5 MRSA in Japan. J Antimicrob Chemother. 2020;75:46–50. doi:10.1093/jac/dkz406
   PubMed Web of Science ®Google Scholar
• Becker K, Sunderkotter C. Hautinfektionen durch MRSA Epidemiologie und Klinik [Skin infections with MRSA. Epidemiology and clinical features]. Hautarzt. 2012;63:371–380. German. doi:10.1007/s00105-011-2255-1
   Web of Science ®Google Scholar
• Hidron AI, Low CE, Honig EG, et al. Emergence of community-acquired meticillin-resistant Staphylococcus aureus strain USA300 as a cause of necrotising community-onset pneumonia. Lancet Infect Dis. 2009;9:384–392. doi:10.1016/S1473-3099(09)70133-1
   PubMed Web of Science ®Google Scholar
• Tam K, Torres VJ, Fischetti VA. Staphylococcus aureus secreted toxins and extracellular enzymes. Microbiol Spectr. 2019;7. doi:10.1128/microbiolspec.GPP3-0039-2018
   PubMed Web of Science ®Google Scholar
• Zhao H, Xu S, Yang H, et al. Molecular typing and variations in amount of tst gene expression of TSST-1-producing clinical Staphylococcus aureus isolates. Front Microbiol. 2019;10:1388. doi:10.3389/fmicb.2019.01388
   Web of Science ®Google Scholar
• Lakhundi S, Zhang K. Clinical, epidemiologic, and Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev. 2018;31. doi:10.1128/CMR.00020-18
   Web of Science ®Google Scholar
• Enright MC, Day NP, Davies CE, et al. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000;38:1008–1015. doi:10.1128/JCM.38.3.1008-1015.2000
   PubMed Web of Science ®Google Scholar
• Koreen L, Ramaswamy SV, Graviss EA, et al. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol. 2004;42:792–799. doi:10.1128/JCM.42.2.792-799.2004
   PubMed Web of Science ®Google Scholar
• Boye K, Bartels MD, Andersen IS, et al. A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I-V. Clin Microbiol Infect. 2007;13:725–727. doi:10.1111/j.1469-0691.2007.01720.x
   PubMed Web of Science ®Google Scholar
• Zhang K, McClure JA, Conly JM. Enhanced multiplex PCR assay for typing of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. Mol Cell Probes. 2012;26:218–221. doi:10.1016/j.mcp.2012.04.002
   Web of Science ®Google Scholar
• Yan XM, Wang J, Tao XX, et al. A conjugative MDR pMG1-like plasmid carrying the lsa(E) gene of enterococcus faecium with potential transmission to Staphylococcus aureus. Front Microbiol. 2021;12:667415. doi:10.3389/fmicb.2021.667415
   Web of Science ®Google Scholar
• Madera S, McNeil N, Serpa PH, et al. Prolonged silent carriage, genomic virulence potential and transmission between staff and patients characterize a neonatal intensive care unit (NICU) outbreak of methicillin-resistant Staphylococcus aureus (MRSA). Infect Control Hosp Epidemiol. 2022;1–7. doi:10.1017/ice.2022.48
   Web of Science ®Google Scholar
• Yoshimura J, Yamakawa K, Umemura Y, et al. Impact of beta-lactamase detection reagent on rapid diagnosis of ESBL-producing pathogens using urine samples of patients with Gram-negative bacteriuria. Int J Infect Dis. 2021;113:18–22. doi:10.1016/j.ijid.2021.09.059
   Web of Science ®Google Scholar
• Algammal AM, Enany ME, El-Tarabili RM, et al. Prevalence, antimicrobial resistance profiles, virulence and enterotoxins-determinant genes of MRSA isolated from subclinical bovine mastitis in Egypt. Pathogens. 2020;9:362. doi:10.3390/pathogens9050362
   Web of Science ®Google Scholar
• Song JH, Hsueh PR, Chung DR, et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother. 2011;66:1061–1069. doi:10.1093/jac/dkr024
   PubMed Web of Science ®Google Scholar
• Challagundla L, Luo X, Tickler IA, et al. Range expansion and the origin of USA300 North American epidemic methicillin-resistant Staphylococcus aureus. mBio. 2018;9. doi:10.1128/mBio.02016-17
   Web of Science ®Google Scholar
• Hsu LY, Harris SR, Chlebowicz MA, et al. Evolutionary dynamics of methicillin-resistant Staphylococcus aureus within a healthcare system. Genome Biol. 2015;16:81. doi:10.1186/s13059-015-0643-z
   Web of Science ®Google Scholar
• Nimmo GR, Coombs GW. Community-associated methicillin-resistant Staphylococcus aureus (MRSA) in Australia. Int J Antimicrob Agents. 2008;31:401–410. doi:10.1016/j.ijantimicag.2007.08.011
   PubMed Web of Science ®Google Scholar
• Mun YS, Hwang YJ. Novel spa and multi-locus sequence types (MLST) of Staphylococcus Aureus samples isolated from clinical specimens in Korean. Antibiotics. 2019;8:202. doi:10.3390/antibiotics8040202
   Web of Science ®Google Scholar
• Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol. 2009;7:629–641. doi:10.1038/nrmicro2200
   PubMed Web of Science ®Google Scholar
• Zhu P, Jiang Y, Wang Y. Molecular typing and drug resistance of methicillin-resistant Staphylococcus aureus in Zhejiang province. 2014.
   Google Scholar
• Fu Y, Xiong M, Li X, et al. Molecular characteristics, antimicrobial resistance and virulence gene profiles of Staphylococcus aureus isolates from Wuhan, Central China. Infect Drug Resist. 2020;13:2063–2072. doi:10.2147/IDR.S249988
   PubMed Web of Science ®Google Scholar
• Guo Y, Wang B, Rao L, et al. Molecular characteristics of rifampin-sensitive and -resistant isolates and characteristics of rpoB gene mutations in methicillin-resistant Staphylococcus aureus. Infect Drug Resist. 2021;14:4591–4600. doi:10.2147/IDR.S336200
   PubMed Web of Science ®Google Scholar
• Wang W, Liu F, Baloch Z, et al. Genotypic characterization of methicillin-resistant Staphylococcus aureus isolated from pigs and retail foods in China. Biomed Environ Sci. 2017;30:570–580. doi:10.3967/bes2017.076
   PubMed Web of Science ®Google Scholar
• Pulingam T, Parumasivam T, Gazzali AM, et al. Antimicrobial resistance: prevalence, economic burden, mechanisms of resistance and strategies to overcome. Eur J Pharm Sci. 2022;170:106103. doi:10.1016/j.ejps.2021.106103
   PubMed Web of Science ®Google Scholar
• Sinsinwar S, Jayaraman A, Mahapatra SK, et al. Anti-virulence properties of catechin-in-cyclodextrin-in-phospholipid liposome through down-regulation of gene expression in MRSA strains. Microb Pathog. 2022;167:105585. doi:10.1016/j.micpath.2022.105585
   Web of Science ®Google Scholar
• Jing S, Ren X, Wang L, et al. Nepetin reduces virulence factors expression by targeting ClpP against MRSA-induced pneumonia infection. Virulence. 2022;13:578–588. doi:10.1080/21505594.2022.2051313
   PubMed Web of Science ®Google Scholar
• Lavecchia A, Chiara M, De Virgilio C, et al. Staphylococcus arlettae genomics: novel insights on candidate antibiotic resistance and virulence genes in an emerging opportunistic pathogen. Microorganisms. 2019;7:580. doi:10.3390/microorganisms7110580
   Web of Science ®Google Scholar
• Wu S, Huang J, Zhang F, et al. Prevalence and characterization of food-related methicillin-resistant Staphylococcus aureus (MRSA) in China. Front Microbiol. 2019;10:304. doi:10.3389/fmicb.2019.00304
   Web of Science ®Google Scholar
• Boswihi SS, Udo EE, Monecke S, et al. Emerging variants of methicillin-resistant Staphylococcus aureus genotypes in Kuwait hospitals. PLoS One. 2018;13:e0195933. doi:10.1371/journal.pone.0195933
   PubMed Web of Science ®Google Scholar
• Yuan W, Liu J, Zhan Y, et al. Molecular typing revealed the emergence of pvl-positive sequence type 22 methicillin-susceptible Staphylococcus aureus in Urumqi, Northwestern China. Infect Drug Resist. 2019;12:1719–1728. doi:10.2147/IDR.S202906
   PubMed Web of Science ®Google Scholar
• Bae JS, Da F, Liu R, et al. Contribution of staphylococcal enterotoxin B to Staphylococcus aureus systemic infection. J Infect Dis. 2021;223:1766–1775. doi:10.1093/infdis/jiaa584
   Web of Science ®Google Scholar
• Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43(10):5026–33. doi: 10.1128/JCM.43.10.5026-5033.2005
   PubMed Web of Science ®Google Scholar
• Zhang K, McClure JA, Conly JM. Corrigendum to “Enhanced multiplex PCR assay for the typing of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus”. Mol Cell Probes. 2019;45:68. doi: 10.1016/j.mcp.2019.03.004
   Web of Science ®Google Scholar
• Alli OA, Ogbolu DO, Shittu AO, Okorie AN, Akinola JO, Daniel JB. Association of virulence genes with mecA gene in Staphylococcus aureus isolates from Tertiary Hospitals in Nigeria. Indian J Pathol Microbiol. 2015;58(4):464–71. doi: 10.4103/0377-4929.168875
   Web of Science ®Google Scholar
• Li X, Fang F, Zhao J, Lou N, Li C, Huang T, Li Y. Molecular characteristics and virulence gene profiles of Staphylococcus aureus causing bloodstream infection. Braz J Infect Dis. 2018;22(6):487–494. doi: 10.1016/j.bjid.2018.12.001
   PubMed Web of Science ®Google Scholar
• Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for simultaneous identification of community-associated methicillin-resistant Staphylococcus aureus strains USA300 and USA400 and detection of mecA and Panton-Valentine leukocidin genes, with discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol. 2008;46(3):1118–22. doi: 10.1128/JCM.01309-07
   PubMed Web of Science ®Google Scholar
• Zimmerli W, Widmer AF, Blatter M, Frei R, Ochsner PE. Role of rifampin for treatment of orthopedic implant-related staphylococcal infections: a randomized controlled trial. Foreign-Body Infection (FBI) Study Group. JAMA. 1998;279(19):1537–41. doi: 10.1001/jama.279.19.1537
   Google Scholar
• Haddad O, Merghni A, Elargoubi A, Rhim H, Kadri Y, Mastouri M. Comparative study of virulence factors among methicillin resistant Staphylococcus aureus clinical isolates. BMC Infect Dis. 2018;18(1):560. doi: 10.1186/s12879-018-3457-2
   Web of Science ®Google Scholar