Distribution of erm genes among Staphylococcus aureus isolates with inducible resistance to clindamycin in Isfahan, Iran


1 Department of Microbiology, Faculty of Bioscience, Falavarjan Branch, Islamic Azad University, Isfahan, Iran

2 Department of Microbiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

3 Department of Endodontics, School of Dentistry, Zahedan University of Medical Sciences, Zahedan, Iran

4 Cellular and Molecular Research Center, Shahrekord University of Medical Sciences, Shahrekord, Iran

5 Department of Medical Bacteriology and Virology, Ghaem Hospital, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

6 Department of Microbiology, School of Medicine, Ahvaz University of Medical Sciences, Ahvaz, Iran


Background: The rising frequency of methicillin resistant Staphylococcus aureus (MRSA) has led to an increased use of antibiotics such as macrolide, lincosamide, streptogramin B (MLSB) for the treatment of S. aureus infections. Resistance to MLSBin S. aureus is commonly encoded by erm genes, which can be constitutive MLSB (cMLSB) or inducible MLSB (iMLSB). The purpose of this study was to determine the frequency of cMLSB, iMLSB, and MS phenotypes using D-test and polymerase chain reaction (PCR) methods.
Materials and Methods: A total of 215 isolates of S. aureus were collected from January 2010 to May 2012 from Al-Zahra Hospital in Isfahan. PCR was performed for detection of mecA gene on all isolates using specific primers. The frequency of MLSB-resistant isolates was determined using D-test, and then a multiplex PCR was performed for detection of ermAermB, and ermC genes.

Results: Among 215 S. aureus isolates examined, 82 (40.9%) were MRSA, and iMLSB, cMLSB, and MS resistance phenotypes had a frequency of 9 (4.18%), 58 (26.9%), and 11 (5.1%), respectively. Among nine isolates with iMLSBresistance phenotype, four isolates contained ermC gene, two isolates ermB gene, and one isolate ermA gene. Two isolates did not have any erm gene.
Conclusion: In the current study, cMLSBwas the most frequent phenotype and ermC was the most common gene in iMLSBresistant phenotypes.


Vivek JS, Rajesh GN, Mukesh S, Manpreet K, Manpreet K, Misra RN, et al. Prevalence of inducible clindamycin resistance among community- and hospital-associated Staphylococcus aureus isolates in a tertiary care hospital in India. Biomed Res 2011;22:465-9.  Back to cited text no. 1
Saderi H, Emadi B, Owlia P. Phenotypic and genotypic study of macrolide, lincosamide and streptogramin B (MLSB) resistance in clinical isolates of Staphylococcus aureus in Tehran, Iran. Med Sci Monit 2011;17:BR48-53.  Back to cited text no. 2
Reddy SP, Suresh R. Phenotypic detection of inducible clindamycin resistance among the clinical isolates of staphylococcus aureus by using the lower limit of inter disk space. J Microbiol Biotechnol Res 2012;2:258-64.  Back to cited text no. 3
Zelazny AM, Ferraro MJ, Glennen A, Hindler JF, Mann LM, Munro S, et al. Selection of strains for quality assessment of the disk induction method for detection of inducible clindamycin resistance in staphylococci: A CLSI collaborative study. J Clin Microbiol 2005;43:2613-5.  Back to cited text no. 4
Seifi N, Kahani N, Askari E, Mahdipour S, Naderi NM. Inducible clindamycin resistance in Staphylococcus aureus isolates recovered from Mashhad, Iran. Iran J Microbiol 2012;4:82-6.  Back to cited text no. 5
Steward CD, Raney PM, Morrell AK, Williams PP, McDougal LK, Jevitt L, et al. Testing for induction of clindamycin resistance in erythromycin-resistant isolates of Staphylococcus aureus. J Clin Microbiol 2005;43:1716-21.  Back to cited text no. 6
Aktas Z, Aridogan A, Kayacan CB, Aydin D. Resistance to macrolide, lincosamide and streptogramin antibiotics in staphylococci isolated in Istanbul, Turkey. J Microbiol 2007;45:286-90.  Back to cited text no. 7
Schmitz FJ, Sadurski R, Kray A, Boos M, Geisel R, Köhrer K, et al. Prevalence of macrolide-resistance genes in Staphylococcus aureus and Enterococcus faecium isolates from 24 European university hospitals. J Antimicrob Chemother 2000;45:891-4.  Back to cited text no. 8
Fiebelkorn KR, Crawford SA, McElmeel ML, Jorgensen JH. Practical disk diffusion method for detection of inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci. J Clin Microbiol 2003;41:4740-4.  Back to cited text no. 9
Coutinho Vde L, Paiva RM, Reiter KC, de-Paris F, Barth AL, Machado AB. Distribution of erm genes and low prevalence of inducible resistance to clindamycin among staphylococci isolates. Braz J Infect Dis 2010;14:564-8.  Back to cited text no. 10
Sedighi I, Yousefi Mashouf R, Pak N, Seif Rabiee MA. D-test method for detection of inducible clindamycin resistance in Staphylococcus aureus. Iran J Pediatr 2009;19:293-7.  Back to cited text no. 11
O'Sullivan MV, Cai Y, Kong F, Zeng X, Gilbert GL. Influence of disk separation distance on accuracy of the disk approximation test for detection of inducible clindamycin resistance in Staphylococcus spp. J Clin Microbiol 2006;44:4072-6.  Back to cited text no. 12
Lina G, Quaglia A, Reverdy ME, Leclercq R, Vandenesch F, Etienne J. Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother 1999;43:1062-6.  Back to cited text no. 13
Lim HS, Lee H, Roh KH, Yum JH, Yong D, Lee K, et al. Prevalence of inducible clindamycin resistance in staphylococcal isolates at a Korean tertiary care hospital. Yonsei Med J 2006;47:480-4.  Back to cited text no. 14
Schreckenberger PC, Ilendo E, Ristow KL. Incidence of constitutive and inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci in a community and a tertiary care hospital. J Clin Microbiol 2004;42:2777-9.  Back to cited text no. 15
Lewis JS 2nd, Jorgensen JH. Inducible clindamycin resistance in Staphylococci: Should clinicians and microbiologists be concerned? Antimicrob Resist 2005;40:280-5.  Back to cited text no. 16
Shoja S, Nahaei M, Nahaei M. Detection of inducible clindamycin resistance in Staphylococcus aureus and Staphylococcus epidermidis by using D-test. Pharma Sci 2009;15:1-8.  Back to cited text no. 17
Aslanimehr M, Yaghobfar R, Peymani A. Detection of MLSB phenotypes and inducible clindamycin resistance in Staphylococcus aureus isolates in-patients of Qazvin and Tehran teaching hospitals. J Qazvin Univ Med Sci 2014;18:30-6.  Back to cited text no. 18
Memariani M, Pourmand MR, Shirazi MH, Soltan Dallal MM, Abdolsamadi Z, Mardani N. The importance of inducible clindamycin resistance in enterotoxin positive S. aureus isolated from clinical samples. Tehran Univ Med J 2009;67:250-6. [Persian]  Back to cited text no. 19
Mahesh CB, Ramakant BK, Jagadeesh VS. The prevalence of inducible and constitutive clindamycin resistance among the nasal isolates of staphylococci. J Clin Diagn Res 2013;7:1620-2.  Back to cited text no. 20
Emaneini M, Eslampour MA, Sedaghat H, Aligholi M, Jabalameli F, Shahsavan S, et al. Characterization of phenotypic and genotypic inducible macrolide resistance in staphylococci in Tehran, Iran. J Chemother 2009;21:595-7.  Back to cited text no. 21
Zmantar T, Chaieb K, Ben Abdallah F, Ben Kahla-Nakbi A, Ben Hassen A, Mahdouani K, et al. Multiplex PCR detection of the antibiotic resistance genes in Staphylococcus aureus strains isolated from auricular infections. Folia Microbiol (Praha) 2008;53:357-62.  Back to cited text no. 22