Analysis of meticillin-susceptible and meticillin-resistant biofilm-forming Staphylococcus aureus from catheter infections isolated in a large Italian hospital
Several characteristics were analysed in 37 Staphylococcus aureus isolates from nosocomial catheter infections: the PFGE profile after SmaI digestion of chromosomal DNA, the ability to form a biofilm on a polystyrene surface, antibiotic susceptibility patterns (penicillin, oxacillin, erythromycin, tetracycline, clindamycin, telithromycin, gentamicin, ciprofloxacin, quinupristin/dalfopristin, rifampicin, vancomycin and linezolid), and the presence of genetic determinants of antibiotic resistance and biofilm formation. All strains but three (92 %) were able to grow on a plastic surface as a biofilm. An almost complete association was found between phenotypes and genotypic traits of antibiotic resistance, whilst PFGE profiling showed the highly polyclonal composition of the set of strains under study. Sixteen isolates (43 %) were meticillin-resistant and were subjected to staphylococcal cassette chromosome mec (SCCmec) and cassette chromosome recombinase (ccr) complex type determination by multiplex PCR. Only a subgroup of six strains belonged to the archaic clone PFGE type and bore the SCCmec/ccrAB type I structure. Among the remaining strains some presented small rearrangements of the SCCmec/ccrAB genetic locus, whilst others could barely be traced back to a known structural type. These observations suggest that, at the local level and at a particular site of infection, S. aureus may show great genetic variability and escape the general rule of expansion of the S. aureus pandemic clones.
Aires de SousaM.,
de LencastreH.,
Santos SanchesI.,
KikuchiK.,
TotsukaK.,
TomaszA.2000; Similarity of antibiotic resistance patterns and molecular typing properties of methicillin-resistant Staphylococcus aureus isolates widely spread in hospitals in New York City and in a hospital in Tokyo, Japan. Microb Drug Resist 6:253–258[CrossRef]
ArciolaC. R.,
BaldassarriL.,
MontanaroL.2002; In catheter infections by Staphylococcus epidermidis the intercellular adhesion ( ica ) locus is a molecular marker of the virulent slime-producing strains. J Biomed Mater Res 59:557–562[CrossRef]
BiswasR.,
VogguL.,
SimonU. K.,
HentschelP.,
ThummG.,
GotzF.2006; Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 259:260–268[CrossRef]
CafisoV.,
BertuccioT.,
SantagatiM.,
CampanileF.,
AmicosanteG.,
PerilliM. G.,
SelanL.,
ArtiniM.,
NicolettiG.,
StefaniS.2004; Presence of the ica operon in clinical isolates of Staphylococcus epidermidis and its role in biofilm production. Clin Microbiol Infect 10:1081–1088[CrossRef]
ChristensenG. D.,
SimpsonW. A.,
YoungerJ. J.,
BaddourL. M.,
BarrettF. F.,
MeltonD. M.,
BeacheyE. H.1985; Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006
ChungM.,
De LencastreH.,
MatthewsP.,
TomaszA.2000; Molecular typing of methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis: comparison of results obtained in a multilaboratory effort using identical protocols and MRSA strains. Microb Drug Resist 6:189–198[CrossRef]
CrisostomoM. I.,
WesthH.,
TomaszA.,
ChungM.,
OliveiraD. C.,
de LencastreH.2001; The evolution of methicillin resistance in Staphylococcus aureus : similarity of genetic backgrounds in historically early methicillin-susceptible and -resistant isolates and contemporary epidemic clones. Proc Natl Acad Sci U S A 98:9865[CrossRef]
CrowcroftN. S.,
RonveauxO.,
MonnetD. L.,
MertensR.1999; Methicillin-resistant Staphylococcus aureus and antimicrobial use in Belgian hospitals. Infect Control Hosp Epidemiol 20:31–36[CrossRef]
de SilvaG. D. I.,
KantzanouM.,
JusticeA.,
MasseyR. C.,
WilkinsonA. R.,
DayN. P. J.,
PeacockS. J.2002; The ica operon and biofilm production in coagulase-negative staphylococci associated with carriage and disease in a neonatal intensive care unit. J Clin Microbiol 40:382–388[CrossRef]
DominguezM. A.,
de LencastreH.,
LinaresJ.,
TomaszA.1994; Spread and maintenance of a dominant methicillin-resistant Staphylococcus aureus (MRSA) clone during an outbreak of MRSA disease in a Spanish hospital. J Clin Microbiol 32:2081–2087
EnrightM. C.,
DayN. P. J.,
DaviesC. E.,
PeacockS. J.,
SprattB. G.2000; Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus
. J Clin Microbiol 38:1008–1015
GouldI. M.2006; Costs of hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) and its control. Int J Antimicrob Agents 28:379–384[CrossRef]
GrundmannH.,
Aires-de-SousaM.,
BoyceJ.,
TiemersmaE.2006; Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368:874–885[CrossRef]
KreiswirthB.,
KornblumJ.,
ArbeitR. D.,
EisnerW.,
MaslowJ. N.,
McGeerA.,
LowD. E.,
NovickR. P.1993; Evidence for a clonal origin of methicillin resistance in Staphylococcus aureus
. Science 259:227[CrossRef]
LeskiT.,
OliveiraD.,
TrzcinskiK.,
SanchesI. S.,
de SousaM. A.,
HryniewiczW.,
de LencastreH.1998; Clonal distribution of methicillin-resistant Staphylococcus aureus in Poland. J Clin Microbiol 36:3532–3539
LimT. T.,
ChongF. N.,
O'BrienF. G.,
GrubbW. B.2003; Are all community methicillin-resistant Staphylococcus aureus related? A comparison of their mec regions. Pathology 35:336–343
MackD.,
NedelmannM.,
KrokotschA.,
SchwarzkopfA.,
HeesemannJ.,
LaufsR.1994; Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun 62:3244–3253
MakiD. G.,
MermelL. A.1998; Infections due to infusion therapy. In Hospital Infections pp 689–724 Edited by
BennettJ. V.,
BrachmanP. S.
Boston, MA: Little Brown;
MermelL. A.,
FarrB. M.,
SherertzR. J.,
RaadI. I.,
O'GradyN.,
HarrisJ. A. S.,
CravenD. E.2001; Guidelines for the management of intravascular catheter-related infections. Clin Infect Dis 32:1249–1272[CrossRef]
MolinS.,
Tolker-NielsenT.2003; Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261[CrossRef]
OliveiraD. C.,
LencastreH.2002; Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus
. Antimicrob Agents Chemother 46:2155–2161[CrossRef]
OliveiraD. C.,
TomaszA.,
de LencastreH.2001; The evolution of pandemic clones of methicillin-resistant Staphylococcus aureus : identification of two ancestral genetic backgrounds and the associated mec elements. Microb Drug Resist 7:349–361[CrossRef]
OliveiraD. C.,
TomaszA.,
LencastreH.2002; Secrets of success of a human pathogen: molecular evolution of pandemic clones of methicillin-resistant Staphylococcus aureus
. Lancet Infect Dis 2:180–189[CrossRef]
PetrelliD.,
ZampaloniC.,
D'ErcoleS.,
PrennaM.,
BallariniP.,
RipaS.,
VitaliL. A.2006; Analysis of different genetic traits and their association with biofilm formation in Staphylococcus epidermidis isolates from central venous catheter infections. Eur J Clin Microbiol Infect Dis 25:773–781[CrossRef]
PrunierA. L.,
MalbrunyB.,
LauransM.,
BrouardJ.,
DuhamelJ. F.,
LeclercqR.2003; High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. J Infect Dis 187:1709–1716[CrossRef]
RipaS.,
ZampaloniC.,
VitaliL. A.,
GiovanettiE.,
MontanariM. P.,
PrennaM.,
VaraldoP. E.2001; Sma I macrorestriction analysis of Italian isolates of erythromycin-resistant Streptococcus pyogenes and correlations with macrolide-resistance phenotypes. Microb Drug Resist 7:65–71[CrossRef]
RobertsR. B.,
de LencastreA.,
EisnerW.,
SeverinaE. P.,
ShopsinB.,
KreiswirthB. N.,
TomaszA.the MRSA Collaborative Study Group1998; Molecular epidemiology of methicillin-resistant Staphylococcus aureus in 12 New York hospitals. J Infect Dis 178:164–171[CrossRef]
RobinsonD. A.,
EnrightM. C.2003; Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus
. Antimicrob Agents Chemother 47:3926–3934[CrossRef]
RohdeH.,
KnoblochJ. K. M.,
HorstkotteM. A.,
MackD.2001; Correlation of Staphylococcus aureus icaADBC genotype and biofilm expression phenotype. J Clin Microbiol 39:4595–4596[CrossRef]
RohdeH.,
KalitzkyM.,
KrogerN.,
ScherpeS.,
HorstkotteM. A.,
KnoblochJ. K. M.,
ZanderA. R.,
MackD.2004; Detection of virulence-associated genes not useful for discriminating between invasive and commensal Staphylococcus epidermidis strains from a bone marrow transplant unit. J Clin Microbiol 42:5614–5619[CrossRef]
SavolainenK.,
PaulinL.,
Westerlund-WikstromB.,
FosterT. J.,
KorhonenT. K.,
KuuselaP.2001; Expression of pls , a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus , prevents bacterial adhesion in vitro
. Infect Immun 69:3013–3020[CrossRef]
StewardC. D.,
RaneyP. M.,
MorrellA. K.,
WilliamsP. P.,
McDougalL. K.,
JevittL.,
McGowanJ. E.,
TenoverF. C.2005; Testing for induction of clindamycin resistance in erythromycin-resistant isolates of Staphylococcus aureus
. J Clin Microbiol 43:1716–1721[CrossRef]
TeixeiraL. A.,
ResendeC. A.,
OrmondeL. R.,
RosenbaumR.,
FigueiredoA. M.,
de LencastreH.,
TomaszA.1995; Geographic spread of epidemic multiresistant Staphylococcus aureus clone in Brazil. J Clin Microbiol 33:2400–2404
van BelkumA.2000; Molecular epidemiology of methicillin-resistant Staphylococcus aureus strains: state of affairs and tomorrow's possibilities. Microb Drug Resist 6:173–188[CrossRef]
VandecasteeleS. J.,
PeetermansW. E.,
MerckxR. R.,
RijndersB. J. A.,
Van EldereJ.2003; Reliability of the ica , aap and atlE genes in the discrimination between invasive, colonizing and contaminant Staphylococcus epidermidis isolates in the diagnosis of catheter-related infections. Clin Microbiol Infect 9:114–119[CrossRef]
ZhangK.,
McClureJ. A.,
ElsayedS.,
LouieT.,
ConlyJ. M.2005; 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 43:5026–5033[CrossRef]
Analysis of meticillin-susceptible and meticillin-resistant biofilm-forming Staphylococcus aureus from catheter infections isolated in a large Italian hospital