1887

Abstract

Purpose. The epidemiological shift in MRSA distribution from healthcare-related facilities to the general population is distressing and requires continuous monitoring to manage and control the rate of incidences.

Method. The retrospective relationship between genetic and phenotypic variability of methicillin-resistant Staphylococcus aureus (MRSA) isolates was determined in respect to the specimen source, patient location, sex and age. A total of 521 MRSA isolates were classified based on SCCmec, mec, agr, pvl and spa genetic markers using three different multiplex PCRs.

Results. Based on the genetic variability, the isolates were divided into 97 profiles, of which 59% belonged to only two profiles (P17 and P33). P17 was the predominate profile, harbouring SCCmecIVa, ccr2, mecB, agr1, spa413 and pvl markers. P17 was more prevalent among the younger population (average 33.9 years) from outpatient (77%) locations and wound (88%) sources. The second largest profile was P33, harbouring SCCmecII, ccr2+ccr3, mecA, agr2, spa413 and no PVL. P33 was more prevalent in the older population (average 70.7 years) and more common in females (62%) than males (38%). With respect to antibiotic resistance, P33 exhibited a high rate of resistance to penicillins, cephalosporins, fluoroquinolones and macrolides, and P17 had a lower resistance to fluoroquinolones.

Conclusion. This report contributes to the existing understanding of evolutionary epidemiology of antibiotic resistance in MRSA. The diversity of MRSA isolates and unique environmental preferences for each profile highlights the importance of epidemiological knowledge of MRSA distribution to determine the best treatment for patients in both community and hospital settings.

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2019-01-22
2019-10-18
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References

  1. Klein EY, Van Boeckel TP, Martinez EM et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA 2018;1–8
    [Google Scholar]
  2. Anonymous Intensive Care Antimicrobial Resistance Epidemiology (ICARE) surveillance report, data summary from January 1996 through December 1997: a report from the National Nosocomial Infections Surveillance (NNIS) system. Am J Infect Control 1999;27:279–284
    [Google Scholar]
  3. Daneman N, Bronskill SE, Gruneir A, Newman AM, Fischer HD et al. Variability in antibiotic use across nursing homes and the risk of antibiotic-related adverse outcomes for individual residents. JAMA Intern Med 2015;175:1331–1339 [CrossRef]
    [Google Scholar]
  4. Costelloe C, Metcalfe C, Lovering A, Mant D, Hay AD. Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. BMJ 2010;340:c2096 [CrossRef]
    [Google Scholar]
  5. Steinke D, Davey P. Association between antibiotic resistance and community prescribing: a critical review of bias and confounding in published studies. Clin Infect Dis 2001;33:S193–S205 [CrossRef]
    [Google Scholar]
  6. Panlilio AL, Culver DH, Gaynes RP, Banerjee S, Henderson TS et al. Methicillin-resistant Staphylococcus aureus in U.S. hospitals, 1975-1991. Infect Control Hosp Epidemiol 1992;13:582–586 [CrossRef]
    [Google Scholar]
  7. Ayliffe GAJ. The progressive intercontinental spread of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 1997;24:S74–S79 [CrossRef]
    [Google Scholar]
  8. Barnes BE, Sampson DA. A literature review on community-acquired methicillin-resistant Staphylococcus aureus in the United States: Clinical information for primary care nurse practitioners. J Am Acad Nurse Pract 2011;23:23–32 [CrossRef]
    [Google Scholar]
  9. Guilbeau JR, Fordham PN. Evidence-based management and treatment of outpatient community-associated MRSA. J Nurse Pract 2010;6:140–145 [CrossRef]
    [Google Scholar]
  10. Harris AL, Fantasia HC. Community-associated MRSA Infections in Women. J Nurse Pract 2010;6:435–441 [CrossRef]
    [Google Scholar]
  11. Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clin Infect Dis 2003;36:131–139 [CrossRef]
    [Google Scholar]
  12. Kluytmans-Vandenbergh MF, Kluytmans JA. Community-acquired methicillin-resistant Staphylococcus aureus: current perspectives. Clin Microbiol Infect 2006;12:9–15 [CrossRef]
    [Google Scholar]
  13. VandenBergh MFQ, Yzerman EPF, Van Belkum A, Boelens HAM, Sijmons M et al. Follow-up of Staphylococcus aureus nasal carriage after 8 years: redefining the persistent carrier state. J Clin Microbiol 1999;37:3133–3140
    [Google Scholar]
  14. Sanford MD, Widmer AF, Bale MJ, Jones RN, Wenzel RP. Efficient detection and long-term persistence of the carriage of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 1994;19:1123–1128 [CrossRef]
    [Google Scholar]
  15. Robinson DA, Enright MC. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2003;47:3926–3934 [CrossRef]
    [Google Scholar]
  16. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 2003;9:978–984 [CrossRef]
    [Google Scholar]
  17. Ito T, Hiramatsu K, Oliveira DC et al. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 2009;53:4961–4967
    [Google Scholar]
  18. Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton–Valentine leukocidin. Lab Invest 2007;87:3–9 [CrossRef]
    [Google Scholar]
  19. Rasigade JP, Sicot N, Laurent F, Lina G, Vandenesch F et al. A history of Panton-Valentine leukocidin (PVL)-associated infection protects against death in PVL-associated pneumonia. Vaccine 2011;29:4185–4186 [CrossRef]
    [Google Scholar]
  20. Kaneko J, Kamio Y. Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: structures, pore-forming mechanism, and organization of the genes. Biosci Biotechnol Biochem 2004;68:981–1003 [CrossRef]
    [Google Scholar]
  21. Yamasaki O, Kaneko J, Morizane S, Akiyama H, Arata J et al. The association between Staphylococcus aureus strains carrying panton-valentine leukocidin genes and the development of deep-seated follicular infection. Clin Infect Dis 2005;40:381–385 [CrossRef]
    [Google Scholar]
  22. Boan P, Tan HL, Pearson J, Coombs G, Heath CH et al. Epidemiological, clinical, outcome and antibiotic susceptibility differences between PVL positive and PVL negative Staphylococcus aureus infections in Western Australia: A case control study. BMC Infect Dis 2015;15: [CrossRef]
    [Google Scholar]
  23. Sakoulas G, Eliopoulos GM, Moellering RC, Novick RP, Venkataraman L et al. Staphylococcus aureus accessory gene regulator (agr) group II: is there a relationship to the development of intermediate-level glycopeptide resistance?. J Infect Dis 2003;187:929–938 [CrossRef]
    [Google Scholar]
  24. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G et al. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 2001;183:7341–7353 [CrossRef]
    [Google Scholar]
  25. Cheung GY, Wang R, Khan BA, Sturdevant DE, Otto M. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect Immun 2011;79:1927–1935 [CrossRef]
    [Google Scholar]
  26. Shopsin B, Gomez M, Montgomery SO et al. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999;37:3556–3563
    [Google Scholar]
  27. Fang H, Hedin G, Li G, Nord CE. Genetic diversity of community-associated methicillin-resistant Staphylococcus aureus in southern Stockholm, 2000–2005. Clin Microbiol Infect 2008;14:370–376 [CrossRef]
    [Google Scholar]
  28. Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM et al. Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 2002;40:4289–4294 [CrossRef]
    [Google Scholar]
  29. Larsen AR, Stegger M, Sørum M. spa typing directly from a mecA, spa and pvl multiplex PCR assay—a cost-effective improvement for methicillin-resistant Staphylococcus aureus surveillance. Clin Microbiol Infect 2008;14:611–614 [CrossRef]
    [Google Scholar]
  30. Zhang K, Sparling J, Chow BL, Elsayed S, Hussain Z et al. New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 2004;42:4947–4955 [CrossRef]
    [Google Scholar]
  31. Hiramatsu K, Ito T, Tsubakishita S, Sasaki T, Takeuchi F et al. Genomic basis for methicillin resistance in Staphylococcus aureus. Infect Chemother 2013;45:117–136 [CrossRef]
    [Google Scholar]
  32. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K-ichi et al. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 2002;359:1819–1827 [CrossRef]
    [Google Scholar]
  33. Hassanzadeh P, Hassanzadeh Y, Mardaneh J, Rezai E, Motamedifar M. Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from HIV patients referring to HIV Referral Center, Shiraz, Iran, 2011–2012. Iran J Med Sci 2015;40:526–530
    [Google Scholar]
  34. Al-Badr A, Al-Shaikh G. Recurrent urinary tract infections management in women: a review. Sultan Qaboos Univ Med J 2013;13:359–367
    [Google Scholar]
  35. Franco AVM. Recurrent urinary tract infections. Best Pract Res Clin Obstet Gynaecol 2005;19:861–873 [CrossRef]
    [Google Scholar]
  36. Mao EF, Lane L, Lee J, Miller JH. Proliferation of mutators in a cell population. J Bacteriol 1997;179:417–422 [CrossRef]
    [Google Scholar]
  37. Soltani J, Poorabbas B, Miri N, Mardaneh J. Health care associated infections, antibiotic resistance and clinical outcome: A surveillance study from Sanandaj, Iran. World J Clin Cases 2016;4:63–70 [CrossRef]
    [Google Scholar]
  38. Poorabbas B, Mardaneh J, Rezaei Z, Kalani M, Pouladfar G et al. Nosocomial infections: multicenter surveillance of antimicrobial resistance profile of Staphylococcus aureus and Gram-negative rods isolated from blood and other sterile body fluids in Iran. Iran J Microbiol 2015;7:127–135
    [Google Scholar]
  39. Jimenez-Truque N, Tedeschi S, Saye EJ, McKenna BD, Langdon W et al. Relationship between maternal and neonatal Staphylococcus aureus colonization. Pediatrics 2012;129:e1252–e1259 [CrossRef]
    [Google Scholar]
  40. Deplano A, Zekhnini A, Allali N, Couturier M, Struelens MJ. Association of mutations in grlA and gyrA topoisomerase genes with resistance to ciprofloxacin in epidemic and sporadic isolates of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 1997;41:2023–2025 [CrossRef]
    [Google Scholar]
  41. Bennett PM. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 2008;153:S347–S357 [CrossRef]
    [Google Scholar]
  42. Balcazar JL. Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog 2014;10:e1004219–4 [CrossRef]
    [Google Scholar]
  43. Garcia A, Delorme T, Nasr P. Patient age as a factor of antibiotic resistance in methicillin-resistant Staphylococcus aureus. J Med Microbiol 2017
    [Google Scholar]
  44. Lysnyansky I, Mikula I, Gerchman I, Levisohn S. Rapid detection of a point mutation in the parC gene associated with decreased susceptibility to fluoroquinolones in Mycoplasma bovis. Antimicrob Agents Chemother 2009;53:4911–4914 [CrossRef]
    [Google Scholar]
  45. Andersson DI. The ways in which bacteria resist antibiotics. Int J Risk Saf Med 2005;17:111–116
    [Google Scholar]
  46. Zhao X, Xu C, Domagala J, Drlica K. DNA topoisomerase targets of the fluoroquinolones: a strategy for avoiding bacterial resistance. Proc Natl Acad Sci 1997;94:13991–13996 [CrossRef]
    [Google Scholar]
  47. Nakano M, Deguchi T, Kawamura T, Yasuda M, Kimura M et al. Mutations in the gyrA and parC genes in fluoroquinolone-resistant clinical isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother 1997;41:2289–2291 [CrossRef]
    [Google Scholar]
  48. Vila J, Ruiz J, Goñi P, Jimenez de Anta T. Quinolone-resistance mutations in the topoisomerase IV parC gene of Acinetobacter baumannii. J Antimicrob Chemother 1997;39:757–762 [CrossRef]
    [Google Scholar]
  49. Ng EY, Trucksis M, Hooper DC. Quinolone resistance mediated by norA: physiologic characterization and relationship to flqB, a quinolone resistance locus on the Staphylococcus aureus chromosome. Antimicrob Agents Chemother 1994;38:1345–1355
    [Google Scholar]
  50. Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry 2014;53:1565–1574 [CrossRef]
    [Google Scholar]
  51. Chen CR, Malik M, Snyder M, Drlica K. DNA gyrase and topoisomerase IV on the bacterial chromosome: Quinolone-induced DNA cleavage. J Mol Biol 1996;258:627–637 [CrossRef]
    [Google Scholar]
  52. Lafaurie M, Porcher R, Donay JL, Touratier S, Molina JM. Reduction of fluoroquinolone use is associated with a decrease in methicillin-resistant Staphylococcus aureus and fluoroquinolone-resistant Pseudomonas aeruginosa isolation rates: a 10 year study. J Antimicrob Chemother 2012;67:1010–1015 [CrossRef]
    [Google Scholar]
  53. Charbonneau P, Parienti JJ, Thibon P, Ramakers M, Daubin C et al. Fluoroquinolone use and methicillin-resistant Staphylococcus aureus isolation rates in hospitalized patients: a quasi experimental study. Clin Infect Dis 2006;42:778–784 [CrossRef]
    [Google Scholar]
  54. Clinical and Laboratory Standards Institute - NCCLS Performance Standards for Antimicrobial Susceptibility TestingVol. 27 2007
    [Google Scholar]
  55. Shopsin B, Mathema B, Alcabes P, Said-Salim B, Lina G et al. Prevalence of agr specificity groups among Staphylococcus aureus strains colonizing children and their guardians. J Clin Microbiol 2003;41:456–459 [CrossRef]
    [Google Scholar]
  56. Rohlf J. F. NTSYSpc, Numerical Taxonomy and Multivariate Analysis System Version 2.0 User Guide. 1998;www.exetersoftware.com/./ntsysguide.pdf
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