Background Children with atopic eczema in infancy often develop allergic rhinoconjunctivitis and asthma, but the term “atopic march” has been questioned as the relations between atopic disorders seem more complicated than one condition progressing into another. Objective In this prospective multicenter study we followed children with eczema from infancy to the age of 10 years focusing on sensitization to allergens, severity of eczema and development of allergic airway symptoms at 4.5 and 10 years of age. Methods On inclusion, 123 children were examined. Hanifin-Rajka criteria and SCORAD index were used to describe the eczema. Episodes of wheezing were registered, skin prick tests and IgE tests were conducted and questionnaires were filled out. Procedures were repeated at 4.5 and 10 years of age with additional examinations for ARC and asthma. Results 94 out of 123 completed the entire study. High SCORAD points on inclusion were correlated with the risk of developing ARC, (B = 9.86, P = 0.01) and asthma, (B = 10.17, P = 0.01). For infants with eczema and wheezing at the first visit, the OR for developing asthma was 4.05(P = 0.01). ARC at 4.5 years of age resulted in an OR of 11.28(P = 0.00) for asthma development at 10 years. Conclusion This study indicates that infant eczema with high SCORAD points is associated with an increased risk of asthma at 10 years of age. Children with eczema and wheezing episodes during infancy are more likely to develop asthma than are infants with eczema alone. Eczema in infancy combined with early onset of ARC seems to indicate a more severe allergic disease, which often leads to asthma development. The progression from eczema in infancy to ARC at an early age and asthma later in childhood shown in this study supports the relevance of the term “atopic march”, at least in more severe allergic disease.
References
[1]
Van Bever HP (2009) Determinants in early life for asthma development. Allergy Asthma Clin Immunol 9 5(1): 6. doi: 10.1186/1710-1492-5-6
[2]
Host A, Halken S (2000) The role of allergy in childhood asthma. Allergy 55(7): 600–608. doi: 10.1034/j.1398-9995.2000.00122.x
[3]
Pedersen SE, Hurd SS, Lemanske RF Jr, Becker A, Zar HJ, et al. (2011) Global strategy for the diagnosis and management of asthma in children 5 years and younger. Pediatr Pulmonol 46(1): 1–17. doi: 10.1002/ppul.21321
[4]
Burgess JA, Lowe AJ, Matheson MC, Varigos G, Abramson MJ, et al. (2009) Does eczema lead to asthma? J Asthma 46(5): 429–436. doi: 10.1080/02770900902846356
Ker J, Hartert TV (2009) The atopic march: what's the evidence? Ann Allergy Asthma Immunol 103(4): 282–289. doi: 10.1016/s1081-1206(10)60526-1
[7]
Scadding GK (2007) Further marches: allergic and non-allergic. Clin Exp Allergy 37(4): 485–487. doi: 10.1111/j.1365-2222.2007.02675.x
[8]
van der Hulst AE, Klip H, Brand PL (2007) Risk of developing asthma in young children with atopic eczema: a systematic review. J Allergy Clin Immunol 120(3): 565–569. doi: 10.1016/j.jaci.2007.05.042
[9]
Nissen SP, Kjaer HF, Host A, Nielsen J, Halken S (2013) The natural course of sensitization and allergic diseases from childhood to adulthood. Pediatr Allergy Immunol 24(6): 549–555. doi: 10.1111/pai.12108
[10]
Carlsten C, Dimich-Ward H, Ferguson A, Watson W, Rousseau R, et al. (2013) Atopic dermatitis in a high-risk cohort: natural history, associated allergic outcomes, and risk factors. Ann Allergy Asthma Immunol 110(1): 24–28. doi: 10.1016/j.anai.2012.10.005
[11]
Dharmage SC, Lowe AJ, Matheson MC, Burgess JA, Allen KJ, et al.. (2013) Atopic dermatitis and the atopic march revisited. Allergy 14..
[12]
Saunes M, Oien T, Dotterud CK, Romundstad PR, Storro O, et al. (2012) Early eczema and the risk of childhood asthma: a prospective, population-based study. BMC Pediatr 24 12: 168–2431-12-168. doi: 10.1186/1471-2431-12-168
[13]
von Kobyletzki LB, Bornehag CG, Hasselgren M, Larsson M, Lindstrom CB, et al. (2012) Eczema in early childhood is strongly associated with the development of asthma and rhinitis in a prospective cohort. BMC Dermatol 27 12: 11–5945-12-11. doi: 10.1186/1471-5945-12-11
[14]
Fitzpatrick AM, Teague WG, Meyers DA, Peters SP, Li X, et al. (2011) Heterogeneity of severe asthma in childhood: confirmation by cluster analysis of children in the National Institutes of Health/National Heart, Lung, and Blood Institute Severe Asthma Research Program. J Allergy Clin Immunol 127(2): 382–389.e1–13. doi: 10.1016/j.jaci.2010.11.015
[15]
Just J, Saint-Pierre P, Gouvis-Echraghi R, Boutin B, Panayotopoulos V, et al. (2013) Wheeze phenotypes in young children have different courses during the preschool period. Ann Allergy Asthma Immunol 111(4): 256–261.e1. doi: 10.1016/j.anai.2013.07.002
[16]
Martinez FD, Wright AL, Taussig LM, Holberg CJ, Halonen M, et al. (1995) Asthma and wheezing in the first six years of life. The Group Health Medical Associates. N Engl J Med 19 332(3): 133–138. doi: 10.1177/000992289503400711
[17]
Agache I, Ciobanu C (2010) Risk factors and asthma phenotypes in children and adults with seasonal allergic rhinitis. Phys Sportsmed 38(4): 81–86. doi: 10.3810/psm.2010.12.1829
[18]
Duncan JM, Sears MR (2008) Breastfeeding and allergies: time for a change in paradigm? Curr Opin Allergy Clin Immunol 8(5): 398–405. doi: 10.1097/aci.0b013e32830d82ed
[19]
Devenney I, Norrman G, Oldaeus G, Stromberg L, Falth-Magnusson K (2006) A new model for low-dose food challenge in children with allergy to milk or egg. Acta Paediatr 95(9): 1133–1139. doi: 10.1080/08035250500516672
[20]
Hanifin JM Rajka G (1980) Diagnostic features of atopic dermatitis. Acta Derm Venereol 92: 44–47.
[21]
European Task Force on Atopic Dermatitis (1993) Severity scoring of atopic dermatitis: the SCORAD index. Consensus Report of the European Task Force on Atopic Dermatitis. Dermatology 186(1): 23–31. doi: 10.1159/000247298
[22]
Devenney I, Falth-Magnusson K (2001) Skin prick test in duplicate: is it necessary? Ann Allergy Asthma Immunol 87(5): 386–389. doi: 10.1016/s1081-1206(10)62919-5
[23]
The European Academy of Allergology and Clinical Immunology (1993) Position paper: Allergen standardization and skin tests. Allergy 48(14 Suppl):48–82.
[24]
Tomicic S, Norrman G, Falth-Magnusson K, Jenmalm MC, Devenney I, et al. (2009) High levels of IgG4 antibodies to foods during infancy are associated with tolerance to corresponding foods later in life. Pediatr Allergy Immunol 20(1): 35–41. doi: 10.1111/j.1399-3038.2008.00738.x
[25]
Swedish National Pediatric Allergy Group (nd) 1st Asthma in Toddlers - terminology and diagnoses. Available: http://www.barnallergisektionen.se/stenc？iler_nya06/b1_astmadefinitioner.html. Accessed 2005.
[26]
Dalen G, Kjellman B (1979) Assessment of lung function on healthy children using an electronic spirometer and an air-flowmeter before and after inhalation of an adrenergic receptor stimulant. Acta Paediatr Scand 68(1): 103–108. doi: 10.1111/j.1651-2227.1979.tb04968.x
[27]
Silverman M AS (1972) Standardization of exercise test in asthmatic children. Arch Dis Child 47: 882–889. doi: 10.1136/adc.47.256.882
[28]
Illi S, von Mutius E, Lau S, Nickel R, Gruber C, et al. (2004) The natural course of atopic dermatitis from birth to age 7 years and the association with asthma. J Allergy Clin Immunol 113(5): 925–931. doi: 10.1016/j.jaci.2004.01.778
[29]
van der Hulst AE, Klip H, Brand PL (2007) Risk of developing asthma in young children with atopic eczema: a systematic review. J Allergy Clin Immunol 120(3): 565–569. doi: 10.1016/j.jaci.2007.05.042
[30]
Spergel JM, Paller AS (2003) Atopic dermatitis and the atopic march. J Allergy Clin Immunol 112 (6 Suppl):S118–27.
[31]
Bergmann RL, Edenharter G, Bergmann KE, Forster J, Bauer CP, et al. (1998) Atopic dermatitis in early infancy predicts allergic airway disease at 5 years. Clin Exp Allergy 28(8): 965–970. doi: 10.1046/j.1365-2222.1998.00371.x
[32]
Gustafsson D, Sjoberg O, Foucard T (2000) Development of allergies and asthma in infants and young children with atopic dermatitis—a prospective follow-up to 7 years of age. Allergy 55(3): 240–245. doi: 10.1034/j.1398-9995.2000.00391.x
[33]
Ballardini N, Kull I, Lind T, Hallner E, Almqvist C, et al. (2012) Development and comorbidity of eczema, asthma and rhinitis to age 12: data from the BAMSE birth cohort. Allergy 67(4): 537–544. doi: 10.1111/j.1398-9995.2012.02786.x
[34]
Ballardini N, Bergstr？m A, B？hme M, van Hage M, Hallner E, et al.. Infantile Eczema - prognosis and risk of asthma an rhinitis in pre-adolescence. J.Allergy Clin.Immunol. In press.
[35]
Schmitt J, Langan S, Williams HC (2007) European Dermato-Epidemiology Network. What are the best outcome measurements for atopic eczema? A systematic review. J Allergy Clin Immunol 120(6): 1389–1398. doi: 10.1016/j.jaci.2007.08.011
[36]
Schram ME, Spuls PI, Leeflang MM, Lindeboom R, Bos JD, et al. (2012) EASI, (objective) SCORAD and POEM for atopic eczema: responsiveness and minimal clinically important difference. Allergy 67(1): 99–106. doi: 10.1111/j.1398-9995.2011.02719.x
[37]
Ricci G, Patrizi A, Baldi E, Menna G, Tabanelli M, et al. (2006) Long-term follow-up of atopic dermatitis: retrospective analysis of related risk factors and association with concomitant allergic diseases. J Am Acad Dermatol 55(5): 765–771. doi: 10.1016/j.jaad.2006.04.064
[38]
Frank PI, Morris JA, Hazell ML, Linehan MF, Frank TL (2008) Long term prognosis in preschool children with wheeze: longitudinal postal questionnaire study 1993–2004. BMJ 21 336(7658): 1423–1426. doi: 10.1136/bmj.39568.623750.be
[39]
Peroni DG, Piacentini GL, Alfonsi L, Zerman L, Di Blasi P, et al. (2003) Rhinitis in pre-school children: prevalence, association with allergic diseases and risk factors. Clin Exp Allergy 33(10): 1349–1354. doi: 10.1046/j.1365-2222.2003.01766.x
[40]
Shaaban R, Zureik M, Soussan D, Neukirch C, Heinrich J, et al. (2008) Rhinitis and onset of asthma: a longitudinal population-based study. Lancet 20 372(9643): 1049–1057. doi: 10.1016/s0140-6736(08)61446-4
[41]
Guerra S, Sherrill DL, Martinez FD, Barbee RA (2002) Rhinitis as an independent risk factor for adult-onset asthma. J Allergy Clin Immunol 109(3): 419–425. doi: 10.1067/mai.2002.121701
[42]
Gaffin JM, Sheehan WJ, Morrill J, Cinar M, Borras Coughlin IM, et al. (2011) Tree nut allergy, egg allergy, and asthma in children. Clin Pediatr (Phila) 50(2): 133–139. doi: 10.1177/0009922810384720
[43]
Gustafsson D, Sjoberg O, Foucard T (2003) Sensitization to food and airborne allergens in children with atopic dermatitis followed up to 7 years of age. Pediatr Allergy Immunol 14(6): 448–452. doi: 10.1046/j.0905-6157.2003.00093.x
[44]
Govaere E, Van Gysel D, Verhamme KM, Doli E, De Baets F (2009) The association of allergic symptoms with sensitization to inhalant allergens in childhood. Pediatr Allergy Immunol 20(5): 448–457. doi: 10.1111/j.1399-3038.2008.00805.x
[45]
Arshad SH, Tariq SM, Matthews S, Hakim E (2001) Sensitization to common allergens and its association with allergic disorders at age 4 years: a whole population birth cohort study. Pediatrics 108(2): E33. doi: 10.1542/peds.108.2.e33
[46]
Burke W, Fesinmeyer M, Reed K, Hampson L, Carlsten C (2003) Family history as a predictor of asthma risk. Am J Prev Med 24: 160. doi: 10.1016/s0749-3797(02)00589-5
[47]
Litonjua AA, Carey VJ, Burge HA, Weiss ST, Gold DR (1998) Parental history and the risk for childhood asthma. Does mother confer more risk than father? Am J Respir Crit Care Med 158(1): 176–181. doi: 10.1164/ajrccm.158.1.9710014
[48]
Strachan DP, Cook DG (1998) Health effects of passive smoking .5. Parental smoking and allergic sensitisation in children. Thorax 53(2): 117–123. doi: 10.1136/thx.53.2.117
[49]
Halken S (2004) Prevention of allergic disease in childhood: clinical and epidemiological aspects of primary and secondary allergy prevention. Pediatr Allergy Immunol 15 Suppl 16:4–5, 9–32.
[50]
Jenkins C, Seccombe L, Tomlins R (2012) Investigating asthma symptoms in primary care. BMJ 344: e2734. doi: 10.1136/bmj.e2734
[51]
Savenije OE, Granell R, Caudri D, Koppelman GH, Smit HA, et al. (2011) Comparison of childhood wheezing phenotypes in 2 birth cohorts: ALSPAC and PIAMA. J Allergy Clin Immunol 127(6): 1505–12.e14. doi: 10.1016/j.jaci.2011.02.002
[52]
Ostblom E, Lilja G, Pershagen G, van Hage M, Wickman M (2008) Phenotypes of food hypersensitivity and development of allergic diseases during the first 8 years of life. Clin Exp Allergy 38(8): 1325–1332. doi: 10.1111/j.1365-2222.2008.03010.x
