Background Community-associated methicillin-resistant Staphylococcus aureus-(CA-MRSA) strains have emerged in Argentina. We investigated the clinical and molecular evolution of community-onset MRSA infections (CO-MRSA) in children of Córdoba, Argentina, 2005–2008. Additionally, data from 2007 were compared with the epidemiology of these infections in other regions of the country. Methodology/Principal Findings Two datasets were used: i) lab-based prospective surveillance of CA-MRSA isolates from 3 Córdoba pediatric hospitals-(CBAH1-H3) in 2007–2008 (compared to previously published data of 2005) and ii) a sampling of CO-MRSA from a study involving both, healthcare-associated community-onset-(HACO) infections in children with risk-factors for healthcare-associated infections-(HRFs), and CA-MRSA infections in patients without HRFs detected in multiple centers of Argentina in 2007. Molecular typing was performed on the CA-MRSA-(n: 99) isolates from the CBAH1-H3-dataset and on the HACO-MRSA-(n: 51) and CA-MRSA-(n: 213) isolates from other regions. Between 2005–2008, the annual proportion of CA-MRSA/CA-S. aureus in Córdoba hospitals increased from 25% to 49%, P<0.01. Total CA-MRSA infections increased 3.6 fold-(5.1 to 18.6 cases/100,000 annual-visits, P<0.0001), associated with an important increase of invasive CA-MRSA infections-(8.5 fold). In all regions analyzed, a single genotype prevailed in both CA-MRSA (82%) and HACO-MRSA(57%), which showed pulsed-field-gel electrophoresis-(PFGE)-type-“I”, sequence-type-5-(ST5), SCCmec-type-IVa, spa-t311, and was positive for PVL. The second clone, pulsotype-N/ST30/CC30/SCCmecIVc/t019/PVL+, accounted for 11.5% of total CA-MRSA infections. Importantly, the first 4 isolates of Argentina belonging to South American-USA300 clone-(USA300/ST8/CC8/SCCmecIVc/t008/PVL+/ACME？) were detected. We also demonstrated that a HA-MRSA clone-(pulsotype-C/ST100/CC5) caused 2% and 10% of CA-MRSA and HACO-MRSA infections respectively and was associated with a SCCmec type closely related to SCCmecIV(2B&5). Conclusions/Significance The dissemination of epidemic MRSA clone, ST5-IV-PVL+ was the main cause of increasing staphylococcal community-onset infections in Argentinean children (2003–2008), conversely to other countries. The predominance of this clone, which has capacity to express the h-VISA phenotype, in healthcare-associated community-onset cases suggests that it has infiltrated into hospital-settings.
References
[1]
David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23: 616–87.
[2]
Deurenberg RH, Stobberingh EE (2009) The molecular evolution of hospital- and community-associated methicillin-resistant Staphylococcus aureus. Curr Mol Med 9: 100–15.
[3]
Deleo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557–68.
[4]
Limbago B, Fosheim GE, Schoonover V, Crane CE, Nadle J, et al. (2009) Characterization of methicillin-resistant Staphylococcus aureus isolates collected in 2005 and 2006 from patients with invasive disease: a population-based analysis. J Clin Microbiol 47: 1344–51.
[5]
Gonzalez BE, Martinez-Aguilar G, Hulten KG, Hammerman WA, Coss-Bu J, et al. (2005) Severe Staphylococcal sepsis in adolescents in the era of community-acquired methicillin-resistant Staphylococcus aureus. Pediatrics 115: 642–8.
[6]
Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML (2010) Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23: 99–139.
[7]
Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, et al. (2011) Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis 52: e18–55.
[8]
Gerber JS, Coffin SE, Smathers SA, Zaoutis TE (2009) Trends in the incidence of methicillin-resistant Staphylococcus aureus infection in children's hospitals in the United States. Clin Infect Dis 49: 65–71.
[9]
David MZ, Glikman D, Crawford SE, Peng J, King KJ, et al. (2008) What is community-associated methicillin-resistant Staphylococcus aureus? J Infect Dis 197: 1235–43.
Ma XX, Galiana A, Pedreira W, Mowszowicz M, Christophersen I, et al. (2005) Community-acquired methicillin-resistant Staphylococcus aureus, Uruguay. Emerg Infect Dis 11: 973–6.
[12]
Sola C, Saka HA, Vindel A, Bocco JL, Cordoba MRSA Collaborative Study Group (2008) Emergence and dissemination of a community-associated methicillin-resistant Panton-Valentine leukocidin-positive Staphylococcus aureus clone sharing the sequence type 5 lineage with the most prevalent nosocomial clone in the same region of Argentina. J Clin Microbiol 46: 1826–31.
[13]
Gardella N, von Specht M, Cuirolo A, Rosato A, Gutkind G, et al. (2008) Community-associated methicillin-resistant Staphylococcus aureus, eastern Argentina. Diagn Microbiol Infect Dis 62: 343–7.
[14]
Reyes J, Rincon S, Diaz L, Panesso D, Contreras GA, et al. (2009) Dissemination of methicillin-resistant Staphylococcus aureus USA300 sequence type 8 lineage in Latin America. Clin Infect Dis 49: 1861–7.
[15]
Sola C, Cortes P, Saka HA, Vindel A, Bocco JL (2006) Evolution and molecular characterization of methicillin-resistant Staphylococcus aureus epidemic and sporadic clones in Cordoba, Argentina. J Clin Microbiol 44: 192–200.
[16]
Paganini H, Della Latta MP, Muller Opet B, Ezcurra G, Uranga M, et al. (2008) [Community-acquired methicillin-resistant Staphylococcus aureus infections in children: multicenter trial]. Arch Argent Pediatr 106: 397–403.
[17]
Rodriguez-Noriega E, Seas C, Guzman-Blanco M, Mejia C, Alvarez C, et al. (2010) Evolution of methicillin-resistant Staphylococcus aureus clones in Latin America. Int J Infect Dis 14: e560–6.
[18]
Chua K, Laurent F, Coombs G, Grayson ML, Howden BP (2011) Antimicrobial resistance: Not community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA)! A clinician's guide to community MRSA - its evolving antimicrobial resistance and implications for therapy. Clin Infect Dis 52: 99–114.
[19]
Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, et al. (2011) A Field Guide to Pandemic, Epidemic and Sporadic Clones of Methicillin-Resistant Staphylococcus aureus. PLoS One 6(4): e17936.
[20]
Kaplan SL, Hulten KG, Gonzalez BE, Hammerman WA, Lamberth L, et al. (2005) Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin Infect Dis 40: 1785–91.
[21]
Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763–71.
[22]
Morrison MA, Hageman JC, Klevens RM (2006) Case definition for community-associated methicillin-resistant Staphylococcus aureus. J Hosp Infect 62: 241.
[23]
Klevens RM, Morrison MA, Fridkin SK, Reingold A, Petit S, et al. (2006) Community-associated methicillin-resistant Staphylococcus aureus and healthcare risk factors. Emerg Infect Dis 12: 1991–3.
[24]
Goldstein B, Giroir B, Randolph A (2005) International pediatric sepsis consensus conference: definitions for sepsis and organ dysfunction in pediatrics. Pediatr Crit Care Med 6: 2–8.
[25]
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing Nineteenth Informational Supplement M100-S19. 2009, Wayne, Pennsylvania, USA: CLSI.
[26]
Wootton M, MacGowan AP, Walsh TR, Howe AR (2007) A multicenter study evaluating the current strategies for isolating Staphylococcus aureus strains with reduced susceptibility to glycopeptides. J Clin Microbiol 45: 329–32.
Satola SW, Farley MM, Anderson KF, Patel JB (2010) Comparison of Detection Methods for Heteroresistant Vancomycin Intermediate Staphylococcus aureus (hVISA) using Population Analysis Profile as the Reference Method. J Clin Microbiol 49(1): 177–83.
[29]
Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38: 1008–15.
[30]
Harmsen D, Claus H, Witte W, Rothganger J, Claus H, et al. (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41: 5442–8.
[31]
Milheirico C, Oliveira DC, de Lencastre H (2007) Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51: 3374–7.
[32]
Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, et al. (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40: 4289–94.
[33]
Milheirico C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: ‘SCCmec IV multiplex’. J Antimicrob Chemother 60: 42–8.
[34]
Oliveira DC, Milheirico C, de Lencastre H (2006) Redefining a structural variant of staphylococcal cassette chromosome mec, SCCmec type VI. Antimicrob Agents Chemother 50: 3457–9.
[35]
Heusser R, Ender M, Berger-Bachi B, McCallum N (2007) Mosaic staphylococcal cassette chromosome mec containing two recombinase loci and a new mec complex, B2. Antimicrob Agents Chemother 51: 390–3.
[36]
Corso A, Santos Sanches I, Aires de Sousa M, Rossi A, de Lencastre H (1998) Spread of a methicillin-resistant and multiresistant epidemic clone of Staphylococcus aureus in Argentina. Microb Drug Resist 4: 277–88.
[37]
Sola C, Gribaudo G, Vindel A, Patrito L, Bocco JL (2002) Identification of a novel methicillin-resistant Staphylococcus aureus epidemic clone in Cordoba, Argentina, involved in nosocomial infections. J Clin Microbiol 40: 1427–35.
[38]
Orscheln RC, Hunstad DA, Fritz SA, Loughman JA, Mitchell K, et al. (2009) contribution of genetically restricted, methicillin-susceptible strains to the ongoing epidemic of community-acquired Staphylococcus aureus infections. Clin Infect Dis 49: 536–42.
[39]
Tokumoto MB, Ybarra V, Torreno M, Rodriguez M, Ramirez MS, et al. (2007) Emergence of community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) paediatric clone among skin and soft-tissue infections in Buenos Aires. Int J Antimicrob Agents 30: 469–71.
[40]
Niniou I, Vourli S, Lebessi E, Foustoukou M, Vatopoulos A, et al. (2008) Clinical and molecular epidemiology of community-acquired, methicillin-resistant Staphylococcus aureus infections in children in central Greece. Eur J Clin Microbiol Infect Dis 27: 831–7.
[41]
Zaoutis TE, Toltzis P, Chu J, Abrams T, Dul M, et al. (2006) Clinical and molecular epidemiology of community-acquired methicillin-resistant Staphylococcus aureus infections among children with risk factors for health care-associated infection: 2001–2003. Pediatr Infect Dis J 25: 343–8.
[42]
Nubel U, Roumagnac P, Feldkamp M, Song JH, Ko KS, et al. (2008) Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 105: 14130–5.
[43]
Sola C, Saka HA, Vindel A, Bocco JL, Cordoba S. aureus Collaborative Study Group (2007) High frequency of Panton-Valentine leukocidin genes in invasive methicillin-susceptible Staphylococcus aureus strains and the relationship with methicillin-resistant Staphylococcus aureus in Cordoba, Argentina. Eur J Clin Microbiol Infect Dis 26: 281–286.
[44]
Breurec S, Zriouil SB, Fall C, Boisier P, Brisse S, et al. (2011) Epidemiology of methicillin-resistant Staphylococcus aureus lineages in five major African towns: emergence and spread of atypical clones. Clin Microbiol Infect 17: 160–5.
[45]
Ellington MJ, Perry C, Ganner M, Warner M, McCormick Smith I, et al. (2009) Clinical and molecular epidemiology of ciprofloxacin-susceptible MRSA encoding PVL in England and Wales. Eur J Clin Microbiol Infect Dis 28: 1113–21.
[46]
Tristan A, Bes M, Meugnier H, Lina G, Bozdogan B, et al. (2007) Global Distribution of Panton-Valentine Leukocidin-positive Methicillin-resistant Staphylococcus aureus, 2006. Emerg Infect Dis 13: 594–600.
[47]
Bhattacharya D, Carleton H, Tsai CJ, Baron EJ, Perdreau-Remington F (2007) Differences in clinical and molecular characteristics of skin and soft tissue methicillin-resistant Staphylococcus aureus isolates between two hospitals in Northern California. J Clin Microbiol 45: 1798–803.
[48]
Rossney AS, Shore AC, Morgan PM, Fitzgibbon MM, O'connell B, et al. (2007) The Emergence and Importation of Diverse Genotypes of MRSA Harboring the Panton-Valentine Leukocidin Gene pvl Reveals that pvl is a Poor Marker for Community-Acquired MRSA in Ireland. J Clin Microbiol 45: 2554–63.
[49]
Monecke S, Berger-Bachi B, Coombs G, Holmes A, Kay I, et al. (2007) Comparative genomics and DNA array-based genotyping of pandemic Staphylococcus aureus strains encoding Panton-Valentine leukocidin. Clin Microbiol Infect 13: 236–49.
[50]
Dauwalder O, Lina G, Durand G, Bes M, Meugnier H, et al. (2008) Epidemiology of invasive methicillin-resistant Staphylococcus aureus clones collected in France in 2006 and 2007. J Clin Microbiol 46: 3454–8.
[51]
Benoit SR, Estivariz C, Mogdasy C, Pedreira W, Galiana A, et al. (2008) Community Strains of Methicillin-Resistant Staphylococcus aureus as Potential Cause of Healthcare-associated Infections, Uruguay, 2002–2004. Emerg Infect Dis 14: 1216–23.
[52]
Monecke S, Ehricht R, Slickers P, Tan HL, Coombs G (2009) The molecular epidemiology and evolution of the Panton-Valentine leukocidin-positive, methicillin-resistant Staphylococcus aureus strain USA300 in Western Australia. Clin Microbiol Infect 15: 770–6.
[53]
Blanco R, Tristan A, Ezpeleta G, Larsen AR, Bes M, et al. (2011) Molecular epidemiology of Panton-Valentine leukocidin-positive Staphylococcus aureus in Spain: emergence of the USA300 clone in an autochthonous population. J Clin Microbiol 49: 433–6.
[54]
Cercenado E, Cuevas O, Marin M, Bouza E, Trincado P, et al. (2008) Community-acquired methicillin-resistant Staphylococcus aureus in Madrid, Spain: transcontinental importation and polyclonal emergence of Panton-Valentine leukocidin-positive isolates. Diagn Microbiol Infect Dis 61: 143–9.
[55]
Sola C, Lamberghini RO, Ciarlantini M, Egea AL, Gonzalez P, et al. (2011) Heterogeneous vancomycin-intermediate susceptibility in a community-associated methicillin-resistant Staphylococcus aureus epidemic clone, in a case of Infective Endocarditis in Argentina. Ann Clin Microbiol Antimicrob 10(1): 15.
