Article Search
닫기

Microbiology and Biotechnology Letters

보문(Article)

View PDF

Molecular and Cellular Microbiology (MCM)  |  Microbial Genetics, Physiology and Metabolism

Microbiol. Biotechnol. Lett. 2021; 49(3): 449-457

https://doi.org/10.48022/mbl.2103.03011

Received: March 24, 2021; Revised: July 17, 2021; Accepted: July 21, 2021

Detection of Inducible Clindamycin Resistance Genes (ermA, ermB, and ermC) in Staphylococcus aureus and Staphylococcus epidermidis

Mohammad Javad Mazloumi1, Reza Akbari1, and Saber Yousefi1,2*

1Department of Microbiology and Virology, Faculty of Medicine, 2Cellular and Molecular Research Center, Faculty of Medicine, Urmia University of Medical Sciences, Urmia 57157-99313, Iran

Correspondence to :
Saber Yousefi,     yousefi_s@umsu.ac.ir

The aim of the present study was to survey the frequency of inducible and constitutive phenotypes and inducible cross-resistant genes by regulating the methylation of 23S rRNA (ermA, ermB, and ermC) and macrolide efflux-related msrA gene in Staphylococcus aureus and S. epidermidis strains. A total of 172 bacterial isolates (identified based on standard tests), were examined in this study. Antibiotic susceptibility was determined by the disk diffusion method, and all isolates were evaluated with respect to inducible and constitutive phenotypes. The presence of ermA, ermB, ermC, and msrA genes was investigated by a PCR assay. The constitutive resistance phenotypes showed a higher distribution among the isolates. R phenotype was detected more among S. epidermidis isolates (46.25%). ermB, ermC, and msrA genes were detected more in methicillin-resistant S. aureus (MRSA) and methicillin-resistant S. epidermidis (MRSE) isolates that had R and HD phenotypes (>77% strains). The ermA gene had the lowest frequency among MRSA, MRSE, MSSA, and MSSE strains (<14% isolates). Distribution of inducible resistance genes in MRSA and MRSE strains, and possibly other species, leads to increased constitutive resistance to erythromycin, clindamycin, and other similar antibiotics. Therefore, it can be challenging to treat infections caused by these resistant strains.

Keywords: D-phenotypes, inducible resistance, constitutive resistance, Staphylococcus aureus, Staphylococcus epidermidis

Graphical Abstract


  1. Miller LS, Fowler Jr VG, Shukla SK, Rose WE, Proctor RA. 2020. Development of a vaccine against Staphylococcus aureus invasive infections: Evidence based on human immunity, genetics and bacterial evasion mechanisms. FEMS Microbiol. Rev. 44: 123-153.
    Pubmed KoreaMed
  2. Goudarzi M, Kobayashi N, Dadashi M, Pantůček R, Nasiri MJ, Fazeli M, et al. 2020. Prevalence, genetic diversity, and temporary shifts of inducible clindamycin resistance Staphylococcus aureus clones in Tehran, Iran: a molecular-epidemiological analysis from 2013 to 2018. Front. Microbiol. 11: 663.
    Pubmed KoreaMed
  3. Yao W, Xu G, Li D, Bai B, Wang H, Cheng H, et al. 2019. Staphylococcus aureus with an erm-mediated constitutive macrolide-lincosamidestreptogramin B resistance phenotype has reduced susceptibility to the new ketolide, solithromycin. BMC Infect. Dis. 19: 175.
    Pubmed KoreaMed
  4. Liu X, Deng S, Huang J, Huang Y, Zhang Y, Yan Q, et al. 2017. Dissemination of macrolides, fusidic acid and mupirocin resistance among Staphylococcus aureus clinical isolates. Oncotarget 8:58086-58097.
    Pubmed KoreaMed
  5. Sabaté Brescó M, Harris LG, Thompson K, Stanic B, Morgenstern M, O'Mahony L, et al. 2017. Pathogenic mechanisms and host interactions in Staphylococcus epidermidis device-related infection. Front. Microbiol. 8: 1401.
    Pubmed KoreaMed
  6. Juda M, Chudzik-Rzad B, Malm A. 2016. The prevalence of genotypes that determine resistance to macrolides, lincosamides, and streptogramins B compared with spiramycin susceptibility among erythromycin-resistant Staphylococcus epidermidis. Mem. Inst. Oswaldo Cruz. 111: 155-160.
    Pubmed KoreaMed
  7. Wayne P. 2017. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-Seventh Informational Supplement M100-S27. Wayne, PA: CLSI.
  8. Tille P. 2017. Bailey & Scott's diagnostic microbiology-E-Book, pp. 252-261. Ed. Elsevier Health Sciences.
  9. Mendem SK, Gangadhara TA, Shivannavar CT, Gaddad SM. 2016. Antibiotic resistance patterns of Staphylococcus aureus: A multi center study from India. Microb. Pathog. 98: 167-170.
    Pubmed
  10. Talebi G, Hashemia A, Goudarzi H, Shariati A, Bostanghadiri N, Sharahi JY, et al. 2019. Survey of ermA, ermB, ermC and mecA genes among Staphylococcus aureus isolates isolated from patients admitted to hospitals in Tehran, Iran by PCR and sequencing. Biomed. Res. 30: 259-263.
  11. Adhikari R, Shrestha S, Barakoti A, Amatya R. 2017. Inducible clindamycin and methicillin resistant Staphylococcus aureus in a tertiary care hospital, Kathmandu, Nepal. BMC Infect. Dis. 17: 483.
    Pubmed KoreaMed
  12. Khashei R, Malekzadegan Y, Ebrahim-Saraie HS, Razavi Z. 2018. Phenotypic and genotypic characterization of macrolide, lincosamide and streptogramin B resistance among clinical isolates of staphylococci in southwest of Iran. BMC Res. Notes 11: 711.
    Pubmed KoreaMed
  13. O'Connor C, Powell J, Finnegan C, O'gorman A, Barrett S, Hopkins K, et al. 2015. Incidence, management and outcomes of the first cfr-mediated linezolid-resistant Staphylococcus epidermidis outbreak in a tertiary referral centre in the Republic of Ireland. J. Hosp. Infect. 90: 316-321.
    Pubmed
  14. Yoo IY, Kang O-K, Shim HJ, Huh HJ, Lee NY. 2020. Linezolid resistance in methicillin-resistant Staphylococcus aureus in Korea:High rate of false resistance to linezolid by the VITEK 2 system. Ann. Lab. Med. 40: 57-62.
    Pubmed KoreaMed
  15. Ruiz-Ripa L, Feßler AT, Hanke D, Eichhorn I, Azcona-Gutiérrez JM, Alonso CA, et al. 2021. Mechanisms of linezolid resistance among clinical Staphylococcus spp. in Spain: Spread of methicillin-and linezolid-resistant S. epidermidis ST2. Microb. Drug Res. 27: 145-153.
    Pubmed
  16. Musumeci R, Calaresu E, Gerosa J, Oggioni D, Bramati S, Morelli P, et al. 2016. Resistance to linezolid in Staphylococcus spp. clinical isolates associated with ribosomal binding site modifications:novel mutation in domain V of 23S rRNA. New Microbiol. 39:269-273.
  17. Majhi S, Dash M, Mohapatra D, Mohapatra A, Chayani N. 2016. Detection of inducible and constitutive clindamycin resistance among Staphylococcus aureus isolates in a tertiary care hospital, Eastern India. Avicenna J. Med. 6: 75-80.
    Pubmed KoreaMed
  18. Ejikeugwu C, Nwezeagu F, Edeh C, Eze P. 2018. Detection of constitutive and inducible-clindamycin-resistance in clinical isolates of Staphylococcus aureus from a Federal Teaching Hospital in Abakaliki, Nigeria. J. Bacteriol. Infect. Dis. 2: 31-34.
  19. Jarajreh Da, Aqel A, Alzoubi H, Al-Zereini W. 2017. Prevalence of inducible clindamycin resistance in methicillin-resistant Staphylococcus aureus: the first study in Jordan. J. Infect. Dev. Ctries. 11:350-354.
    Pubmed
  20. da Paz Pereira JN, Rabelo MA, da Costa Lima JL, Neto AMB, de Souza Lopes AC, Maciel MAV. 2016. Phenotypic and molecular characterization of resistance to macrolides, lincosamides and type B streptogramin of clinical isolates of Staphylococcus spp. of a university hospital in Recife, Pernambuco, Brazil. Braz. J. Infect. Dis. 20: 276-281.
    Pubmed

Starts of Metrics

Share this article on :

  • mail

Most KeyWord ?

What is Most Keyword?

  • It is most registrated keyword in articles at this journal during for 2 years.