Prevalence of atopic eczema in adolescents from a very low prevalence area (Kosovo): role of wheezing, gender, exercise, and paracetamol
Main Article Content
Keywords
adolescents, atopic eczema, epidemiology, exercise, Kosovo, Paracetamol
Abstract
Background: The epidemiology of atopic eczema in adolescents in Kosovo is virtually unknown, and the risk factors for the condition in very low-prevalence areas (as it was the case) are not well studied. The objective of the present study was to better know those factors and whether the presence of comorbid wheezing symptoms modifies the factors.
Methods: The cross-sectional survey, Global Asthma Network-validated questionnaire, which includes questions on eczema symptoms and environmental factors (such as smoking, pet ownership, paracetamol usage, truck traffic, siblings, time spent using screens or watching television, and physical exercise), was administered to adolescents in the following main cities of Kosovo: Ferizaj, Gjakova, Gjilan, Peja, Prishtina, and Prizren. Additionally, height and weight were measured at school.
Results: Prevalence of eczema symptoms ranged from 2.2% in Ferizaj to 5.5% in Gjakova. Severe symptoms were <1% in all cities. Eczema ever ranged from 3.0% in Ferizaj to 6.4% in Prizren. Factors significantly associated with the prevalence of current eczema symptoms in the meta-analysis were males (pooled adjusted odds ratio [aOR] 0.50, 95% Confidence Interval [95% CI] 0.37–0.66); physical exercise (pooled aOR 2.79, 95% CI 1.89–4.10); and paracetamol intake (pooled 1.86, 95% CI 1.32–2.64). The corresponding figures for eczema ever were as follows: pooled aOR: 0.68, 95% CI 0.44–1.06; pooled aOR 2.07, 95% CI 1.48–2.90; and pooled aOR 1.19, 95% CI 0.88–1.60. The associations tended to be higher in the subpopulation with eczema and wheezing comorbidity.
Conclusions: The prevalence of atopic eczema is very low in Kosovo and is associated with females, physical exercise, and paracetamol intake. These associations are higher when eczema and wheezing are comorbid conditions.
References
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19 Barbarot S, Auziere S, Gadkari A, Girolomoni G, Puig L, Simpson EL, et al. Epidemiology of atopic dermatitis in adults: Results from an international survey. Allergy. 2018;73(6):1284–93. 10.1111/all.13401
20 Ronmark EP, Ekerljung L, Lotvall J, Wennergren G, Ronmark E, Toren K, et al. Eczema among adults: prevalence, risk factors and relation to airway diseases. Results from a large-scale population survey in Sweden. Br J Dermatol. 2012;166(6):1301–8. 10.1111/j.1365-2133.2012.10904.x
21 Abuabara K, Ye M, McCulloch CE, Sullivan A, Margolis DJ, Strachan DP, et al. Clinical onset of atopic eczema: Results from 2 nationally representative British birth cohorts followed through midlife. J Allergy Clin Immunol. 2019;144(3):710–9. 10.1016/j.jaci.2019.05.040
22 Saeki H, Tsunemi Y, Fujita H, Kagami S, Sasaki K, Ohmatsu H, et al. Prevalence of atopic dermatitis determined by clinical examination in Japanese adults. J Dermatol. 2006;33(11):817–9. 10.1111/j.1346-8138.2006.00187.x
23 Johansson EK, Bergstrom A, Kull I, Melen E, Jonsson M, Lundin S, et al. Prevalence and characteristics of atopic dermatitis among young adult females and males–report from the Swedish population-based study BAMSE. J Eur Acad Dermatol Venereol. 2022;36(5):698–704. 10.1111/jdv.17929
24 Kanda N, Hoashi T, Saeki H. The roles of sex hormones in the course of atopic dermatitis. Int J Mol Sci. 2019;20(19):4660. 10.3390/ijms20194660
25 Kim A, Silverberg JI. A systematic review of vigorous physical activity in eczema. Br J Dermatol. 2016;174(3):660–2. 10.1111/bjd.14179
26 Al-Sahab B, Atoui M, Musharrafieh U, Zaitoun F, Ramadan F, Tamim H. Epidemiology of eczema among Lebanese adolescents. Int J Public Health. 2008;53(5):260–7. 10.1007/s00038-008-7085-2
27 Mitchell EA, Beasley R, Keil U, Montefort S, Odhiambo J. The association between tobacco and the risk of asthma, rhinoconjunctivitis and eczema in children and adolescents: Analyses from phase three of the ISAAC programme. Thorax. 2012;67(11):941–9. 10.1136/thoraxjnl-2011-200901
28 Foliaki S, Annesi-Maesano I, Tuuau-Potoi N, Waqatakirewa L, Cheng S, Douwes J, et al. Risk factors for symptoms of childhood asthma, allergic rhinoconjunctivitis and eczema in the Pacific: An ISAAC phase III study. Int J Tuberc Lung Dis. 2008;12(7):799–806.
29 Brescianini S, Brunetto B, Iacovacci P, D'Ippolito C, Alberti G, Schirru MA, et al. Prevalence of self-perceived allergic diseases and risk factors in Italian adolescents. Pediatr Allergy Immunol. 2009;20(6):578–84. 10.1111/j.1399-3038.2008.00793.x
30 Jago R, Salway RE, Ness AR, Shield JPH, Ridd MJ, Henderson AJ. Associations between physical activity and asthma, eczema and obesity in children aged 12–16: An observational cohort study. BMJ Open. 2019;9(1):e024858. 10.1136/bmjopen-2018-024858
31 Schwartzman G, Lei D, Ahmed A, Chavda R, Gabriel S, Silverberg JI. Association of adult atopic dermatitis severity with decreased physical activity: A cross-sectional study. Dermatitis.2023;34(3):218–23.10.1097/DER.0000000000000921
32 Honjo S, Murakami Y, Odajima H, Adachi Y, Yoshida K, Ohya Y, et al. An independent relation of atopic dermatitis to exercise-induced wheezing in asthmatic children. Allergol Int. 2019;68(1):26–32. 10.1016/j.alit.2018.04.013
33 Beasley R, Clayton T, Crane J, von Mutius E, Lai CK, Montefort S, et al. Association between paracetamol use in infancy and childhood, and risk of asthma, rhinoconjunctivitis, and eczema in children aged 6–7 years: Analysis from phase three of the ISAAC programme. Lancet. 2008;372(9643):1039–48. 10.1016/S0140-6736(08)61445-2
34 Beasley RW, Clayton TO, Crane J, Lai CK, Montefort SR, Mutius E, et al. Acetaminophen use and risk of asthma, rhinoconjunctivitis, and eczema in adolescents: International Study of Asthma and Allergies in Childhood phase three. Am J Respir Crit Care Med. 2011;183(2):171–8. 10.1164/rccm.201005-0757OC
35 Suárez-Varela MM, García-Marcos L, Fernández-Espinar JF, Bercedo-Sanz A, Aguinaga-Ontoso I, González-Díaz C, et al. Is acetaminophen use associated with atopic eczema and other allergic diseases in adolescents? Iran J Allergy Asthma Immunol. 2013;12(2):115–23.
36 Xiao D, Su X, Qu Y, Zhou Y, Pan L, Li X, et al. Association of acetaminophen exposure with increased risk of eczema in children: A meta-analysis. J Am Acad Dermatol. 2019;81(2):642–4. 10.1016/j.jaad.2019.04.017
37 Garcia-Marcos L, Gonzalez-Diaz C, Garvajal-Uruena I, Pac-Sa MR, Busquets-Monge RM, Suarez-Varela MM, et al. Early exposure to paracetamol or to antibiotics and eczema at school age: modification by asthma and rhinoconjunctivitis. Pediatr Allergy Immunol. 2010;21(7):1036–42. 10.1111/j.1399-3038.2010.01037.x
38 Puri P, Nandar SK, Kathuria S, Ramesh V. Effects of air pollution on the skin: A review. Indian J Dermatol Venereol Leprol. 2017;83(4):415–23. 10.4103/0378-6323.199579
2 Langan SM, Mulick AR, Rutter CE, Silverwood Richard J, Asher I, García-Marcos L, et al. Trends in eczema prevalence in children and adolescents: A Global Asthma Network Phase I Study. Clin Exp Allergy 2023;53(3):337–52. 10.1111/cea.14276
3 García-Marcos L, Asher MI, Pearce N, Ellwood E, Bissell K, Chiang CY, et al. The burden of asthma, hay fever and eczema in children in 25 countries: GAN Phase I study. Eur Respir J 2022; 60(3):2102866. 10.1183/13993003.02866-2021
4 Serajuddin B and Hamadeh. New World Bank country classifications by income level: 2020-2021. [Internet]. [cited 2020]. Available from: https://blogs.worldbank.org/opendata/new-world-bank-country-classifications-income-level-2020-2021 (Accessed: March 15, 2021).
5 Odhiambo JA, Williams HC, Clayton TO, Robertson CF, Asher MI. Global variations in prevalence of eczema symptoms in children from ISAAC phase three. J Allergy Clin Immunol. 2009;124(6):1251–8.e23. 10.1016/j.jaci.2009.10.009
6 Suárez-Varela MM, García-Marcos Alvarez L, Kogan MD, González AL, Gimeno AM, Aguinaga Ontoso I, et al. Climate and prevalence of atopic eczema in 6-to 7-year-old school children in Spain. ISAAC phase III. Int J Biometeorol. 2008;52(8):833–40.10.1007/s00484-008-0177-0
7 Zivković Z, Vukašinović Z, Cerović S, Radulović S, Zivanović S, Panić E, et al. Prevalence of childhood asthma and allergies in Serbia and Montenegro. World J Pediatr. 2010;6(4):331–6. 10.1007/s12519-010-0207-y
8 Banac S, Tomulic KL, Ahel V, Rozmanic V, Simundic N, Zubovic S, et al. Prevalence of asthma and allergic diseases in Croatian children is increasing: Survey study. Croat Med J. 2004;45(6):721–6.
9 Stipic-Markovic A, Pevec B, Pevec MR, Custovic A. Prevalence of symptoms of asthma, allergic rhinitis, conjunctivitis and atopic eczema: ISAAC (International Study of Asthma and Allergies in Childhood) in a population of schoolchildren in Zagreb]. Acta Med Croatica. 2003;57(4):281–5.
10 Munivrana Skvorc H, Plavec D, Munivrana S, Skvorc M, Nogalo B, Turkalj M. Prevalence of and risk factors for the development of atopic dermatitis in schoolchildren aged 12–14 in northwest Croatia. Allergol Immunopathol (Madr). 2014;42(2):142–8. 10.1016/j.aller.2012.10.008
11 Vlaski E, Stavric K, Seckova L, Kimovska Hristova M, Isjanovska R. The self-reported density of truck traffic on residential streets and the impact on asthma, hay fever and eczema in young adolescents. Allergol Immunopathol (Madr). 2014;42(3):224–9. 10.1016/j.aller.2012.10.011
12 Ellwood P, Asher MI, Billo NE, Bissell K, Chiang CY, Ellwood EM, et al. The Global Asthma Network rationale and methods for phase I global surveillance: Prevalence, severity, management and risk factors. Eur Respir J. 2017;49(1):1601605. 10.1183/13993003.01605-2016
13 Ellwood P, Williams H, Ait-Khaled N, Bjorksten B, Robertson C, Group IPIS. Translation of questions: The International Study of Asthma and Allergies in Childhood (ISAAC) experience. Int J Tuberc Lung Dis. 2009;13(9):1174–82.
14 Ellwood P, Ellwood E, Rutter C, Perez-Fernandez V, Morales E, Garcia-Marcos L, et al. Global Asthma Network Phase I surveillance: Geographical coverage and response rates. J Clin Med. 2020;9(11) :3688. 10.3390/jcm9113688
15 Ahmetaj L, Martinez-Torres AE, Ahmetaj Y, Ismajli I, Gashi V, Kurhasani X, et al. The role of Human Development Index in the epidemiology of asthma in adolescents in Kosovo: A cross-sectional multicentre Global Asthma Network (GAN) study. Allergol Immunopathol (Madr). 2023;51(2):59–70. 10.15586/aei.v51i2.781
16 Mercer MJ, Joubert G, Ehrlich RI, Nelson H, Poyser MA, Puterman A, et al. Socioeconomic status and prevalence of allergic rhinitis and atopic eczema symptoms in young-adolescents. Pediatr Allergy Immunol. 2004;15(3):234–41. 10.1111/j.1399-3038.2004.00125.x
17 Silverberg JI, Barbarot S, Gadkari A, Simpson EL, Weidinger S, Mina-Osorio P, et al. Atopic dermatitis in the pediatric population: A cross-sectional, international epidemiologic study. Ann Allergy Asthma Immunol. 2021;126(4):417–28 e2. 10.1016/j.anai.2020.12.020
18 Ballardini N, Kull I, Soderhall C, Lilja G, Wickman M, Wahlgren CF. Eczema severity in preadolescent children and its relation to sex, filaggrin mutations, asthma, rhinitis, aggravating factors and topical treatment: A report from the BAMSE birth cohort. Br J Dermatol. 2013;168(3):588–94. 10.1111/bjd.12196
19 Barbarot S, Auziere S, Gadkari A, Girolomoni G, Puig L, Simpson EL, et al. Epidemiology of atopic dermatitis in adults: Results from an international survey. Allergy. 2018;73(6):1284–93. 10.1111/all.13401
20 Ronmark EP, Ekerljung L, Lotvall J, Wennergren G, Ronmark E, Toren K, et al. Eczema among adults: prevalence, risk factors and relation to airway diseases. Results from a large-scale population survey in Sweden. Br J Dermatol. 2012;166(6):1301–8. 10.1111/j.1365-2133.2012.10904.x
21 Abuabara K, Ye M, McCulloch CE, Sullivan A, Margolis DJ, Strachan DP, et al. Clinical onset of atopic eczema: Results from 2 nationally representative British birth cohorts followed through midlife. J Allergy Clin Immunol. 2019;144(3):710–9. 10.1016/j.jaci.2019.05.040
22 Saeki H, Tsunemi Y, Fujita H, Kagami S, Sasaki K, Ohmatsu H, et al. Prevalence of atopic dermatitis determined by clinical examination in Japanese adults. J Dermatol. 2006;33(11):817–9. 10.1111/j.1346-8138.2006.00187.x
23 Johansson EK, Bergstrom A, Kull I, Melen E, Jonsson M, Lundin S, et al. Prevalence and characteristics of atopic dermatitis among young adult females and males–report from the Swedish population-based study BAMSE. J Eur Acad Dermatol Venereol. 2022;36(5):698–704. 10.1111/jdv.17929
24 Kanda N, Hoashi T, Saeki H. The roles of sex hormones in the course of atopic dermatitis. Int J Mol Sci. 2019;20(19):4660. 10.3390/ijms20194660
25 Kim A, Silverberg JI. A systematic review of vigorous physical activity in eczema. Br J Dermatol. 2016;174(3):660–2. 10.1111/bjd.14179
26 Al-Sahab B, Atoui M, Musharrafieh U, Zaitoun F, Ramadan F, Tamim H. Epidemiology of eczema among Lebanese adolescents. Int J Public Health. 2008;53(5):260–7. 10.1007/s00038-008-7085-2
27 Mitchell EA, Beasley R, Keil U, Montefort S, Odhiambo J. The association between tobacco and the risk of asthma, rhinoconjunctivitis and eczema in children and adolescents: Analyses from phase three of the ISAAC programme. Thorax. 2012;67(11):941–9. 10.1136/thoraxjnl-2011-200901
28 Foliaki S, Annesi-Maesano I, Tuuau-Potoi N, Waqatakirewa L, Cheng S, Douwes J, et al. Risk factors for symptoms of childhood asthma, allergic rhinoconjunctivitis and eczema in the Pacific: An ISAAC phase III study. Int J Tuberc Lung Dis. 2008;12(7):799–806.
29 Brescianini S, Brunetto B, Iacovacci P, D'Ippolito C, Alberti G, Schirru MA, et al. Prevalence of self-perceived allergic diseases and risk factors in Italian adolescents. Pediatr Allergy Immunol. 2009;20(6):578–84. 10.1111/j.1399-3038.2008.00793.x
30 Jago R, Salway RE, Ness AR, Shield JPH, Ridd MJ, Henderson AJ. Associations between physical activity and asthma, eczema and obesity in children aged 12–16: An observational cohort study. BMJ Open. 2019;9(1):e024858. 10.1136/bmjopen-2018-024858
31 Schwartzman G, Lei D, Ahmed A, Chavda R, Gabriel S, Silverberg JI. Association of adult atopic dermatitis severity with decreased physical activity: A cross-sectional study. Dermatitis.2023;34(3):218–23.10.1097/DER.0000000000000921
32 Honjo S, Murakami Y, Odajima H, Adachi Y, Yoshida K, Ohya Y, et al. An independent relation of atopic dermatitis to exercise-induced wheezing in asthmatic children. Allergol Int. 2019;68(1):26–32. 10.1016/j.alit.2018.04.013
33 Beasley R, Clayton T, Crane J, von Mutius E, Lai CK, Montefort S, et al. Association between paracetamol use in infancy and childhood, and risk of asthma, rhinoconjunctivitis, and eczema in children aged 6–7 years: Analysis from phase three of the ISAAC programme. Lancet. 2008;372(9643):1039–48. 10.1016/S0140-6736(08)61445-2
34 Beasley RW, Clayton TO, Crane J, Lai CK, Montefort SR, Mutius E, et al. Acetaminophen use and risk of asthma, rhinoconjunctivitis, and eczema in adolescents: International Study of Asthma and Allergies in Childhood phase three. Am J Respir Crit Care Med. 2011;183(2):171–8. 10.1164/rccm.201005-0757OC
35 Suárez-Varela MM, García-Marcos L, Fernández-Espinar JF, Bercedo-Sanz A, Aguinaga-Ontoso I, González-Díaz C, et al. Is acetaminophen use associated with atopic eczema and other allergic diseases in adolescents? Iran J Allergy Asthma Immunol. 2013;12(2):115–23.
36 Xiao D, Su X, Qu Y, Zhou Y, Pan L, Li X, et al. Association of acetaminophen exposure with increased risk of eczema in children: A meta-analysis. J Am Acad Dermatol. 2019;81(2):642–4. 10.1016/j.jaad.2019.04.017
37 Garcia-Marcos L, Gonzalez-Diaz C, Garvajal-Uruena I, Pac-Sa MR, Busquets-Monge RM, Suarez-Varela MM, et al. Early exposure to paracetamol or to antibiotics and eczema at school age: modification by asthma and rhinoconjunctivitis. Pediatr Allergy Immunol. 2010;21(7):1036–42. 10.1111/j.1399-3038.2010.01037.x
38 Puri P, Nandar SK, Kathuria S, Ramesh V. Effects of air pollution on the skin: A review. Indian J Dermatol Venereol Leprol. 2017;83(4):415–23. 10.4103/0378-6323.199579
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Ahmetaj, L., Martínez-Torres, A. E., Ahmetaj, Y., Gashi, V., Kurhasani, X., Lokaj-Berisha, V., Gacaferri-Lumezi, B., Shahini, M., Zhjeqi, V., García-Marcos, L., & the Global Asthma Network Phase I Kosovo Study Group. (2024). Prevalence of atopic eczema in adolescents from a very low prevalence area (Kosovo): role of wheezing, gender, exercise, and paracetamol. Allergologia Et Immunopathologia, 52(6), 40-50. https://doi.org/10.15586/aei.v52i6.1155
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Ahmetaj, L., Martínez-Torres, A. E., Ahmetaj, Y., Gashi, V., Kurhasani, X., Lokaj-Berisha, V., Gacaferri-Lumezi, B., Shahini, M., Zhjeqi, V., García-Marcos, L., & the Global Asthma Network Phase I Kosovo Study Group. (2024). Prevalence of atopic eczema in adolescents from a very low prevalence area (Kosovo): role of wheezing, gender, exercise, and paracetamol. Allergologia Et Immunopathologia, 52(6), 40-50. https://doi.org/10.15586/aei.v52i6.1155