Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About JCM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Journal of Clinical Microbiology
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About JCM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Epidemiology

Prevalence of Methicillin-Resistant Staphylococcus aureus Nasal Colonization among Taiwanese Children in 2005 and 2006

Yhu-Chering Huang, Kao-Pin Hwang, Po-Yen Chen, Chih-Jung Chen, Tzou-Yien Lin
Yhu-Chering Huang
1Division of Pediatric Infectious Diseases, Chang Gung Children's Hospital and Chang Gung Memorial Hospital at Linko
3College of Medicine, Chang Gung University, Taoyuan, Taiwan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: ychuang@adm.cgmh.org.tw
Kao-Pin Hwang
2Kaohsiung, Taiwan
3College of Medicine, Chang Gung University, Taoyuan, Taiwan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Po-Yen Chen
4Department of Pediatrics, Taichung Veterans General Hospital, Taichung, Taiwan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Chih-Jung Chen
1Division of Pediatric Infectious Diseases, Chang Gung Children's Hospital and Chang Gung Memorial Hospital at Linko
3College of Medicine, Chang Gung University, Taoyuan, Taiwan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tzou-Yien Lin
1Division of Pediatric Infectious Diseases, Chang Gung Children's Hospital and Chang Gung Memorial Hospital at Linko
3College of Medicine, Chang Gung University, Taoyuan, Taiwan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/JCM.01202-07
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

From July 2005 to October 2006, a total of 3,046 children, of ages between 2 months and 5 years, presented for a well-child health care visit to one of three medical centers, which are located in the northern, central, and southern parts of Taiwan, and were surveyed for nasal carriage of methicillin-resistant Staphylococcus aureus (MRSA). The overall prevalences of S. aureus and MRSA nasal carriage among the children were 23% and 7.3%, respectively (18% and 4.8% in the central region, 25% and 6.7% in the southern region, and 27% and 9.5% in the northern region). Of the 212 MRSA isolates (96%) available for analysis, a total of 10 pulsed-field gel electrophoresis (PFGE) patterns with two major patterns (C [61%] and D [28%]) were identified. One hundred forty-nine isolates (70%) contained type IV staphylococcal cassette chromosome mec (SCCmec) DNA, and 55 isolates (26%) contained SCCmec VT. The presence of Panton-Valentine Leukocidin (PVL) genes was detected in 60 isolates (28%). Most MRSA isolates belonged to one of two major clones, characterized as sequence type 59 (ST59)/PFGE C/SCCmec IV/absence of PVL genes (59%) and ST59/PFGE D/SCCmec VT/presence of PVL genes (25%). We concluded that between 2005 and 2006, 7.3% of healthy Taiwanese children were colonized by MRSA in nares. MRSA harbored in healthy children indicates an accelerated spread in the community.

Recent reports indicate that community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) infections are increasing worldwide and may now involve persons without risk factors predisposing them for acquisition (2, 11-14, 20, 24). Asymptomatic CA-MRSA colonization has been documented in healthy children attending the emergency departments and outpatient clinics of children's hospitals (6, 19, 25, 27, 28).

Carriage of S. aureus, including MRSA, is well known to be a significant risk factor for subsequent infection (7, 29), and the anterior nares are the most consistent sites of colonization. The presence of S. aureus nasal colonization can provide an indication of a high risk for subsequent infection.

In Taiwan, previous reports (1, 3, 9, 15, 17, 23, 31) have indicated that during the period from 1997 to 2003, MRSA accounted for 9.8% to 36% of CA S. aureus infections in children without risk factors and the MRSA colonization rate in the general population ranged from 1.9% to ∼3.3% for school children and 5.3% for healthy children presented for health care visits to 10.8% for health care workers and 13.6% for contacts of CA-MRSA infection. It is noteworthy, however, that most of these studies were conducted in the northern part of Taiwan and no island-wide survey has yet been conducted to elucidate this issue. To estimate the extent of MRSA in the community in Taiwan and to assess if there is an increasing trend of MRSA nasal colonization in healthy children during the past 5 years, we conducted this island-wide survey between 2005 and 2006. All collected MRSA isolates were also further characterized by molecular methods.

MATERIALS AND METHODS

This study was approved by the Institutional Review Board of the Chang Gung Memorial Hospital. From July 2005 to October 2006, all children of ages between 2 months and 5 years who presented for a well-child health care visit to any one of three medical centers in Taiwan were invited to participate in this study. The three medical centers involved were the Chang Gung Children's Hospitals at Linko (hospital A) and Kaohsiung (hospital C) and Taichung Veterans General Hospital (hospital B), which are situated, respectively, in northern, southern, and central parts of Taiwan. In each hospital, around 80 subjects were recruited for study for each month, and the ages of the subjects were evenly distributed in seven separate age ranges, which included >2 to 6 months, >6 to 12 months, >12 to 18 months, >18 to 24 months, >2 to 3 years, >3 to 4 years, and >4 to 5 years. A culture from the anterior nares for the detection of MRSA was obtained from each subject after written consent was obtained from their parents/guardians.

Survey specimens for culture were obtained with a cotton swab, placed in the transport medium (Venturi Transystem; Copan Innovation Ltd., Limerick, Ireland), and then brought to and processed in the microbiological laboratories within 4 hours of the sampling. All S. aureus isolates were sent to Chang Gung Memorial Hospital at Linko for microbiological characterization. Identification of MRSA was confirmed according to Clinical and Laboratory Standards Institute 2005 guidelines (5). Pulsed-field gel electrophoresis (PFGE) with SmaI digestion was used in this study to fingerprint the MRSA isolates and was performed according to procedures described previously (3, 16, 18). The genotypes were designated in alphabetical order, as in our previous studies (3, 15-18); any new genotype, if identified, was designated consecutively. PFGE patterns with fewer than four band differences from an existing genotype were defined as subtypes of that genotype.

SCCmec typing of isolates was done using a multiplex PCR strategy described previously (26). Control strains for SCCmec types I, II, III, and IVa, kindly provided by Keiichi Hiramatsu, were as follows: type I, NCTC10442; type II, N315; type III, 85/2082; and type IVa, JCSC4744. SCCmec typing for type VT was determined by using a particular primer described elsewhere (1), and strain TSGH-17, kindly provided by Chi-Chien Wang, was used as a control. However, the SCCmec typing method for type VT yielded inconsistent results; thus, an alternative method was used. The appearance of an isolate with only two bands (414 bp and 243 bp) in the multiplex PCR analysis may have indicated that the isolate contained SCCmec VT. To confirm their identities, a novel pair of primers, ccrC-5F (5′-CAC TTA ATC CAT TGA CAC AG-3′) and ccrC-5R (5′-AAA GAT TGA GGG ATA AGA CT-3′), was designed according to the published sequence (GenBank accession no. AY894416) of the ccrC gene of a Taiwanese strain, S. aureus TSGH-17. Amplification of a specific 1,081-bp DNA fragment, which was subjected to further sequence analysis for some representative isolates in preliminary experiments, confirmed that the isolates contained SCCmec VT.

The presence of Panton-Valentine leukocidin (PVL) genes was determined by a PCR strategy described previously (22). Some isolates of representative PFGE patterns were selected and underwent multilocus sequence typing (MLST) as described elsewhere (8). The allelic profiles were assigned through comparison of the sequences at each locus with those of the known alleles in the S. aureus MLST database and were defined as sequence types accordingly.

RESULTS

During the study period, 1,279 subjects were recruited from hospital A, 1,011 subjects from hospital B (from July 2005 to June 2006), and 756 subjects from hospital C (from October 2005 to June 2006). All the children enrolled are Taiwanese. The number of subjects enrolled in each age group ranged from 430 for children of ages >6 to 12 months to 443 for children of ages >2 to 3 years. Of the total of 3,046 subjects enrolled in this study, 713 (23%) were colonized with S. aureus. Of the 713 isolates, 221 (31%) were demonstrated to be MRSA. The details of the nasal MRSA colonization prevalence for subjects in the different parts of Taiwan are shown in Table 1. The MRSA colonization rate in northern Taiwan was significantly higher than that in the central (P < 0.001) and southern (P < 0.039) parts of Taiwan. The nasal MRSA colonization prevalences for the subjects in each age group were 8.4% for the children of ages >2 to 6 months and 6.3%, 3.2%, 3.9%, 9.0%, 9.5%, and 10.1% for children of ages >6 to 12 months, >12 to 18 months, >18 to 24 months, >2 to 3 years, >3 to 4 years, and >4 to 5 years, respectively. For those less than 18 months of age, the carriage rate decreased with increasing age (P = 0.0011; Mantel-Haenszel test for trend), while for those older than 12 months of age, the carriage rate increased with increasing age (P < 0.0001).

View this table:
  • View inline
  • View popup
TABLE 1.

Nasal carriage of MRSA among infants and children presented for a well-child health care visit in Taiwan

Of the 221 MRSA isolates, 212 isolates were available for analysis. All of these 212 isolates were sensitive to vancomycin and teicoplanin. All but two of the isolates identified from hospital A were resistant to penicillin. Most isolates were resistant to erythromycin and clindamycin but sensitive to trimethoprim-sulfamethoxazole (SXT) and doxycycline. The detailed susceptibility distribution of various antibiotics for the isolates is shown in Table 2. No significant difference in antibiotic susceptibility patterns was noted among the isolates from the three different regions of Taiwan.

View this table:
  • View inline
  • View popup
TABLE 2.

Antibiotic susceptibility rates of 212 colonizing MRSA isolates from children in Taiwan

Table 3 illustrates the detailed distribution of PFGE patterns, SCCmec types, and the presence/absence of PVL genes among these isolates. A total of 10 PFGE patterns were identified. Patterns C and D were the two most common patterns and accounted for 62% and 28% of the isolates analyzed, respectively. The distribution of PFGE patterns among the three regions showed a trend for a difference (P = 0.09 by a log-likelihood contingency test). Four types (types II, III, IV, and VT) of SCCmec genes were identified among the isolates, with type IV (70%) being the predominant type, followed by type VT (26%). The distribution of SCCmec types among the three regions was significantly different (P = 0.03). Four isolates of the AF PFGE pattern were untypeable by the methods used in this study. PVL genes were present in 60 isolates (28%). Twenty-five isolates underwent MLST, and eight sequence types were identified. Sequence type 59 (ST59) was the most common sequence type and accounted for 9 of 10 PFGE type C isolates, 4 of 6 PFGE type D isolates, and the isolate of PFGE type AN. The other two isolates of PFGE type D were ST338, which is a single-locus variant of ST59 (a single nucleotide difference in the gmk locus). The remaining isolate of PFGE type C belonged to a new sequence type, which is a single-locus variant of ST59 (a single nucleotide difference in the pta locus). One isolate of PFGE type F also belonged to a new sequence type, which is also a single-locus variant of ST9 (a single nucleotide difference in the gmk locus). The detailed association of PFGE patterns with sequence types and SCCmec types and the presence of the PVL gene of these isolates are shown in Table 4. The MRSA isolates characterized by ST59/PFGE type C/SCCmec IV/absence of PVL genes and ST59/PFGE type D/SCCmec VT/presence of PVL genes were the two most common clones and accounted for 59% and 25% of the isolates analyzed, respectively.

View this table:
  • View inline
  • View popup
TABLE 3.

Distribution of PFGE patterns, SCCmec types, and presence of PVL genes among 212 colonizing MRSA isolates

View this table:
  • View inline
  • View popup
TABLE 4.

Association of PFGE patterns with MLST, SCCmec types, and presence of PVL genes for 212 MRSA isolates

DISCUSSION

Results from this study indicate that the national prevalence of nasal MRSA colonization among otherwise healthy children in Taiwan was 7.3% during the period from July 2005 to October 2006 inclusively, with values ranging from 4.8% in the central region of Taiwan to 9.5% in the northern region of Taiwan. Compared with those among the healthy children during the period of 2001 to 2002 (1, 17, 23) (Table 5), though the study population was different for these studies, the nasal MRSA colonization prevalence among healthy children in Taiwan increased significantly, from 1.9% in 2001 to 9.5% (P < 0.0001 by chi-square test) during the period of 2005 to 2006 for northern Taiwan and significantly from 3.3% to 6.7% for southern Taiwan (P < 0.001 by chi-square test). This increasing trend of nasal MRSA colonization prevalence might account for the increasing incidence of CA-MRSA infection in children in Taiwan (3, 9, 31). In the United States, where CA-MRSA is also being increasingly reported, the MRSA colonization prevalence for the general population appeared to have been relatively low until the year 2002 (19, 21, 25, 27, 28). In a survey (21) involving 9,622 persons conducted between 2001 and 2002, national S. aureus and MRSA nasal colonization prevalence estimates were 32.4% and 0.8%, respectively. For healthy children, the nasal colonization rates ranged from 0.2% to 2.2% (19, 25, 27, 28), as reported in several pediatric studies; however, an increasing trend in this regard has been noted in certain areas of the United States recently (6). Creech et al. (6) reported that the nasal MRSA colonization rate among healthy children in Nashville, TN, increased significantly from 0.8% in 2001 to 9.2% in 2004, a picture not dissimilar to what we show in the present study from Taiwan.

View this table:
  • View inline
  • View popup
TABLE 5.

Reported prevalence rates of MRSA nasal colonization for healthy Taiwanese children between 2001 and 2006

In the United States, CA-MRSA strains have been recognized as representing a novel pathogen which was genetically different from the nosocomial MRSA strains (14, 24). They have limited antibiotic resistance (except to β-lactams), have two common PFGE patterns (USA 300 and USA 400), possess different exotoxin gene profiles (e.g., PVL), and contain SCCmec DNA (10). In contrast, the CA-MRSA clinical isolates in Taiwan were multiresistant and shared two common PFGE patterns (patterns D and C in this study) (1, 3, 4, 30). In the current study, more than 90% of the MRSA colonization isolates were multiresistant to erythromycin and clindamycin but sensitive to SXT and doxycycline. In addition, most colonization isolates shared common molecular characteristics, and more than 80% of the isolates belonged to one of two major clones, characterized by ST59/PFGE type C/SCCmec IV/absence of PVL genes or ST59/PFGE type D/SCCmec VT/presence of PVL genes. However, among the clinical isolates, the clone characterized by ST59/PFGE type D/SCCmec VT/presence of PVL genes was the dominant clone (1, 3, 30), while among the colonized isolates, the clone characterized by ST59/PFGE type C/SCCmec IV/absence of PVL genes was dominant. It seemed that PVL genes, reported to be a virulence factor associated with necrotizing pneumonia and abscesses (22), may be associated with the ability of a PVL-positive clone to cause infection.

There existed several limitations in the current study. First, the demographic characteristics and the risk factors associated with MRSA acquisition were not analyzed and compared between the children with and without CA-MRSA colonization, though all the children were healthy and presented for health care visits. Living with a family member who works in a hospital or clinic and demographic characteristics (e.g., age and gender) were reported to be associated with an increased risk of MRSA colonization (6, 21, 25). Second, the persistence of MRSA carriage in the subjects could not be determined and the incidence of subsequent MRSA infection in the subjects could not be measured in this cross-sectional analysis of MRSA nasal colonization prevalence.

In summary, 7.3% of healthy children in Taiwan were colonized by MRSA in the nares during the period from 2005 to 2006. MRSA carriage in the children may accelerate the spread in the community. Two major CA-MRSA clones were identified and would appear to have spread island-wide. Further studies are needed to determine the host factors of colonization and to develop strategies to disrupt transmission of CA-MRSA to susceptible hosts.

ACKNOWLEDGMENTS

This study was supported by a grant from National Science Counseling of Executive Yuan of Taiwan (NSC95-2314-B182A-145).

We have no financial relationships relevant to this article to disclose.

FOOTNOTES

    • Received 15 June 2007.
    • Returned for modification 20 August 2007.
    • Accepted 4 October 2007.
  • Copyright © 2007 American Society for Microbiology

REFERENCES

  1. 1.↵
    Boyle-Vavra, S., B. Ereshefsky, C. C. Wang, and R. S. Daum. 2005. Successful multiresistant community-associated methicillin-resistant Staphylococcus aureus lineage from Taipei, Taiwan, that carries either the novel staphylococcal chromosome cassette mec (SCCmec) type VT or SCCmec type IV. J. Clin. Microbiol.43:4719-4730.
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    Chambers, H. F. 2001. The changing epidemiology of Staphylococcus aureus? Emerg. Infect. Dis.7:178-182.
    OpenUrlCrossRefPubMedWeb of Science
  3. 3.↵
    Chen, C. J., Y. C. Huang, C. H. Chiu, L. H. Su, and T. Y. Lin. 2005. Clinical features and genotyping analysis of community-acquired methicillin-resistant Staphylococcus aureus infections in Taiwanese children. Pediatr. Infect. Dis. J.24:40-45.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    Chen, F. J., T. L. Lauderdale, I. W. Huang, et al. 2005. Methicillin-resistant Staphylococcus aureus in Taiwan. Emerg. Infect. Dis.11:1761-1763.
    OpenUrlCrossRef
  5. 5.↵
    Clinical and Laboratory Standards Institute. 2005. Performance standards for antimicrobial disk diffusion susceptibility testings: 15th informational supplement. Clinical and Laboratory Standards Institute, Wayne, PA.
  6. 6.↵
    Creech, C. B., II, D. S. Kernodle, A. Alsentzer, C. Wilson, and K. M. Edwards. 2005. Increasing rates of nasal carriage of methicillin-resistant Staphylococcus aureus in healthy children. Pediatr. Infect. Dis. J.24:617-621.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    Ellis, M. W., D. R. Hospenthal, D. P. Dooley, P. J. Gray, and C. K. Murray. 2004. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin. Infect. Dis.39:971-979.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    Enright, M. C., N. P. Day, C. E. Davies, 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.
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    Fang, Y. H., P. R. Hsueh, J. J. Hu, P. I. Lee, J. M. Chen, C. Y. Lee, et al. 2004. Community-acquired methicillin-resistant Staphylococcus aureus in children in northern Taiwan. J. Microbiol. Immunol. Infect.37:29-34.
    OpenUrlPubMed
  10. 10.↵
    Fey, P. D., B. Said-Salim, M. E. Rupp, S. H. Hinrichs, D. J. Boxrud, C. C. Davis, et al. 2003. Comparative molecular analysis of community- or hospital-acquired methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother.47:196-203.
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    Frank, A. L., J. F. Marcinak, P. D. Mangat, and P. C. Schreckenberger. 1999. Community-acquired and clindamycin-susceptible methicillin-resistant Staphylococcus aureus in children. Pediatr. Infect. Dis. J.18:993-1000.
    OpenUrlCrossRefPubMedWeb of Science
  12. 12.
    Gonzalez, B. E., G. Martinez-Aguilar, K. G. Hulten, W. A. Hammerman, J. Coss-Bu, A. valos-Mishaan, et al. 2005. Severe staphylococcal sepsis in adolescents in the era of community-acquired methicillin-resistant Staphylococcus aureus. Pediatrics115:642-648.
    OpenUrlAbstract/FREE Full Text
  13. 13.
    Gorak, E. J., S. M. Yamada, and J. D. Brown. 1999. Community-acquired methicillin-resistant Staphylococcus aureus in hospitalized adults and children without known risk factors. Clin. Infect. Dis.29:797-800.
    OpenUrlCrossRefPubMedWeb of Science
  14. 14.↵
    Herold, B. C., L. C. Immergluck, M. C. Maranan, D. S. Lauderdale, R. E. Gaskin, S. Boyle-Vavra, et al. 1998. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA279:593-598.
    OpenUrlCrossRefPubMedWeb of Science
  15. 15.↵
    Huang, Y. C., L. H. Su, and T. Y. Lin. 2004. Nasal carriage of methicillin-resistant Staphylococcus aureus in contacts of an adolescent with community-acquired disseminated disease. Pediatr. Infect. Dis. J.23:919-922.
    OpenUrlPubMedWeb of Science
  16. 16.↵
    Huang, Y. C., L. H. Su, T. L. Wu, C. E. Liu, T. G. Young, P. Y. Chen, et al. 2004. Molecular epidemiology of clinical isolates of methicillin-resistant Staphylococcus aureus in Taiwan. J. Clin. Microbiol.42:307-310.
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    Huang, Y. C., L. H. Su, C. J. Chen, and T. Y. Lin. 2005. Nasal carriage of methicillin-resistant Staphylococcus aureus in school children without identifiable risk factors in northern Taiwan. Pediatr. Infect. Dis. J.24:276-278.
    OpenUrlCrossRefPubMedWeb of Science
  18. 18.↵
    Huang, Y. C., L. H. Su, T. L. Wu, and T. Y. Lin. 2005. Molecular surveillance of methicillin-resistant Staphylococcus aureus in neonatal intensive care units. Infect. Control Hosp. Epidemiol.26:157-160.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.↵
    Hussain, F. M., S. Boyle-Vavra, C. D. Bethel, and R. S. Daum. 2001. Community-acquired methicillin-resistant Staphylococcus aureus colonization in healthy children attending an outpatient pediatric clinic. Pediatr. Infect. Dis. J.20:763-767.
    OpenUrlCrossRefPubMedWeb of Science
  20. 20.↵
    Kaplan, S. L., K. G. Hulten, B. E. Gonzalez, W. A. Hammerman, L. Lamberth, J. Versalovic, et al. 2005. Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin. Infect. Dis.40:1785-1791.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Kuehnert, M. J., D. Kruszon-Moran, H. A. Hill, et al. 2006. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. J. Infect. Dis.193:172-179.
    OpenUrlCrossRefPubMedWeb of Science
  22. 22.↵
    Lina, G., Y. Piemont, F. Godail-Gamot, M. Bes, M. Peter, V. Gauduchon, F. Vandenesch, and J. Etienne. 1999. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis.29:1128-1132.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    Lu, P. L., L. C. Chin, C. F. Peng, Y. H. Chiang, T. P. Chen, L. Ma, and L. K. Siu. 2005. Risk factors and molecular analysis of community methicillin-resistant Staphylococcus aureus carriage. J. Clin. Microbiol.43:132-139.
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    Naimi, T. S., K. H. LeDell, K. Como-Sabetti, S. M. Borchardt, D. J. Boxrud, J. Etienne, et al. 2003. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA290:2976-2984.
    OpenUrlCrossRefPubMedWeb of Science
  25. 25.↵
    Nakamura, M. M., K. L. Rohling, M. Shashaty, H. Lu, Y. W. Tang, and K. M. Edwards. 2002. Prevalence of methicillin-resistant Staphylococcus aureus nasal carriage in the community pediatric population. Pediatr. Infect. Dis. J.21:917-922.
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    Oliveira, D. C., and H. de Lencastre. 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.
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    Shopsin, B., B. Mathema, J. Martinez, et al. 2000. Prevalence of methicillin-resistant and methicillin-susceptible Staphylococcus aureus in the community. J. Infect. Dis.182:359-362.
    OpenUrlCrossRefPubMedWeb of Science
  28. 28.↵
    Suggs, A. H., M. C. Maranan, S. Boyle-Vavra, and R. S. Daum. 1999. Methicillin-resistant and borderline methicillin-resistant asymptomatic Staphylococcus aureus colonization in children without identified risk factors. Pediatr. Infect. Dis.18:410-414.
    OpenUrlCrossRef
  29. 29.↵
    von Eiff, C., K. Becker, K. Machka, H. Stammer, and G. Peters. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. N. Engl. J. Med.344:11-16.
    OpenUrlCrossRefPubMedWeb of Science
  30. 30.↵
    Wang, C. C., W. T. Lo, M. L. Chu, and L. K. Siu. 2004. Epidemiological typing of community-acquired methicillin-resistant Staphylococcus aureus isolates from children in Taiwan. Clin. Infect. Dis.39:481-487.
    OpenUrlCrossRefPubMedWeb of Science
  31. 31.↵
    Wu, K. C., H. H. Chiu, J. H. Wang, N. S. Lee, H. C. Lin, C. C. Hsieh, et al. 2002. Characteristics of community-acquired methicillin-resistant Staphylococcus aureus in infants and children without known risk factors. J. Microb. Immunol. Infect.35:53-56.
    OpenUrl
PreviousNext
Back to top
Download PDF
Citation Tools
Prevalence of Methicillin-Resistant Staphylococcus aureus Nasal Colonization among Taiwanese Children in 2005 and 2006
Yhu-Chering Huang, Kao-Pin Hwang, Po-Yen Chen, Chih-Jung Chen, Tzou-Yien Lin
Journal of Clinical Microbiology Dec 2007, 45 (12) 3992-3995; DOI: 10.1128/JCM.01202-07

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Journal of Clinical Microbiology article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Prevalence of Methicillin-Resistant Staphylococcus aureus Nasal Colonization among Taiwanese Children in 2005 and 2006
(Your Name) has forwarded a page to you from Journal of Clinical Microbiology
(Your Name) thought you would be interested in this article in Journal of Clinical Microbiology.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Prevalence of Methicillin-Resistant Staphylococcus aureus Nasal Colonization among Taiwanese Children in 2005 and 2006
Yhu-Chering Huang, Kao-Pin Hwang, Po-Yen Chen, Chih-Jung Chen, Tzou-Yien Lin
Journal of Clinical Microbiology Dec 2007, 45 (12) 3992-3995; DOI: 10.1128/JCM.01202-07
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • MATERIALS AND METHODS
    • RESULTS
    • DISCUSSION
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

Carrier State
methicillin resistance
Nose
Staphylococcal Infections
Staphylococcus aureus

Related Articles

Cited By...

About

  • About JCM
  • Editor in Chief
  • Board of Editors
  • Editor Conflicts of Interest
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Resources for Clinical Microbiologists
  • Ethics
  • Contact Us

Follow #JClinMicro

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

 

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0095-1137; Online ISSN: 1098-660X