Clonal complexes and diversity of exotoxin gene profiles in methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from patients in a Spanish hospital

Journal of Clinical Microbiology

Volumn 47, Issue 7, 2009, Pages 2097-2105

  Argudin M A ^a   Mendoza, M C ^a   Mendez F J ^a,b   Martin M C ^c   Guerra, B ^d   Rodicio, M R ^a,e  

^a DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^b HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^c DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^d FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^e Inst U   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EXFOLIATIN; EXOTOXIN; HEMOLYSIN; LEUKOTOXIN; STAPHYLOCOCCUS TOXIN;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE CLUSTER; GENETIC VARIABILITY; GENOTYPE; HUMAN; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PRIORITY JOURNAL; SEPSIS; SPAIN; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS AUREUS;

EID: 67650082455     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.01486-08     Document Type: Article

References (60)

1. Aires de Sousa, M., T. Conceição, C. Simas, and H. de Lencastre. 2005. Comparison of genetic backgrounds of methicillin-resistant and -susceptible Staphylococcus aureus isolates from Portuguese hospitals and the community. J. Clin. Microbiol. 43:5150-5157.
2. Asensio, A., R. Canton, J. Vaque, J. Rossello, F. Calbo, J. Garcia-Caballero, V. Dominguez, A. Hernandez, A. Trilla, and EPINE Working Group. 2006. Nosocomial and community-acquired methicillin-resistant Staphylococcus aureus infections in hospitalized patients (Spain, 1993-2003). J. Hosp. Infect. 63:465-471.
3. Becker, K., A. W. Friedrich, G. Lubritz, M. Weilert, G. Peters, and C. Von Eiff. 2003. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J. Clin. Microbiol. 41:1434-1439.
4. Cookson, B. D., D. A. Robinson, A. B. Monk, S. Murchan, A. Deplano, R. de Ryck, M. J. Struelens, C. Scheel, V. Fussing, S. Salmenlinna, J. Vuopio-Varkila, C. Cuny, W. Witte, P. T. Tassios, N. J. Legakis, W. van Leeuwen, A. van Belkum, A. Vindel, J. Garaizar, S. Haeggman, B. Olsson-Liljequist, U. Ransjo, M. Muller-Premru, W. Hryniewicz, A. Rossney, B. O'Connell, B. D. Short, J. Thomas, S. O'Hanlon, and M. C. Enright. 2007. Evaluation of molecular typing methods in characterizing a European collection of epidemic methicillin-resistant Staphylococcus aureus strains: the HARMONY collection. J. Clin. Microbiol. 45:1830-1837.
5. Cuevas, O., E. Cercenado, E. Bouza, C. Castellares, P. Trincado, R. Cabrera, A. Vindel, and Spanish Group for the Study of Staphylococcus. 2007. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Spain: a multicentre prevalence study (2002). Clin. Microbiol. Infect. 13:250-256.
6. Dauwalder, O., G. Lina, G. Durand, M. Bes, H. Meugnier, V. Jarlier, B. Coignard, F. Vandenesch, J. Etiene, and F. Laurent. 2008. Epidemiology of invasive methicillin-resistant Staphylococcus aureus clones collected in France in 2006 and 2007. J. Clin. Microbiol. 46:3454-3458.
7. Deurenberg, R. H., and E. E. Stobbering. 2008. The evolution of Staphylococcus aureus. Infect. Genet. Evol. 8:747-763.
8. Dinges, M. M., P. M. Orwin, and M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13:16-34.
9. Enright, M. C., N. P. Day, C. E. Davis, S. J. Peacock, and B. G. Spratt. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38:1008-1015.
10. Faria, N. A., J. A. Carrico, D. C. Oliveira, M. Ramirez, and H. de Lencastre. 2008. Analysis of typing methods for epidemiological surveillance of both methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. J. Clin. Microbiol. 46:136-144.
11. Feng, Y., C.-J. Chen, L.-H. Su, S. Hu, J. Yu, and C.-H. Chiu. 2008. Evolution and pathogenesis of Staphylococcus aureus: lessons learned from genotyping and comparative genomics. FEMS Microbiol. Rev. 32:23-37.
12. Ferry, T., T. Perpoint, F. Vandenesch, and J. Etienne. 2005. Virulence determinants in Staphylococcus aureus and their involvement in clinical syndromes. Curr. Infect. Dis. Rep. 7:420-428.
13. Fossum, A. E., and G. Butcholm. 2006. Increased incidence of methicillin-resistant Staphylococcus aureus ST80, novel ST125 and SCCmecIV in the south-eastern part of Norway during a 12-year period. Clin. Microbiol. Infect. 12:627-633.
14. Fraser, J. D., and T. Proft. 2008. The bacterial superantigen and superantigen-like proteins. Inmunol. Rev. 225:226-243.
15. Fueyo, J. M., M. C. Mendoza, M. A. Alvarez, and M. C. Martin. 2005. Relationships between toxin gene content and genetic background in nasal carried isolates of Staphylococcus aureus from Asturias, Spain. FEMS Microbiol. Lett. 243:447-454.
16. Fueyo, J. M., M. C. Mendoza, M. R. Rodicio, J. Muñiz, M. A. Alvarez, and M. C. Martin. 2005. Cytotoxin and pyrogenic toxin superantigen gene profiles of Staphylococcus aureus associated with subclinical mastitis in dairy cows and relationships with macrorestriction genomic profiles. J. Clin. Microbiol. 43:1278-1284.
17. Gomes, A. R., H. Westh, and H. de Lencastre. 2006. Origins and evolution of methicillin-resistant Staphylococcus aureus clonal lineages. Antimicrob. Agents Chemother. 50:3237-3244.
18. Grundmann, H., S. Hori, M. C. Enright, C. Webster, A. Tami, E. J. Feil, and T. Pitt. 2002. Determining the genetic structure of the natural population of Staphylococcus aureus: a comparison of multilocus sequence typing with pulsed-field gel electrophoresis, randomly amplified polymorphic DNA analysis, and phage typing. J. Clin. Microbiol. 40:4544-4546.
19. Hallin, M., O. Denis, A. Deplano, R. De Mendonça, R. De Ryck, S. Rottiers, and M. J. Struelens. 2007. Genetic relatedness between methicillin-susceptible and methicillin-resistant Staphylococcus aureus: results of a national survey. J. Antimicrob. Chemother. 59:465-472.
20. Hallin, M., A. Deplano, O. Denis, R. De Mendonça, R. De Ryck, and M. J. Strudels. 2007. Validation of pulsed-field gel electrophoresis and spa typing for long-term, nationwide epidemiological surveillance studies of Staphylococcus aureus infections. J. Clin. Microbiol. 45:127-133.
21. Hisata, K., K. Kuwahara-Arai, M. Yamanoto, T. Ito, Y. Nakatomi, L. Cui, T. Baba, M. Terasawa, C. Sotozono, S. Kinoshita, Y. Yamashiro, and K. Hiramatsu. 2005. Dissemination of methicillin-resistant staphylococci among healthy Japanese children. J. Clin. Microbiol. 43:3364-3372.
22. Holtfreter, S., D. Grumann, M. Schmudde, H. T. T. Nguyen, P. Eichler, B. Strommenger, K. Kopron, J. Kotola, S. Giedrys-Kalemba, I. Steinmetz, W. White, and B. M. Bröker. 2007. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J. Clin. Microbiol. 45:2669-2680.
23. Ito, T., Y. Katayama, and K. Hiramatsu. 1999. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob. Agents Chemother. 43:1449-1458.
24. Ito, T., Y. Katayama, K. Asada, N. Mori, K. Tsutsumimoto, C. Tiensasitorn, and K. Hiramatsu. 2001. Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome of MRSA strains in the world. Antimicrob. Agents Chemother. 45:1323-1336.
25. Ito, T., X. X. Ma, F. Takeuchi, K. Okuma, H. Yuzawa, and K. Hiramatsu. 2004. Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob. Agents Chemother. 48:2637-2651.
26. Jarraud, S., G. J. Lyon, A. M. Figueiredo, G. Lina, F. Vandenesch, J. Etienne, T. W. Muir, and R. P. Novick. 2000. Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J. Bacteriol. 182:6517-6522.
27. Jarraud, S., M. A. Peyrat, A. Lim, A. Tristan, M. Bes, C. Mougel, J. Etienne, F. Vandenesch, M. Bonneville, and G. Lina. 2001. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J. Immunol. 166:669-677.
28. Ji, G., R. Beavis, and R. P. Novick. 1997. Bacterial interference caused by autoinducing peptide variants. Science 276:2027-2030.
29. Kaneko, J., and Y. Kamio. 2004. Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: structures, pore-forming mechanism, and organization of the genes. Biosci. Biotechnol. Biochem. 68:981-1003.
30. Katayama, Y., T. Ito, and K. Hiramatsu. 2000. A new class of genetic element, staphylococcal cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 44:1549-1555.
31. Kwon, N. H., K. T. Park, J. S. Moon, W. K. Jung, S. H. Kim, J. M. Kim, S. K. Hong, H. C. Koo, Y. S. Joo, and Y. H. Park. 2005. Staphylococcal cassette chromosome mec (SCCmec) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCmec subtype IVg isolated from bovine milk in Korea. J. Antimicrob. Chemother. 56:624-632.
32. Labandeira-Rey, M., F. Couzon, S. Boisset, E. L. Brown, M. Bes, Y. Benito, E. M. Barbu, V. Vazquez, M. Höök, J. Etienne, F. Vandenesch, and M. G. Bowden. 2007. Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315:1130-1133.
33. Letertre, C., S. Perelle, F. Dilasser, and P. Fach. 2003. Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J. Appl. Microbiol. 95:38-43.
34. Lindsay, J. A., and M. T. G. Holden. 2004. Staphylococcus aureus: superbug, super genome? Trends Microbiol. 12:378-385.
35. Lindsay, J. A., C. E. Moore, N. P. Day, S. J. Peacock, A. A. Witney, R. A. Stabler, S. E. Husain, P. D. Butcher, and J. Hinds. 2006. Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J. Bacteriol. 188: 669-676.
36. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
37. Lyon, G. J., and R. P. Novick. 2004. Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25:1389-1403.
38. Ma, X. X., T. Ito, C. Tiensasitorn, M. Jamklang, P. Chongtrakool, S. Boyle-Vavra, R. S. Daum, and K. Hiramatsu. 2002. Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob. Agents Chemother. 46: 1147-1152.
39. McClure, J. A., J. M. Conly, V. Lau, S. Elsayed, T. Louie, W. Hutchins, and K. Zhang. 2006. 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. 44:1141-1144.
40. McDougal, L. K., C. D. Steward, G. E. Killgore, J. M. Chaitram, S. K. McAllister, and F. C. Tenover. 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.
41. Moore, P. C. L., and J. A. Lindsay. 2001. Genetic variation among hospital isolates of methicillin-sensitive Staphylococcus aureus: evidence of horizontal transfer of virulence genes. J. Clin. Microbiol. 39:2760-2767.
42. Murchan, S., M. E. Kaufmann, A. Deplano, R. de Ryck, M. Struelens, C. E. Zinn, V. Fussing, S. Salmenlinna, J. Vuopio-Varkila, N. El Solh, C. Cuny, W. Witte, P. T. Tassios, N. Legakis, W. van Leeuwen, A. van Belkum, A. Vindel, I. Laconcha, J. Garaizar, S. Haeggman, B. Olsson-Liljequist, U. Ransjo, G. Coombes, and B. Cookson. 2003. Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J. Clin. Microbiol. 41:1574-1585.
43. Nishifuji, K., M. Sugai, and M. Amagai. 2008. Staphylococcal exfoliative toxins: "molecular scissors" of bacteria that attack the cutaneous defense barrier in mammals. J. Dermatol. Sci. 49:21-31.
44. Nulens, E., E. E. Stobberingh, H. van Dessel, S. Sebastian, F. H. van Tiel, P. B. Beisser, and R. H. Deurenberg. 2008. Molecular characterization of Staphylococcus aureus bloodstream isolates collected in a Dutch university hospital between 1999 and 2006. J. Clin. Microbiol. 46:2438-2441.
45. Oliveira, D. C., A. Tomasz, and H. de Lencastre. 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.
46. Pérez-Roth, E., F. Lorenzo-Díaz, N. Batista, A. Moreno, and S. Méndez-Alvarez. 2004. Tracking methicillin-resistant Staphylococcus aureus clones during a 5-year period (1998 to 2002) in a Spanish hospital. J. Clin. Microbiol. 42:4649-4656.
47. Pérez-Vázquez, M., A. Vindel, C. Marcos, J. Oteo, O. Cuevas, P. Trincado, V. Bautista, H. Grundmann, J. Campos, et al. 2009. Spread of invasive Spanish Staphylococcus aureus spa-type t067 associated with a high prevalence of aminoglycoside-modifying enzyme ant(4′)- Ia and the efflux pump genes mrsA/mrsB. J. Antimicrob. Chem. 63:21-31.
48. Robinson, D. A., and M. C. Enright. 2003. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 47:3926-3934.
49. Sá-Leão, R., I. Santos Sanches, D. Dias, I. Peres, R. M. Barros, and H. de Lencastre. 1999. Detection of an archaic clone of Staphylococcus aureus with low-level resistance to methicillin in a pediatric hospital in Portugal and in international samples: relics of a formerly widely disseminated strain? J. Clin. Microbiol. 37:1913-1920.
50. Shopsin, B., M. Gomez, S. O. Montgomery, D. H. Smith, M. Waddington, D. E. Dodge, D. A. Bost, M. Riehman, S. Naidich, and B. N. Kreiswirth. 1999. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J. Clin. Microbiol. 37:3556-3563.
51. Shore, A., A. S. Rossney, C. T. Keane, M. C. Enright, and D. C. Coleman. 2005. Seven novel variants of the staphylococcal chromosomal cassette mec in methicillin-resistant Staphylococcus aureus isolates from Ireland. Antimicrob. Agents Chemother. 49:2070-2083.
52. Strommenger, B., C. Braulke, D. Heuck, C. Schmidt, B. Pasemann, U. Nubel, and W. Witte. 2008. spa typing of Staphylococcus aureus as a frontline tool in epidemiological typing. J. Clin. Microbiol. 46:574-581.
53. Struelens, M. J., A. Bauernfeind, A. Van Belkum, D. Blanc, B. D. Cookson, L. Dijkshoorn, N. El Solh, J. Etienne, J. Garaizar, P. Gerner-Smidh, N. Legakis, H. de Lencastre, M. H. Nicolas, T. L. Pitt, U. Römling, V. Rosdahl, and W. Witte. 1996. Consensus guidelines for appropriate use and evaluation of microbial epidemiologic typing systems. Clin. Microbiol. Infect. 2:2-11.
54. Takano, T., W. Higuchi, T. Otsuka, T. Baranovich, S. Enany, K. Saito, H. Isobe, S. Dohmae, K. Ozaki, M. Takano, Y. Iwao, M. Shibuya, T. Okubo, S. Yabe, D. Shi, I. Reva, L.-J. Teng, and T. Yamamoto. 2008. Novel characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains belonging to multilocus sequence type 59 in Taiwan. Antimicrob. Agents Chemother. 52:837-845.
55. Tenover, F. C., L. K. McDougal, R. V. Goering, G. Killgore, S. J. Projan, J. B. Patel, and P. M. Dunman. 2006. Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J. Clin. Microbiol. 44:108-118.
56. Vindel, A., P. Trincado, E. Gómez, R. Cabrera, T. Boquete, C. Solá, S. Valdezate, and J. A. Saez-Nieto. 2006. Prevalence and evolution of methicillin resistant Staphylococcus aureus in Spanish hospitals between 1996 and 2002. J. Clin. Microbiol. 44:266-270.
57. Vivoni, A. M., B. A. Diep, A. C. de Gouveia Magalhães, K. R. N. Santos, L. W. Riley, G. F. Sensabaugh, and B. Moreira. 2006. Clonal composition of Staphylococcus aureus isolates at a Brazilian university hospital: identification of international circulating lineages. J. Clin. Microbiol. 44:1686-1691.
58. Voyich, J. M., K. R. Braughton, D. E. Sturdevant, A. R. Whitney, B. Saïd-Salim, S. F. Porcella, R. D. Long, D. W. Dorward, D. J. Gardner, B. N. Kreiswirth, J. M. Musser, and F. R. DeLeo. 2005. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175:3907-3919.
59. Waldron, D. E., and J. A. Lindsay. 2006. SauI: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus of different lineages. J. Bacteriol. 188:5578-5585.
60. Zhang, K., J. A. McClure, E. Sameer, T. Louie, and J. M. Conly. 2005. Novel multiple PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to IV in methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 43:5026-5033.