Antibiotic resistance and typing of the methicillin-resistant Staphylococcus aureus clones in Kuwait hospitals, 2016-2017

Affiliations


Abstract

Background: Methicillin-resistant Staphylococcus aureus (MRSA) belong to diverse genetic backgrounds that differ in antibiotic resistance. Knowledge of the local clonal composition of MRSA strains is important for patients' management and for designing effective control and eradication methods. The aim of this study was to compare the antibiotic resistance patterns and genotypic characteristics of MRSA isolates obtained in public hospitals in Kuwait in 2016 and 2017 for changes in their resistance patterns and clonal composition.

Methods: A total of 4726 MRSA isolates obtained in 2016-2017 from clinical specimens in Kuwait public hospitals were characterized using antibiogram, SCCmec typing, spa typing and DNA microarray.

Results: The isolates expressed resistance to fusidic acid (52.9%), kanamycin (41.6%), gentamicin (32.5%) and erythromycin (36.2%). The prevalence of high-level mupirocin resistance decreased from 3.7% in 2016 to 2.4% in 2017, while the proportion of resistance to other antibiotics remained relatively stable. A total of 382 spa types were detected with eight spa types, t688 (N = 547), t304 (N = 428), t860 (N = 394), t127 (N = 306), t044 (N = 230), t311 (N = 243), t223 (N = 184) and t002 (N = 181) constituting 53.1% of the MRSA isolates in 2016-2017. Of the 3004 MRSA isolates obtained in 2016 (N = 1327) and 2017 (N = 1677) selected for DNA microarray analysis, 26 clonal complexes (CCs) were identified. Most of the isolates belonged to CC1 (N = 248), CC5 (N = 833), CC6 (N = 241), CC8 (N = 292), CC22 (N = 421), CC30 (N = 177), CC80 (N = 177) and CC97 (N = 171). The prevalence of CC5 isolates has significantly (p ≤ 0.05) increased from 294 isolates in 2016 to 539 isolates in 2017. Although CC22 increased from 196 isolates in 2016 to 225 isolates in 2017, CC1 increased from 112 isolates in 2016 to 136 isolates in 2017, CC6 increased from 103 isolates in 2016 to 138 isolates in 2017, these changes were not significant (p ≥ 0.05).

Conclusion: These results revealed the diversity in the genetic backgrounds of MRSA isolates and the stable maintenance of the dominant MRSA clones in Kuwait hospitals in 2016 and 2017 suggesting an on-going transmission of these clones. Novel and creative infection prevention and control measures are required to curtail further transmission.

Keywords: Antibiotic resistance; Clonal complex; DNA microarray; Genotypes; MRSA.

Conflict of interest statement

The authors declare that they have no competing interests.


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KMEL References


References

  1.  
    1. Jevons MP. Celbenin-resistant staphylococci. Br Med J. 1961;1:124–125. doi: 10.1136/bmj.1.5219.124-a. - DOI
  2.  
    1. Lakhundi S, Zhang K. Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev. 2018;31(4):e00020–e00018. doi: 10.1128/CMR.00020-18. - DOI - PMC - PubMed
  3.  
    1. Gordon RJ, Lowy FD. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis. 2008;46(Suppl 5):S350–S359. doi: 10.1086/533591. - DOI - PMC - PubMed
  4.  
    1. Udo EE, Pearman JW, Grubb WB. Genetic analysis of community isolates of methicillin-resistant Staphylococcus aureus in Western Australia. J Hosp Infect. 1993;25:97–108. doi: 10.1016/0195-6701(93)90100-E. - DOI - PubMed
  5.  
    1. Boswihi SS, Udo EE, Al-Sweih N. Shifts in the clonal distribution of methicillin-resistant Staphylococcus aureus in Kuwait hospitals: 1992-2010. PLoS One. 2016;11(9):e0162744. doi: 10.1371/journal.pone.0162744. - DOI - PMC - PubMed
  6.  
    1. Hsu LY, Koh TH, Kurup A, Low J, Chlebicki MP, Tan BH. High incidence of Panton-valentine leukocidin-producing Staphylococcus aureus in a tertiary care public hospital in Singapore. Clin Infect Dis. 2005;40(3):486–489. doi: 10.1086/427033. - DOI - PubMed
  7.  
    1. Sonnevend A, Blair I, Alkaabi M, Jumaa P, Al Haj M, Ghazawi A, et al. Change in meticillin-resistant Staphylococcus aureus clones at a tertiary care hospital in the United Arab Emirates over a 5-year period. J Clin Pathol. 2012;65(2):178–182. doi: 10.1136/jclinpath-2011-200436. - DOI - PubMed
  8.  
    1. Aires de Sousa M, Correia B, de Lencastre H. Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol. 2008;46(9):2912–2917. doi: 10.1128/JCM.00692-08. - DOI - PMC - PubMed
  9.  
    1. Udo EE, Boswihi SS. Antibiotic resistance trends in methicillin-resistant Staphylococcus aureus isolated in Kuwait hospitals: 2011-2015. Med Princ Pract. 2017;26(5):485–490. doi: 10.1159/000481944. - DOI - PMC - PubMed
  10.  
    1. Boswihi SS, Udo EE, Monecke S, Mathew B, Noronha B, Verghese T, Tappa SB. Emerging variants of methicillin-resistant Staphylococcus aureus genotypes in Kuwait hospitals. PLoS One. 2018;13(4):e0195933. doi: 10.1371/journal.pone.0195933. - DOI - PMC - PubMed
  11.  
    1. Heffernan H, Bakker S, Dyet K, Williamson D. Annual survey of methicillin-resistant Staphylococcus aureus (MRSA), 2015. Porirua: Nosocomial Infections Laboratory, Institute of Environmental Science and Research Ltd.; 2016.
  12.  
    1. Seidl K, Leimer N, Palheiros Marques M, Furrer A, Holzmann-Burgel A, Senn G, et al. Clonality and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus at the University Hospital Zurich, Switzerland between 2012 and 2014. Ann Clin Microbiol Antimicrob. 2015;14:14. doi: 10.1186/s12941-015-0075-3. - DOI - PMC - PubMed
  13.  
    1. Asadollahi P, Farahani NN, Mirzaii M, Khoramrooz SS, van Belkum A, Asadollahi K, Dadashi M, Darban-Sarokhalil D. Distribution of the Most Prevalent Spa Types among Clinical Isolates of Methicillin-Resistant and -Susceptible Staphylococcus aureus around the World: A Review. Front Microbiol. 2018;12(9):163. doi: 10.3389/fmicb.2018.00163. - DOI - PMC - PubMed
  14.  
    1. Abou Shady HM, Bakr AE, Hashad ME, Alzohairy MA. Staphylococcus aureus nasal carriage among outpatients attending primary health care centers: a comparative study of two cities in Saudi Arabia and Egypt. Braz J Infect Dis. 2015;19:68–76. doi: 10.1016/j.bjid.2014.09.005. - DOI - PMC - PubMed
  15.  
    1. Arias CA, Reyes J, Carvajal LP, Rincon S, Diaz L, Panesso D, et al. A prospective cohort multicenter study of molecular epidemiology and Phylogenomics of Staphylococcus aureus bacteremia in nine Latin American countries. Antimicrob Agents Chemother. 2017;61(10):e00816–e00817. doi: 10.1128/AAC.00816-17. - DOI - PMC - PubMed
  16.  
    1. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol. 2009;7(9):629–641. doi: 10.1038/nrmicro2200. - DOI - PMC - PubMed
  17.  
    1. Ko KS, Lee JY, Suh JY, Oh WS, Peck KR, Lee NY, et al. Distribution of major genotypes among methicillin-resistant Staphylococcus aureus clones in Asian countries. J Clin Microbiol. 2005;43(1):421–426. doi: 10.1128/JCM.43.1.421-426.2005. - DOI - PMC - PubMed
  18.  
    1. Dai Y, Liu J, Guo W, Meng H, Huang Q, He L, et al. Decreasing methicillin-resistant Staphylococcus aureus (MRSA) infections is attributable to the disappearance of predominant MRSA ST239 clones, Shanghai, 2008-2017. Emerg Microbes Infect. 2019;8(1):471–478. doi: 10.1080/22221751.2019.1595161. - DOI - PMC - PubMed
  19.  
    1. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One. 2011;6(4):e17936. doi: 10.1371/journal.pone.0017936. - DOI - PMC - PubMed
  20.  
    1. Monecke S, Skakni L, Hasan R, Ruppelt A, Ghazal SS, Hakawi A, et al. Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia. BMC Microbiol. 2012;12:146. doi: 10.1186/1471-2180-12-146. - DOI - PMC - PubMed
  21.  
    1. Senok A, Ehricht R, Monecke S, Al-Saedan R, Somily A. Molecular characterization of methicillin-resistant Staphylococcus aureus in nosocomial infections in a tertiary-care facility: emergence of new clonal complexes in Saudi Arabia. New Microbes New Infect. 2016;14:13–18. doi: 10.1016/j.nmni.2016.07.009. - DOI - PMC - PubMed
  22.  
    1. Senok A, Somily AM, Nassar R, Garaween G, Kim Sing G, Muller E, et al. Emergence of novel methicillin-resistant Staphylococcus aureus strains in a tertiary care facility in Riyadh, Saudi Arabia. Infect Drug Resist. 2019;12:2739–2746. doi: 10.2147/IDR.S218870. - DOI - PMC - PubMed
  23.  
    1. Khokhlova OE, Hung WC, Wan TW, Iwao Y, Takano T, Higuchi W, et al. Healthcare- and community-associated methicillin-resistant Staphylococcus aureus (MRSA) and fatal pneumonia with pediatric deaths in Krasnoyarsk, Siberian Russia: unique MRSA's multiple virulence factors, genome, and stepwise evolution. PLoS One. 2015;10(6):e0128017. doi: 10.1371/journal.pone.0128017. - DOI - PMC - PubMed
  24.  
    1. Carrel M, Perencevich EN, David MZ. USA300 methicillin-resistant Staphylococcus aureus, United States, 2000-2013. Emerg Infect Dis. 2015;21(11):1973–1980. doi: 10.3201/eid2111.150452. - DOI - PMC - PubMed
  25.  
    1. Richardson JF, Reith S. Characterization of a strain of methicillin-resistant Staphylococcus aureus (EMRSA-15) by conventional and molecular methods. J Hosp Infect. 1993;25:45–52. doi: 10.1016/0195-6701(93)90007-M. - DOI - PubMed
  26.  
    1. Campanile F, Bongiorno D, Borbone S, Stefani S. Hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) in Italy. Ann Clin Microbiol Antimicrob. 2009;8:22. doi: 10.1186/1476-0711-8-22. - DOI - PMC - PubMed
  27.  
    1. Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, Warner M, et al. Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European antimicrobial resistance surveillance system (EARSS) J Antimicrob Chemother. 2001;48:143–144. doi: 10.1093/jac/48.1.143. - DOI - PubMed
  28.  
    1. Melter O, Urbaskova P, Jakubu V, Mackova B, Zemlickova H. Emergence of EMRSA-15 clone in hospitals throughout the Czech Republic. Euro Surveill. 2006;11(8):E060803.6. - PubMed
  29.  
    1. Udo EE, Boswihi SS, Al-Sweih N. High prevalence of toxic shock syndrome toxin–producing epidemic methicillin-resistant Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals. New Microbes New Infect. 2016;12:24–30. doi: 10.1016/j.nmni.2016.03.008. - DOI - PMC - PubMed
  30.  
    1. Biber A, Abuelaish I, Rahav G, Raz M, Cohen L, Valinsky L, et al. A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza strip. PLoS One. 2012;7(8):e42864. doi: 10.1371/journal.pone.0042864. - DOI - PMC - PubMed
  31.  
    1. Aqel AA, Alzoubi HM, Vickers A, Pichon B, Kearns AM. Molecular epidemiology of nasal isolates of methicillin-resistant Staphylococcus aureus from Jordan. J Infect Public Health. 2015;8(1):90–97. doi: 10.1016/j.jiph.2014.05.007. - DOI - PubMed
  32.  
    1. Clinical and Laboratory Standard Institute . Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement M100-S25. Wayne: CLSI; 2015.
  33.  
    1. British Society to Antimicrobial Chemotherapy (BSAC) (BSAC, 2013). http://bsac.org.uk/susceptibility. Accessed 30 Jan 2020.
  34.  
    1. 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):5026–5033. doi: 10.1128/JCM.43.10.5026-5033.2005. - DOI - PMC - PubMed
  35.  
    1. Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41(12):5442–5448. doi: 10.1128/JCM.41.12.5442-5448.2003. - DOI - PMC - PubMed
  36.  
    1. Monecke S, Jatzwauk L, Weber S, Slickers P, Ehricht R. DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from eastern Saxony. Clin Microbiol Infect. 2008;14:534–545. doi: 10.1111/j.1469-0691.2008.01986.x. - DOI - PubMed