Food allergy as an asthma comorbidity in children and adolescents: a practical approach through a real-world study

Main Article Content

Ignacio Esteban-Gorgojo
María Puy Gorgojo
Joaquin Sastre
Santiago Quirce

Keywords

Asthma, food allergy, eosinophilia, children, LTP, pollen

Abstract

Introduction: Several studies have shown interactions between food allergy (FA) and asthma, but the influence of FA in asthma traits has been scarcely studied.


Methods: A real-world retrospective observational study was conducted among patients between 3 and 18 years old referred to our Asthma Clinic from November 2014 to November 2017. Data were obtained from daily clinical practice. Only patients properly diagnosed with asthma and FA were included.


Results: 815 patients were included: 483 asthmatics and 332 non-asthmatics and 180 FA and 635 no FA. Food allergy was statistically more prevalent among asthma patients (p = 0.014). In a high pollen exposure area, Madrid, among subjects with asthma (121 FA, 362 no-FA), sensitization to lipid transfer protein (LTP) (p = 0.016, OR: 3.064, RR: 2.512) and pollen (p = 0.016, OR: 3.064, RR: 2.512) are risk factors to have a concomitant FA diagnosis, whereas sensitization to profilin is not. Peripheral blood eosinophils were higher in subjects with asthma and FA (≥450 eos/µL) than in asthmatics without FA (≤300 eos/µL) (p = 0.031). Blood eosinophilia, using a cut-off >300 eos/µL, was only present in the FA group. Therefore, this trait should be considered when phenotyping a patient as eosinophilic asthma. Sex had an impact on several variables: height, weight, BMI, blood eosinophils count, sensitization profile, and early-onset asthma.


Conclusions: Asthma and FA are closely related and the presence of FA should be investigated in every asthma patient. This study shows an association between asthma with concomitant FA and sensitization to pollen and LTP, blood eosinophilia, and growth alterations. Differences between boys and girls were also described, so a sex-specific approach is recommended.

Abstract 26 | PDF Downloads 13 XML Downloads 0 HTML Downloads 0

References

1. Global Initiative for Asthma. Global strategy for the diag-nosis and prevention. Global Initiative for Asthma (updated 2016) 2016. Last accessed April 2020. https://ginasthma.org/

2. Loh W, Tang MLK. The epidemiology of food allergy in the global context. Int J Environ Res Public Health. 2018;15:2043. https://doi.org/10.3390/ijerph15092043

3. Backman H, Räisänen P, Hedman L, Stridsman C, Andersson M, Lindberg A, et al. Increased prevalence of allergic asthma from 1990 to 2006 and further to 2016 – results from three population surveys. Clin Exp Allergy. 2017;47:1426–1435. https://doi.org/10.1111/cea.12963

4. Alduraywish SA, Standl M, Lodge CJ, Abramson MJ, Allen KJ, Erbas B. Is there a march from early food sensitization to later childhood allergic airway disease? Results from two prospective birth cohort studies. Pediatr Allergy Immunol. 2016;28:30–37.https://doi.org/10.1111/pai.12651

5. Foong RX, du Toit G, Fox AT. Asthma, food allergy, and how they relate to each other. Front Pediatr. 2017;5:89. https:// doi.org/10.3389/fped.2017.00089

6. Bock SA, Muñoz-Furlong A, Sampson HA. Further fatalities caused by anaphylactic reactions to food, 2001-2006. J Allergy Clin Immunol. 2007;119:1016–1018. https://doi.org/10.1016/j. jaci.2006.12.622

7. Garcia-Rio F, Alvarez-Puebla MJ, Esteban-Gorgojo I, Barranco P, Olaguibel JM. Obesity and asthma. Key clinical questions. J Investig Allergol Clin Immunol. 2019;29:262–271. https://doi. org/10.18176/jiaci.0316

8. Sicherer SH. Epidemiology of food allergy. J Allergy Clin Immunol. 2011;127:594–602. https://doi.org/10.1016/j.jaci.2010.11.044

9. Loh W, Tang MLK. The epidemiology of food allergy in the global context. Int J Environ Res Public Health. 2018;15:2043. https://doi.org/10.3390/ijerph15092043

10. Osterballe M, Hansens TK, Mortz CG, Høst A, Bindslev-Jensen C. The prevalence of food hypersensitivity in an unselected population of children and adults. Pediatr Allergy Immunol. 2005;16:567–573. https://doi. org/10.1111/j.1399-3038.2005.00251.x

11. McBride D, Keil T, Grabenhenrich L, Dubakiene R, Drasutiene G, Fiocchi A, et al. The EuroPrevall birth cohort study on food allergy: baseline characteristics of 12,000 new-borns and their families from nine European countries. Pediatr Allergy Immunol. 2012;23(3):230–239. https://doi. org/10.1111/j.1399-3038.2011.01254.x

12. Burney P, Summers C, Chinn S, Hooper R, van Ree R, Lidholm J. Prevalence and distribution of sensitization to foods in the European Community Respiratory Health Survey: a EuroPrevall analysis. Allergy. 2010;65:1182–1188. https://doi. org/10.1111/j.1398-9995.2010.02346.x

13. Grabenhenrich L, Trendelenburg V, Bellach J, Yürek S, Reaich A, Fiandor A, et al. Frequency of food allergy in school-aged children in eight European countries - the EuroPrevall-iFAAM birth cohort. Allergy. 2020;75:2294–2308.https://doi. org/10.1111/all.14290

14. Ojeda P, Ibañez MD, Olaguibel JM, Sastre J, Chivato T. Alergológica 2015: a national survey on allergic diseases in the Spanish pediatric population. J Investig Allergol Clin Immunol. 2018 28:321–329.https://doi.org/10.18176/jiaci.0308

15. Ojeda P, Sastre J, Olaguibel JM, Chivato T. Alergológica 2015: a national survey on allergic diseases in the adult Spanish population. J Investig Allergol Clin Immunol. 2018;28:151–164. https://doi.org/10.18176/jiaci.0264

16. Faber MA, Van Gasse AM, Decuyper II, Sabato V, Hagendorens MM, Mertens C, et al. Cross reactive aeroallergens: Which need to cross our mind in food allergy diagnosis? J Allergy Clin Immunol Pract. 2018;6:1813–1823.https://doi.org/10.1016/j. jaip.2018.08.010

17. Shirasaki h, Yamamoto T, Abe S, Kanaizumi E, Kikuchi M, Himi T. Clinical benefit of component-resolved diagnosis in Japanese birch-allergic patients with a convincing history of apple or peach allergy. Auris Nasus Larynx. 2017;44:442–446. https://doi.org/10.1016/j.anl.2016.10.004

18. Ciprandi G, Del Barba P, Silvestri M, Barberi S, Tosca MA. Pru p 3 sensitization in children with allergy to Parietaria pollens. Acta Biomed. 2019;90(2):265–268. https://doi.org/10.23750/ abm.v90i2.7611

19. Rosace D, Gomez-Casado C, Fernandez P, Perez-Gordo M, Dominguez MDC, Vega A, et al. Profilin-mediated food-induced allergic reactions are associated with oral epithelial remodel-ing. J Allergy Clin Immunol. 2019;143;2:681.e1–690.e1.https:// doi.org/10.1016/j.jaci.2018.03.013

20. Gámez C, Zafra M, Boquete M, Sanz V, Mazzeo C, Ibáñez MD, et al. New shrimp IgE-binding proteins involved in mite-sea-food cross-reactivity. Mol Nutr Food Res. 2014 Sep;58(9):1915– 1925.https://doi.org/10.1002/mnfr.201400122

21. Pali Schöll I, Jensen-Jarolim E. Gender aspects in food allergy. Curr Opin Allergy Clin Immunol. 2019 Jun;19(3):249–255. https://doi.org/10.1097/ACI.0000000000000529

22. Lang JE, Bunnell HT, Lima JJ, Hossain MJ, Wysocki T, Bacharier L, et al. Effects of age, sex, race/ethnicity, and allergy status in obesity-related pediatric asthma. Pediatr Pulmonol. 2019 Nov;54(11):1684 1693.https://doi.org/10.1002/ppul.24470

23. Hohmann C, Keller T, Gehring U, Wijga A, Standl M, Kull I, et al. Sex-specific incidence of asthma, rhinitis and respiratory multimorbidity before and after puberty onset: individual participant meta-analysis of five birth cohorts collaborating in MeDALL. BMJ Open Respir Res. 2019 Sep 13;6(1):e000460. https://doi.org/10.1136/bmjresp-2019-000460

24. Boyano-Martinez T, Pedrosa M, Belver T, Quirce S, Garcia-Ara C. Peach allergy in Spanish children: tolerance to the pulp and molecular sensitization profile. Pediatr Allergy Immunol. 2013;24:168–172.https://doi.org/10.1111/pai.12037

25. Rodriguez Del Rio P, Diaz-Perales A, Sánchez-García S, Escudero C, Ibáñez Md, Mendez-Brea P, et al. Profilin, a change in the paradigm. J Investig Allergol Clin Immunol. 2018;28:1–12.https://doi.org/10.18176/jiaci.0193

26. Pavic I, Kolaček S. Growth of children with food allergy. Horm Res Paediatr. 2017;88(1):91–100. https://doi.org/10.1159/ 000462973

27. Wolthers OD. Questionnaire about the risk of growth suppression on inhaled corticosteroids. BMJ Paediatr Open. 2019 Aug 30;3(1):e000533.https://doi.org/10.1136/bmjpo-2019-000533

28. Yung JA, Fuseini H, Newcomb DC. Horomes, sex and asthma. Ann Allergy Asthma Immunol. 2018;120(5):488–494.https://doi. org/10.1016/j.anai.2018.01.016

29. Alduraywish S, Luzak A, Lodge C, Aldakheel F, Erbas B, Allen K, et al. The role of early life food sensitization in adolescent lung function: results from 2 birth cohort studies. J Allergy Clin Immunol Pract. 2019;7:1825.e12–1834.e12.https://doi. org/10.1016/j.jaip.2019.01.050

30. Holguin F, Bleecker ER, Busse WW, Calhoun WJ, Castro M, et al. Obesity and asthma: an association modified by age of asthma onset. J Allergy Clin Immunol. 2011 Jun;127(6):1486– 1493.https://doi.org/10.1016/j.jaci.2011.03.036

31. Nelson RK, Bush a, Stokes J, Nair P, Akuthota P. Eosinophilic asthma. J Allergy Clin Immunol Pract. 2020 Feb;8(2):465–473. https://doi.org/10.1016/j.jaip.2019.11.024

32. Esteban-Gorgojo I, Antolín-Amérigo D, Domínguez-Ortega J, Quirce S. Non-eosinophilic asthma: current perspectives. J Asthma allergy. 2018;11:267–281.https://doi.org/10.2147/JAA. S153097

33. Longo G, Scornavacca G, Strinati R, Poli F. [Food allergy in asthma. Diagnostic significance of peripheral eosinophils]. Pediatr Med Chir. 1987;9(6):663–668. http://www.pediatrmed-chir.org/index.php/pmc/index

34. Cello JP. Eosinophilic gastroenteritis – a complex dis-ease entity. Am J Med. 1979;67:1097–1104.https://doi. org/10.1016/0002-9343(79)90652-1

35. Dellon ES, Guo R, McGee SJ, Hamilton DK, Nicolai E, Convington J, et al. A novel allergen-specific immune signature-directed approach to dietary elimination in eosinophilic esophagitis. Clin Transl Gastroenterol. 2019;10(12):e00099. https://doi.org/10.14309/ctg.0000000000000099

36. Fineman SM, Rosen FS, Geha RS. Transient hypogamma-globulinemia, elevated immunoglobulin E levels, and food allergy. J Allergy Clin Immunol. 1979;64:216–222. https://doi. org/10.1016/0091-6749(79)90098-8

37. Preece K, Bhatia R, Belcher J, Patchett K, McElduff P, Collison A, et al. The fraction of exhaled nitric oxide improves prediction of clinical allergic reaction to peanut challenge in children. Clin Exp Allergy. 2014;44:371–380. https://doi. org/10.1111/cea.12258

38. Benhamou AH, Koehli A, Rochat I, Inci D, Moeller A, Taramarcaz P, et al. Exhaled nitric oxide decreases after positive food-allergen challenge. Clin Transl Allergy. 2011;1:14. https://doi.org/10.1186/2045-7022-1-14

39. Walford HH, Doherty TA. Diagnosis and management of eosinophilic asthma: a US perspective. J Asthma Allergy. 2014;7:53– 65. https://doi.org/10.2147/JAA.S39119

40. Ochfeld EN, Pongracic JA. Food allergy: diagnosis and treatment. Allergy Asthma Proc. 2019;40:446–449. https://doi. org/10.2500/aap.2019.40.4268