Clinical Investigation| Volume 351, ISSUE 3, P279-285, March 2016

Download started.


Virulence Factors in Staphylococci Isolated From Nasal Cavities of Footballers



      This study aimed to investigate the rate of Panton-Valentine Leukocidin producing Staphylococcus aureus and methicillin (mecA) and slime (icaA/icaD) genes in staphylococcal strains isolated from nasal cavities of footballers.

      Materials and Methods

      Nasal swab samples were taken from each footballers and a healthy control group for the isolation of staphylococcal strains. The polymerase chain reaction technique was used to determine Panton-Valentine Leukocidin, mecA and icaA/icaD genes in staphylococcal isolates.


      Among 91 S. aureus strains, the presence of mecA gene was detected as 9.9%. This ratio was 17.9% (27 of 151) among the coagulase-negative staphylococci. A significant difference was found between coagulase-negative staphylococci and S. aureus isolates regarding the presence of mecA gene (P < 0.001). As for the genes of the slime, icaA/icaD genes were detected in 198 of 242 (81.8%) strains. The occurrence of slime genes was 91.2% and 89.4% among the S. aureus coagulase and negative staphylococci, respectively (P > 0.05). There was a statistically significant difference between the frequency of the mecA and slime genes when compared with the healthy control group and the football players (P < 0.01). Of 91 isolates, 22 were found to be methicillin resistant by the oxacillin disc diffusion method, whereas the remaining (220) were methicillin susceptible. Methicillin resistance was detected as 14.9% by the polymerase chain reaction method, whereas it was found as 9.1% by phenotypic methods.


      Early and accurate diagnosis of virulent staphylococcal strains is crucial because the virulent coagulase-negative and coagulase-positive staphylococcal strains in the nasal floras of footballers may be major potential sources of superficial and deep tissue infections.

      Key Indexing Terms

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to The American Journal of the Medical Sciences
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Finch C.
        • Owen N.
        • Price R.
        Current injury or disability as a barrier to being more physically active.
        Med Sci Sports Exerc. 2001; 33: 778-782
        • Kluytmans J.
        • van Belkum A.
        • Verbrugh H.
        Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks.
        Clin Microbiol Rev. 1997; 10: 505-520
        • Bowers A.L.
        • Huffman G.R.
        • Sennett B.J.
        Methicillin-resistant Staphylococcus aureus infections in collegiate football players.
        Med Sci Sports Exerc. 2008; 40: 1362-1367
        • Waninger K.N.
        • Rooney T.P.
        • Miller J.E.
        • et al.
        Community-associated methicillin-resistant Staphylococcus aureus survival on artificial turf substrates.
        Med Sci Sports Exerc. 2011; 43: 779-784
        • Stacey A.R.
        • Endersby K.E.
        • Chan P.C.
        • et al.
        An outbreak of methicillin resistant Staphylococcus aureus infection in a rugby football team.
        Br J Sports Med. 1998; 32: 153-154
        • Hodde P.J.
        • Badylak F.S.
        • May L.C.
        • et al.
        Infective endocarditis in a collegiate wrestler.
        J Athl Train. 1995; 30: 105-107
        • Gillet Y.
        • Issartel B.
        • Vanhems P.
        • et al.
        Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients.
        Lancet. 2002; 359: 753-759
        • Kinney K.K.
        Treatment of infections caused by antimicrobial-resistant gram-positive bacteria.
        Am J Med Sci. 2010; 340: 209-217
        • Holt J.G.
        • Krieg N.R.
        • Sneath P.H.A.
        Bergey׳s Manual of Determinative Bacteriology. 9th ed. William and Wilkins, Baltimore, MD1994
      1. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing [17th informational supplement. CLSI document M100-S17. Wayne, PA: Clinical and Laboratory Standards Institute; 2007.
        • Duran N.
        • Dogramaci Y.
        • Demir C.
        • et al.
        Detection of slime and methicillin resistance genes in Staphylococci isolated from nasal samples of patients with orthopaedic implants.
        Med Sci Monit. 2010; 16: BR271-BR277
        • Vasudevan P.
        • Nair M.K.
        • Annamalai T.
        • et al.
        Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation.
        Vet Microbiol. 2003; 92: 179-185
        • Lari A.R.
        • Pourmand M.R.
        • Moghadam S.O.
        • et al.
        Prevalence of PVL-containing MRSA isolates among hospital staff nasal carriers.
        Labmed. 2011; 42: 283-286
        • Lear A.
        • McCord G.
        • Peiffer J.
        • et al.
        Incidence of Staphylococcus aureus nasal colonization and soft tissue infection among high school football players.
        J Am Board Fam Med. 2011; 24: 429-435
        • Vandecasteele S.J.
        • Boelaert J.R.
        • De Vriese A.S.
        Staphylococcus aureus infections in hemodialysis: what a nephrologist should know.
        Clin J Am Soc Nephrol. 2009; 4: 1388-1400
        • Duran N.
        • Ocak S.
        • Eskiocak A.F.
        Staphylococcus aureus nasal carriage among the diabetic and non-diabetic haemodialysis patients.
        Int J Clin Pract. 2006; 60: 1204-1209
        • Usery J.B.
        • Vo N.H.
        • Finch C.K.
        • et al.
        Evaluation of the treatment of methicillin-resistant Staphylococcus aureus bacteremia.
        Am J Med Sci. 2015; 349: 36-41
        • Horino T.
        • Sato F.
        • Hosaka Y.
        • et al.
        Predictive factors for metastatic infection in patients with bacteremia caused by methicillin-sensitive Staphylococcus aureus.
        Am J Med Sci. 2015; 349: 24-28
        • Kazakova S.V.
        • Hageman J.C.
        • Matava M.
        • et al.
        A clone of methicillin resistant Staphylococcus aureus among professional football players.
        N Engl J Med. 2005; 352: 468-475
        • Stacey A.R.
        • Endersby K.E.
        • Chan P.C.
        • et al.
        An outbreak of methicillin-resistant Staphylococcus aureus infection in a rugby football team.
        Br J Sports Med. 1998; 32: 153-154
        • Benjamin H.J.
        • Nikore V.
        • Takagishi J.
        Practical management: community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA): the latest sports epidemic.
        Clin J Sport Med. 2007; 17: 393-397
        • Lindenmayer J.M.
        • Schoenfeld S.
        • O׳Grady R.
        • et al.
        Methicillin-resistant Staphylococcus aureus in a high school wrestling team and the surrounding community.
        Arch Intern Med. 1998; 158: 895-899
        • Zapun A.
        • Contreras-Martel C.
        • Vernet T.
        Penicillin-binding proteins and beta-lactam resistance.
        FEMS Microbiol Rev. 2008; 32: 361-385
        • William J.L.
        • Radu S.
        • Aziz S.A.
        • et al.
        Prevalence of Staphylococcus aureus carriage by young Malaysian footballers during indoor training.
        Br J Sports Med. 2004; 38: 12-14
        • Creech C.B.
        • Saye E.
        • McKenna B.D.
        • et al.
        One-year surveillance of methicillin-resistant Staphylococcus aureus nasal colonization and skin and soft tissue infections in collegiate athletes.
        Arch Pediatr Adolesc Med. 2010; 164: 615-620
        • Romano R.
        • Lu D.
        • Holtom P.
        Outbreak of community-acquired methicillin-resistant Staphylococcus aureus skin infections among a collegiate football team.
        J Athl Train. 2006; 41: 141-145
        • Tong A.
        • Tong S.Y.
        • Zhang Y.
        • et al.
        Panton-Valentine leukocidin is not the primary determinant of outcome for Staphylococcus aureus skin infections: evaluation from the CANVAS studies.
        PLoS One. 2012; 7: e37212
        • Kirkland E.B.
        • Adams B.B.
        Methicillin-resistant Staphylococcus aureus and athletes.
        J Am Acad Dermatol. 2008; 59: 494-502
        • McClure J.A.
        • Conly J.M.
        • Lau V.
        • et al.
        Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from resistant staphylococci.
        J Clin Microbiol. 2006; 44: 1141-1144
        • Agarwal A.
        • Jain A.
        Association between drug resistance & production of biofilm in staphylococci.
        Indian J Med Res. 2012; 135: 562-564
        • Duran N.
        • Dogramaci Y.
        • Ozer B.
        • et al.
        Detection of adhesin genes and slime production among Staphylococci in orthopaedic surgical wounds.
        Afr J Microbiol Res. 2010; 4: 708-715
        • Duran N.
        • Ozer B.
        • Duran G.G.
        • et al.
        Antibiotic resistance genes & susceptibility patterns in staphylococci.
        Indian J Med Res. 2012; 135: 389-396
        • Arciola C.R.
        • Baldassarri L.
        • Montanaro L.
        Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections.
        J Clin Microbiol. 2001; 39: 2151-2156
        • Arciola C.R.
        • Campoccia D.
        • Gamberini S.
        • et al.
        Detection of slime production by means of an optimised Congo red agar plate test based on a colourimetric scale in Staphylococcus epidermidis clinical isolates genotyped for ica locus.
        Biomaterials. 2002; 23: 4233-4239