Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) is the causal agent of multiple nosocomial infections worldwide, including catheter-associated bacteremia in hemodialysis patients. The purposes of this work were to genetically characterize a group of MRSA isolates from catheter-related infections of ambulatory Mexican hemodialysis patients and to determine whether the strains are the same as those carried by the patients in their anterior nares. Sixteen pairs of MRSA isolates from the catheter (cat) and anterior nares (N) of hemodialysis patients were compared using pulsed-field gel electrophoresis (PFGE), PCR detection of adhesion genes and other virulence markers, and an antibiogram. Three pairs of N/cat MRSA isolates (18.7 %) with identical resistograms also showed the same combination of PCR-detected markers and PFGE pattern; one additional pair showed only an identical electrophoretic PFGE pattern. Of the MRSA isolates, 75 % (n = 24) were resistant to ≥7 antibiotics, 4 isolates were resistant to 11 antibiotics, and 7 isolates were resistant to the 12 antibiotics tested. The most frequent virulence marker combination found was spa, clfA, clfB, cna, bbp, ebps, map/eap, sdrC, sdrD, sdrE, ica, agr (65.6 %, n = 21). The SCCmec alleles of the 32 MRSA isolates were IV (n = 20), I (n = 7), II (n = 4), and V (n = 1), and no SCCmec type III MRSA was found. The genotypic characterization of the MRSA isolates studied in this work will contribute to a better understanding of the virulence gene makeup of catheter-colonizing S. aureus strains and will help to lower the infection risk in these patients.
Similar content being viewed by others
References
Ayala-Gaytán JJ, Alemán-Bocanegra MC, Guajardo-Lara CE, Valdovinos-Chávez SB (2010) Catheter-associated bloodstream infections. Review of five-year surveillance among hospitalized patients. Rev Méd IMSS 48:145–150
Boye K, Bartels MD, Andersen IS, Møller JA, Westh HA (2007) A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I–V. Clin Microbiol Infect 13:725–727
Brakstad O, Aasbakk K, Maeland J (1992) Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 30:1654–1660
Buck JM, Como-Sabetti K, Harriman KH, Danila RN, Boxrud DJ, Glennen A, Lynfield R (2005) Community-associated methicillin-resistant Staphylococcus aureus, Minnesota, 2000–2003. Emerging infectious diseases www.cdc.gov/eid Vol. 11, No. 10
Campbell SJ, Deshmukh HS, Nelson CL, Bae IG, Stryjewski ME, Federspiel JJ, Tonthat GT, Rude TH, Barriere SL, Corey R, Fowler VG Jr (2008) Genotypic characteristics of Staphylococcus aureus isolates from a multinational trial of complicated skin and skin structure infections. J Clin Microbiol 46:678–684
Clinical and Laboratory Standards Institute (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, vol 32, 9th edn. Clinical and Laboratory Standards Institute, Wayne, no. 2, document M07-A9
Clinical and Laboratory Standards Institute (CLSI) (2007) Performance standards for antimicrobial susceptibility testing; 17th informational supplement. CLSI, Wayne, CLSI document M100-S17
Deurenberg RH, Stobberingh EE (2008) The evolution of Staphylococcus aureus. Infect Genet Evol 8:747–763
Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE (2007) The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13(3):222–235
Frenay HME, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbrouke-Grauls CMJE, Verhoef J, Mooi FR (1996) Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis 15:60–64
Geha DJ, Uhl JR, Gustaferro CA, Persing DH (1994) Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol 32:1768–1772
Gilot P, Lina G, Cochard T, Poutrel B (2002) Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol 40:4060–4067
Götz F (2002) Staphylococcus and biofilms. Mol Microbiol 43:1367–1378
Hanssen AM, Sollid JU (2007) Multiple staphylococcal cassette chromosomes and allelic variants of cassette chromosome recombinases in Staphylococcus aureus and coagulase-negative staphylococci from Norway. Antimicrob Agents Chemother 51:1671–1677
Hookey JV, Richardson JF, Cookson BD (1998) Molecular typing of Staphylococcus aureus based on PCR restriction fragment length polymorphism and DNA sequence analysis of the coagulase gene. J Clin Microbiol 36:1083–1089
Jean G, Charra B, Chazot C, Vanel T, Terrat JC, Hurot JM, Laurent G (2002) Risk factors analysis for long-term tunneled dialysis catheter-related bacteremias. Nephron 91:399–405. doi:10.1159/000064279
Ji G, Beavis RC, Novick RP (1995) Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc Natl Acad Sci U S A 92:12055–12059. doi:10.1073/pnas.92.26.12055
Johnson LB, Jose J, Yousif F, Pawlak J, Saravolatz LD (2009) Prevalence of colonization with community-associated methicillin-resistant Staphylococcus aureus among end-stage renal disease patients and healthcare workers. Infect Control Hosp Epidemiol 30:4–8
Jönsson K, Signäs C, Müller HP, Lindberg M (1991) Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 202:1041–1048
Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R (2006) Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992–2003. Clin Infect Dis 42:389–391
Kobayashi N, Wu H, Kojima K, Taniguchi K, Urasawa S, Uehara N, Omizu Y, Kishi Y, Yagihashi A, Kurokawa I (1994) Detection of mecA, femA and femB genes in clinical strains of staphylococci using polymerase chain reaction. Epidemiol Infect 113:259–266
Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132. doi:10.1086/313461
Luzar MA, Coles GA, Faller B, Slingeneyer A, Dah GD, Briat C, Wone C, Knefati Y, Kessler M, Peluso F (1990) Staphylococcus aureus nasal carriage and infection in patients on continuous ambulatory peritoneal dialysis. N Engl J Med 322:505–509
McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC (2003) Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 41:5113–5120
Mombach Pinheiro Machado AB, Reiter KC, Paiva RM, Barth AL (2007) Distribution of staphylococcal cassette chromosome mec (SCCmec) types I, II, III, and IV in coagulase-negative staphylococci from patients attending a tertiary hospital in southern Brazil. J Med Microbiol 56:1328–1333
Mongodin E, Bajolet O, Cutrona J, Bonnet N, Du-puit F, Puchelle E, de Bentzmann S (2002) Fibronectin-binding proteins of Staphylococcus aureus are involved in adherence to human airway epithelium. Infect Immun 70:620–630
Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, Johnson SK, Vandenesch F, Fridkin S, O’Boyle C, Danila RN, Lynfield R (2003) Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 290:2976–2984
Nastaly P, Grinholc M, BielawskiK P (2010) Molecular characteristics of community-associated methicillin-resistant Staphylococcus aureus strains for clinical medicine. Arch Microbiol 192:603–617. doi:10.1007/s00203-010-0594-4
Navarre W, Schneewind O (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229
Paniagua-Contreras G, Sáinz-Espuñes T, Monroy-Pérez E, Rodríguez-Moctezuma JR, Arenas-Aranda D, Negrete-Abascal E, Vaca S (2012) Virulence markers in Staphylococcus aureus strains isolated from hemodialysis catheters of Mexican patients. AiM 2:476–487. doi:10.4236/aim.2012.24061
Peacock SJ, Day NPJ, Thomas MG, Berendt AR, Foster TJ (2000) Clinical isolates of Staphylococcus aureus exhibit diversity in fnb genes and adhesion to human fibronectin. J Infect 41:23–31. doi:10.1053/jinf.2000.0657
Peacock SJ, Moore CE, Justice A, Kantzanou M, Story L, Mackie K, O’Neill G, Day NP (2002) Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70:4987–4996. doi:10.1128/IAI.70.9.4987-4996.2002
Plata K, Rosato AE, Wegrzyn G (2009) Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity. Acta Biochim Pol 56:597–612
Sabath A, Melles DC, Martirosian G, Grundmann H, van Belkum A, Hryniewicz W (2006) Distribution of the serine-aspartate repeat protein-encoding sdr genes among nasal and invasive Staphylococcus aureus strains. J Clin Microbiol 44:1135–1138. doi:10.1128/JCM.44.3.1135-1138.2006
Sidhu MS, Heir E, Leegaard T, Wiger K, Holck A (2002) Frequency of disinfectant resistance genes and genetic linkage with β-lactamase transposon Tn552 among clinical staphylococci. Antimicrob Agents Chemother 46:2797–2803
Signäs C, Raucci G, Jönsson K, Lindgren PE, Anantharamaiah GM, Höök M, Lindberg M (1989) Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci U S A 86:699–703
Stefani S, Chung DR, Lindsay JA, Friedrich AW, Kearns AM, Westh H, Mackenzie FM (2012) Methicillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonization of typing methods. Int J Antimicrob Agents 39:273–282. doi:10.1016/j.ijatimicag.2011.09.030
Stephan R, Annemüller C, Hassan AA, Lämmler C (2001) Characterization of enterotoxigenic Staphylococcus aureus strains isolated from bovine mastitis in north-east Switzerland. Vet Microbiol 78:373–382
Stolić R, Trajković G, Perić V, Jovanović A, Stolić D, Sovtić S, Lazarević T, Zivić Z, Subarić-Gorgieva G (2008) Central venous catheters in hemodialysis: to accept recommendations or to stick to own experience. Vojnosanit Pregl 65:21–26. doi:10.2298/VSP0801021S
Strandén AM, Frei R, Adler H, Flückiger U, Widmer AF (2009) Emergence of SCCmec type IV as the most common type of methicillin-resistant Staphylococcus aureus in a university hospital. Infection 37:44–48
Straub JA, Hertel C, Hammes WP (1999) A 23S rRNA targeted polymerase chain reaction-based system for detection of Staphylococcus aureus in meat starter cultures and dairy products. J Food Prot 62:1150–1156
Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239
Trad S, Allignet J, Frangeul L, Davi M, Vergassola M, Couve E, Morvan A, Kechrid A, Buchrieser C, Glaser P, El-Solh N (2004) DNA macroarray for identification and typing of Staphylococcus aureus isolates. J Clin Microbiol 42:2054–2064. doi:10.1128/JCM.42.5.2054-2064.2004
von Eiff C, Becker K, Machka K, Stammer H, Peters G (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study group. N Engl J Med 344:11–16
Weinke T, Schiller R, Fehrenbach FJ, Pohle HD (1992) Association between Staphylococcus aureus nasopharyngeal colonization and septicemia in patients infected with the human immunodeficiency virus. Eur J Clin Microbiol Infect Dis 11:985–989
Weinstein HJ (1959) The relationship between the nasal staphylococcal carrier state and the incidence of post-operative complications. N Engl J Med 260:1303–1308
Wisplinghoff H, Rosato AE, Enright MC, Noto M, Craig W, Archer GL (2003) Related clones containing SCCmec type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrob Agents Chemother 47:3574–3579
Yu VL, Goetz A, Wagener M, Smith PB, Rihs JD, Hanchett J, Zuravleff JJ (1986) Staphylococcus aureus nasal carriage and infection in patients on hemodialysis. Efficacy of antibiotic prophylaxis. N Engl J Med 315:91–96
Zetola N, Francis JS, Nuermberger EL, Bishai WR (2005) Community-acquired methicillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis 5:275–286
Acknowledgments
This work was supported in part by grants from UNAM-DGAPA-PAPIIT IN218211 and PAPCA FES Iztacala (2011–2012, Project 6) and UAM-Xochimilco. We thank Guadalupe Cruz Gregorio for the technical support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Paniagua-Contreras, G., Monroy-Pérez, E., Gutiérrez-Lucas, R. et al. Genotypic characterization of methicillin-resistant Staphylococcus aureus strains isolated from the anterior nares and catheter of ambulatory hemodialysis patients in Mexico. Folia Microbiol 59, 295–302 (2014). https://doi.org/10.1007/s12223-013-0300-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-013-0300-4