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Recent Advances in Anti-Infective Drug Discovery


ISSN (Print): 2772-4344
ISSN (Online): 2772-4352

Research Article

The Staphylococcal Cassette Chromosome mec (SCCmec) Analysis and Biofilm Formation of Methicillin-resistant Staphylococcus cohnii Isolated from Clinical Samples in Tehran, Iran

Author(s): Somayeh Delfani, Faranak Rezaei, Setareh Soroush* and Pegah Shakib*

Volume 16, Issue 1, 2021

Published on: 10 February, 2021

Page: [63 - 73] Pages: 11

DOI: 10.2174/1574891X16666210210101912

Price: $65


Background: Methicillin-resistant coagulase-negative staphylococci is responsible for hospital and community-acquired infections.

Objective: This study aimed to investigate the antibiotic-resistance patterns, antibiotic-resistance genes, namely, ermA, ermB, ermC, blaZ, msrA, tetK, tetM, mup, and vanA, biofilm formation, and prevalence of different SCCmec types among the Staphylococcus cohnii strains isolated from clinical samples in Tehran, Iran.

Methods: In this study, S. cohnii isolates were screened from the clinical samples from March 2012 to February 2013 in Tehran, Iran. Antimicrobial susceptibility test and inducible clindamycin resistance were evaluated by disc diffusion method, and resistance genes were examined using Polymerase Chain Reaction (PCR) assays. Then, biofilm formation assay was analyzed by Microtiter-plate test to detect the icaA and icaD genes. The SCCmec and the Arginine Catabolite Mobile Element (ACME) typing were performed using the PCR method.

Results: From twenty S. cohnii, all isolates were resistant to cefoxitin. 95% of the S. cohnii was defined as Multidrug Resistance (MDR) strains. The ermB, ermC, and vanA genes were not detected in any isolates; however, the blaZ gene had the highest frequency. 95% of the S. cohnii isolates produced biofilm. Also, 4 SCCmec types, including V, IV, III+ (C2), VIII+ (AB1), were identified. Therefore, the majority of SCCmec were untypable. Based on the ACME typing, arcA and opp3 genes were positive in 13 (65%) and 1 (5%) isolates, respectively.

Conclusion: Due to the high antimicrobial resistance and the spread of untypable SCCmec among the isolates studied, the control and treatment of methicillin-resistant S. cohnii in hospitals and public health centers is a significant concern.

Keywords: Staphylococcal cassette chromosome mec (SCCmec), drug resistance, biofilms, Staphylococcus cohnii, clinical samples, ACME.

Vanderhaeghen W, Piepers S, Leroy F, Van Coillie E, Haesebrouck F, De Vliegher S. Invited review: effect, persistence, and virulence of coagulase-negative Staphylococcus species associated with ruminant udder health. J Dairy Sci 2014; 97(9): 5275-93.
[] [PMID: 24952781]
Goldstein MH, Kowalski RP, Gordon YJ. Emerging fluoroquinolone resistance in bacterial keratitis: a 5-year review. Ophthalmology 1999; 106(7): 1313-8.
[] [PMID: 10406613]
Huebner J, Goldmann DA. Coagulase-negative staphylococci: role as pathogens. Annu Rev Med 1999; 50(1): 223-36.
[] [PMID: 10073274]
von Eiff C, Peters G, Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2002; 2(11): 677-85.
[] [PMID: 12409048]
Ruppé E, Barbier F, Mesli Y, et al. Diversity of staphylococcal cassette chromosome mec structures in methicillin-resistant Staphylococcus epidermidis and Staphylococcus haemolyticus strains among outpatients from four countries. Antimicrob Agents Chemother 2009; 53(2): 442-9.
[] [PMID: 19001111]
Pereira EM, Schuenck RP, Malvar KL, et al. Staphylococcus aureus, Staphylococcus epidermidis and Staphylococcus haemolyticus: methicillin-resistant isolates are detected directly in blood cultures by multiplex PCR. Microbiol Res 2010; 165(3): 243-9.
[] [PMID: 19616418]
Szewczyk EM, Nowak T, Cieślikowski T, Różalska M. Potential role of Staphylococcus cohnii in a hospital environment. Microb Ecol Health Dis 2003; 15(1): 51-6.
Szewczyk EM, Rózalska M, Cieślikowski T, Nowak T. Plasmids of Staphylococcus cohnii isolated from the intensive-care unit. Folia Microbiol (Praha) 2004; 49(2): 123-31.
[] [PMID: 15227782]
Chen H, Wu W, Ni M, et al. Linezolid-resistant clinical isolates of enterococci and Staphylococcus cohnii from a multicentre study in China: molecular epidemiology and resistance mechanisms. Int J Antimicrob Agents 2013; 42(4): 317-21.
[] [PMID: 23880167]
Szewczyk EM, Rózalska M. Staphylococcus cohnii--resident of hospital environment: cell-surface features and resistance to antibiotics. Acta Microbiol Pol 2000; 49(2): 121-33.
[PMID: 11093675]
Klingenberg C, Aarag E, Rønnestad A, et al. Coagulase-negative staphylococcal sepsis in neonates. Association between antibiotic resistance, biofilm formation and the host inflammatory response. Pediatr Infect Dis J 2005; 24(9): 817-22.
[] [PMID: 16148849]
Zong Z, Peng C, Lü X. Diversity of SCCmec elements in methicillin-resistant coagulase-negative staphylococci clinical isolates. PLoS One 2011; 6(5)e20191
[] [PMID: 21637845]
Zong Z, Lü X. Characterization of a new SCCmec element in Staphylococcus cohnii. PLoS One 2010; 5(11)e14016
[] [PMID: 21103346]
Saber H, Jasni AS, Jamaluddin TZMT, Ibrahim R. A review of Staphylococcal cassette chromosome mec (SCCmec) types in coagulase-negative staphylococci (CoNS) species. Malays J Med Sci 2017; 24(5): 7-18.
[] [PMID: 29386968]
Otto M. Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: Staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence. BioEssays 2013; 35(1): 4-11.
[] [PMID: 23165978]
Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 1989; 42(8): 872-4.
[] [PMID: 2475530]
Zhang K, McClure J-A, 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.
[] [PMID: 16207957]
CLSI E. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement M100-S21. Wayne, Pennsylvania, 160s. 2011. Available from:
Koksal F, Yasar H, Samasti M. Antibiotic resistance patterns of coagulase-negative staphylococcus strains isolated from blood cultures of septicemic patients in Turkey. Microbiol Res 2009; 164(4): 404-10.
[] [PMID: 17475456]
Boamah VE, Agyare C, Odoi H, Adu F, Gbedema SY, Dalsgaard A. Prevalence and antibiotic resistance of coagulase-negative Staphylococci isolated from poultry farms in three regions of Ghana. Infect Drug Resist 2017; 10: 175-83.
[] [PMID: 28652785]
Heß S, Gallert C. Resistance behaviour of inducible clindamycin-resistant staphylococci from clinical samples and aquatic environments. J Med Microbiol 2014; 63(Pt 11): 1446-53.
[] [PMID: 25106860]
Aghazadeh M, Ghotaslou R, Ahangarzadeh Rezaee M, Moshafi MH, Hojabri Z, Saffari F. Determination of antimicrobial resistance profile and inducible clindamycin resistance of coagulase negative staphylococci in pediatric patients: the first report from Iran. World J Pediatr 2015; 11(3): 250-4.
[] [PMID: 25410671]
Olsen JE, Christensen H, Aarestrup FM. Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. J Antimicrob Chemother 2006; 57(3): 450-60.
[] [PMID: 16449305]
Lenhard JR, Brown T, Rybak MJ, Meaney CJ, Norgard NB, Bulman ZP, et al. Sequential evolution of vancomycin-intermediate resistance alters virulence in Staphylococcus aureus: PK/PD targets for vancomycin exposure. Antimicrob Agents Chemother 2015; 60(3): 1584-91.
Relhan N, Albini TA, Pathengay A, Kuriyan AE, Miller D, Flynn HW. Endophthalmitis caused by Gram-positive organisms with reduced vancomycin susceptibility: literature review and options for treatment. Br J Ophthalmol 2016; 100(4): 446-52.
[] [PMID: 26701686]
Pitts B, Hamilton MA, Zelver N, Stewart PS. A microtiter-plate screening method for biofilm disinfection and removal. J Microbiol Methods 2003; 54(2): 269-76.
[] [PMID: 12782382]
Zmantar T, Kouidhi B, Miladi H, Mahdouani K, Bakhrouf A. A microtiter plate assay for Staphylococcus aureus biofilm quantification at various pH levels and hydrogen peroxide supplementation. New Microbiol 2010; 33(2): 137-45.
[PMID: 20518275]
Jones RN, Ross JE, Castanheira M, Mendes RE. United States resistance surveillance results for linezolid (LEADER Program for 2007). Diagn Microbiol Infect Dis 2008; 62(4): 416-26.
[] [PMID: 19022153]
Ito T, Kuwahara-Arai K, Katayama Y, Uehara Y, Han X, Kondo Y, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis of MRSA In: Ji Y, Ed. Methicillin-Resistant Staphylococcus Aureus (MRSA) Protocols. In: Methods in Molecular Biology (Methods and Protocols) Totowa, NJ. Springer 2014; 1085: pp. 131-48.
Diep BA, Stone GG, Basuino L, et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 2008; 197(11): 1523-30.
[] [PMID: 18700257]
Gatermann SG, Koschinski T, Friedrich S. Distribution and expression of macrolide resistance genes in coagulase-negative staphylococci. Clin Microbiol Infect 2007; 13(8): 777-81.
[] [PMID: 17501977]
Schuster D, Josten M, Janssen K, et al. Detection of methicillin-resistant coagulase-negative staphylococci harboring the class A mec complex by MALDI-TOF mass spectrometry. Int J Med Microbiol 2018; 308(5): 522-6.
[] [PMID: 29764754]
Klibi A, Maaroufi A, Torres C, Jouini A. Detection and characterization of methicillin-resistant and susceptible coagulase-negative staphylococci in milk from cows with clinical mastitis in Tunisia. Int J Antimicrob Agents 2018; 52(6): 930-5.
[] [PMID: 30077662]
Cui J, Liang Z, Mo Z, Zhang J. The species distribution, antimicrobial resistance and risk factors for poor outcome of coagulase-negative staphylococci bacteraemia in China. Antimicrob Resist Infect Control 2019; 8(1): 65.
[] [PMID: 31044070]
Soroush S, Jabalameli F, Taherikalani M, Eslampour MA, Beigverdi R, Emaneini M. Characterization of biofilm formation, antimicrobial resistance, and staphylococcal cassette chromosome mec analysis of methicillin resistant Staphylococcus hominis from blood cultures of children. Rev Soc Bras Med Trop 2017; 50(3): 329-33.
[] [PMID: 28700050]
Lim KT, Hanifah YA, Yusof M, Thong KL. ermA, ermC, tetM and tetK are essential for erythromycin and tetracycline resistance among methicillin-resistant Staphylococcus aureus strains isolated from a tertiary hospital in Malaysia. Indian J Med Microbiol 2012; 30(2): 203-7.
[] [PMID: 22664438]
Teeraputon S, Santanirand P, Wongchai T, et al. Prevalence of methicillin resistance and macrolide-lincosamide-streptogramin B resistance in Staphylococcus haemolyticus among clinical strains at a tertiary-care hospital in Thailand. New Microbes New Infect 2017; 19: 28-33.
[] [PMID: 28702199]
Duran N, Ozer B, Duran GG, Onlen Y, Demir C. Antibiotic resistance genes & susceptibility patterns in staphylococci. Indian J Med Res 2012; 135(3): 389-96.
[PMID: 22561627]
Fessler AT, Billerbeck C, Kadlec K, Schwarz S. Identification and characterization of methicillin-resistant coagulase-negative staphylococci from bovine mastitis. J Antimicrob Chemother 2010; 65(8): 1576-82.
[] [PMID: 20525989]
Xu Z, Mkrtchyan HV, Cutler RR. Antibiotic resistance and mecA characterization of coagulase-negative staphylococci isolated from three hotels in London, UK. Front Microbiol 2015; 6: 947.
[] [PMID: 26441881]
Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev 2014; 27(4): 870-926.
[] [PMID: 25278577]
Garza-González E, López D, Pezina C, et al. Diversity of staphylococcal cassette chromosome mec structures in coagulase-negative staphylococci and relationship to drug resistance. J Med Microbiol 2010; 59(Pt 3): 323-9.
[] [PMID: 20007762]
Ghanbari F, Saberianpour S. Staphylococcal Cassette Chromosome mec (SCCmec) Typing of Methicillin-Resistant Staphylococcus aureus Strains Isolated from Community-and Hospital-Acquired Infections. Avicenna J Clin Microbiol Infect 2017; 4(2): 42244.

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