Prevalence of asthma, its correlates, and validation of the Pre-School Asthma Risk Factors Scale (PS-ARFS) among preschool children in Lebanon
Main Article Content
Keywords
Asthma, Preschool, Children, ARFS score
Abstract
Objectives: The Asthma Risk Factor Scale (ARFS) is used to screen for asthma in Lebanese preschool children (aged 3–16 years). The study objective was to describe factors associated with asthma, confirm ARFS score validity among Lebanese preschool children, and develop a risk score for asthma diagnosis in this age group (Pre-School Asthma Risk Factor Scale [PS-ARFS]).
Methods: A cross-sectional study enrolled 515 preschool children (November 2018 and March 2019). The ARFS is a 15-item tool that assesses children’s environmental exposure, parental history of asthma, and dietary habits.
Results: The percentage of asthmatic children was 8.2%. Higher odds of asthma in children were associated with living near a prairie sprayed with pesticides (odds ratio [OR] = 2.33), playing outdoors (OR = 2.89), having a heater in the bedroom (OR = 10.73), attending a nursery (OR = 2.91), having a mother who smokes cigarettes (OR = 3.35) or water pipe (OR = 2.46), a sister with a history of seasonal allergy (OR = 6.81), and a parental history (mother and father) of asthma (OR = 6.15 and OR = 9.83, respectively). Higher ARFS scores (OR = 1.144) were associated with higher odds of asthma. Accordingly, the PS-ARFS was created according to the following formula: ARFS score + (playing outdoor × 2.4) + (heating system in the bedroom × 12.9) + (having attended a nursery × 2.5) (area under the curve = 0.908 [0.860–0.957]; P < 0.001); at value: 14.20, Se = 84.3% and Sp = 90.9%.
Conclusion: PS-ARFS is suggested for screening of asthma in preschool children in an epidemiological setting and in the absence of spirometry.
References
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14. Thavagnanam S, Fleming J, Bromley A, Shields MD, Cardwell CR. A meta-analysis of the association between Caesarean section and childhood asthma. Clin Exp Allergy. 2008;38(4):629–33. 10.1111/j.1365-2222.2007.02780.x
15. Rona RJ, Duran-Tauleria E, Chinn S. Family size, atopic disorders in parents, asthma in children, and ethnicity. J Allergy Clin Immunol 1997;99(4):454–60. 10.1016/S0091-6749(97)70070-8
16. Thakkar K, Boatright RO, Gilger MA, El-Serag HB. Gastroesophageal reflux and asthma in children: A systematic review. Pediatrics. 2010;125(4):e925–30. 10.1542/peds.2009-2382
17. Peat JK, Woolcock AJ. Sensitivity to common allergens: Relation to respiratory symptoms and bronchial hyper-responsiveness in children from three different climatic areas of Australia. Clin Exp Allergy. 1991;21(5):573–81. 10.1111/j.1365-2222.1991.tb00849.x
18. Oddy WH. Breastfeeding, childhood asthma, and allergic disease. Ann Nutr Metab. 2017;70 Suppl 2:26–36. 10.1159/000457920
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20. Swartz A, Collier T, Young CA, Cruz E, Bekmezian A, Coffman J, et al. The effect of early child care attendance on childhood asthma and wheezing: A meta-analysis. J Asthma. 2019;56(3):252–62. 10.1080/02770903.2018.1445268
21. Castro-Rodriguez JA, Holberg CJ, Wright AL, Martinez FD. A clinical index to define risk of asthma in young children with recurrent wheezing. Am J Respir Crit Care Med. 2000;162(4 Pt 1):1403–6. 10.1164/ajrccm.162.4.9912111
22. Hafkamp-de Groen E, Lingsma HF, Caudri D, Levie D, Wijga A, Koppelman GH, et al. Predicting asthma in preschool children with asthma-like symptoms: Validating and updating the PIAMA risk score. J Allergy Clin Immunol. 2013;132(6):1303–10. 10.1016/j.jaci.2013.07.007
23. Hallit S, Raherison C, Malaeb D, Hallit R, Waked M, Kheir N, et al. Development of an asthma risk factors scale (ARFS) for risk assessment asthma screening in children. Pediatr Neonatol. 2019;60(2):156–65. 10.1016/j.pedneo.2018.05.009
24. Saadeh R, Klaunig J. Children’s inter-individual variability and asthma development. Int J Health Sci. (Qassim) 2015;9(4):456–67. 10.12816/0031236
25. Collective AR. Comparative regional analysis of ECCE in four Arab countries (Lebanon, Jordan, Syria, and Sudan). Paper commissioned for the EFA Global Monitoring Report 2007.
26. Asher M, Keil U, Anderson H, Beasley R, Crane J, Martinez F, et al. International Study of Asthma and Allergies in Childhood (ISAAC): Rationale and methods. Eur Resp J. 1995;8(3):483–91. 10.1183/09031936.95.08030483
27. Hallit S, Raherison C, Abou Abdallah R, Hallit R, Salameh P. Correlation of types of food and asthma diagnosis in childhood: A case-control study. J Asthma. 2018 Sep 55(9):966-974. doi: 10.1080/02770903.2017.1379535
28. Hallit S, Raherison C, Malaeb D, Hallit R, Kheir N, Salameh P. The AAA Risk Factors Scale: A new model to screen for the risk of asthma, allergic rhinitis and atopic dermatitis in children. Med Princ Pract. 2018;27(5):472–80. 10.1159/000490704
29. Hallit S, Raherison C, Waked M, Hallit R, Layoun N, Salameh P. Validation of the mini pediatric asthma quality of life questionnaire and identification of risk factors affecting quality of life among Lebanese children. J Asthma. 2019;56(2):200–10. 10.1080/02770903.2018.1441417
30. Hallit S, Assi TB, Hallit R, Salameh P. Allergic diseases, smoking, and environmental exposure among university students in Lebanon. J Asthma. 2018;55(1):35–42. 10.1080/02770903.2017.1306075
31. Malaeb D, Hallit S, Sacre H, Hallit R, Salameh P. Factors associated with wheezing among Lebanese children: Results of a cross-sectional study. Allergol Immunopathol (Madr). 2020 May 10:S0301-0546(20)30058-6. 10.1016/j.aller.2020.02.003.
32. Ellies-Oury MP, Chavent M, Conanec A, Bonnet M, Picard B, Saracco J. Statistical model choice, including variable selection based on variable importance: A relevant way for biomarkers selection to predict meat tenderness. Sci Rep. 2019;9(1):10014. 10.1038/s41598-019-46202-y
33. Whittaker TA, Fouladi RT, Williams NJ. Determining predictor importance in multiple regression under varied correlational and distributional conditions. J Modern Appl Stat Methods 2002;1(2):44. 10.22237/jmasm/1036110360
34. Salem MB, Al-Sadoon IO, Hassan MK. Prevalence of wheeze among preschool children in Basra governonate, southern Iraq. East Mediterr Health J. 2002;8(4–5):503–8.
35. Branco PT, Nunes RA, Alvim-Ferraz MC, Martins FG, Ferraz C, Vaz LG, et al. Asthma prevalence in Portuguese preschool children: The latest scientific evidence. Rev Port Pneumol. (2006) 2016;22(5):293–5. 10.1016/j.rppnen.2016.03.013
36. Worldwide variations in the prevalence of asthma symptoms: The International Study of Asthma and Allergies in Childhood (ISAAC). Eur Respir J. 1998;12(2):315–35. 10.1183/09031936.98.12020315
37. Merchant JA, Naleway AL, Svendsen ER, Kelly KM, Burmeister LF, Stromquist AM, et al. Asthma and farm exposures in a cohort of rural Iowa children. Environ Health Perspect. 2005;113(3): 350–6. 10.1289/ehp.7240
38. Free S, Howden-Chapman P, Pierse N, Viggers H, Housing H, Health Study Research Team. More effective home heating reduces school absence for children with asthma. J Epidemiol Community Health. 2010;64(5):379–86. 10.1136/jech.2008.086520
39. Sublett JL, Seltzer J, Burkhead R, Williams PB, Wedner HJ, Phipatanakul W, et al. Air filters and air cleaners: Rostrum by the American Academy of Allergy, Asthma & Immunology Indoor Allergen Committee. J Allergy Clin Immunol. 2010;125(1):32–8. 10.1016/j.jaci.2009.08.036
40. Kuo-Wei Y, Ou L-S, Yao T-C, Li-Chen C, Wen L, Jing-Long H. Prevalence and risk factors for early presentation of asthma among preschool children in Taiwan. Asian Pac J Allergy Immunol. 2011;29(2):120.
41. Wang Z, May SM, Charoenlap S, Pyle R, Ott NL, Mohammed K, et al. Effects of secondhand smoke exposure on asthma morbidity and health care utilization in children: A systematic review and meta-analysis. Ann Allergy Asthma Immunol. 2015;115(5):396–401 e2. 10.1016/j.anai.2015.08.005
42. US Department of Health and Human Services, Centers for Disease Control and Prevention, Coordinating Center for Health Promotion, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health. The health consequences of involuntary exposure to tobacco smoke: A report of the surgeon general, Atlanta, Georgia. 2006. Available from: http://www.cdc.gov/tobacco/data_statistics/sgr/sgr_2006/index.htm [Accessed on December 17, 2019]
43. Shargorodsky J, Garcia-Esquinas E, Navas-Acien A, Lin SY. Allergic sensitization, rhinitis, and tobacco smoke exposure in US children and adolescents. Int Forum Allergy Rhinol. 2015;5(6):471–6. 10.1002/alr.21444
44. Hansen K, Mangrio E, Lindstrom M, Rosvall M. Early exposure to secondhand tobacco smoke and the development of allergic diseases in 4-year-old children in Malmo, Sweden. BMC Pediatr. 2010;10:61. 10.1186/1471-2431-10-61
45. Bilton H. Outdoor learning in the early years: Management and innovation. Oxon, UK: Routledge, 2010. 10.4324/9780203860137
46. von Mutius E. The microbial environment and its influence on asthma prevention in early life. J Allergy Clin Immunol. 2016;137(3):680–9. 10.1016/j.jaci.2015.12.1301
47. Zalzal J, Alameddine I, El-Fadel M, Weichenthal S, Hatzopoulou M. Drivers of seasonal and annual air pollution exposure in a complex urban environment with multiple source contributions. Environ Monit Assess. 2020;192(7):415. 10.1007/s10661-020-08345-8
48. Salameh P, Karaki C, Awada S, Rachidi S, Al Hajje A, Bawab W, et al. Asthma, indoor and outdoor air pollution: A pilot study in Lebanese school teenagers. Rev Mal Respir. 2015;32(7):692–704. 10.1016/j.rmr.2014.11.073
49. Strina A, Barreto ML, Cooper PJ, Rodrigues LC. Risk factors for non-atopic asthma/wheeze in children and adolescents: A systematic review. Emerg Themes Epidemiol. 2014;11:5. 10.1186/1742-7622-11-5
50. Huffaker MF, Phipatanakul W. Utility of the Asthma Predictive Index in predicting childhood asthma and identifying disease-modifying interventions. Ann Allergy Asthma Immunol. 2014;112(3):188–90. 10.1016/j.anai.2013.12.001
51. Martinez FD, Wright AL, Taussig LM, Holberg CJ, Halonen M, Morgan WJ. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. N Engl J Med. 1995;332(3):133–8. 10.1056/NEJM199501193320301
2. Hallit S, Leynaert B, Delmas MC, Rocchi S, De Blic J, Marguet C, Scherer E, Dufourg MN, Bois C, Reboux G, Millon L, Charles MA, Raherison C. Wheezing phenotypes and risk factors in early life: The ELFE cohort. PLoS One. 2018 Apr 27;13(4): e0196711. doi: 10.1371/journal.pone.0196711.
3. Pearce N, Ait-Khaled N, Beasley R, Mallol J, Keil U, Mitchell E, et al. Worldwide trends in the prevalence of asthma symptoms: Phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2007;62(9):758–66. 10.1136/thx.2006.070169
4. Migliore E, Pearce N, Bugiani M, Galletti G, Biggeri A, Bisanti L, et al. Prevalence of respiratory symptoms in migrant children to Italy: the results of SIDRIA-2 study. Allergy. 2007;62(3):293–300. 10.1111/j.1398-9995.2007.01238.x
5. Moorman JE, Rudd RA, Johnson CA, King M, Minor P, Bailey C, et al. National surveillance for asthma–United States, 1980–2004. MMWR Surveill Summ. 2007;56(8):1–54.
6. Waked M, Salameh P. Asthma, allergic rhinitis and eczema in 5–12-year-old school children across Lebanon. Public Health. 2008;122(9):965–73. 10.1016/j.puhe.2007.10.006
7. Waked M, Salameh P. Asthma, allergic rhinitis and eczema in 13–14-year-old schoolchildren across Lebanon. J Med Liban. 2006;54(4):181–90.
8. Jat KR: Spirometry in children. Prim Care Resp J. 2013;22(2): 221. 10.4104/pcrj.2013.00042
9. Castro-Rodriguez JA, Forno E, Rodriguez-Martinez CE, Celedon JC. Risk and protective factors for childhood asthma: What is the evidence? J Allergy Clin Immunol Pract. 2016;4(6):1111–22. 10.1016/j.jaip.2016.05.003
10. Lotvall J, Akdis CA, Bacharier LB, Bjermer L, Casale TB, Custovic A, et al. Asthma endotypes: A new approach to classification of disease entities within the asthma syndrome. J Allergy Clin Immunol. 2011;127(2):355–60. 10.1016/j.jaci.2010.11.037
11. Hallit S, Raherison C, Waked M, Salameh P. Association between caregiver exposure to toxics during pregnancy and childhood-onset asthma: A case-control study. Iran J Allergy Asthma Immunol. 2017;16(6):488–500.
12. Hallit S, Salameh P. Exposure to toxics during pregnancy and childhood and asthma in children: A pilot study. J Epidemiol Glob Health. 2017;7(3):147–54. 10.1016/j.jegh.2017.04.004
13. Harju M, Keski-Nisula L, Georgiadis L, Heinonen S. Parental smoking and cessation during pregnancy and the risk of childhood asthma. BMC Public Health. 2016;16:428. 10.1186/s12889-016-3029-6
14. Thavagnanam S, Fleming J, Bromley A, Shields MD, Cardwell CR. A meta-analysis of the association between Caesarean section and childhood asthma. Clin Exp Allergy. 2008;38(4):629–33. 10.1111/j.1365-2222.2007.02780.x
15. Rona RJ, Duran-Tauleria E, Chinn S. Family size, atopic disorders in parents, asthma in children, and ethnicity. J Allergy Clin Immunol 1997;99(4):454–60. 10.1016/S0091-6749(97)70070-8
16. Thakkar K, Boatright RO, Gilger MA, El-Serag HB. Gastroesophageal reflux and asthma in children: A systematic review. Pediatrics. 2010;125(4):e925–30. 10.1542/peds.2009-2382
17. Peat JK, Woolcock AJ. Sensitivity to common allergens: Relation to respiratory symptoms and bronchial hyper-responsiveness in children from three different climatic areas of Australia. Clin Exp Allergy. 1991;21(5):573–81. 10.1111/j.1365-2222.1991.tb00849.x
18. Oddy WH. Breastfeeding, childhood asthma, and allergic disease. Ann Nutr Metab. 2017;70 Suppl 2:26–36. 10.1159/000457920
19. Sharma S, Sood M, Sood A. Environmental risk factors in relation to childhood asthma in rural area. Curr Pediatr Rev. 2011;15(1):29–32. 10.1186/s13104-019-4670-9
20. Swartz A, Collier T, Young CA, Cruz E, Bekmezian A, Coffman J, et al. The effect of early child care attendance on childhood asthma and wheezing: A meta-analysis. J Asthma. 2019;56(3):252–62. 10.1080/02770903.2018.1445268
21. Castro-Rodriguez JA, Holberg CJ, Wright AL, Martinez FD. A clinical index to define risk of asthma in young children with recurrent wheezing. Am J Respir Crit Care Med. 2000;162(4 Pt 1):1403–6. 10.1164/ajrccm.162.4.9912111
22. Hafkamp-de Groen E, Lingsma HF, Caudri D, Levie D, Wijga A, Koppelman GH, et al. Predicting asthma in preschool children with asthma-like symptoms: Validating and updating the PIAMA risk score. J Allergy Clin Immunol. 2013;132(6):1303–10. 10.1016/j.jaci.2013.07.007
23. Hallit S, Raherison C, Malaeb D, Hallit R, Waked M, Kheir N, et al. Development of an asthma risk factors scale (ARFS) for risk assessment asthma screening in children. Pediatr Neonatol. 2019;60(2):156–65. 10.1016/j.pedneo.2018.05.009
24. Saadeh R, Klaunig J. Children’s inter-individual variability and asthma development. Int J Health Sci. (Qassim) 2015;9(4):456–67. 10.12816/0031236
25. Collective AR. Comparative regional analysis of ECCE in four Arab countries (Lebanon, Jordan, Syria, and Sudan). Paper commissioned for the EFA Global Monitoring Report 2007.
26. Asher M, Keil U, Anderson H, Beasley R, Crane J, Martinez F, et al. International Study of Asthma and Allergies in Childhood (ISAAC): Rationale and methods. Eur Resp J. 1995;8(3):483–91. 10.1183/09031936.95.08030483
27. Hallit S, Raherison C, Abou Abdallah R, Hallit R, Salameh P. Correlation of types of food and asthma diagnosis in childhood: A case-control study. J Asthma. 2018 Sep 55(9):966-974. doi: 10.1080/02770903.2017.1379535
28. Hallit S, Raherison C, Malaeb D, Hallit R, Kheir N, Salameh P. The AAA Risk Factors Scale: A new model to screen for the risk of asthma, allergic rhinitis and atopic dermatitis in children. Med Princ Pract. 2018;27(5):472–80. 10.1159/000490704
29. Hallit S, Raherison C, Waked M, Hallit R, Layoun N, Salameh P. Validation of the mini pediatric asthma quality of life questionnaire and identification of risk factors affecting quality of life among Lebanese children. J Asthma. 2019;56(2):200–10. 10.1080/02770903.2018.1441417
30. Hallit S, Assi TB, Hallit R, Salameh P. Allergic diseases, smoking, and environmental exposure among university students in Lebanon. J Asthma. 2018;55(1):35–42. 10.1080/02770903.2017.1306075
31. Malaeb D, Hallit S, Sacre H, Hallit R, Salameh P. Factors associated with wheezing among Lebanese children: Results of a cross-sectional study. Allergol Immunopathol (Madr). 2020 May 10:S0301-0546(20)30058-6. 10.1016/j.aller.2020.02.003.
32. Ellies-Oury MP, Chavent M, Conanec A, Bonnet M, Picard B, Saracco J. Statistical model choice, including variable selection based on variable importance: A relevant way for biomarkers selection to predict meat tenderness. Sci Rep. 2019;9(1):10014. 10.1038/s41598-019-46202-y
33. Whittaker TA, Fouladi RT, Williams NJ. Determining predictor importance in multiple regression under varied correlational and distributional conditions. J Modern Appl Stat Methods 2002;1(2):44. 10.22237/jmasm/1036110360
34. Salem MB, Al-Sadoon IO, Hassan MK. Prevalence of wheeze among preschool children in Basra governonate, southern Iraq. East Mediterr Health J. 2002;8(4–5):503–8.
35. Branco PT, Nunes RA, Alvim-Ferraz MC, Martins FG, Ferraz C, Vaz LG, et al. Asthma prevalence in Portuguese preschool children: The latest scientific evidence. Rev Port Pneumol. (2006) 2016;22(5):293–5. 10.1016/j.rppnen.2016.03.013
36. Worldwide variations in the prevalence of asthma symptoms: The International Study of Asthma and Allergies in Childhood (ISAAC). Eur Respir J. 1998;12(2):315–35. 10.1183/09031936.98.12020315
37. Merchant JA, Naleway AL, Svendsen ER, Kelly KM, Burmeister LF, Stromquist AM, et al. Asthma and farm exposures in a cohort of rural Iowa children. Environ Health Perspect. 2005;113(3): 350–6. 10.1289/ehp.7240
38. Free S, Howden-Chapman P, Pierse N, Viggers H, Housing H, Health Study Research Team. More effective home heating reduces school absence for children with asthma. J Epidemiol Community Health. 2010;64(5):379–86. 10.1136/jech.2008.086520
39. Sublett JL, Seltzer J, Burkhead R, Williams PB, Wedner HJ, Phipatanakul W, et al. Air filters and air cleaners: Rostrum by the American Academy of Allergy, Asthma & Immunology Indoor Allergen Committee. J Allergy Clin Immunol. 2010;125(1):32–8. 10.1016/j.jaci.2009.08.036
40. Kuo-Wei Y, Ou L-S, Yao T-C, Li-Chen C, Wen L, Jing-Long H. Prevalence and risk factors for early presentation of asthma among preschool children in Taiwan. Asian Pac J Allergy Immunol. 2011;29(2):120.
41. Wang Z, May SM, Charoenlap S, Pyle R, Ott NL, Mohammed K, et al. Effects of secondhand smoke exposure on asthma morbidity and health care utilization in children: A systematic review and meta-analysis. Ann Allergy Asthma Immunol. 2015;115(5):396–401 e2. 10.1016/j.anai.2015.08.005
42. US Department of Health and Human Services, Centers for Disease Control and Prevention, Coordinating Center for Health Promotion, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health. The health consequences of involuntary exposure to tobacco smoke: A report of the surgeon general, Atlanta, Georgia. 2006. Available from: http://www.cdc.gov/tobacco/data_statistics/sgr/sgr_2006/index.htm [Accessed on December 17, 2019]
43. Shargorodsky J, Garcia-Esquinas E, Navas-Acien A, Lin SY. Allergic sensitization, rhinitis, and tobacco smoke exposure in US children and adolescents. Int Forum Allergy Rhinol. 2015;5(6):471–6. 10.1002/alr.21444
44. Hansen K, Mangrio E, Lindstrom M, Rosvall M. Early exposure to secondhand tobacco smoke and the development of allergic diseases in 4-year-old children in Malmo, Sweden. BMC Pediatr. 2010;10:61. 10.1186/1471-2431-10-61
45. Bilton H. Outdoor learning in the early years: Management and innovation. Oxon, UK: Routledge, 2010. 10.4324/9780203860137
46. von Mutius E. The microbial environment and its influence on asthma prevention in early life. J Allergy Clin Immunol. 2016;137(3):680–9. 10.1016/j.jaci.2015.12.1301
47. Zalzal J, Alameddine I, El-Fadel M, Weichenthal S, Hatzopoulou M. Drivers of seasonal and annual air pollution exposure in a complex urban environment with multiple source contributions. Environ Monit Assess. 2020;192(7):415. 10.1007/s10661-020-08345-8
48. Salameh P, Karaki C, Awada S, Rachidi S, Al Hajje A, Bawab W, et al. Asthma, indoor and outdoor air pollution: A pilot study in Lebanese school teenagers. Rev Mal Respir. 2015;32(7):692–704. 10.1016/j.rmr.2014.11.073
49. Strina A, Barreto ML, Cooper PJ, Rodrigues LC. Risk factors for non-atopic asthma/wheeze in children and adolescents: A systematic review. Emerg Themes Epidemiol. 2014;11:5. 10.1186/1742-7622-11-5
50. Huffaker MF, Phipatanakul W. Utility of the Asthma Predictive Index in predicting childhood asthma and identifying disease-modifying interventions. Ann Allergy Asthma Immunol. 2014;112(3):188–90. 10.1016/j.anai.2013.12.001
51. Martinez FD, Wright AL, Taussig LM, Holberg CJ, Halonen M, Morgan WJ. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. N Engl J Med. 1995;332(3):133–8. 10.1056/NEJM199501193320301
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Hallit, S., Sacre, H., Kheir, N., Hallit, R., Waked, M., & Salameh, P. (2021). Prevalence of asthma, its correlates, and validation of the Pre-School Asthma Risk Factors Scale (PS-ARFS) among preschool children in Lebanon. Allergologia Et Immunopathologia, 49(1), 40-49. https://doi.org/10.15586/aei.v49i1.25
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Hallit, S., Sacre, H., Kheir, N., Hallit, R., Waked, M., & Salameh, P. (2021). Prevalence of asthma, its correlates, and validation of the Pre-School Asthma Risk Factors Scale (PS-ARFS) among preschool children in Lebanon. Allergologia Et Immunopathologia, 49(1), 40-49. https://doi.org/10.15586/aei.v49i1.25