Change in Antimicrobial Susceptibility of Skin-Colonizing Staphylococcus Aureus in Korean Patients with Atopic Dermatitis During Ten-Year Period
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JM Park, et al pISSN 1013-9087ㆍeISSN 2005-3894 Ann Dermatol Vol. 28, No. 4, 2016 http://dx.doi.org/10.5021/ad.2016.28.4.470 ORIGINAL ARTICLE Change in Antimicrobial Susceptibility of Skin-Colonizing Staphylococcus aureus in Korean Patients with Atopic Dermatitis during Ten-Year Period Jung-Min Park1, Ju-Hyun Jo2, Hyunju Jin1, Hyun-Chang Ko1,3, Moon-Bum Kim1,3, Jung-Min Kim4, Do-Won Kim5, Ho-Sun Jang6, Byung-Soo Kim1,3 1Department of Dermatology, Pusan National University School of Medicine, 2Bon Dermatologic Clinic, 3Biomedical Research Institute, Pusan National University Hospital, Busan, Departments of 4Microbiology and 5Dermatology, Kyungpook National University School of Medicine, Deagu, 6Jang Ho Sun Dermatologic Clinic, Busan, Korea Background: A small subset of adolescents atopic dermatitis served during about 10-year period. The increased trend of (AD) tends to persist. This also leads to get more antibiotics MRSA isolation in recent adolescent AD outpatients suggest exposure with advancing years. Antibiotic resistance has that the community including school could be the source of been regarded as a serious problem during Staphylococcus S. aureus antibiotic resistance and higher fusidic acid resist- aureus treatment, especially methicillin-resistant S. aureus ance rates provides evidence of imprudent topical use. (MRSA). Objective: It was investigated the S. aureus colo- Conclusion: Relatively high MRSA isolation and fusidic acid nization frequency in the skin lesions and anterior nares of resistance rates in recent AD patients suggest that the com- adolescent AD patients and evaluated the changes in S. aur- munity harbors antibiotic-resistant S. aureus. (Ann Dermatol eus antimicrobial susceptibility for years. Methods: Patients 28(4) 470∼478, 2016) who visited our clinic from September 2003 to August 2005 were classified into group A, and patients who visited from -Keywords- August 2010 to March 2012 were classified into group B. To Anti-bacterial agent, Antimicrobial resistance, Antimicro- investigate the differences with regard to patients’ age and bial susceptibility, Atopic dermatitis, Staphylococcus aur- disease duration, the patients were subdivided into groups eus according to age. Lesional and nasal specimens were examined. Results: Among the 295 AD patients, the total S. aureus colonization rate in skin lesions was 66.9% (95/142) INTRODUCTION for group A and 78.4% (120/153) for group B. No significant changes in the systemic antimicrobial susceptibilities of S. Atopic dermatitis (AD) is a genetically determined, chroni- aureus strains isolated from adolescent AD patients were ob- cally relapsing inflammatory skin disease with multiple pathogenic factors. While AD occurs most commonly dur- Received January 27, 2015, Revised October 21, 2015, Accepted for ing infancy and children, a smaller subset of adolescents publication November 16, 2015 has persistent or new-onset AD. The association between Corresponding author: Byung-Soo Kim, Department of Dermatology, Pusan Staphylococcus aureus infection and AD is well demon- National University School of Medicine, 179 Gudeok-ro, Seo-gu, Busan 1,2 49241, Korea. Tel: 82-51-240-7338, Fax: 82-51-245-9467, E-mail: dockbs@ strated by many investigators . S. aureus can be found pusan.ac.kr from dermatitic lesions of more than 90% of patients with This is an Open Access article distributed under the terms of the Creative AD, but also from approximately 70% taken from un- Commons Attribution Non-Commercial License (http://creativecommons. affected areas1-3. S. aureus plays an important role as a org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, 3,4 distribution, and reproduction in any medium, provided the original work triggering factor . The relationship between AD and ex- is properly cited. acerbation mechanism by S. aureus is mainly due to the Copyright © The Korean Dermatological Association and The Korean superantigens (sAgs) and sAgs-specific immunoglobulin E Society for Investigative Dermatology that stimulate various numbers of different T-cell clones 470 Ann Dermatol Antimicrobial Susceptibility of S. aureus and cytokine secretion. It has been often proposed that August 2010 to March 2012 were classified into group B. bacterial skin infections are uncommon in AD, while AD To investigate the differences with regard to patient age patients are commonly colonized with S. aureus. Recently and disease duration, the patients were subdivided into lesional S. aureus colonization correlates positively with groups according to age (younger than 18 years and older AD clinical severity, and anti-staphylococcal antibiotic than 18 years) and disease duration (less than 1 year, 1∼5 therapy can reduce the severity of AD characteristic in- years, and more than 5 years). At the first visit, the patient flammation5,6 . age and disease duration were estimated and AD severity The anterior nares are an important S. aureus colonization was assessed according to the SCORing Atopic Dermatitis reservoir. High rate (75%∼90%) of nasal carriage of S. (SCORAD) index12. The exclusion criteria were the pres- aureus has been reported in adults and children with AD. ence of other skin or allergic diseases; a recent (within 4 In contrast, nasal colonization has ranged from 10% to weeks) history of inpatient hospital admission; recent 50% in normal controls. Thus S. aureus carriage in the (within 4 weeks) treatment with antibiotics, systemic corti- nose should be targeted for decolonization7,8. costeroids, or immunosuppressants; and treatment with Antibiotic resistance is increasing around the world to topical antibiotics in the previous 2 weeks. date and has been regarded as an important issue during Methods S. aureus treatment since a long time ago, especially me- thicillin-resistant S. aureus (MRSA). MRSA is more difficult The study protocol was approved by the Pusan National to treat because it is resistant to a number of widely used University Hospital Institutional Review Board (IRB no. antibiotics. The increasing incidence of community-ac- 1409-012-035). Lesional skin specimens were obtained by quired MRSA (CA-MRSA) in skin infections presents major rolling sterile cotton-tipped swab sticks (transport medium challenges in the treatment direction. It also raises con- swab; Micromedia Co., Seoul, Korea) over the most af- cerns that the eczematous skin lesions of AD patients fected skin areas twice for at least 5 seconds each. Nasal might be favorable CA-MRSA reservoirs9,10. Topical fusidic swabs were obtained by reaching upward toward the top acid and mupirocin have been commonly prescribed to of both anterior nares with sterile cotton-tipped swab eradicate different skin infections via over-the-counter stick, followed by a 360o twist to sweep the entire pharmacy in Korea. Although many Asian countries have vestibule. The swab specimens were immediately placed high MRSA infection rates, there have been no pub- in Amie’s medium (Micromedia Co.) and were streaked lications about changes in the prevalence of anti- on sheep blood agar plates (Asan Medical Co., Seoul, biotic-resistant S. aureus, including CA-MRSA, in AD Korea), incubated at 35oC, and examined at 24 and 48 patients. Moreover, few studies have dealt with adolescent hours. Colonies were identified in a blind manner by oth- AD about S. aureus colonization and its susceptibilities to er investigator. In some selected samples of two groups, various antibiotics. antibiotic susceptibility tests were performed with the In present study, it was investigated the S. aureus colo- same Vitek 2 system (BioMérieux, Durham, NC, USA) ac- nization frequency in the skin lesions and anterior nares of cording to the manufacturer’s instructions. AD patients and evaluated the changes in S. aureus anti- For group A, a panel of 8 antibiotics (clindamycin, eryth- microbial susceptibility for years. Differences were also romycin, habekacin, oxacillin, gentamicin, penicillin, bac- analyzed with regard to patient age and disease duration. trim, and vancomycin) was used to test for gram-positive Also, we investigated the prevalence of topical fusidic bacteria. For group B, a panel of 11 antibiotics or combi- acid- and mupirocin-resistant S. aureus in adolescent AD. nations (ciprofloxacin, fusidic acid, rifampin, teicoplanin, tetracycline, nitrofurantoin, quinupristin/dalfopristin, line- MATERIALS AND METHODS zolid, telithromycin, mupirocin, and tigecycline) was add- ed to the previous panel. Patients Statistical analysis Adolescent AD patients with no evidence of skin in- fection, who visited the outpatient clinic of the The Shapiro-Wilk normality test was performed to eval- Department of Dermatology, Pusan National University uate differences between the groups with regard to patient Hospital (Busan, Korea), were enrolled in the study. AD age, disease duration, and severity, using the Predictive was diagnosed according to the Hanifin and Rajka diag- Analytics Software package (PASW for Windows; IBM nostic criteria11. Total 295 patients who initially visited Co., Armonk, NY, USA). The chi-square and Fisher’s exact our clinic from September 2003 to August 2005 were clas- tests were performed to estimate differences in the colo- sified into group A, and patients who initially visited from nization rates between groups that were subdivided ac- Vol. 28, No. 4, 2016 471 JM Park, et al cording to time period, age, and disease duration. were used in each of group B. Statistical significance was defined as a p-value of <0.05. In group A, 2 of 64 (3.1%) and 4 of 57 (7.0%) patients car- ried MRSA in the lesional skin and the anterior nares, re- RESULTS spectively, whereas in group B, 11 of 106 (10.4%) and 3 of 23 (13.0%) patients carried MRSA in the lesional skin Clinical and demographic data and the anterior nares, respectively (p>0.05; Table 2). The clinical and demographic data for groups A and B are Changes in S. aureus antimicrobial susceptibility presented in Table 1. Overall, 142 and 153 patients were enrolled in groups A and B, respectively. The mean pa- Changes in S. aureus antimicrobial susceptibility in ado- tient age in group A was 13.7 years, and the mean disease lescent AD patients over time are shown in Table 3.