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Study |

Staphylococcus aureus Carriage in the Anterior Nares of Close Contacts of Patients With Atopic Dermatitis FREE

Lai Shan Chiu, MBChB, MRCP; Viola Chi Ying Chow, MRCP, FRCPath, FHKCPath; Julia Mei Lun Ling, MLS, MPhil, PhD; Kam Lun Hon, MD, (CUHK), FAAP, FCCM
[+] Author Affiliations

Author Affiliations: Dermatology Research Center (Drs Chiu and Hon) and Departments of Medicine and Therapeutics (Dr Chiu), Microbiology (Drs Chow and Ling), and Paediatrics (Dr Hon), Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong.


Arch Dermatol. 2010;146(7):748-752. doi:10.1001/archdermatol.2010.129.
Text Size: A A A
Published online

Objective  To study the prevalence of Staphylococcus aureus colonization in close contacts of patients with atopic dermatitis (AD) and the influence on AD severity.

Design  Prospective case-control study.

Setting  Pediatric dermatology clinic in a Hong Kong university hospital.

Patients  We recruited 211 subjects prospectively, including 50 AD patients, 50 non-AD control subjects, 60 close contacts of AD patients, and 51 close contacts of controls.

Intervention  Nasal swabs and skin swabs were taken. Severity of AD was assessed using the SCORAD (Scoring Atopic Dermatitis) index.

Main Outcome Measures  The prevalence of S aureus colonization in the close contacts of AD patients was compared with that of the close contacts of non-AD controls. Between-group differences were assessed, where appropriate, by unpaired t test or Pearson χ2 test. Multivariate logistic regression using the forward stepwise method was performed to identify independent predictors of severe AD. A probability value of P < .05 was considered statistically significant.

Results  Significantly more nasal carriers of S aureus were found among the close contacts of AD patients (14 of 60 [23%]) than among the close contacts of non-AD controls (4 of 51 [8%] [P = .03]). The difference was still significant after the exclusion of the AD patients' close contacts who also had AD (24% vs 8% [P = .03]). By multivariate analysis, only skin colonization of S aureus was independently associated with severe AD (odds ratio, 17.0; 95% confidence interval, 1.60-181.1 [P = .02]).

Conclusions  Anterior nares of close contacts of AD patients are reservoirs of S aureus. The presence of S aureus carriers among close contacts does not predict AD severity. Skin colonization is associated with severe AD.

Atopic dermatitis (AD) is a common chronic, relapsing inflammatory skin condition characterized by pruritus and erythematous patches with typical morphological features and distribution. Lifetime prevalence ranges from 10% to 20% in children and 1% to 3% in adults.1 The prevalence of AD in schoolchildren is estimated to be 15% in Hong Kong.2 Environmental factors play a crucial role in the immunopathologic mechanism of AD.3

Staphylococcus aureus colonization is one of the most important and frequently reported triggers, and up to 90% of patients with AD may be colonized with S aureus compared with one-third of the general community.3,4 The severity of AD correlates well with S aureus colonization.57 Recolonization by S aureus is frequent and may contribute to AD severity.810 We proposed that close contacts of AD patients may be important reservoirs of S aureus. We compared the prevalence of S aureus colonization in the anterior nares of close contacts of AD patients and that of non-AD patients and determined the clinical correlation of S aureus colonization in close contacts and of AD severity.

STUDY DESIGN AND STUDY SUBJECTS

In a prospective case-control study, a total of 211 subjects were recruited from a pediatric dermatology clinic at a tertiary university hospital (the Prince of Wales Hospital) from November 1, 2007, through August 31, 2008. These consisted of 4 groups of subjects: 50 AD patients younger than 21 years; 60 close contacts of the AD patients; 50 age- and sex-matched non-AD controls; and 51 close contacts of the non-AD controls. We defined cases of AD according to the UK Working Party’s Diagnostic Criteria for Atopic Dermatitis.1113 Non-AD controls were recruited from the pediatric dermatology clinic and were followed up for non-AD dermatological conditions, including nevi, hemangiomas, viral warts, alopecia, vitiligo, nail problems, and pigmentation. Close contacts were defined as people who lived together and spent a significant amount of time (>12 h/d) with the AD index case in the past 3 months. These people included parents, grandparents, household members, domestic helpers, and siblings. Exclusion criteria of the study included recent admission to the hospital, recent residency in institutions, and recent exposure to antibiotics in the past 4 weeks. This study was reviewed and approved by the Joint Chinese University of Hong Kong and New Territories East Cluster Clinical Research Ethics Committee.

CLINICAL EVALUATION

Severity of AD was assessed by a single investigator (L.S.C.) using the SCORAD (Scoring Atopic Dermatitis) index.14 Moderate disease was defined as an objective SCORAD index of at least 15, and severe disease was defined as an objective SCORAD index of at least 40.15 Clinical and demographic data of all subjects, including age, sex, and history of allergic rhinitis and asthma, were recorded. Written informed consent was obtained from all subjects or their legal guardians and their close contacts.

SAMPLE COLLECTION

Nasal swabs were obtained from AD patients, non-AD controls, and the close contacts of both groups. A sterile cotton-tipped swab was used to collect the specimen by approaching upward toward the top of both nares followed by a 360° twist to cover the whole vestibule. In addition, skin swabs were taken from the AD patients by rolling a sterile cotton-tipped swab stick over their worst affected skin area twice for at least 5 seconds. All samples were sent within the same day to the laboratory of the Department of Microbiology in the Prince of Wales Hospital for analysis.

LABORATORY ANALYSIS OF S aureus ISOLATES

Bacterial cultures of the nasal and skin swabs were performed using standard laboratory techniques. The identity of S aureus was confirmed by colony morphologic features, coagulation of citrated rabbit plasma with EDTA, and production of clumping factor and protein A. Bacterial growth was classified as scanty (<104 colony-forming units [CFU]/mL), moderate (104 to 105 CFU/mL), or heavy (>105 CFU/mL).

STATISTICAL ANALYSIS

Data were analyzed using statistical software (SPSS for Windows, version 11.5.1; SPSS Inc, Chicago, Illinois). Normality of continuous data was analyzed using the Kolmogorov-Smirnov test. All continuous variables were normally distributed. Results are expressed as mean (SD) or number (percentage) of patients as appropriate. Between-group differences were assessed, where appropriate, by the unpaired t test or the Pearson χ2 test. Correlations between normally distributed variables were tested by the Pearson coefficient. Multivariate logistic regression using the forward stepwise method was performed to identify independent predictors of severe AD. The predictors tested were age, sex, asthma, allergic rhinitis, nasal or skin colonization of S aureus in AD patients, and nasal colonization of S aureus in the close contacts of AD patients. A probability value of P < .05 was considered statistically significant.

CHARACTERISTICS OF STUDY PARTICIPANTS

The age of 50 AD patients ranged from 4 months to 20 years. The mean objective and total SCORAD index values of the AD patients were 25.2 (15.6) (range, 0.2-63.7) and 35.1 (18.7) (range, 5.5-78.7), respectively. Among the 50 AD patients, 10 (20%) had severe AD, 23 (46%) had moderate AD, and 17 (34%) had mild AD. The age of the 50 controls ranged from 3 months to 17 years. The characteristics of the AD patients and the non-AD controls were similar, with details summarized in Table 1.

Table Graphic Jump LocationTable 1 Characteristics of AD Patients and Non-AD Control Subjectsa

Sixty close contacts of AD patients and 51 close contacts of non-AD control subjects were recruited. The age of close contacts of AD patients ranged from 8 to 70 years, whereas that of close contacts of non-AD controls ranged from 7 to 70 years. There was a significantly higher prevalence of AD among the close contacts of AD patients compared with those of non-AD controls (11 of 60 [18%] vs 1 of 51 [2%] [P = .01]). The characteristics of close contacts of AD patients and non-AD controls are compared in Table 2.

Table Graphic Jump LocationTable 2 Characteristics of Close Contacts of AD Patients and Non-AD Control Subjectsa
S aureus COLONIZATION

Twenty-six AD patients (52%) were colonized by S aureus in the nose and 22 (44%) on the skin. Nasal colonization of S aureus was significantly more common (P = .04) among AD patients (26 of 50 [52%]) than among non-AD controls (16 of 50 [32%]). Notably, skin colonization of S aureus was present in all 10 patients with severe AD as opposed to only 12 of 40 (30%) among those with mild to moderate disease (P < .001) Table 3. There were significantly more nasal carriers of S aureus among the close contacts of AD patients (14 of 60 [23%]) than among the close contacts of non-AD controls (4 of 51 [8%] [P = .03]). The difference was still significant after the exclusion of the AD patients' close contacts who also had AD (12 of 49 [24%] vs 4 of 50 [8%] [P = .03]). The microbiological findings among AD patients, non-AD controls, and their respective close contacts are summarized in Tables 1 and 2.

Table Graphic Jump LocationTable 3 Comparisons Between AD Patients With Severe and Nonsevere Diseasea
COLONIZATION OF OTHER MICROBIALS

Apart from S aureus, cultures from the skin and nasal swabs yielded other microbials. Streptococcus pneumoniae was cultured from anterior nares of 1 AD patient (2%) and 1 non-AD control subject (2%). One AD patient had diphtheroid bacterium (2%) and 1 had group G streptococcus (2%) isolated from the anterior nares. Moraxella catarrhalis was cultured from the anterior nares of 2 AD patients (4%). Serratia species were found in the nasal culture of 1 AD patient (2%). Diphtheroid bacteria were found on the skin of 3 AD patients (6%), and Streptococcus agalactiae was found on the skin of 1 AD patient (2%). None of the microbials had a significant association with AD severity.

DETERMINING FACTORS OF AD SEVERITY

Among the 50 AD patients studied, the total SCORAD index of patients with skin colonization of S aureus was significantly higher than for those without skin colonization (48.3 [16.8] vs 24.6 [12.5] [P < .001]). The total SCORAD index of AD patients with S aureus nasal colonization (42.5 [18.8]) was also significantly higher than that of patients without nasal colonization (26.9 [15.0] [P = .002]). The density of growth of S aureus from the nasal and skin swabs was not associated with AD severity. Patient age, sex, and history of asthma or allergic rhinitis also did not predict AD severity. The presence of close contacts with S aureus colonization was not related to an increase in AD severity.

By multivariate analysis, only skin colonization of S aureus was independently associated with severe AD (odds ratio, 17.0; 95% confidence interval, 1.60-181.1 [P = .02]). Comparisons of clinical and microbiological findings between AD patients with severe and those with mild to moderate disease are summarized in Table 3.

We found a higher rate of S aureus nasal colonization in the close contacts of AD patients than in those of non-AD controls. The finding still held true after exclusion of the AD patients' close contacts who also had AD. The higher colonization rate, therefore, cannot be explained only by the higher prevalence of AD among close contacts of AD patients. We believe that the anterior nares of close contacts of AD patients serve as reservoirs of S aureus and contribute to the transmission of S aureus between AD patients and their close contacts. A recently published study in Singapore showed a high concordance of S aureus isolates in AD patients and their close contacts,16 which supports our hypothesis of intrafamilial transmission of S aureus. The next question is whether S aureus colonization among close contacts affects AD severity. Leung et al17 reported that a high burden of environmental S aureus was associated with an increase in AD severity. They collected dust from the bed, bedroom floor, and vacuum bag and extracted S aureus DNA from the dust particles. They found that AD severity correlated with the amount of S aureus DNA from bed and bedroom floor dust. Similarly, close contacts of AD patients who have S aureus nasal colonization may contribute to a high burden of environmental S aureus. However, we were unable to demonstrate any association between S aureus colonization in close contacts and AD severity in our study, possibly because of the small sample size. The importance of S aureus colonization in the close contacts of AD patients needs to be further clarified. Additional studies are needed to investigate whether decolonization of S aureus from the close contacts influences AD disease control, which may affect the management of AD in the future.

Our study demonstrated a higher prevalence of S aureus colonization on the skin and in the nose among AD patients than among the non-AD controls. However, the overall nasal and skin colonization rates of AD patients (52% and 44%, respectively) were lower than those in previous studies.3,4 The lower colonization rate can be explained by the fact that about one-third (34%) of our AD patients had mild disease only, and it is known that S aureus colonization correlates with AD severity.57 The colonization rate was higher in those with severe AD, with a nasal colonization rate of 90% and skin colonization rate of 100%. Our finding was very similar to that of the study by Goh et al18 in Singapore. In that study, the skin colonization rate was only 53% in those with mild disease but reached 100% in patients with severe disease. Their overall nasal colonization rate in AD patients was 55%. Two major factors have been found to be responsible for the increased carriage of S aureus in AD patients, namely, a defective skin barrier function and a compromised innate skin immunity.19 The stratum corneum of healthy skin is an important, functionally active cell layer that serves as a major barrier to soluble environmental substances and provides water-retaining properties. There is a decreased level of ceramides in the stratum corneum of AD skin.20 Ceramides are major water-retaining molecules in the stratum corneum. A reduction of ceramides leads to an increase in transepidermal water loss and ultimately results in dry, cracked skin. In addition, the expression of barrier proteins such as filaggrin, loricrin, and involucrin are reduced in AD patients, resulting in a defective skin barrier.2123 Inducible antimicrobial peptides are produced by keratinocytes and include β-defensins and cathelicidins.24 They have antimicrobial activities against viruses, fungi, and bacteria, including S aureus. Levels of both cathelicidin LL-37 and human β-defensin 2 are reduced in AD patients.25 The compromised innate skin immunity, together with the defective skin barrier, makes skin with AD highly susceptible to S aureus.

Nasal and skin colonization of S aureus were both found to be associated with AD severity in terms of a higher SCORAD index in our study. Similar findings have been reported in other studies.58 However, we found that only skin colonization was independently associated with severe AD on multivariate analysis. Staphylococcus aureus colonized on the skin can produce superantigens that contribute to the increased cutaneous inflammation in AD via several mechanisms.3,26 First, they directly interact with the major histocompatibility complex class II molecules and the β chain of the T-cell receptor to induce T-cell proliferation and activation of the inflammatory cascade, without the need for antigen-presenting cells. Second, superantigens upregulate the expression of cutaneous lymphocyte-associated antigen on T cells and the production of several keratinocyte-derived chemokines that increase T-cell recruitment into the skin.3 Finally, superantigens have been found to contribute to the development of resistance to local corticosteroid treatment by causing the upregulation of the β-isoform of the glucocorticoid receptor in mononuclear cells, which does not bind to corticosteroids.26 We believe that S aureus can be transmitted from the skin to the anterior nares or vice versa in AD patients through autoinoculation. The rate of S aureus skin colonization is expected to parallel that of nasal colonization, and the latter is therefore indirectly associated with AD severity.

Our study had several limitations. First, we recruited controls from the pediatric clinic. It would be a better representation of the normal healthy population if we could have recruited non-AD healthy controls from the community. Second, we were unable to recruit all the close contacts of AD patients because some of them were not available at the time of the study. The sample size was therefore smaller than expected. Third, we took swabs only from the nares of the close contacts. Other areas, such as the hands and flexural and intertriginous areas, might also be involved in the transmission of S aureus. The overall colonization rate might therefore be underestimated.

In conclusion, the anterior nares of close contacts of AD patients are important reservoirs of S aureus. Nasal colonization of S aureus among close contacts of AD patients is not associated with AD severity. Skin colonization is the only factor independently associated with severe AD.

Correspondence: Lai Shan Chiu, MBChB, MRCP, Department of Medicine and Therapeutics, Ninth Floor, Clinical Science Building, Prince of Wales Hospital, Shatin, NT, Hong Kong SAR (monachiu@gmail.com).

Accepted for Publication: January 26, 2010.

Author Contributions: Drs Chiu, Chow, and Ling had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Chiu and Hon. Acquisition of data: Chiu, Chow, and Ling. Analysis and interpretation of data: Chiu and Ling. Drafting of the manuscript: Chiu. Critical revision of the manuscript for important intellectual content: Chiu, Chow, Ling, and Hon. Statistical analysis: Chiu. Obtained funding: Chow and Ling. Administrative, technical, and material support: Chiu, Chow, and Ling. Study supervision: Chiu and Hon.

Financial Disclosure: None reported.

Funding/Support: This study was supported in part by the Department of Microbiology, The Chinese University of Hong Kong.

Role of the Sponsor: The sponsors had no role in the design and conduct of the study; in the collection, analysis, and interpretation of data; or in the preparation, review, or approval of the manuscript.

Larsen  F SchultzHanifin  JM Epidemiology of atopic dermatitis. Immunol Allergy Clin North Am 2002;22 (1) 1- 2410.1016/S0889-8561(03)00066-3
Leung  RWong  GLau  J  et al.  Prevalence of asthma and allergy in Hong Kong schoolchildren: an ISAAC study. Eur Respir J 1997;10 (2) 354- 360
PubMed
Bieber  T Atopic dermatitis. N Engl J Med 2008;358 (14) 1483- 1494
PubMed
Kluytmans  Jvan Belkum  AVerbrugh  H Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 1997;10 (3) 505- 520
PubMed
Guzik  TJBzowska  MKasprowicz  A  et al.  Persistent skin colonization with Staphylococcus aureus in atopic dermatitis: relationship to clinical and immunological parameters. Clin Exp Allergy 2005;35 (4) 448- 455
PubMed
Kedzierska  AKapińska-Mrowiecka  MCzubak-Macugowska  MWójcik  KKedzierska  J Susceptibility testing and resistance phenotype detection in Staphylococcus aureus strains isolated from patients with atopic dermatitis, with apparent and recurrent skin colonization. Br J Dermatol 2008;159 (6) 1290- 1299
PubMed
Hon  KLLam  MCLeung  TF  et al.  Clinical features associated with nasal Staphylococcus aureus colonisation in Chinese children with moderate-to-severe atopic dermatitis. Ann Acad Med Singapore 2005;34 (10) 602- 605
PubMed
Lever  RHadley  KDowney  SMackie  R Staphylococcal colonization in atopic dermatitis and the effect of topical mupirocin therapy. Br J Dermatol 1988;119 (2) 189- 198
PubMed
Breuer  KHÄussler  SKapp  AWerfel  T Staphylococcus aureus: colonizing features and influence of an antibacterial treatment in adults with atopic dermatitis. Br J Dermatol 2002;147 (1) 55- 61
PubMed
Gilani  SJGonzalez  MHussain  IFinlay  AYPatel  GK Staphylococcus aureus re-colonization in atopic dermatitis: beyond the skin. Clin Exp Dermatol 2005;30 (1) 10- 13
PubMed
Williams  HCBurney  PGJHay  RJ  et al.  The UK Working Party's diagnostic criteria for atopic dermatitis, I: derivation of a minimum set of discriminators for atopic dermatitis. Br J Dermatol 1994;131 (3) 383- 396
PubMed
Williams  HCBurney  PGJStrachan  DHay  RJ The UK Working Party's diagnostic criteria for atopic dermatitis, II: observer variation of clinical diagnosis and signs of atopic dermatitis. Br J Dermatol 1994;131 (3) 397- 405
PubMed
Williams  HCBurney  PGJPembroke  ACHay  RJ The UK Working Party's diagnostic criteria for atopic dermatitis, III: independent hospital validation. Br J Dermatol 1994;131 (3) 406- 416
PubMed
European Task Force on Atopic Dermatitis, Severity scoring of atopic dermati-tis: the SCORAD index: consensus report of the European Task Force on Atopic Dermatitis. Dermatology 1993;186 (1) 23- 31
PubMed
Kunz  BOranje  APLabrèze  LStalder  JFRing  JTaïeb  A Clinical validation and guidelines for the SCORAD index: consensus report of the European Task Force on Atopic Dermatitis. Dermatology 1997;195 (1) 10- 19
PubMed
Chiu  LSHo  MSHsu  LYTang  MB Prevalence and molecular characteristics of Staphylococcus aureus isolates colonizing patients with atopic dermatitis and their close contacts in Singapore. Br J Dermatol 2009;160 (5) 965- 971
PubMed
Leung  ADSchiltz  AMHall  CFLiu  AH Severe atopic dermatitis is associated with a high burden of environmental Staphylococcus aureus. Clin Exp Allergy 2008;38 (5) 789- 793
PubMed
Goh  CLWong  JSGiam  YC Skin colonization of Staphylococcus aureus in atopic dermatitis patients seen at the National Skin Centre, Singapore. Int J Dermatol 1997;36 (9) 653- 657
PubMed
Leung  DY Infection in atopic dermatitis. Curr Opin Pediatr 2003;15 (4) 399- 404
PubMed
Arikawa  JIshibashi  MKawashima  MTakagi  YIchikawa  YImokawa  G Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J Invest Dermatol 2002;119 (2) 433- 439
PubMed
O’Regan  GMIrvine  AD The role of filaggrin loss-of-function mutations in atopic dermatitis. Curr Opin Allergy Clin Immunol 2008;8 (5) 406- 410
PubMed
Howell  MDFairchild  HRKim  BE  et al.  Th2 cytokines act on S100/A11 to downregulate keratinocyte differentiation. J Invest Dermatol 2008;128 (9) 2248- 2258
PubMed
Kim  BELeung  DYBoguniewicz  MHowell  MD Loricrin and involucrin expression is down-regulated by Th2 cytokines through STAT-6. Clin Immunol 2008;126 (3) 332- 337
PubMed
Gallo  RLMurakami  MOhtake  TZaiou  M Biology and clinical relevance of naturally occurring antimicrobial peptides. J Allergy Clin Immunol 2002;110 (6) 823- 831
PubMed
Ong  PYOhtake  TBrandt  C  et al.  Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002;347 (15) 1151- 1160
PubMed
Leung  D Superantigens, steroid insensitivity and innate immunity in atopic eczema. Acta Derm Venereol Suppl (Stockh) 2005; (215) 11- 15
PubMed

Figures

Tables

Table Graphic Jump LocationTable 1 Characteristics of AD Patients and Non-AD Control Subjectsa
Table Graphic Jump LocationTable 2 Characteristics of Close Contacts of AD Patients and Non-AD Control Subjectsa
Table Graphic Jump LocationTable 3 Comparisons Between AD Patients With Severe and Nonsevere Diseasea

References

Larsen  F SchultzHanifin  JM Epidemiology of atopic dermatitis. Immunol Allergy Clin North Am 2002;22 (1) 1- 2410.1016/S0889-8561(03)00066-3
Leung  RWong  GLau  J  et al.  Prevalence of asthma and allergy in Hong Kong schoolchildren: an ISAAC study. Eur Respir J 1997;10 (2) 354- 360
PubMed
Bieber  T Atopic dermatitis. N Engl J Med 2008;358 (14) 1483- 1494
PubMed
Kluytmans  Jvan Belkum  AVerbrugh  H Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 1997;10 (3) 505- 520
PubMed
Guzik  TJBzowska  MKasprowicz  A  et al.  Persistent skin colonization with Staphylococcus aureus in atopic dermatitis: relationship to clinical and immunological parameters. Clin Exp Allergy 2005;35 (4) 448- 455
PubMed
Kedzierska  AKapińska-Mrowiecka  MCzubak-Macugowska  MWójcik  KKedzierska  J Susceptibility testing and resistance phenotype detection in Staphylococcus aureus strains isolated from patients with atopic dermatitis, with apparent and recurrent skin colonization. Br J Dermatol 2008;159 (6) 1290- 1299
PubMed
Hon  KLLam  MCLeung  TF  et al.  Clinical features associated with nasal Staphylococcus aureus colonisation in Chinese children with moderate-to-severe atopic dermatitis. Ann Acad Med Singapore 2005;34 (10) 602- 605
PubMed
Lever  RHadley  KDowney  SMackie  R Staphylococcal colonization in atopic dermatitis and the effect of topical mupirocin therapy. Br J Dermatol 1988;119 (2) 189- 198
PubMed
Breuer  KHÄussler  SKapp  AWerfel  T Staphylococcus aureus: colonizing features and influence of an antibacterial treatment in adults with atopic dermatitis. Br J Dermatol 2002;147 (1) 55- 61
PubMed
Gilani  SJGonzalez  MHussain  IFinlay  AYPatel  GK Staphylococcus aureus re-colonization in atopic dermatitis: beyond the skin. Clin Exp Dermatol 2005;30 (1) 10- 13
PubMed
Williams  HCBurney  PGJHay  RJ  et al.  The UK Working Party's diagnostic criteria for atopic dermatitis, I: derivation of a minimum set of discriminators for atopic dermatitis. Br J Dermatol 1994;131 (3) 383- 396
PubMed
Williams  HCBurney  PGJStrachan  DHay  RJ The UK Working Party's diagnostic criteria for atopic dermatitis, II: observer variation of clinical diagnosis and signs of atopic dermatitis. Br J Dermatol 1994;131 (3) 397- 405
PubMed
Williams  HCBurney  PGJPembroke  ACHay  RJ The UK Working Party's diagnostic criteria for atopic dermatitis, III: independent hospital validation. Br J Dermatol 1994;131 (3) 406- 416
PubMed
European Task Force on Atopic Dermatitis, Severity scoring of atopic dermati-tis: the SCORAD index: consensus report of the European Task Force on Atopic Dermatitis. Dermatology 1993;186 (1) 23- 31
PubMed
Kunz  BOranje  APLabrèze  LStalder  JFRing  JTaïeb  A Clinical validation and guidelines for the SCORAD index: consensus report of the European Task Force on Atopic Dermatitis. Dermatology 1997;195 (1) 10- 19
PubMed
Chiu  LSHo  MSHsu  LYTang  MB Prevalence and molecular characteristics of Staphylococcus aureus isolates colonizing patients with atopic dermatitis and their close contacts in Singapore. Br J Dermatol 2009;160 (5) 965- 971
PubMed
Leung  ADSchiltz  AMHall  CFLiu  AH Severe atopic dermatitis is associated with a high burden of environmental Staphylococcus aureus. Clin Exp Allergy 2008;38 (5) 789- 793
PubMed
Goh  CLWong  JSGiam  YC Skin colonization of Staphylococcus aureus in atopic dermatitis patients seen at the National Skin Centre, Singapore. Int J Dermatol 1997;36 (9) 653- 657
PubMed
Leung  DY Infection in atopic dermatitis. Curr Opin Pediatr 2003;15 (4) 399- 404
PubMed
Arikawa  JIshibashi  MKawashima  MTakagi  YIchikawa  YImokawa  G Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J Invest Dermatol 2002;119 (2) 433- 439
PubMed
O’Regan  GMIrvine  AD The role of filaggrin loss-of-function mutations in atopic dermatitis. Curr Opin Allergy Clin Immunol 2008;8 (5) 406- 410
PubMed
Howell  MDFairchild  HRKim  BE  et al.  Th2 cytokines act on S100/A11 to downregulate keratinocyte differentiation. J Invest Dermatol 2008;128 (9) 2248- 2258
PubMed
Kim  BELeung  DYBoguniewicz  MHowell  MD Loricrin and involucrin expression is down-regulated by Th2 cytokines through STAT-6. Clin Immunol 2008;126 (3) 332- 337
PubMed
Gallo  RLMurakami  MOhtake  TZaiou  M Biology and clinical relevance of naturally occurring antimicrobial peptides. J Allergy Clin Immunol 2002;110 (6) 823- 831
PubMed
Ong  PYOhtake  TBrandt  C  et al.  Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002;347 (15) 1151- 1160
PubMed
Leung  D Superantigens, steroid insensitivity and innate immunity in atopic eczema. Acta Derm Venereol Suppl (Stockh) 2005; (215) 11- 15
PubMed

Correspondence

CME


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