Aminoglycoside and chlorhexidine resistance genes in Staphylococcus aureus isolated from surgical wound infections.


  • Hamdia Askar Faculty of Medicine, Mansoura University, Egypt
  • Wafaa Badaway
  • Enas Hammad



Keywords, Staphylococcal Infections, Surgical Site Infections, Disinfectant Resistance, Drug Resistance.


Hamdia Askar1, Wafaa Badawy2  and Enas Hammad1

1Medical Microbiology and Immunology Department, Faculty of Medicine, Mansoura University, Egypt

2MD.MansouraUniversity Students'Hospital,Egypt.


Background:   Staphylococcus aureus is a major human pathogen resistant to many antimicrobial agents especially the methicillin-resistant Staphylococcus aureus (MRSA). In surgical site infections, MRSA is known to be an important etiologic factor. Infections range from skin and soft-tissue infections to deep tissue infections such as osteomyelitis, bacteremia, and endocarditis that are much more common in hospital environment. In staphylococci the main mechanism of aminoglycoside resistance is the drug inactivation by aminoglycoside-modifying enzymes (AMEs) and reduced biocide susceptibility is associated with the acquisition of quaternary ammonium compound (qac) gene-encoding for Qac efflux proteins.

Aim of the work: To investigate the prevalence of the aminoglycosides resistance genes aac(6′)aph(2″), aph(3′)-IIIa, Ant(4′)-Ia) and the biocide resistance genes (qacA/qacB, qacC) in  S. aureus  isolated from surgical site infections.

Methods:  Swabs from 280 infected surgical sites were sent to our laboratory from different surgical words at Mansoura University Hospitals between January 2014 and December 2014. Sixty- six staphylococcal strains were isolated and included in this study. Verification of the presence of methicillin resistance gene (mecA), chlorhexidine MIC and qac resistance genes (qacA/qacB, qacC) were detected by PCR. The presence of aminoglycoside resistance genes [(aac(6′)/aph (2″), ant (4′)-1a and aph(3′)-IIIa)] in S. aureus was also tested by PCR.

Results:   Seventeen of the 66 S. aureus isolates (25.75 %) were phenotypically MRSA and mecA gene was detected in 19 S. aureus isolates (28.7 %) by PCR. Aminoglycoside resistant S. aureus were 21/66 (31.8%). AME genes were detected in all aminoglycoside-resistant S. aureus; aac(6′)/aph (2″) was the most frequently detected 11/21(52.4%) followed by aph(3′)-IIIa 6/21 (28.6%) and the least frequent was ant (4′)-1a 4/21(19%). Aminoglycoside resistance in 9 out of the 21 (42.9%) aminoglycoside resistance S. aureus isolates was solely plasmid mediated being lost after plasmid curing. A total of 14 out of the 21 aminoglycoside-resistant S. aureus isolates (66.7 %) carried the mecA gene. Among the 45 aminoglycoside-sensitive S. aureus isolates 5 (11.1%) were mecA positive. Nine of the 21 aminoglycoside-resistant S. aureus isolates (42.9%) were positive for qacA/qacB genes and in all of them mecA gene co-existed. Five aminoglycoside resistant S. aureus isolates were qacC positive (23.8%).  

Conclusion: In the Staphylococcus aureus isolated from infected surgical wounds, quaternary ammonium compounds resistance genes were positive at a considerable ratio and co-existed with aminoglycosides and methicillin-resistance genes in S. aureus isolates.



Author Biography

Hamdia Askar, Faculty of Medicine, Mansoura University, Egypt

Medical Microbiology and Immunology Department

Faculty of Medicine

Mansoura University


Nystrom B., (1994): Impact of handwashing on mortality in intensive care: examination of the evidence. Infect. Control. Hosp. Epidemiol., 15, 435-436.

Noguchi N., Suwa J., Narui K., Sasatsu M., Ito T., Hiramatsu K., Song J. H., J. (2005): Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol, 54(Pt 6): 557–65

Nakaminami H, Noguchi N, Sasatsu M (2010): Fluoroquinolone efflux by the plasmid-mediated multidrug efflux pump QacB variant QacBIII in Staphylococcus aureus. Antimicrob Agents Chemother. 54(10):4107-11.

Mitchell, B. A., Brown, M. H. & Skurray, R. A. (1998): qacA multidrug efflux pump from Staphylococcus aureus: comparative analysis of resistance to diamines, biguanides, and buanylhydrazones. Antimicrobial Agents and Chemotherapy 42, 475–7.

Leelaporn A, Firth N, Paulsen IT, Hettiaratchi A, Skurray RA (1995): Multidrug resistance plasmid pSK108 from coagulase-negative staphylococci; relationships to Staphylococcus aureus qacC plasmids. Plasmid, 34:62-67.

Noguchi N, Hase M, Kitta M, Sasatsu M, Deguchi K, Kono M (1999): Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett, 172:247-253.

Berg T, Firth N, Apisiridej S, Hettiaratchi A, Leelaporn A, Skurray RA (1998): Complete nucleotide sequence of pSK41: Evolution of staphylococcal conjugative multiresistance plasmids. J Bacteriol. 180:4350-4359.

Paulsen, I. T., Brown, M. H., Littlejohn, T. G., Mitchell, B. A. & Skurray, R. A. (1996): Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity. Proceedings of the National Academy of Sciences, USA 93, 3630–5.

Milstone AM, Passaretti CL, Perl TM. (2008): Chlorhexidine: expanding the armamentarium for infection control and prevention. Clin. Infect. Dis.46:274–281.

McDonnell G, Russell AD. (1999): Antiseptics and disinfectants: activity, action, and resistance. Clin. Microbiol. Rev. 12:147–179.

Kim HB, Kim T, Lee BB, et al. (2002): Frequency of resistance to aminoglycoside antibiotics in Staphylococcus aureus isolates from tertiary hospitals. Korean J Infect Dis., 34:39–46.

Choi SM, Kim SH, Kim HJ, et al. (2003): Multiplex PCR for the detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species. J Korean Med Sci; 18:631–36.

Sekiguchi J, Fujino T, Saruta K, Konosaki H, Nishimura H, Kawana A,,et al. (2004): Prevalence of erythromycin-, tetracycline-, and aminoglycoside-resistance genes in methicillin-resistant Staphylococcus aureus in hospitals in Tokyo and Kumamoto. Jpn J Infect Dis. 57:74–77.

Bianchi DM, Gallina S, Bellio A, Chiesa F, Civera T, Decastelli L. (2014): Enterotoxin gene profiles of Staphylococcus aureus isolated from milk and dairy products in Italy. Lett Appl Microbiol 58(2):190-196.

National Committee for Clinical Laboratory Standard Performance for Antimicrobial Disk Susceptibility Tests, Aproved standards, Viallanova, PA: NCLLS, 2000.

Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M7-A7. Clinical and Laboratory Standards Institute, Wayne, PA, 2006.

Lacey RW, Grinsted J (1972): Linkage of fusidic acid resistance to the penicillinase plasmid in Staphylococcus aureus. J Gen Microbiol, 73(3):501–508.

Lannergard J, Norstrom T, HughesD (2009): Genetic determinants of resistance to fusidic acid among clinical bacteremia isolates of Staphylococcus aureus. Antimicrob Agents Chemother, 53(5):2059–2065.

Geha DJ, Uhl JR, Gustaferro CA, Persing DH. (1994): Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol. 32(7):1768-72.

Rouch D.A., Cram D.S., DiBerardino D., Littlejohn T.G., Skurray R.A. (1990) Efflux-mediated antiseptic gene qacA from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol. Microbiol. 4,2051–2062.

Zmantar T, Kouidhi B, Miladi H, et al. (2011): Detection of macrolide and disinfectant resistance genes in clinical. Staphylococcus aureus and coagulase-negative staphylococci. BMC Res Notes. 4:453–64.

Duran N, Ozer B, Duran GG, et al. (2012): Antibiotic resistance genes & susceptibility patterns in staphylococci, Indian J Med Res. 135.389–96.

Gray G S, Fitch W M. (1984) Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene from Staphylococcus aureus. Mol Biol Evol. 1:57–66

Matsumura M, Katakura Y, Imanaka T, Aiba S. (1984) Enzymatic and nucleotide sequence studies of a kanamycin-inactivating enzyme encoded by a plasmid from thermophilic bacilli in comparison with that encoded by plasmid pUB110. J Bacteriol. 160:413–420.

Fatholahzadeh B, Emaneini M, Feizabadi MM, et al. (2009): Characterisation of genes encoding aminoglycoside-modifying enzymes among meticillin-resistant Staphylococcus aureus isolated from two hospitals in Tehran, Iran. Int J Antimicrob Agents, 33:264–5.

Carneiro LA, Queiroz ML, Merquior VL, et al. (2004): Antimicrobial-resistance and enterotoxin-encoding genes among staphylococci isolated from expressed human breast milk. J Med Microbiol. 53:761–8.

Emaneini M, Bigverdi R, Kalantar D, Soroush S, Jabalameli F, Noorazar Khoshgnab B, Asadollahi P, Taherikalani M. (2013) Distribution of genes encoding tetracycline resistance and aminoglycoside modifying enzymes in Staphylococcus aureus strains isolated from a burn center. Ann Burns Fire Disasters. 30;26(2):76-80.

Fatholahzadeh B, Emaneini M, Gilbert G, et al. (2008): Staphylococcal cassette chromosome mec (SCCmec) analysis and antimicrobial susceptibility patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolates in Tehran, Iran. Microb Drug Resist. 14:217–20.

Duran N, Temiz M, Duran GG, Eryılmaz N, Jenedi K. (2014): Relationship between the resistance genes to quaternary ammonium compounds and antibiotic resistance in staphylococci isolated from surgical site infections Med Sci Monit. 2; 20:544-50.

Zhang M, O’Donoghue MM, Ito T et al: (2011) Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong. J Hosp Infect, 78(2): 113–17

Shamsudin MN, Alreshidi MA, Hamat RA, et al. (2012): High prevalence of qacA/B carriage among clinical isolates of meticillin-resistant Staphylococcus aureus in Malaysia. J Hosp Infect. 81(3):206–8.

Nakipoğlu Y, Ignak S, Gürler N et al: (2012): [The prevalence of antiseptic resistance genes (qacA/B and smr) and antibiotic resistance in clinical Staphylococcus aureus strains]. Mikrobiyol Bul, 46(2): 180–89