Acta Derm Venereol 2012; 92': 467-471

INVESTIGATIVE REPORT

Included in the theme issue;ATOPIC DERMATITIS, URTICARIA AND ITCH

Acta Derm Venereol 2012; 92; 449-581

Prevalence and Risk Factors for Atopic Dermatitis: A Cross-sectionalStudy of 6,453 Korean Preschool Children

Won Jun CHOI', Joo Yeon KO', Jin Wou KIIVF, Kwang Hoon LEE^ Chun Wook PARK^ Kyu Han KIM', Myeung Nam KIM*, AiYoung LEE', Sang Hyun CHO ,̂ Young Lip PARK^ Jee Ho CHOP, Seong Jun SEO«, Yang Won LEE'", Joo Young ROH", YoungMin PARK ,̂ Dong Jae KIM'̂ and Young Suck RO'Departments of Dermatology, 'College of Medicine, Hanyang University, 'The Catholic University of Korea, 'Yonsei University, ^Hallym University, 'SeoulNational University, ^Chung-Ang University, ̂ Dongguk University, "Soonchunhyang University, 'University of Ulsan, "Konkuk University, "Gachón Uni-versity, and "Division ofBiostatics, Department of Medical Lifescience, College of Medicine, The Catholic University, Seoul, Korea

The aims of this study were to evaluate the prevalence,severity and risk factors for atopic dermatitis in Koreanpreschool children as determined by dermatological exa-mination vs questionnaire survey. A total of 6,453 pre-school children from 59 kindergartens and 14 day-carecentres were evaluated. Parents responded to an Inter-national Study of Asthma and Allergies in Childhood(ISAAC)-based questionnaire containing questions con-cerning 23 risk factors, as well as the prevalence, andseverity of atopic dermatitis. Fourteen dermatologiststhen examined the participants according to the Koreandiagnostic criteria for atopic dermatitis, and the EczemaArea and Severity Index (EASI) score. Atopic dermati-tis prevalence determined by dermatological examina-tion was lower than the questionnaire-based prevalence(9.2% vs 19.1%). Most patients (96.2%) had mild atopicdermatitis according to the EASI score (meantSD3.91 ±4.73; median 1.5; range 0.2-38.0). However, 17.4%had sleep disturbance, and 56.7% had not obtained com-plete remission of their rash over the previous 12 months.Among the 12 risk factors, "changing the patient's houseto a newly built house during the first year of life" hadsignificant odds ratio. In conclusion, the prevalence ofatopic dermatitis in Korea in the ISAAC-based surveyconducted by paediatricians was similar to that in seve-ral European countries, and lower than the 2006 Koreanfigure (28.9%). In addition, the prevalence of atopic der-matitis was lower when assessed by dermatological exami-nation than by questionnaire. Key words: atopic dermatitis;children; dermatological examination; prevalence; ques-tionnaire; risk factors.

(Accepted August 17, 2011.)

Acta Derm Venereol 2012; 92: 467-471.

Young Suck Ro, Department of Dermatology, HanyangUniversity College of Medicine, Seoul 133-792, Republicof Korea. E-mail: romio(§hanyang.ac.kr

Atopic dermatitis (AD) can have a considerable impacton the quality of life of patients and their families (1),and the direct and indirect costs of AD are increasing an-

nually worldwide (1-3). To formulate a societal solutionto these problems, an epidemiological study of the pre-valence and risk factors of AD is needed. The prevalenceof AD has increased worldwide in the past decades (4);it was reported to be 28.9% in Korea in 2006, comparedwith 16.6% in 1995 according to an International Studyof Asthma and Allergies in Childhood (ISAAC)-basedquestionnaire survey conducted by paediatricians (5,6). However, this figure was high compared with othercountries (7-14) and even to a recent Korean study bydermatologists (15).

The present study used a dermatological examinationand a questionnaire to gather information on preschoolchildren and the prevalence, severity, and risk factors ofAD in Seoul, the capital ofthe Republic of Korea. Wealso compared estimates of prevalence and severity ofAD based on physical examination by dermatologistsand on the questionnaire.

MATERIALS AND METHODS

Study population

The target population consisted of preschool children (age range0-6 years) in kindergartens and day-care centres in Seoul. Inorder to assess AD prevalence in the entire city of Seoul, wedivided the city into 5 regions: downtown, northeast, northwest,southeast, and southwest. In each region, we selected 2 to 4districts and obtained a list of kindergartens and day-care centresfrom the Seoul municipal government. These were selected inthe order of enrolment in each district.

Data collection

The study was conducted from April to October 2008, using aquestionnaire based on the ISAAC study format and under the di-rect supervision of 14 participating dermatologists and the Seoulmunicipal government. The study was carried out after obtainingwritten consent from the subjects' parents. Questionnaires weredistributed prior to visiting kindergartens and day-care centres,and one week later 3 to 5 dermatologists visited the aforemen-tioned places to examine the children (Fig. 1).

Diagnostic criteria for atopic dermatitis

AD was diagnosed during the dermatological examination,yielding point prevalence, when a patient had two major and

©2012 The Authors, doi: 10.2340/00015555-1252

Joumal Compilation © 2012 Acta Dermato-Venereologica. ISSN 0001-5555Ada Derm Venereol 92

468 W. J. Choi et al.

Questionnaires distributed in 59 kindergartens and 114 day care-centres: n = 8,592 I

Dropout: n = 2,117Questionnaires not returned

]Questionnaires collected: n = 6,475

14 dermatologists examined participants: n = 6,4751

Drop out: n = 22Questionnaires

incorrectly completed

[ 6,453 preschool children included in the study |

Fig. 1. Study flow-chart.

4 minor feattires consistent with the 2005 Korean diagnosticcriteria for AD (Table SI; available from http: //www.medieal-joumals.se/aeta/eontent/?doi=10.2340/00015555-1252) (16).In regard to the questionnaire, yielding one-year prevalence,if a subject met the 3 ISAAC criteria, a diagnosis of AD wasestablished (Table SII; available from http: //www.medical-journals.se/aeta/eontent/?doi=10.2340/00015555-1252) (17,18). The three ISAAC criteria were as follows: intermittentitehy rash for at least 6 months; itchy rash at any time in thelast 12 months; and itchy rash at any time affecting the foldsof the elbows, behind the knees, in fi-ont of the ankles, underthe buttocks, or around the neck, ears or eyes.

Assessment of severity

Dtiring the dermatologieal examination, the severity of eczemawas measured by 14 dermatologists working in the various insti-tutions using the Eezema Area and Severity Index (EASI) seore.Eezema was scored in eaeh patient as mild (< 15), moderate(16-26) or severe (>27), as defined in previous studies (19).In the questionnaire, if a patient experienced any form of sleepdisturbance due to AD at least once a week, or if the symptomshad not disappeared in the last 12 months, the diagnosis wassevere AD (Table SII) (20).

Riskfactors

The risk factors for AD that were evaluated in the study were:present passive smoking (at least once a week), receiving vac-cines according to the Korean immimization schedule, parentaleducational background, breastfeeding or formula-milk feeding,type of house (apartment, multiplex house, detached house,or others), age of house (>10 years, 6-10 years, 2-6 years,< 2 years, or unknown), moving to a newly-built or renovatedhouse during the first year of life, air pollution (living in a re-sidential area or others), type of house heating system (centralheating system, separate heating, portable heating, or others),keeping pets in the present or past, or never having kept pets,and keeping pets during pregnancy or the first year of children'slife (Tahle SII).

Statistical analysis

Demographic characteristics and AD risk factors between ADand non-AD groups from the dermatologieal examination andquestionnaire survey were analysed using the x̂ test. Then, theodds ratio (OR) and 95% confidence interval (CI) was calcula-ted by logistic regression analysis hy the stepwise selectionmethod. Ap-value lower than 0.05 was considered statisticallysignificant.

RESULTS

Demographic characteristics

The epidemiological study was performed in 59 kin-dergartens and 14 day-care centres in 14 districts ofSeoul. In total, 8,592 questionnaires were distributed,and 75.4% of them (« = 6,475) were returned (TableSIII; available from: http://www.medicaljoumals.se/acta/content/?doi=10.2340/00015555-1252). Of the6,475 questionnaires, 22 were incorrectly completed,thus a final total of 6,453 preschool children wereexamined by dermatologists. Table I shows the demo-graphic characteristics ofthe children. There were nosignificant differences in these characteristics betweenthe patient and non-AD groups.

Prevalence of atopic dermatitis

Fig. SI (available from: http://www.medicaljoumals.se/acta/content/?doi=10.2340/00015555-1252) summa-rizes the prevalence of AD assessed by dermatologicalexamination and by questiomiaire. The prevalences ofAD in Seoul according to the dermatological examina-tion and questionnaire were 9.2% and 19.1%, respecti-vely. The differences in AD prevalence between regionswere statistically significant for both research methods(dermatological examinations,/? = 0.0008; question-naire survey,/? = 0.0001). The prevalence was higher inthe downtown, southeast, and northwest regions thanin the other regions.

Severity of atopic dermatitis

The mean± SD EASI score in the dermatological exa-mination was 3.91 ±4.73, and the median, 1.5 (range0.2-38.0) (Table II). The numbers of mild, moderate,and severe AD cases were 571 (96.2%), 18 (3.0%) and5 (0.8%), respectively. In the questionnaire, 17.4% ofrespondents reported that they had experienced sleepdisturbance due to AD at least once a week in the last12 months. In addition, 56.7% of respondents reportedtheir symptoms had not completely cleared up in thelast 12 months (Table II).

Table I. Demographic characteristics

Seoul(n=6,453)

Gender, nMale 3,254Female 3,199

Age, years, meaniSD 4.56±1.16Body weight, kg, mean±SD 18.73 ±3.75Height, cm, mean±SD 108.87±8.66Birthweight, kg, meaniSD 3.32±1.77

SD: standard deviation.

Acta Derm Venereol 92

Prevalence and risk factors for AD in Korean children 469

Table II. Severity of atopic dermatitis (AD) investigated by dermatologists and by written questionnaire

Sleep disturbance due to AD in the last 12 months Complete remission of itchy rash during the last 12 months

Area

EASI score

MeaniSD Nothing (%) < I/week (%) > I/week (%) Yes (%) No (%)

SeoulDowntownNortheastNorthwestSoutheast

Southwest

3.91 ±4.733.63 ±4.283.69 ±4.303.23 ±3.745.85 ±6.582.81 ±2.88

47.750.545.643.251.449.0

34.937.835.536.632.134.2

17.411.718.920,216,516,8

43.339.148.046,338.043,1

56.760.952.053.762.056.9

Risk factors for atopic dermatitis

For the AD group diagnosed by dermatologists, "mo-ving to a newly built or renovated house during the firstyear of life" (OR= 1.392, 95% CI 1.067-1.654) wassignificantly associated with the occurrence of AD. Inthe analysis ofthe AD group defined by questionnaire,the same factor was also significant: "moving to a newlybuilt or renovated house during the first year of life"(0R= 1.603, 95% CI 1.368-1.878) (Table III).

DISCUSSION

Many epidemiological studies of AD have been perfor-med worldwide, and it is generally accepted that ADis increasingly prevalent. The most recent estimate ofits prevalence in Korea was close to 30% based on the2006 ISAAC-based questionnaire survey. However,this prevalence appears rather high compared withthe prevalence in other countries, which have rates ofup to 20% (18). Furthermore, some countries, such asSwitzerland, Denmark, Hungary, Norway, and Japan,have recently documented a decline in or levelling offof prevalence (Table IV) (7-14).

In the present study, the prevalence of AD by ques-tionnaire survey was 19.1%, which is lower than the 2006Korean data (6). A major reason could be a differencein the definition of AD. In the 2006 study, emphasis wasplaced on a positive response to "diagnosis of atopicdermatitis, ever" among the prevalence-related questions.On the other hand, in this study, a diagnosis of AD wasmade only if the patient satisfied the aforementioned 3conditions of the previous epidemiological study usingthe ISAAC questionnaire (17, 18). Moreover, the so-cietal culture in Korea may infiuence the estimates ofAD prevalence. For instance, because of Korea's stronginformation-technology industry and high intemet accessrate, AD may be overemphasized via the Intemet andmass media. Indeed, Korean patients with dermatosesare often misdiagnosed and treated for AD by physiciansother than dermatologists, herbal doctors, or even phar-macologists. As a result, non-atopic Korean patients oftenthink their dermatosis is AD. Thus, the prevalence of AD,as given by the response to the question "diagnosis ofatopic dermatitis, ever", might be higher than by usingthe 3 ISAAC criteria.

Furthermore, the prevalence of AD based on derma-tological examination was lower than the questionnaire-

Table III. Results ofx' test (p-value) and logistic regression analysis (odds ratio (OR)) to identify risk factors associated with atopicdermatitis (AD) diagnosed by dermatologists and questionnaire. Two risk factors were selected by the stepwise selection method in eachAD group. Significant results are in bold type

Risk factors

Type of houseApartmentMultiplex houseDetached houseOthers

Age of house, years>106-102-6<2Unknown

Changing the patient'shouse to a newly buiithouse during the firstyear of lifeNoYes

Dermatoiogical

Non-AD« (%)

2,599 (89.7)1,367 (92.4)1,293 (89.6)

374 (93.3)69 (93.2)

4,835(91.2)1,007 (88.3)

examination

ADn (%) p-value

297 (10.3) 0.0075112(7.6)150(10.4)27(6.7)

5 (6.8)

469 (8.8) 0.0030133(11.7)

OR (95% CI)

0.676(0,268-1.706)0.916(0.357-2.351)0.686(0,269-1.751)1.010(0.371-2.750)

11.329(1,067-1.654)

Questionnaire

Non-ADn (%)

3,419(82.1)1,219(77.9)

401 (78,9)91 (80.5)

4,346 (82.3)847 (74.5)

AD

"(%)

748 (17.9)346(22.1)107(21.1)22 (19.5)

933 (17.7)290 (25.5)

p-value OR (95% CI)

0.0031 11.170(0.710-1.930)0.835(0,502-1.389)0.869(0,505-1.497)

<0.0001 11.603(1.368-1.878)

CI: confidence interval.

Ada Derm Venereol 92

470 W J. Choi et al

Table IV. Prevalence of atopic dermatitis (AD) reported in countries showing a decline or levelling off of prevalence

Country

Switzerland

Detimark

Japan

Hungary

Norway

Korea

Author

Grize et al. (7)

Olesen (8)

Schultz et al. (9)Saeki et al. (10)Saeki et al. (11)Harangi et al. (12)

Seines et al. (13)

Smidesang et al. (14)Lee et al. (6)This study

Study year («)

1992(988)2001 (1,274)1993 (1,060)1998 (9,744)2000 (622)2001 (12,292)2007 (7,362)2002(1,454)2005(1,454)1995(1,432)2000 (3,853)2005 (4,784)2006 (37,365)2008 (6,453)

Study method

QuestiormaireQuestiormaireQuestionnaireQuestionnaireQuestionnaireDermatological examinationQuestionnaireQuestionnaireQuestiotmaireQuestiotmaireQuestiotmaireQuestiormaireQuestionnaireDermatological examinationQuestionnaire

Prevalence, %

18.415.218.919.614.012.712.115.116.121.120.816.528.9

9.219.1

based prevalence. In a review of previous studies,ISAAC questiormaire responses were found to reveal ahigher prevalence of AD than dermatological examina-tion for several reasons (18). First, the prevalence rateby the dermatological examination is point prevalence,whereas the questionnaire-based prevalence is periodprevalence. In general, symptoms of AD are known to beinfluenced by seasonality. Therefore, point prevalencemight give a lower incidence than period prevalence,since AD patients may improve during the study period,especially if it is summer (21). However, in the ques-tiormaire survey the seasonal effect is negligible becausethe questiormaire contains "Itchy rash at any time inthe last 12 months" as a diagnostic criterion. Anotherissue may be the accuracy ofthe Korean version oftheISAAC questionnaire. In many European countries, thevalidity ofthe ISAAC questiormaire has been confirmedby much research, and the questionnaire has undergonemany modifications (18, 21), but the questionnaire isnot validated in the Korean setting.

There was a greater prevalence in the southeast,downtown, and northwest regions of Seoul accordingto both research methods (Fig. SI). Although we didnot focus on the cause ofthe high prevalence of AD inthese regions, it is possible that air pollution (downtowTi,northwest) and high education and economic levels(southeast) increase the incidence of AD.

In terms of severity, the results ofthe questionnaire sur-vey pointed to more severe AD than did the dermatologicalexamination. One possible cause for the low EASI scorewas that the dermatological examination took place duringthe summer, when patients' symptoms generally improve.Secondly, the severity data fi-om the questionnaire maysuffer firom recall bias, leading to inaccurate severityresults. Thirdly, some answers to the questionnaire maybe inaccurate; for instance, the reason for patients' sleepdisturbance may not always have been itchy rash, sincethere are many other possible causes, such as nightmaresor hunger, especially in very young children aged 0-2years with limited vocabularies of 8-10 words.

In the analysis of the risk factors for AD, we foundthat "changing the patient's house to a newly-built houseduring the first year of life" was a risk factor. Accordingto some reports, sick-building syndrome is a contributorycause of AD (22-24). Gustafsson et al. (23) reported thatmoving into a newly built house increases the occurrenceof AD, and Wen et al. (24) reported that renovating andredecorating a home also increases AD.

There were several limitations to this study. Becauseit was conducted from April to October rather thanthroughout the year, the prevalence of AD was not per-fectly represented. In addition, the data may also be af-fected by the fact that the 14 dermatologists allocated tothe different regions judged the symptoms subjectively.The return rate ofthe questiormaire is another issue. Thereturn rate was initially expected to be over 95%, butthe actual rate was 75.4%. This lower return rate meansthat the questionnaire subjects are not quite the same asthose that underwent dermatological examination andthis could affect the results ofthe study. Selection biasmight also exist, as some kindergartens and day-carecentres declined to cooperate with the study. Further-more, our analyses are based on cross-sectional data,which may be subject to recall bias.

In conclusion, the prevalence of AD in this studywas lower than the Korean estimates from 2006. In ad-dition, the prevalence of AD based on dermatologicalexamination was lower than the questionnaire-basedprevalence. We hope that our Korean data will be ofuse in understanding worldwide AD epidemiology.More refined studies with larger numbers of subjectsare warranted.

ACKNOWLEDGEMENTSThe authors would like to thank the many university hospitaldermatologists in the Korean Atopic Dermatitis Association, andProfessor Dong Jae Kim (Division of Biostatics, Departmentof Medical Lifescience, College of Medicine, The CatholicUniversity of Korea). The authors would also like to thank theparents and teachers at the day-care centres and kindergartens

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Prevalence and risk factors for AD in Korean children 471

for their participation in this project. This study was supportedby the Seoul Mtmicipal Government.

The authors declare no conflicts of interest.

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