PDF herunterladen
CC BY-NC-ND 4.0 · J Lab Physicians 2023; 15(03): 450-461
DOI: 10.1055/s-0043-1764483
Original Article

Spectrum of Virulence Factors in Clinical Isolates of Staphylococcus aureus and Prevalence of SCCmec Types in Methicillin-Resistant Staphylococcus aureus in a Tertiary Care Center

Rhea Michelle J. Khodabux
1   Department of Microbiology, Sri Ramachandra Institute of Higher Education and Research (SRIHER), Porur, Chennai, Tamil Nadu, India
,
Shanthi Mariappan
1   Department of Microbiology, Sri Ramachandra Institute of Higher Education and Research (SRIHER), Porur, Chennai, Tamil Nadu, India
,
Uma Sekar
1   Department of Microbiology, Sri Ramachandra Institute of Higher Education and Research (SRIHER), Porur, Chennai, Tamil Nadu, India
› Institutsangaben Funding This study was supported by the Founder chancellor Shri N.P.V. Ramasamy Udayar fellowship, provided by Sri Ramachandra Institute of Higher Education and Research.
› Weitere Informationen
   Lizenzen und Reprints

Abstract

Background Methicillin-resistant Staphylococcus aureus (MRSA) is a widely recognized multidrug-resistant bacteria presenting a major therapeutic challenge to clinicians. Staphylococcus aureus possesses a number of pathogenicity factors that attribute to the severity of infections. This study was undertaken to investigate the common virulence genes in clinical isolates of Staphylococcus aureus, determine their antimicrobial susceptibility profile, and to characterize the staphylococcal cassette chromosome mec (SCCmec) types among MRSA in a tertiary care center.

Materials and Methods A total of 133 clinical isolates were included in this study. Susceptibility to various antibiotics was determined by disc diffusion method. Methicillin resistance was screened using cefoxitin disc; mecA and mecC genes were detected using polymerase chain reaction (PCR). PCR was done to detect 12 virulence factors such as hla, hlb, fnbA, fnbB, sea, seb, sec, icaA, clfA, tst, pvl, and eta. SCCmec typing was done by multiplex PCR.

Results Of the 133 clinical isolates, 54 (40.6%) were MRSA. The most common virulence gene detected was hlb (61.6%), hla (39%), and fnbA (37%). SCCmec type I was the most predominant. Mortality rate of 6.7% was observed among patients with staphylococcal infections. Univariate analysis of mortality associated virulence genes did not reveal any significant association between virulence genes and mortality.

Conclusion The distribution of virulence genes is similar in both MRSA and methicillin-sensitive Staphylococcus aureus. MRSA belongs to the SCCmec types I to IV. Possession of multiple virulence factors and multidrug resistance profile makes Staphylococcus aureus a formidable pathogen in clinical settings.

Keywords

methicillin-resistant Staphylococcus aureus - MRSA - Staphylococcus aureus - virulence genes - SCCmec typing


Publikationsverlauf

Eingereicht: 15. August 2022

Angenommen: 03. Januar 2023

Artikel online veröffentlicht:
27. März 2023

© 2023. The Indian Association of Laboratory Physicians. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Thieme Medical and Scientific Publishers Pvt. Ltd.
A-12, 2nd Floor, Sector 2, Noida-201301 UP, India

 

  • References

  • 1 Degaim ZD, Shani WS, Hamim SS. Virulence factors of Methicillin Resistant Staphylococcus aureus (MRSA) isolated from burn patients. Int J Curr Microbiol Appl Sci 2015; 4 (07) 898-906
    Google Scholar
  • 2 Liang Y, Tu C, Tan C. et al. Antimicrobial resistance, virulence genes profiling and molecular relatedness of methicillin-resistant Staphylococcus aureus strains isolated from hospitalized patients in Guangdong Province, China. Infect Drug Resist 2019; 12: 447-459
    CrossrefPubMedGoogle Scholar
  • 3 Souza SG, Campos GB, Oliveira PS. et al. Virulence factors in methicillin-resistant Staphylococcus aureus isolated from ICU units in Brazil. Adv Microbiol 2014; 4: 207-215
    CrossrefGoogle Scholar
  • 4 Uehara Y. Current status of staphylococcal cassette chromosome mec (SCCmec). Antibiotics (Basel) 2022; 11 (01) 86
    CrossrefPubMedGoogle Scholar
  • 5 Sharma H, Smith D, Turner CE. et al. Clinical and molecular epidemiology of staphylococcal toxic shock syndrome in the United Kingdom. Emerg Infect Dis 2018; 24 (02) 258-266
    CrossrefPubMedGoogle Scholar
  • 6 Bhowmik D, Chetri S, Das BJ, Dhar Chanda D, Bhattacharjee A. Distribution of virulence genes and SCCmec types among methicillin-resistant Staphylococcus aureus of clinical and environmental origin: a study from community of Assam, India. BMC Res Notes 2021; 14 (01) 58
    CrossrefPubMedGoogle Scholar
  • 7 Bien J, Sokolova O, Bozko P. Characterization of virulence factors of Staphylococcus aureus: novel function of known virulence factors that are implicated in activation of airway epithelial proinflammatory response. J Pathogens 2011; 2011: 601905
    CrossrefPubMedGoogle Scholar
  • 8 Wang X, Lin D, Huang Z. et al. Clonality, virulence genes, and antibiotic resistance of Staphylococcus aureus isolated from blood in Shandong, China. BMC Microbiol 2021; 21 (01) 281
    CrossrefPubMedGoogle Scholar
  • 9 Moraveji Z, Tabatabaei M, Shirzad Aski H, Khoshbakht R. Characterization of hemolysins of Staphylococcus strains isolated from human and bovine, southern Iran. Majallah-i Tahqiqat-i Dampizishki-i Iran 2014; 15 (04) 326-330
    Google Scholar
  • 10 Koosha RZ, Fooladi AA, Hosseini HM, Aghdam EM. Prevalence of exfoliative toxin A and B genes in Staphylococcus aureus isolated from clinical specimens. J Infect Public Health 2014; 7 (03) 177-185
    CrossrefPubMedGoogle Scholar
  • 11 McAdow M, Kim HK, Dedent AC, Hendrickx AP, Schneewind O, Missiakas DM. Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog 2011; 7 (10) e1002307
    CrossrefPubMedGoogle Scholar
  • 12 Wang W, Hu Y, Baker M. et al. Novel SCCmec type XV (7A) and two pseudo-SCCmec variants in foodborne MRSA in China. J Antimicrob Chemother 2022; 77 (04) 903-909
    CrossrefPubMedGoogle Scholar
  • 13 Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. 29th ed.. CLSI supplement. Wayne, PA: CLSI; 2019
    Google Scholar
  • 14 Abdel Halim RM, Kassem NN, Mahmoud BS. Detection of biofilm producing staphylococci among different clinical isolates and its relation to methicillin susceptibility. Open Access Maced J Med Sci 2018; 6 (08) 1335-1341
    CrossrefPubMedGoogle Scholar
  • 15 Murugesan S, Perumal N, Mahalingam SP, Dilliappan SK, Krishnan P. Analysis of antibiotic resistance genes and its associated SCCmec types among nasal carriage of methicillin resistant coagulase negative staphylococci from community settings, Chennai, Southern India. J Clin Diagn Res 2015; 9 (08) DC01-DC05
    PubMedGoogle Scholar
  • 16 Hirotaki S, Sasaki T, Kuwahara-Arai K, Hiramatsu K. Rapid and accurate identification of human-associated staphylococci by use of multiplex PCR. J Clin Microbiol 2011; 49 (10) 3627-3631
    CrossrefPubMedGoogle Scholar
  • 17 Bhatt P, Tandel K, Singh A, Kumar M, Grover N, Sahni AK. Prevalence and molecular characterization of methicillin resistance among Coagulase-negative Staphylococci at a tertiary care center. Med J Armed Forces India 2016; 72 (Suppl. 01) S54-S58
    CrossrefPubMedGoogle Scholar
  • 18 Stegger M, Andersen PS, Kearns A. et al. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect 2012; 18 (04) 395-400
    CrossrefPubMedGoogle Scholar
  • 19 Campbell SJ, Deshmukh HS, Nelson CL. et al. Genotypic characteristics of Staphylococcus aureus isolates from a multinational trial of complicated skin and skin structure infections. J Clin Microbiol 2008; 46 (02) 678-684
    CrossrefPubMedGoogle Scholar
  • 20 Li X, Fang F, Zhao J. et al. Molecular characteristics and virulence gene profiles of Staphylococcus aureus causing bloodstream infection. Braz J Infect Dis 2018; 22 (06) 487-494
    CrossrefPubMedGoogle Scholar
  • 21 Arciola CR, Campoccia D, Gamberini S, Baldassarri L, Montanaro L. Prevalence of cna, fnbA and fnbB adhesin genes among Staphylococcus aureus isolates from orthopedic infections associated to different types of implant. FEMS Microbiol Lett 2005; 246 (01) 81-86
    CrossrefPubMedGoogle Scholar
  • 22 Tabandeh M, Kaboosi H, Taghizadeh Armaki M, Pournajaf A, Peyravii Ghadikolaii F. New update on molecular diversity of clinical Staphylococcus aureus isolates in Iran: antimicrobial resistance, adhesion and virulence factors, biofilm formation and SCCmec typing. Mol Biol Rep 2022; 49 (04) 3099-3111
    CrossrefPubMedGoogle Scholar
  • 23 Singhal T, Rodrigues C, Soman R. et al. Treatment of MRSA infections in India: clinical insights from a Delphi analysis. Indian J Med Microbiol 2022; 40 (01) 35-45
    CrossrefPubMedGoogle Scholar
  • 24 Rajkumar S, Sistla S, Manoharan M. et al. Prevalence and genetic mechanisms of antimicrobial resistance in Staphylococcus species: a multicentre report of the Indian Council of Medical Research antimicrobial resistance surveillance network. Indian J Med Microbiol 2017; 35 (01) 53-60
    CrossrefPubMedGoogle Scholar
  • 25 Lohan K, Sangwan J, Mane P, Lathwal S. Prevalence pattern of MRSA from a rural medical college of North India: a cause of concern. J Family Med Prim Care 2021; 10 (02) 752-757
    CrossrefPubMedGoogle Scholar
  • 26 Rathinam KK, Immanuel JM. Prevalence of Methicillin-Resistant Staphylococcus Aureus (MRSA) in India: A Systematic Review and Meta-Analysis
  • 27 Lee AS, de Lencastre H, Garau J. et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers 2018; 4: 18033
    CrossrefPubMedGoogle Scholar
  • 28 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 (04) 464-471
    CrossrefPubMedGoogle Scholar
  • 29 Azmi K, Qrei W, Abdeen Z. Screening of genes encoding adhesion factors and biofilm production in methicillin resistant strains of Staphylococcus aureus isolated from Palestinian patients. BMC Genomics 2019; 20 (01) 578
    CrossrefPubMedGoogle Scholar
  • 30 Gowrishankar S, Kamaladevi A, Balamurugan K, Pandian SK. In vitro and in vivo biofilm characterization of methicillin-resistant Staphylococcus aureus from patients associated with pharyngitis infection. BioMed Res Int 2016; 2016: 1289157
    CrossrefPubMedGoogle Scholar
  • 31 Malik N, Bisht D, Aggarwal J, Rawat A. Phenotypic detection of biofilm formation in clinical isolates of Methicillin-resistant Staphylococcus aureus. Asian Journal of Pharmaceutical Research and Health Care 2022; 14 (01) 43-47
    CrossrefGoogle Scholar
  • 32 Yu F, Li T, Huang X. et al. Virulence gene profiling and molecular characterization of hospital-acquired Staphylococcus aureus isolates associated with bloodstream infection. Diagn Microbiol Infect Dis 2012; 74 (04) 363-368
    CrossrefPubMedGoogle Scholar
  • 33 Mirzaee M, Najar Peerayeh S, Ghasemian AM. Detection of icaABCD genes and biofilm formation in clinical isolates of methicillin resistant Staphylococcus aureus. Iran J Pathol 2014; 9 (04) 257-262
    Google Scholar
  • 34 Sabouni F, Mahmoudi S, Bahador A. et al. Virulence factors of Staphylococcus aureus isolates in an Iranian referral children's hospital. Osong Public Health Res Perspect 2014; 5 (02) 96-100
    CrossrefPubMedGoogle Scholar
  • 35 Hoseini Alfatemi SM, Motamedifar M, Hadi N, Sedigh Ebrahim Saraie H. Analysis of virulence genes among methicillin resistant Staphylococcus aureus (MRSA) strains. Jundishapur J Microbiol 2014; 7 (06) e10741
    CrossrefPubMedGoogle Scholar
  • 36 Budzyńska A, Skowron K, Kaczmarek A, Wietlicka-Piszcz M, Gospodarek-Komkowska E. Virulence factor genes and antimicrobial susceptibility of Staphylococcus aureus strains isolated from blood and chronic wounds. Toxins (Basel) 2021; 13 (07) 491
    CrossrefPubMedGoogle Scholar
  • 37 Rossato AM, Reiter KC, d'Azevedo PA. Coexistence of virulence genes in methicillin-resistant Staphylococcus aureus clinical isolates. Rev Soc Bras Med Trop 2018; 51 (03) 361-363
    CrossrefPubMedGoogle Scholar
  • 38 Abbasi M, BaseriSalehi M, Bahador N. et al. Antibiotic resistance patterns and virulence determinants of different SCCmec and pulsotypes of Staphylococcus aureus isolated from a major hospital in Ilam, Iran. Open Microbiol J 2017; 11: 211-223
    CrossrefPubMedGoogle Scholar
  • 39 Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, Von Eiff C. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 2003; 41 (04) 1434-1439
    CrossrefPubMedGoogle Scholar
  • 40 Pereira-Franchi EPL, Barreira MRN, da Costa NSLM. et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in the Brazilian primary health care system. Trop Med Int Health 2019; 24 (03) 339-347
    CrossrefPubMedGoogle Scholar
  • 41 Bratu S, Landman D, Gupta J, Trehan M, Panwar M, Quale J. A population-based study examining the emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 in New York City. Ann Clin Microbiol Antimicrob 2006; 5 (01) 29
    CrossrefPubMedGoogle Scholar
  • 42 Chen X, Wu Z, Zhou Y. et al. Molecular and virulence characteristics of methicillin-resistant Staphylococcus aureus in burn patients. Frontiers in Laboratory Medicine 2017; 1 (01) 43-47
    CrossrefGoogle Scholar
  • 43 Jiménez JN, Ocampo AM, Vanegas JM. et al. Characterisation of virulence genes in methicillin susceptible and resistant Staphylococcus aureus isolates from a paediatric population in a university hospital of Medellín, Colombia. Mem Inst Oswaldo Cruz 2011; 106 (08) 980-985
    CrossrefPubMedGoogle Scholar
  • 44 Horváth A, Dobay O, Sahin-Tóth J. et al. Characterisation of antibiotic resistance, virulence, clonality and mortality in MRSA and MSSA bloodstream infections at a tertiary-level hospital in Hungary: a 6-year retrospective study. Ann Clin Microbiol Antimicrob 2020; 19 (01) 17
    CrossrefPubMedGoogle Scholar
  • 45 Bhutia KO, Singh T, Adhikari L, Biswas S. Molecular characterization of community- & hospital-acquired methicillin-resistant & methicillin-sensitive Staphylococcus aureus isolates in Sikkim. Indian J Med Res 2015; 142 (03) 330-335
    CrossrefPubMedGoogle Scholar
  • 46 Archana GJ, Sinha AY, Annamanedi M. et al. Molecular characterisation of methicillin-resistant Staphylococcus aureus isolated from patients at a tertiary care hospital in Hyderabad, South India. Indian J Med Microbiol 2020; 38 (02) 183-191
    CrossrefPubMedGoogle Scholar
  • 47 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
    CrossrefPubMedGoogle Scholar
  • 48 Aggarwal S, Jena S, Panda S. et al. Antibiotic susceptibility, virulence pattern, and typing of Staphylococcus aureus strains isolated from variety of infections in India. Front Microbiol 2019; 10: 2763
    CrossrefPubMedGoogle Scholar
  • 49 Abimannan N, Sumathi G, Krishnarajasekhar OR, Sinha B, Krishnan P. Clonal clusters and virulence factors of methicillin-resistant Staphylococcus Aureus: evidence for community-acquired methicillin-resistant Staphylococcus Aureus infiltration into hospital settings in Chennai, South India. Indian J Med Microbiol 2019; 37 (03) 326-336
    CrossrefPubMedGoogle Scholar
  • 50 Lim K, Lee G, Park M. et al. Genetic relationship between SCCmec types and virulence factors of methicillin-resistant Staphylococcus aureus clinical isolates in Korea. J Exp Biomed Sci 2010; 16: 75-78
    Google Scholar
  • 51 Inagaki K, Lucar J, Blackshear C, Hobbs CV. Methicillin-susceptible and methicillin-resistant Staphylococcus aureus bacteremia: nationwide estimates of 30-day readmission, in-hospital mortality, length of stay, and cost in the United States. Clin Infect Dis 2019; 69 (12) 2112-2118
    PubMedGoogle Scholar
  • 52 Abdulgader SM, van Rijswijk A, Whitelaw A, Newton-Foot M. The association between pathogen factors and clinical outcomes in patients with Staphylococcus aureus bacteraemia in a tertiary hospital, Cape Town. Int J Infect Dis 2020; 91: 111-118
    CrossrefPubMedGoogle Scholar