1887

Abstract

Meticillin-resistant (MRSA) is a major nosocomial pathogen in Pakistan and is emerging in the community. This is one of the first reports of the prevalent genotypes of MRSA in both hospital and community settings in Pakistan. Isolates collected in 2006–2007 were characterized by PFGE, staphylococcal cassette chromosome (SCC) typing and multilocus sequence typing (MLST). PFGE identified nine pulsotypes, the majority of isolates belonging to pulsotypes A (=70) and B (=38), which were predominant among hospital-onset MRSA (HO-MRSA) and community-onset MRSA (CO-MRSA) isolates, respectively. Among the HO-MRSA isolates, variants of SCC type III were prevalent, whilst SCC type IV or variants were predominant in the CO-MRSA isolates. MLST identified two principal sequence types, ST8 and ST239. An association was observed between ST8, PFGE pulsotype B and SCC type IV in the CO-MRSA (ST8-MRSA-IV). Similarly, ST239, PFGE pulsotype A and SCC type III were associated with HO-MRSA (ST239-MRSA-III). Therefore, the prevalent genotypes circulating in Pakistan at the time of study were ST8-MRSA-IV and ST239-MRSA-III in the community and hospital settings, respectively. A set of HO-MRSA isolates collected in 1997 were characterized by PFGE and SCC typing for comparison. The isolates belonged to two PFGE pulsotypes (A, =28; B, =11) and contained just two SCC types. These results suggest that an increase in genetic diversity occurred over the period 1997–2007 as a result of either microevolution or the importation of strains from surrounding areas.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.022707-0
2011-01-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/jmm/60/1/56.html?itemId=/content/journal/jmm/10.1099/jmm.0.022707-0&mimeType=html&fmt=ahah

References

  1. Aires de Sousa, M., de Lencastre, H., Santos Sanches, I., Kikuchi, K., Totsuka, K. & Tomasz, A. ( 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]
    [Google Scholar]
  2. Aires de Sousa, M., Correia, B. & de Lencastre, H. ( 2008; ). Temporal waves in the frequency of five MRSA clones in Portuguese hospitals – surveillance over a 16-year period. J Clin Microbiol 46, 2912–2917.[CrossRef]
    [Google Scholar]
  3. Bannerman, T. L., Hancock, G. A., Tenover, F. C. & Miller, J. M. ( 1995; ). Pulsed-field gel electrophoresis as a replacement for bacteriophage typing of Staphylococcus aureus. J Clin Microbiol 33, 551–555.
    [Google Scholar]
  4. Berglund, C., Mölling, P., Sjöberg, L. & Söderquist, B. ( 2005; ). Predominance of staphylococcal cassette chromosome mec (SCCmec) type IV among methicillin-resistant Staphylococcus aureus (MRSA) in a Swedish county and presence of unknown SCCmec types with Panton-Valentine leukocidin genes. Clin Microbiol Infect 11, 447–456.[CrossRef]
    [Google Scholar]
  5. Bogut, A., Kozioł-Montewka, M., Baranowicz, I., Józwiak, L., Al-Doori, Z., Morrison, D., Kaczor, D. & Ksiazek, A. ( 2008; ). Community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) in Poland: further evidence for the changing epidemiology of MRSA. New Microbiol 31, 229–234.
    [Google Scholar]
  6. Branger, C., Gardye, C., Galdbart, J. O., Deschamps, C. & Lambert, N. ( 2003; ). Genetic relationship between methicillin-sensitive and methicillin-resistant Staphylococcus aureus strains from France and from international sources: delineation of genomic groups. J Clin Microbiol 41, 2946–2951.[CrossRef]
    [Google Scholar]
  7. BSAC ( 2008; ). Standardized Disc Susceptibility Testing Method. Version 7.1. British Society for Antimicrobial Chemotherapy.
  8. Butt, T., Ahmed, R. N., Usman, M. & Mahmood, A. ( 2004; ). Methicillin-resistant Staphylococcus aureus, Pakistan 1996–2003. Emerg Infect Dis 10, 1691–1692.[CrossRef]
    [Google Scholar]
  9. Chambers, H. F. ( 2001; ). The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 7, 178–182.[CrossRef]
    [Google Scholar]
  10. Chongtrakool, P., Ito, T., Ma, X. X., Kondo, Y., Trakulsomboon, S., Tiensasitorn, C., Jamklang, M., Chavalit, T., Song, J. H. & Hiramatsu, K. ( 2006; ). Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother 50, 1001–1012.[CrossRef]
    [Google Scholar]
  11. Crisóstomo, M. I., Westh, H., Tomasz, A., Chung, M., Oliveira, D. C. & de Lencastre, H. ( 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, 9865–9870.[CrossRef]
    [Google Scholar]
  12. Das, N., Khan, A. N., Badini, Z. A., Baloch, H. & Parkash, J. ( 2001; ). Prescribing practices of consultants in Karachi, Pakistan. J Pak Med Assoc 51, 74–77.
    [Google Scholar]
  13. Dominguez, M. A., de Lencastre, H., Linares, J. & Tomasz, A. ( 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.
    [Google Scholar]
  14. Enright, M. C., Day, N. P., Davies, C. E., Peacock, S. J. & Spratt, B. G. ( 2000; ). Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38, 1008–1015.
    [Google Scholar]
  15. Enright, M. C., Robinson, D. A., Randle, G., Feil, E. J., Grundmann, H. & Spratt, B. G. ( 2002; ). The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99, 7687–7692.[CrossRef]
    [Google Scholar]
  16. Feil, E. J. & Enright, M. C. ( 2004; ). Analyses of clonality and the evolution of bacterial pathogens. Curr Opin Microbiol 7, 308–313.[CrossRef]
    [Google Scholar]
  17. Fluit, A. C., Wielders, C. L. C., Verhoef, J. & Schmitz, F. J. ( 2001; ). Epidemiology and susceptibility of 3,051 Staphylococcus aureus isolates from 25 university hospitals participating in the European SENTRY Study. J Clin Microbiol 39, 3727–3732.[CrossRef]
    [Google Scholar]
  18. Hafiz, S., Hafiz, A. N., Ali, L., Chughtai, A. S., Memon, B., Ahmed, A., Hussain, S., Sarwar, G., Mughal, T. & other authors ( 2002; ). Methicillin resistant Staphylococcus aureus: a multicentre study. J Pak Med Assoc 52, 312–315.
    [Google Scholar]
  19. Hanssen, A.-M., Kjeldsen, G. & Sollid, J. U. E. ( 2004; ). Local variants of staphylococcal cassette chromosome mec in sporadic methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase negative staphylococci: evidence of horizontal gene transfer? Antimicrob Agents Chemother 48, 285–296.[CrossRef]
    [Google Scholar]
  20. Heym, B., Le Moal, M., Armand-Lefevre, L. & Nicolas-Chanoine, M.-H. ( 2002; ). Multilocus sequence typing (MLST) shows that the ‘Iberian’ clone of methicillin-resistant Staphylococcus aureus has spread to France and acquired reduced susceptibility to teicoplanin. J Antimicrob Chemother 50, 323–329.[CrossRef]
    [Google Scholar]
  21. Huang, Y. C., Su, L. H., Wu, T. L. & Lin, T. Y. ( 2006; ). Changing molecular epidemiology of methicillin-resistant Staphylococcus aureus bloodstream isolates from a teaching hospital in Northern Taiwan. J Clin Microbiol 44, 2268–2270.[CrossRef]
    [Google Scholar]
  22. Ichiyama, S., Ohta, M., Shimokata, K., Kato, N. & Takeuchi, J. ( 1991; ). Genomic DNA fingerprinting by pulsed-field gel electrophoresis as an epidemiological marker for study of nosocomial infections caused by methicillin-resistant Staphylococcus aureus. J Clin Microbiol 29, 2690–2695.
    [Google Scholar]
  23. Ito, T., Katayama, Y., Asada, K., Mori, N., Tsutsuminmoto, K., Tiensasitorn, C. & Hiramatsu, K. ( 2001; ). Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45, 1323–1336.[CrossRef]
    [Google Scholar]
  24. Ito, T., Okuma, K., Ma, X. X., Yuzawa, H. & Hiramatsu, K. ( 2003; ). Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Updat 6, 41–52.[CrossRef]
    [Google Scholar]
  25. Ito, T., Ma, X. X., Takeuchi, F., Okuma, K., Yuzawa, H. & Hiramatsu, K. ( 2004; ). Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48, 2637–2651.[CrossRef]
    [Google Scholar]
  26. Johnson, A. P., Aucken, H. M., Cavendish, S., Ganner, M., Wale, M. C. J., Warner, M., Livermore, D. M. & Cookson, B. D., the UK EARSS Participants ( 2001; ). Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). J Antimicrob Chemother 48, 143–144.[CrossRef]
    [Google Scholar]
  27. Ko, K. S., Lee, J. Y., Suh, J. Y., Oh, W. S., Peck, K. R., Lee, N. Y. & Song, J. H. ( 2005; ). Distribution of major genotypes among methicillin-resistant Staphylococcus aureus clones in Asian countries. J Clin Microbiol 43, 421–426.[CrossRef]
    [Google Scholar]
  28. Łuczak-Kadłubowska, A., Sulikowska, A., Empel, J., Piasecka, A., Orczykowska, M., Kozinska, A. & Hryniewicz, W. ( 2008; ). Countrywide molecular survey of methicillin-resistant Staphylococcus aureus strains in Poland. J Clin Microbiol 46, 2930–2937.[CrossRef]
    [Google Scholar]
  29. Ma, X. X., Ito, T., Tiensasitorn, C., Jamklang, M., Chongtrakool, P., Boyle-Vavra, S., Daum, R. S. & Hiramatsu, K. ( 2002; ). Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 46, 1147–1152.[CrossRef]
    [Google Scholar]
  30. Maiden, M. C. J., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K. & other authors ( 1998; ). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95, 3140–3145.[CrossRef]
    [Google Scholar]
  31. McDougal, L. K., Steward, C. D., Killgore, G. E., Chaitram, J. M., McAllister, S. K. & Tenover, F. C. ( 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.[CrossRef]
    [Google Scholar]
  32. Murakami, K., Minamide, W., Wada, K., Nakamura, E., Teraoka, H. & Watanabe, S. ( 1991; ). Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 29, 2240–2244.
    [Google Scholar]
  33. NCCLS ( 2004; ). Performance Standards for Antimicrobial Susceptibility Testing; Fourteenth Informational Supplement. M100-S14. Wayne, PA: National Committee for Clinical Laboratory Standards.
  34. Okuma, K., Iwakawa, K., Turnidge, J. D., Grubb, W. B., Bell, J. M., O'Brien, F. G., Coombs, G. W., Pearman, J. W., Tenover, F. C. & other authors ( 2002; ). Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40, 4289–4294.[CrossRef]
    [Google Scholar]
  35. Oliveira, D. C. & de Lencastre, H. ( 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]
    [Google Scholar]
  36. Otter, J. A. & French, G. L. ( 2006; ). Nosocomial transmission of community-associated methicillin resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis 6, 753–755.[CrossRef]
    [Google Scholar]
  37. Pérez-Roth, E., Lorenzo-Díaz, F., Batista, N., Moreno, A. & Méndez-Alvarez, S. ( 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.[CrossRef]
    [Google Scholar]
  38. Perwaiz, S., Barakzi, Q., Farooqi, B. J., Khursheed, N. & Sabir, N. ( 2007; ). Antimicrobial susceptibility pattern of clinical isolates of methicillin resistant Staphylococcus aureus. J Pak Med Assoc 57, 2–4.
    [Google Scholar]
  39. Robinson, D. A. & Enright, M. C. ( 2004; ). Evolution of Staphylococcus aureus by large chromosomal replacements. J Bacteriol 186, 1060–1064.[CrossRef]
    [Google Scholar]
  40. Sá-Leão, R., Santos Sanches, I., Dias, D., Peres, I., Barros, R. M. & de Lencastre, H. ( 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.
    [Google Scholar]
  41. Shabir, S., Hardy, K. J., Abbasi, W. S., McMurray, C. L., Malik, S. A. & Hawkey, P. M. ( 2010; ). Epidemiological typing of meticillin-resistant Staphylococcus aureus from Pakistan and India. J Med Microbiol 59, 330–337.[CrossRef]
    [Google Scholar]
  42. Shopsin, B., Gomez, M., Montgomery, S. O., Smith, D. H., Waddington, M., Dodge, D. E., Bost, D. A., Riehman, M., Naidich, S. & Kreiswirth, B. N. ( 1999; ). Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37, 3556–3563.
    [Google Scholar]
  43. Shopsin, B., Gomez, M., Waddington, M., Riehman, M. & Kreiswirth, B. N. ( 2000; ). Use of coagulase gene (coa) repeat region nucleotide sequences for typing of methicillin-resistant Staphylococcus aureus strains. J Clin Microbiol 38, 3453–3456.
    [Google Scholar]
  44. Shore, A., Rossney, A. S., Keane, C. T., Enright, M. C. & Coleman, D. C. ( 2005; ). Seven novel variants of the staphylococcal chromosomal cassette mec in methicillin-resistant Staphylococcus aureus isolates from Ireland. Antimicrob Agents Chemother 49, 2070–2083.[CrossRef]
    [Google Scholar]
  45. Shukla, S. K., Stemper, M. E., Ramaswamy, S. V., Conradt, J. M., Reich, R., Graviss, E. A. & Reed, K. D. ( 2004; ). Molecular characteristics of nosocomial and Native American community-associated methicillin-resistant Staphylococcus aureus clones from rural Wisconsin. J Clin Microbiol 42, 3752–3757.[CrossRef]
    [Google Scholar]
  46. Siddiqi, S., Hamid, S., Rafique, G., Chaudhry, S. A., Ali, N., Shahab, S. & Sauerborn, R. ( 2002; ). Prescription practices of public and private health care providers in Attock District of Pakistan. Int J Health Plann Manage 17, 23–40.[CrossRef]
    [Google Scholar]
  47. Struelens, M. J., Deplano, A., Godard, C., Maes, N. & Serruys, E. ( 1992; ). Epidemiologic typing and delineation of genetic relatedness of methicillin-resistant Staphylococcus aureus by macrorestriction analysis of genomic DNA by using pulsed-field gel electrophoresis. J Clin Microbiol 30, 2599–2605.
    [Google Scholar]
  48. Tai, P. W., Huang, C. H., Lin, Q. D. & Huang, Y. Y. ( 2006; ). Molecular pattern and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolates at a teaching hospital in Northern Taiwan. J Microbiol Immunol Infect 39, 225–230.
    [Google Scholar]
  49. Takizawa, Y., Taneike, I., Nakagawa, S., Oishi, T., Nitahara, Y., Iwakura, N., Ozaki, K., Takano, M., Nakayama, T. & Yamamoto, T. ( 2005; ). A Panton-Valentine leucocidin (PVL)-positive community-acquired methicillin-resistant Staphylococcus aureus (MRSA) strain, another such strain carrying a multiple-drug resistance plasmid, and other more-typical PVL-negative MRSA strains found in Japan. J Clin Microbiol 43, 3356–3363.[CrossRef]
    [Google Scholar]
  50. Teixeira, L. A., Resende, C. A., Ormonde, L. R., Rosenbaum, R., Figueiredo, A. M. S., de Lencastre, H. & Tomasz, A. ( 1995; ). Geographic spread of epidemic multiresistant Staphylococcus aureus clone in Brazil. J Clin Microbiol 33, 2400–2404.
    [Google Scholar]
  51. Tenover, F. C., Arbeit, R. D., Goering, R. V., Mickelsen, P. A., Murray, B. E., Persing, D. H. & 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.
    [Google Scholar]
  52. Vandenesch, F., Naimi, T., Enright, M. C., Lina, G., Nimmo, G. R., Heffernan, H., Liassine, N., Bes, M., Greenland, T. & other authors ( 2003; ). Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9, 978–984.[CrossRef]
    [Google Scholar]
  53. Wang, J. T., Chen, Y. C., Yang, T. L. & Chang, S. C. ( 2002; ). Molecular epidemiology and antimicrobial susceptibility of methicillin resistant Staphylococcus aureus in Taiwan. Diagn Microbiol Infect Dis 42, 199–203.[CrossRef]
    [Google Scholar]
  54. Witte, W., Cuny, C., Halle, E. & Wagner, J. ( 1994; ). Methicillin resistance in an epidemic Staphylococcus aureus strain with genomic fingerprints corresponding to those of a sensitive strain in the community. Med Microbiol Lett 3, 388–395.
    [Google Scholar]
  55. Zafar, S. N., Syed, R., Waqar, S., Irani, F. A. & Saleem, S. ( 2008; ). Prescription of medicines by medical students of Karachi, Pakistan: a cross-sectional study. BMC Public Health 8, 162.[CrossRef]
    [Google Scholar]
  56. Zhang, K., McClure, J.-A., Elsayed, S., Louie, T. & Conly, J. 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]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.022707-0
Loading
/content/journal/jmm/10.1099/jmm.0.022707-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error