Cited by 18Antimicrobial Resistance in StaphylococcusOtolaryngology and Infectious DiseasesDermatological diseases and infestations

Risk factors for and molecular characteristics of methicillin-resistant Staphylococcus aureus nasal colonization among healthy children in southern Taiwan, 2005–2010

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Chen, Chih-Ho, Kuo, Kuang-Che, Hwang, Kao-Pin, Lin, Tzou-Yien, Huang, Yhu-Chering·2019·Journal of Microbiology, Immunology and Infection

Abstract

Background/purpose Nasal colonization of Staphylococcus aureus is a well-defined risk factor for subsequent infection. This study investigated the prevalence of methicillin-resistant S. aureus (MRSA) in southern Taiwan and aimed to identify the host factors for S. aureus colonization and the virulence factor of Panton-Valentine Leukocidin (PVL) genes. Methods In a hospital-based study in Kaohsiung from Oct. 2005 to Dec. 2010, we performed nasal swab in the healthy children aged 2–60 months. We examined the relationship between the demographic characteristics and S. aureus nasal colonization. MRSA isolates were further analyzed for antimicrobial susceptibility and molecular characteristics. Results Among 3020 healthy children, 840 (27.8%) children had S. aureus nasal colonization. Of 840 isolates, 246 (29.3%) isolates were MRSA. MRSA colonization was significantly associated with age 2–6 months, day care attendance, and influenza vaccination. Breastfeeding was a protective factor against MRSA colonization. Most MRSA isolates were susceptible to trimethoprim-sulfamethoxazole and doxycycline. Ninety-four percent of MRSA isolates carried either type IV staphylococcal cassette chromosome mec (SCC mec ) or SCC mec V T and 87% belonged to the local community strains, namely clonal complex 59/SCC mec IV or V T . MRSA isolates with PVL-negative was associated with children with passive smoking. Conclusions Between 2005 and 2010, 27.8% and 8.14% of healthy children in southern Taiwan had nasal carriage of S. aureus and MRSA, respectively. Most MRSA isolates were local community strains. Several demographic factors associated with nasal MRSA colonization were identified.

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Research works printed but not linked: 43

  1. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009;7:629e41.
  2. Jevons MP. "Celbenin" e resistant Staphylococci. Br Med J 1961;1:124e5.
  3. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, et al. Invasive methicillin-resistant Staphylococcus aureus in- fections in the United States. JAMA 2007;298:1763e71.
  4. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 1998;279:593e8.
  5. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005;5:751e62.
  6. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, et al. Risk and outcome of nosocomial Staphy- lococcus aureus bacteraemia in nasal carriers versus non-car- riers. Lancet 2004;364:703e5.
  7. von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 2001;344:11e6.
  8. Kazakova SV, Hageman JC, Matava M, Srinivasan A, Phelan L, Garfinkel B, et al. A clone of methicillin-resistant Staphylo- coccus aureus among professional football players. N Engl J Med 2005;352:468e75.
  9. Huang YC, Hwang KP, Chen PY, Chen CJ, Lin TY. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among Taiwanese children in 2005 and 2006. J Clin Microbiol 2007;45:3992e5.
  10. Chen CJ, Hsu KH, Lin TY, Hwang KP, Chen PY, Huang YC. Fac- tors associated with nasal colonization of methicillin-resistant Staphylococcus aureus among healthy children in Taiwan. J Clin Microbiol 2011;49:131e7.
  11. Lu PL, Chin LC, Peng CF, Chiang YH, Chen TP, Ma L, et al. Risk factors and molecular analysis of community methicillin- resistant Staphylococcus aureus carriage. J Clin Microbiol 2005;43:132e9.
  12. Huang YC, Su LH, Wu TL, Liu CE, Young TG, Chen PY, et al. Molecular epidemiology of clinical isolates of methicillin- resistant Staphylococcus aureus in Taiwan. J Clin Microbiol 2004;42:307e10.
  13. Huang YC, Su LH, Lin TY. Nasal carriage of methicillin-resistant Staphylococcus aureus in contacts of an adolescent with community-acquired disseminated disease. Pediatr Infect Dis J 2004;23:919e22.
  14. Huang YC, Su LH, Chen CJ, Lin TY. Nasal carriage of methicillin- resistant Staphylococcus aureus in school children without identifiable risk factors in northern Taiwan. Pediatr Infect Dis J 2005;24:276e8.
  15. Huang YC, Chou YH, Su LH, Lien RI, Lin TY. Methicillin-resistant Staphylococcus aureus colonization and its association with infection among infants hospitalized in neonatal intensive care units. Pediatrics 2006;118:469e74.
  16. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995;33:2233e9.
  17. Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Anti- microb Agents Chemother 2002;46:2155e61.
  18. Boyle-Vavra S, Ereshefsky B, Wang CC, Daum RS. 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 2005;43:4719e30.
  19. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, et al. Involvement of Panton-Valentine leuko- cidin-producing Staphylococcus aureus in primary skin in- fections and pneumonia. Clin Infect Dis 1999;29:1128e32.
  20. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multi- locus sequence typing for characterization of methicillin- resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 2000;38:1008e15.
  21. Lo WT, Wang CC, Lin WJ, Wang SR, Teng CS, Huang CF, et al. Changes in the nasal colonization with methicillin-resistant Staphylococcus aureus in children: 2004-2009. PLoS One 2010;5, e15791.
  22. Huang YC, Chao AS, Su LH, Chang SD. A cluster of methicillin- sensitive Staphylococcus aureus colonization in a nursery. J Perinat Med 2012;40:307e10.
  23. Tsai MS, Chen CJ, Lin TY, Huang YC. Nasal methicillin-resistant Staphylococcus aureus colonization among otherwise healthy children aged between 2 months and 5 years in northern Taiwan, 2005-2010. J Microbiol Immunol Infect 2018;51: 756e62. https://doi.org/10.1016/j.jmii.2017.07.014. · DOI
  24. Chen CJ, Wang SC, Chang HY, Huang YC. Longitudinal analysis of methicillin-resistant and methicillin-susceptible Staphylo- coccus aureus carriage in healthy adolescents. J Clin Microbiol 2013;51:2508e14.
  25. Tsai MH, Huang SH, Chen CL, Chiu CY, Hua MC, Liao SL, et al. Pathogenic bacterial nasopharyngeal colonization and its impact on respiratory diseases in the first year of life: the PATCH Birth Cohort Study. Pediatr Infect Dis J 2015;34:652e8.
  26. Gray BM, Turner ME, Dillon Jr HC. Epidemiologic studies of Streptococcus pneumoniae in infants. The effects of season and age on pneumococcal acquisition and carriage in the first 24 months of life. Am J Epidemiol 1982;116:692e703.
  27. Leekha S, Diekema DJ, Perencevich EN. Seasonality of staph- ylococcal infections. Clin Microbiol Infect 2012;18:927e33.
  28. Shak JR, Vidal JE, Klugman KP. Influence of bacterial in- teractions on pneumococcal colonization of the nasopharynx. Trends Microbiol 2013;21:129e35.
  29. Chien YW, Vidal JE, Grijalva CG, Bozio C, Edwards KM, Williams JV, et al. Density interactions among Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus in the nasopharynx of young Peruvian children. Pediatr Infect Dis J 2013;32:72e7.
  30. Regev-Yochay G, Dagan R, Raz M, Carmeli Y, Shainberg B, Derazne E, et al. Association between carriage of Strepto- coccus pneumoniae and Staphylococcus aureus in children. JAMA 2004;292:716e20.
  31. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. Community- associated meticillin-resistant Staphylococcus aureus. Lancet 2010;375:1557e68.
  32. Huang YC, Chen CJ. Nasal carriage of methicillin-resistant Staphylococcus aureus during the first 2 years of life in chil- dren in northern Taiwan. Pediatr Infect Dis J 2015;34:131e5.
  33. Mulcahy ME, McLoughlin RM. Host-bacterial crosstalk de- termines Staphylococcus aureus nasal colonization. Trends Microbiol 2016;24:872e86.
  34. Chua K, Laurent F, Coombs G, Grayson ML, Howden BP. Anti- microbial resistance: not community-associated methicillin- resistant Staphylococcus aureus (CA-MRSA)! A clinician's guide to community MRSA e its evolving antimicrobial resistance and implications for therapy. Clin Infect Dis 2011;52:99e114.
  35. Kang YC, Hsiao CH, Yeh LK, Ma DH, Chen PY, Lin HC, et al. Methicillin-resistant Staphylococcus aureus ocular Infection in Taiwan: clinical features, genotying, and antibiotic suscepti- bility. Medicine (Baltimore) 2015;94:e1620.
  36. Lee CY, Tsai HC, Kunin CM, Lee SS, Chen YS. Clinical and microbiological characteristics of purulent and non-purulent cellulitis in hospitalized Taiwanese adults in the era of community-associated methicillin-resistant Staphylococcus aureus. BMC Infect Dis 2015;15:311.
  37. Hsiao CH, Ong SJ, Chuang CC, Ma DH, Huang YC. A comparison of clinical features between community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus keratitis. J Ophthalmol 2015;2015:923941.
  38. Chen YJ, Liu KL, Chen CJ, Huang YC. Comparative molecular characteristics of community-associated and healthcare- associated methicillin-resistant Staphylococcus aureus iso- lates from adult patients in northern Taiwan. Medicine (Bal- timore) 2015;94:e1961.
  39. Huang YC, Ho CF, Chen CJ, Su LH, Lin TY. Comparative mo- lecular analysis of community-associated and healthcare- associated methicillin-resistant Staphylococcus aureus iso- lates from children in northern Taiwan. Clin Microbiol Infect 2008;14:1167e72.
  40. Chen CJ, Unger C, Hoffmann W, Lindsay JA, Huang YC, Gotz F. Characterization and comparison of 2 distinct epidemic community-associated methicillin-resistant Staphylococcus aureus clones of ST59 lineage. PLoS One 2013;8, e63210.
  41. Lo WT, Lin WJ, Tseng MH, Wang SR, Chu ML, Wang CC. Risk factors and molecular analysis of panton-valentine leukocidin- positive methicillin-resistant Staphylococcus aureus coloniza- tion in healthy children. Pediatr Infect Dis J 2008;27:713e8.
  42. Nguyen DM, Mascola L, Brancoft E. Recurring methicillin- resistant Staphylococcus aureus infections in a football team. Emerg Infect Dis 2005;11:526e32.
  43. Nakamura MM, Rohling KL, Shashaty M, Lu H, Tang YW, Edwards KM. Prevalence of methicillin-resistant Staphylo- coccus aureus nasal carriage in the community pediatric pop- ulation. Pediatr Infect Dis J 2002;21:917e22.

Cited by

Authors
Chen, C.-H., Kuo, K.-C., Hwang, K.-P., Lin, T.-Y., & Huang, Y.-C.
Affiliations
  • Chang Gung Memorial Hospital (TW)
  • China Medical University (TW)
  • Chang Gung University (TW)
Corresponding author
Huang, Yhu-Chering
Venue
Journal of Microbiology, Immunology and Infection
Publisher
Elsevier BV
Published
2019-12
Volume
52
Issue
6
Pages
929-936
ISSN
1684-1182 (ISSN-L)
OpenAlex
W2891740098
Cited by
18
References
1
Citations by year
2025: 3 · 2024: 2 · 2023: 3 · 2022: 1 · 2021: 4 · 2020: 3 · 2019: 1
FWCI
1.51
Type
journal article
Language
en
Open access
Locations
  • Journal of Microbiology Immunology and Infection (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Chang Gung Memorial Hospital
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
  • Health Sciences › Medicine › Infectious Diseases › Otolaryngology and Infectious Diseases
  • Health Sciences › Medicine › Infectious Diseases › Dermatological diseases and infestations
Keywords
methicillin-resistant Staphylococcus aureus, nasal carriage, children, risk factors, Panton-Valentine leukocidin, staphylococcal cassette chromosome mec, community-acquired MRSA, passive smoking, breastfeeding, daycare attendance, influenza vaccination, antimicrobial susceptibility, southern Taiwan
MeSH terms
Anti-Bacterial Agents, Bacterial Proteins, Bacterial Toxins, Carrier State, Doxycycline, Exotoxins, Female, Humans, Infant, Leukocidins, Male, Microbial Sensitivity Tests, Nose, Prospective Studies, Risk Factors, Staphylococcal Infections, Taiwan, Virulence, Trimethoprim, Sulfamethoxazole Drug Combination, Prevalence, Methicillin-Resistant Staphylococcus aureus, Healthy Volunteers

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