Prevalence of Skin Diseases Among Schoolchildren in Magong, Penghu, Taiwan

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ORIGINAL ARTICLE

Prevalence of Skin Diseases Among Schoolchildren in Magong, Penghu, Taiwan: A Community-based Clinical Survey Guan-Yu Chen,1,2 Yu-Wen Cheng,3 Cheng-Yu Wang,3 Tsung-Jen Hsu,4 M. Ming-Long Hsu,5 Pei-Tun Yang,6 Wen-Chieh Chen3*

Background/Purpose: Skin diseases are common in children. Epidemiologic studies of skin diseases in schoolchildren performed by direct inspection by dermatologists are limited in Taiwan. The current study surveyed the prevalence of selected childhood dermatoses in Magong City, Penghu, the largest offshore island of Taiwan. Methods: A cross-sectional study was carried out in June 2005, in which a total of 3273 children aged 6–11 years living in Magong were examined by at least two board-certified dermatologists, with regard to the point prevalence of acne, ephelides, atopic dermatitis, warts, keloids, vitiligo, fungal infections, alope- cia areata and psoriasis. The skin of the scalp, face, neck, trunk and extremities were inspected; that of the breast, genitalia and feet were skipped for privacy. Results: Acne vulgaris was found at the age of 7 in both genders, with comedones being the earliest man- ifestation. The overall prevalence of acne was 17.3% (95% CI, 16–18.6%). Ephelides were frequently ob- served in the children (prevalence rate, 15.24%; 95% CI, 14–16.47%). The prevalence of atopic dermatitis was 4.33% (95% CI, 3.63–5.03%), with more boys affected than girls (1.49:1) (p = 0.03). The prevalence of warts on the hands was 2.81% (95% CI, 2.24–3.38%). Keloids were identified in seven boys and four girls, accounting for 0.33% of the children (95% CI, 0.13–0.53%). Three children had vitiligo (prevalence rate, 0.09%; 95% CI, 0–0.19%). The prevalence of fungal infection including tinea nigra, tinea versicolor and tinea corporis was 0.24% (95% CI, 0.07–0.41%). Neither alopecia areata nor psoriasis was identified. Conclusion: Compared with our previous study in Kaohsiung County using similar methodology, the point prevalence of atopic dermatitis and ephelides was significantly higher whereas that of fungal infec- tion was lower in Penghu. Unexpectedly, tinea nigra was not rare in Penghu. [J Formos Med Assoc 2008;107(1):21–29]

Key Words: child, Penghu, prevalence, skin diseases

©2008 Elsevier & Formosan Medical Association ...... 1Department of Dermatology, Armed Forces Taichung General Hospital, 2Central Taiwan University of Science and Technology, Taichung, 3Department of Dermatology, Chang Gung Memorial Hospital–Kaohsiung Medical Center, Chang Gung University College of Medicine, Kaohsiung, 4Department of Dermatology, Penghu General Hospital, Department of Health, Penghu, 5Department of Dermatology, College of Medicine, National Cheng Kung University, Tainan, and 6Department of Information Management, Tri-Service General Hospital, Taipei, Taiwan.

Received: April 2, 2007 *Correspondence to: Dr Wen-Chieh Chen, Department of Dermatology, Chang Gung Revised: May 8, 2007 Memorial Hospital–Kaohsiung Medical Center, 123 Ta-Pei Road, Niao-Sung, Kaohsiung Accepted: October 2, 2007 833, Taiwan. E-mail: [email protected]

J Formos Med Assoc | 2008 • Vol 107 • No 1 21 G.Y. Chen, et al

Skin diseases are common in schoolchildren.1 all the children in each class were individually Epidemiologic studies of the general population, examined in the nursing room. The sampled however, are still limited, especially in Taiwan. children were selected from a population of ap- Many previous studies have the following restric- proximately 53,000 people living in an area of tions: (1) survey of referred patients in hospital- 33.9918km2, accounting for 58.44% of the total based settings could not entirely reflect the real population of Penghu. A total of 3273 school- situation in the general population;2 (2) self- children (1659 boys, 1614 girls; age range, 6–11 administered questionnaire studies or survey con- years) from grades 1 to 6 were examined, which ducted by non-dermatologists make the validity is 71.87% of the total of 4554 schoolchildren in of the diagnosis problematic.3–5 Magong. Skin diseases such as acne and alopecia areata, although not life-threatening, may be particularly Assessment distressing for this age group. For some chronic The assessment was conducted and confirmed by refractory skin diseases such as atopic dermatitis, at least two board-certified dermatologists through- psoriasis and vitiligo, the psychologic impact, dis- out the body, including head, scalp, neck and ease course and complications as well as thera- extremities but excluding the feet, because it is peutic decisions concerning long-term safety may labor-intensive and time-consuming for an aver- seriously concern affected families. Treatment of age of 26 children per class to take off their shoes intractable warts and keloids in children may pose and socks for examination. The chest, groin and a challenge for dermatologists. genital areas were also skipped due to privacy Penghu is the largest offshore island of Taiwan, concerns. The presence of at least three to five with Magong City being its most populous district. comedones was required for the diagno-sis of acne. As a relatively isolated area with little people Ephelides were identified by their characteristic migration, especially of children and the elderly, appearance on sun-exposed areas as groups of Penghu may serve as an ideal place for an epi- discrete, brown to yellowish, round or speckled demiologic prevalence study. The aim of this study macules with diameters of 2–3 mm.6 For a diagno- was to investigate the disease prevalence in the sis of atopic dermatitis to be made, all three of the general child population of Penghu by dermatol- following criteria had to be met: (1) pruritus; (2) ogist’s direct inspection in order to understand chronic or relapsing history for at least 6 months; the effect and impact of skin diseases on school- (3) typical morphology and distribution includ- children. Excluded were commonly encountered ing acute eczematous change or chronic licheni- or easily manageable diseases such as impetigo fication, prurigo and hyperpigmentation.7 Keloid and folliculitis or relatively innocuous conditions was defined as an overgrowth of dense fibrous such as pityriasis alba. tissue extending beyond the borders of the injury lasting for over 6 months. The diagnosis of warts, tinea versicolor, tinea corporis and vitiligo was Methods made by clinical observation without laboratory examination. The diagnosis of tinea nigra was con- Patients firmed by fungal culture on Sabouraud’s glucose This was a cross-sectional point-prevalence study agar and microscopic examination of the fungal carried out in June 2005 using a purposive slide culture of the scales scrapped from the le- sampling method to survey schoolchildren from sion. The collected data were encoded, registered 4/14 primary schools in Magong City, Penghu. and verified in a relevant database. Children who On the day of visit, the classes available for phys- required further management were referred to ical checkup were enlisted by school officials and Armed Forces Penghu Hospital.

22 J Formos Med Assoc | 2008 • Vol 107 • No 1 Skin diseases among schoolchildren in Magong, Penghu, Taiwan

Statistical analysis Statistical analyses were performed using SPSS version 11.5 (SPSS Inc., Chicago, IL, USA) for Windows. Associations between skin diseases and the height, body weight or body mass index (BMI) of the respective children were examined by t test, while ANOVA was used to compare skin diseases and height, body weight and BMI. The χ2 test was used to determine the association of skin diseases with age, gender, and also the dis- tribution among different schools. A p value of less than 0.05 was considered to be significant.

Results fungal infection. =

Acne was the most common dermatosis followed by ephelides. No cases of psoriasis or alopecia areata were detected in our series. The prevalence

of individual skin disorders was not associated atopic dermatitis; FI = with gender (p = 0.674) or age (p = 0.352). No differences existed between individual skin dis- eases and height, body weight or BMI. An interest- ing observation was that the number of children acne vulgaris; AD with ephelides seemed to cluster in certain schools; = Zong-Zheng primary school with 999 school- children had the highest prevalence of ephelides at 19.91% as compared to the mean prevalence of 15.24% (p < 0.05). Table 1 summarizes the data of the examined schoolchildren and the estimated disease prevalence. Table 2 compares the results total subjects examined; AV total subjects examined; AV of the epidemiologic studies conducted in school- = children in Penghu, Kaohsiung and Taitung. The first two studies had applied the same methodo- female; T = logy with regard to sampling, disease definition 5

and examination. male; F =

Acne The overall prevalence of acne was 17.3% (95% CI, 16–18.6%), increasing with age from 5.7% at 6–8 years to 28.8% at 9–11 years. The clinical manifestations included comedones and papu- and estimated disease prevalence* of the examined schoolchildren profile Background lopustules, with comedones being the earliest

manifestation, noticed in children as young as 6789 255/221/476 284/282/566 285/263/548 4/6/10 (2.1) 256/283/539 13/11/24 (4.2) 22/19/41 (7.4) 14/50/64 (11.8) 22/22/44 (4.9) 37/33/70 (12.3) 40/42/82 (14.9) 36/40/76 (14.1) 11/11/22 (3.8) 5/6/11 (2.3) 4/9/13 (2.3) 21/11/32 (5.6) 5/5/10 (1.8) 21/10/31 (6.5) 1/1/2 (0.3) 15/6/21 (3.8) 10/19/29 (5.3) 0/0/0 0/2/2 (0.3) 0/0/0 0/0/0 1/1/2 (0.3) 1/1/2 (0.4) 0/1/1 (0.1) 2/0/2 (0.4) 0/0/0 1/0/1 (0.1) 0/1/1 (0.1) Age(yr) All children (M/F/T)1011 AVOverall (M/F/T) 278/288/566 1659/1614/3273 301/277/578 212/354/566 (17.3) 45/101/146 (25.7) 114/167/281 (48.6) 240/259/499 (15.2) Ephelides (M/F/T) 45/53/98 (17.3) 60/69/129 (22.3) 45/47/92 (2.8) 85/57/142 (4.3) 5/7/12 (2.1) 15/9/24 (4.1) 2/1/3 (0.09) Warts (M/F/T) 10/5/15 (2.6) 8/6/14 (2.4) 2/6/8 (0.2) 7/4/11 (0.3) 1/0/1 (0.1) 0/0/0 (M/F/T) 0/1/1 (0.1) AD 1/1/2 (0.3) 0/0/0 (M/F/T) 4/1/5 (0.8) Vitiligo (M/F/T) FI (M/F/T) Keloids Table 1. Table

7 years of age (prevalence rate, 10.4%), while as n or (%). M presented *Data are

J Formos Med Assoc | 2008 • Vol 107 • No 1 23 G.Y. Chen, et al

Table 2. Comparison of the prevalence of surveyed skin diseases in schoolchildren in Penghu, Kaohsiung and Taitung*

Penghu (n = 3273) Kaohsiung (n = 4067) Taitung (n = 3029)

Acne 17.3 17.5 Unknown

Ephelides 15.24† 8.38 Unknown

Atopic dermatitis 4.32† 1.7 Unknown

Warts Verruca vulgaris 2.78 2.4 5.08† Verruca plana 0.03 None 0.86† Verruca plantaris Unknown Unknown 1.78

Keloids 0.33 0.6 Unknown

Fungal infection Tinea nigra 0.09 Unknown None Tinea versicolor 0.09 Unknown 4.42† Tinea corporis 0.06 Unknown 0.13 Tinea pedis Unknown Unknown 4.06

Bacterial infection Folliculitis Unknown Unknown 0.69 Pyoderma Unknown Unknown 0.82

Ectoparasitosis Pediculosis capitis None None 12.94 Scabies None None 1.38

Vitiligo 0.09 None Unknown

Alopecia areata None 0.1 Unknown

Psoriasis None None Unknown

*Data are presented as % and differences in the distribution of skin diseases among the different counties were examined using the χ2 test; †p < 0.05.

inflammatory acne was first seen in children at Warts the age of 10–11 years. Nodulocystic acne was Wart infection was found in 2.81% (95% CI, not found in our series. 2.24–3.38%) of students, without age or gender difference. Except in two children who had ver- Ephelides ruca vulgaris on the face, all of the other 90 lesions The overall prevalence of ephelides was 15.24% were on the upper limbs or hands. Verruca planae (95% CI, 14–16.47%). It was unrelated to gender was diagnosed in one boy. (p = 0.674) and advancing age (p = 0.352). Keloids Atopic dermatitis Keloids were observed in seven boys and four The point prevalence of atopic dermatitis in the girls, with an overall prevalence of 0.33% (95% inspected children was 4.33% (95% CI, 3.63– CI, 0.13–0.53%) and without age difference (p = 5.03%), with more boys affected than girls 0.352). Seven keloids were found at previous (1.49:1) (p = 0.03). The prevalence in high grade sites of BCG vaccination, while four children had students was significantly lower than those in the trauma- or operation-induced keloids on the mid and low grades (2.53% vs. 5.30%) (p=0.0002). forearm, leg and chest, respectively.

24 J Formos Med Assoc | 2008 • Vol 107 • No 1 Skin diseases among schoolchildren in Magong, Penghu, Taiwan

A B

Figure. (A) Tinea nigra manifesting as one well-demarcated brown to black patch on the left palm in an 11-year-old girl. (B) Mount of the culture shows branching septate hyphae and budding cells with a central cross wall characteristic of tinea nigra (lactophenol cotton blue, 20×).

Fungal infection socioeconomic status, living conditions and med- Tinea nigra was found in one boy and two ical resources.8 Our study in Penghu is unique in girls, with a prevalence rate of 0.09% (95% CI, Taiwan because: (1) the climate in Penghu is 0–0.19%). Two cases were on the left palm and warmer, windy and arid (mean annual tempera- the other was on the right palm (Figure A). Exam- ture, 23.4°C; mean annual rainfall, 951mm3) ination of the skin scrapings from the lesions compared to the rest of Taiwan (mean annual tem- with 10% potassium hydroxide revealed brown perature, 21°C; mean annual rainfall, 2611mm3);9 branched separate fragmented hyphae. Fungal (2) Penghu differs from Taiwan in its special culture from each patient showed moist, shiny, geographic environment, socioeconomic status, black yeast-like colonies on Sabouraud’s glucose occupation and living conditions. agar, which were microscopically determined to The definitions used to diagnose acne varies be Phaeoannellomyces werneckii with a character- diversely in different studies, ranging from “one istic central cross wall or “two-celled conidia” closed or open comedone” to “more than 20 in- (Figure B). All of the lesions disappeared com- flammatory and retentional lesions”.10 In Penghu, pletely within 2 weeks under treatment with mi- the overall prevalence of acne of 28.8% in conazole cream. Tinea versicolor was found in 9–11-year olds is equivalent to data from Victoria one boy and two girls, with a prevalence rate of in Australia and Glasgow in the United Kingdom, 0.09% (95% CI, 0–0.19%). Two girls (one kept a which were derived from visual inspection of the rabbit as a pet) had tinea corporis (prevalence, general population.11,12 A comparison to a simi- 0.06%; 95% CI, 0–0.14%). lar study in Kaohsiung County was addressed in our previous report.13 In brief, the overall Vitiligo prevalence did not differ in these two popula- Vitiligo was identified in two boys and one girl, tions of children (17.3% in Penghu vs. 17.5% in with an overall prevalence of 0.09% (95% CI, Kaohsiung) (p = 0.67), but remained much higher 0–0.19%). than the prevalence of acne in Lanyu at 1.29% of the same age group (p < 0.001).14 The possible reason for this discrepancy may be explained Discussion by the degree of westernization of lifestyle.15 The early appearance of inflammatory acne before Many factors determine the results of epidemio- the age of 9 is also reflected in another similar logic studies on skin diseases, including ethnic study from Australia.11 It remains to be determined background, geographic area, climate, season, if such a trend in the onset of acne in Taiwan is

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related to the increased dietary dairy intake of range, 6–18 years), Kim et al found a signifi- our children over the generations.5 cantly lower frequency of atopic dermatitis in in- The point prevalence of ephelides in our school- dustrial areas (3.3%) compared to rural (6.6%) children was significantly higher than a similar and urban (7.8%) areas,22 while Saeki et al re- study performed in Kaohsiung County (15.24% ported no apparent difference in prevalence in Penghu vs. 8.38% in Kaohsiung) (p < 0.001). between urban and rural districts in the age The mean annual relative humidity of Penghu is group of 6–12 years in Japan.23 Food allergies are higher than that of Kaohsiung County (82% in causal factors for atopic dermatitis in 43% of Penghu vs. 77% in Kaohsiung) but the mean annu- children aged 0–2 years and around 30% in other al ultraviolet index is similar (6.11 in Penghu vs. age groups; of them, seafood allergy (shrimp, 6.24 in Kaohsiung).9 The occurrence of ephelides crab) accounts for about 15% in children aged is influenced by both genetic and environmental 3–11 years and increases gradually in adolescents factors. Further information is needed to under- and young adults.24 It is not clear if more school- stand whether the higher prevalence of ephelides children in Penghu had an early exposure to in Penghu’s schoolchildren is caused by higher seafood compared to those in Kaohsiung or else- frequency of sun exposure and/or inadequate where in Taiwan. The higher prevalence of atopic sun protection. Fair skin, red hair and ephelides dermatitis in Penghu suggests that factors such are indicators for an increased risk of melanoma as climate (e.g. relative humidity in June, 87% and non-melanoma skin cancers, especially in in Penghu vs. 81% in Kaohsiung) and inade- Caucasians.16 However, it is unclear why the high quacy of medical resources may also influence the prevalence of ephelides in Taiwan and Penghu is manifestation and detection of atopic dermatitis. not associated with melanoma development as Warts, though found in all age groups, are shown in many previous epidemiologic studies extremely common in primary schoolchildren, carried out in Western countries.17 and are estimated to affect 1.8–22% of children Atopic dermatitis was the most common en- aged 6–16 years.8 Warts are located predomi- dogenous eczema and tended to decline with nantly at sites of trauma, such as the extremities age.18 The prevalence of atopic dermatitis varies and face.25 There is no gender or age preponder- in different communities and countries, and is ance,1 which is also confirmed in our study (p = estimated to range from less than 1% to more 0.674 and p = 0.352, respectively). A higher infec- than 20% depending on the disease definition, tion rate was indicated in a previous study in age groups recruited and methods applied.19 In Taitung County, in which 8.1% of the students our experience, many of the children with papu- from a rural region versus 1.6% from urban lar urticaria or lichen urticatus were misdiagnosed Taitung City had common warts (verruca vul- with atopic dermatitis by practicing doctors due garis), and 1.29% in a rural area versus 0.35% in to the perplexing clinical picture.5 In a review of an urban area had planar warts (verruca planae).8 previous studies based on dermatologists’ clinical Our previous study in urban areas of Kaohsiung examination, the atopic dermatitis prevalence of County showed a prevalence rate of 2.4%. The 1.6% in Taiwan (age range, 6–11 years) is much prevalence rate of 2.81% in Penghu is significantly lower than that in Korea (3.3–7.8%; age range, higher than the 1.6% in Taitung City (p = 0.011) 6–18 years), Japan (11.2%; age range, 6–12 years), but lower than that in Taitung County (p < Victoria/Australia (16.3%; age range, 4–18 years) 0.001). The contributing factors to wart infection and Singapore (21.6%; age range, 7–16 years).5,20,21 may include increase in outdoor and sports ac- The prevalence of atopic dermatitis was sig- tivities, having a father with manual occupation, nificantly higher in Penghu (4.32%) than in large household, urbanization, eczema, and nail Kaohsiung County (1.62%). In a direct examina- biting.1,25,26 Other risk factors such as type of tion of the general population in Korea (age footwear, general nutrition and personal hygiene

26 J Formos Med Assoc | 2008 • Vol 107 • No 1 Skin diseases among schoolchildren in Magong, Penghu, Taiwan remain to be determined.25 Although direct person- unexpected. Between 1978 and 1993, only seven to-person transmission is suspected, class size cases of tinea nigra were diagnosed at the Depart- appeared to be unrelated to the prevalence of ment of Dermatology, National Taiwan University warts in the three above-mentioned studies in Hospital,30 while from 1988 to 2005, only six cases Taiwan. A clustering effect of wart distribution as of tinea nigra were confirmed at the Department observed in Kaohsiung County did not exist in of Dermatology, National Cheng Kung University. the series in Penghu.5 The niche of Phaeoannellomyces werneckii (Hortaea Keloid is a common disease encountered by werneckii), the causative agent of tinea nigra, is dermatologists in Taiwan but its treatment has been thought to be on the seashore or in coastal re- disappointing. Keloids occur more commonly in gions.31 It is presumed that the mycosis is con- dark-skinned people than in Caucasians.27 Our tracted from sandy soil, probably through minor survey showed that only 0.34% of children aged trauma and moisture to facilitate the attachment 6–11 had keloids; there was no gender variation of the organism to the skin surface.32 The high (boys to girls, 1.75; p = 0.674). In accordance with prevalence of tinea nigra in Penghu may be the study carried out in Kaohsiung, the preva- explained by: (1) extensive seashore or coastal lence of BCG-induced keloids was much lower in regions with profuse sandy soil; (2) strong north- children compared to that in the general popula- eastern wind and easily accessible ocean leading tion, which was estimated at 2–4%.28,29 On the to a moist salty environment; (3) close work other hand, there appeared to be more children with fisheries and processing of salted dried fish, with trauma-associated keloids (4/11 keloids in all of which reinforce the occurrence of tinea total) in Penghu than in Kaohsiung (1/23). nigra. Being asymptomatic and harmless, the di- In a hospital-based epidemiologic study of agnosis of tinea nigra may be ignored by the children aged 0–12, dermatophyte infection was patient and misdiagnosed after many years of more prevalent in boys than in girls.1 A similar evolution, which probably makes its prevalence finding was also reported in Wu et al’s study of underestimated in hospital settings. Taitung County.8 However, no sex preponderance Vitiligo is an acquired, sometimes familial existed in our general survey of schoolchildren in cutaneous depigmentary disease caused by the de- Penghu. In Taitung County, tinea versicolor was struction of melanocytes.33 In a general population- found to be the most common fungal infection based, direct-inspection study, vitiligo involved (4.4%), followed by tinea pedis (4.1%) and approximately 0.19% of Chinese Han people, with tinea capitis (0.067%), with more fungal infec- more females affected (p < 0.05).34 Childhood tions in rural areas (12.9%) than in Taitung City vitiligo or vitiligo occurring before the age of 12 (4.2%).8 The absence of tinea capitis in our is a distinct subset of vitiligo with the following series may be explained by the improvement in characteristics: (1) common site of onset on the general hygiene and medical care in Taiwan. The head/neck (58.8%), followed by trunk and lower much lower prevalence of tinea versicolor and limbs; (2) mean age of onset at 5.6 years; (3) seg- tinea corporis in Penghu (0.09% and 0.06%) mental vitiligo and positive family history more compared to that in Taitung City (2.06% and common than in adults; (4) less common associ- 0.13%), respectively, may be due to: (1) incom- ation with other autoimmune and endocrine plete examination because we did not ask the disease than in adults.33 Another hospital-based children to expose their bodies; (2) seasonal dif- study in China found more than 20% of pedi- ference because our study was performed in June atric vitiligo in 541 patients with vitiligo.35 Our while the study period in Taitung spanned March study found that childhood vitiligo was rare in to October, including the summer period. our population, even though we may have missed The identification of three cases of tinea nigra cases of non-segmental vitiligo, which usually in our time-point study is quite unusual and involves the trunk.

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