Advertisement

Clinical Reviews in Allergy & Immunology

, Volume 55, Issue 1, pp 65–69 | Cite as

Does Aeroallergen Sensitization Cause or Contribute to Eosinophilic Esophagitis?

  • Jesus R. Guajardo
  • Melissa A. Zegarra-Bustamante
  • Edward G. Brooks
Article

Abstract

Eosinophilic esophagitis is an atopic disease defined clinically by esophageal symptoms in combination with a dense esophageal eosinophilia. EoE is triggered and maintained by exposure to certain foods and it is known that dietary modification controls symptoms and achieves disease remission. Recently, aeroallergens have been implicated in the pathogenesis of EoE. To examine the role of aeroallergens in EoE, we reviewed the published literature. Sensitization and production of IgE antibodies to foods and aeroallergens in subjects with EoE has been demonstrated. However, the evidence suggests only a minor role for IgE-mediated immune reactions in EoE. There is some evidence to support an association of EoE diagnosis and flares with environmental allergen exposure, and animal studies support the notion that EoE may be induced by exposure to inhalant allergens. Some studies show that newly diagnosed cases of EoE follow a seasonal pollen distribution (summer and spring), but the weight of evidence does not support the seasonal occurrence of diagnosis or worsening of symptoms. Overall, we conclude that the current evidence does not support causality in inhalant allergen exposure and the genesis nor exacerbations of EoE in humans, although there is a possibility that inhalant allergen sensitization could play a modifying role in EoE in the context of cross-reacting food allergens.

Keywords

Eosinophilic esophagitis Aeroallergen Pollen Cross-reactivity 

Abbreviations

EoE

eosinophilic esophagitis

SPT

skin prick test

SLIT

sub-lingual immunotherapy

OAS

oral allergy syndrome

APT

atopy patch test

PR

pathogenesis related

CRD

component-resolved diagnosis

Notes

Compliance with Ethical Standards

Conflict of Interest

JRG and MAZ-B declare that they have no conflict of interest. EGB has received a research contract from ALK-Abello investigating allergen T cell epitopes and serves on the Scientific Advisory Board for United Allergy Services.

Research Involving Human Participants and/or Animals

There is no research involving humans or animals

Informed Consent

No human research.

References

  1. 1.
    Gomez Torrijos E, Sanchez Miranda P, Donado Palencia P, Castro Jimenez A, Rodriguez Sanchez J, Mendez Diaz Y, Moreno Lozano L, Garcia Rodriguez R (2017) Eosinophilic esophagitis: demographic, clinical, endoscopic, histologic, and atopic characteristics of children and teenagers in a region in central Spain. J Investig Allergol Clin Immunol 27(2):104–110.  https://doi.org/10.18176/jiaci.0112 CrossRefPubMedGoogle Scholar
  2. 2.
    Simon D, Marti H, Heer P, Simon H-U, Braathen LR, Straumann A (2005) Eosinophilic esophagitis is frequently associated with IgE-mediated allergic airway diseases. J Allergy Clin Immunol 115(5):1090–1092.  https://doi.org/10.1016/j.jaci.2005.01.017 CrossRefPubMedGoogle Scholar
  3. 3.
    Roy-Ghanta S, Larosa DF, Katzka DA (2008) Atopic characteristics of adult patients with eosinophilic esophagitis. Clin Gastroenterol Hepatol 6(5):531–535.  https://doi.org/10.1016/j.cgh.2007.12.045 CrossRefPubMedGoogle Scholar
  4. 4.
    Clayton F, Fang JC, Gleich GJ, Lucendo AJ, Olalla JM, Vinson LA, Lowichik A, Chen X, Emerson L, Cox K, O’Gorman MA, Peterson KA (2014) Eosinophilic esophagitis in adults is associated with IgG4 and not mediated by IgE. Gastroenterology 147(3):602–609.  https://doi.org/10.1053/j.gastro.2014.05.036 CrossRefPubMedGoogle Scholar
  5. 5.
    Stein ML, Collins MH, Villanueva JM, Kushner JP, Putnam PE, Buckmeier BK, Filipovich AH, Assa'ad AH, Rothenberg ME (2006) Anti-IL-5 (mepolizumab) therapy for eosinophilic esophagitis. J Allergy Clin Immunol 118(6):1312–1319.  https://doi.org/10.1016/j.jaci.2006.09.007 CrossRefPubMedGoogle Scholar
  6. 6.
    Lucendo AJ, Arias A, Tenias JM (2014) Relation between eosinophilic esophagitis and oral immunotherapy for food allergy: a systematic review with meta-analysis. Ann Allergy Asthma Immunol 113(6):624–629.  https://doi.org/10.1016/j.anai.2014.08.004 CrossRefPubMedGoogle Scholar
  7. 7.
    Lucendo AJ, Molina-Infante J, Arias Á, von Arnim U, Bredenoord AJ, Bussmann C, Amil Dias J, Bove M, González-Cervera J, Larsson H, Miehlke S, Papadopoulou A, Rodríguez-Sánchez J, Ravelli A, Ronkainen J, Santander C, Schoepfer AM, Storr MA, Terreehorst I, Straumann A, Attwood SE (2017) Guidelines on eosinophilic esophagitis: evidence-based statements and recommendations for diagnosis and management in children and adults. United European Gastroenterol J 5(3):335–358.  https://doi.org/10.1177/2050640616689525 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Philpott H, Nandurkar S, Royce SG, Thien F, Gibson PR (2016) Allergy tests do not predict food triggers in adult patients with eosinophilic oesophagitis. A comprehensive prospective study using five modalities. Aliment Pharmacol Ther 44(3):223–233.  https://doi.org/10.1111/apt.13676 CrossRefPubMedGoogle Scholar
  9. 9.
    Mishra A, Hogan SP, Brandt EB, Rothenberg ME (2001) An etiological role for aeroallergens and eosinophils in experimental esophagitis. J Clin Invest 107(1):83–90.  https://doi.org/10.1172/JCI10224 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Rayapudi M, Mavi P, Zhu X, Pandey AK, Abonia JP, Rothenberg ME, Mishra A (2010) Indoor insect allergens are potent inducers of experimental eosinophilic esophagitis in mice. J Leukoc Biol 88(2):337–346.  https://doi.org/10.1189/jlb.0110025 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Fogg MI, Ruchelli E, Spergel JM (2003) Pollen and eosinophilic esophagitis. J Allergy Clin Immunol 112(4):796–797CrossRefPubMedGoogle Scholar
  12. 12.
    Fahey L, Robinson G, Weinberger K, Giambrone AE, Solomon AB (2017) Correlation between aeroallergen levels and new diagnosis of eosinophilic esophagitis in New York City. J Pediatr Gastroenterol Nutr 64(1):22–25.  https://doi.org/10.1097/mpg.0000000000001245 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Ram G, Lee J, Ott M, Brown-Whitehorn TF, Cianferoni A, Shuker M, Wang M-L, Verma R, Liacouras CA, Spergel JM (2015) Seasonal exacerbation of esophageal eosinophilia in children with eosinophilic esophagitis and allergic rhinitis. Ann Allergy Asthma Immunol 115(3):224–228.e221.  https://doi.org/10.1016/j.anai.2015.07.004 CrossRefPubMedGoogle Scholar
  14. 14.
    Philpott HL, Nandurkar S, Thien F, Bloom S, Lin E, Goldberg R, Boyapati R, Finch A, Royce SG, Gibson PR (2015) Seasonal recurrence of food bolus obstruction in eosinophilic esophagitis. Intern Med J 45(9):939–943.  https://doi.org/10.1111/imj.12790 CrossRefPubMedGoogle Scholar
  15. 15.
    Wang FY, Gupta SK, Fitzgerald JF (2007) Is there a seasonal variation in the incidence or intensity of allergic eosinophilic esophagitis in newly diagnosed children? J Clin Gastroenterol 41(5):451–453.  https://doi.org/10.1097/01.mcg.0000248019.16139.67 CrossRefPubMedGoogle Scholar
  16. 16.
    Prasad GA, Alexander JA, Schleck CD, Zinsmeister AR, Smyrk TC, Elias RM, Locke GR 3rd, Talley NJ (2009) Epidemiology of eosinophilic esophagitis over three decades in Olmsted County, Minnesota. Clin Gastroenterol Hepatol 7(10):1055–1061.  https://doi.org/10.1016/j.cgh.2009.06.023 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Almansa C, Krishna M, Buchner AM, Ghabril MS, Talley N, DeVault KR, Wolfsen H, Raimondo M, Guarderas JC, Achem SR (2009) Seasonal distribution in newly diagnosed cases of eosinophilic esophagitis in adults. Am J Gastroenterol 104(4):828–833.  https://doi.org/10.1038/ajg.2008.169 CrossRefPubMedGoogle Scholar
  18. 18.
    Moawad FJ, Veerappan GR, Lake JM, Maydonovitch CL, Haymore BR, Kosisky SE, Wong RK (2010) Correlation between eosinophilic oesophagitis and aeroallergens. Aliment Pharmacol Ther 31(4):509–515.  https://doi.org/10.1111/j.1365-2036.2009.04199.x CrossRefPubMedGoogle Scholar
  19. 19.
    Wolf WA, Jerath MR, Dellon ES (2013) De-novo onset of eosinophilic esophagitis after large volume allergen exposures. J Gastrointestin Liver Dis 22(2):205–208PubMedPubMedCentralGoogle Scholar
  20. 20.
    Jensen ET, Shah ND, Hoffman K, Sonnenberg A, Genta RM, Dellon ES (2015) Seasonal variation in detection of oesophageal eosinophilia and eosinophilic oesophagitis. Aliment Pharmacol Ther 42(4):461–469.  https://doi.org/10.1111/apt.13273 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Iwanczak B, Janczyk W, Ryzko J, Banaszkiewicz A, Radzikowski A, Jarocka-Cyrta E, Kaczmarski M, Czkwianianc E, Korczowski B, Czaja-Bulsa G, Zielinska I, Czerwionka-Szaflarska M, Kwiecien J, Ogrodowska M, Daukszewicz A, Pytrus T, Iwanczak F (2011) Eosinophilic esophagitis in children: frequency, clinical manifestations, endoscopic findings, and seasonal distribution. Adv Med Sci 56(2):151–157.  https://doi.org/10.2478/v10039-011-0038-7 CrossRefPubMedGoogle Scholar
  22. 22.
    Elias MK, Kopacova J, Arora AS, Dierkhising RA, Enders FT, Katzka DA, Kryzer LA, Halland M, Smyrk TC, Talley NJ, Alexander JA (2015) The diagnosis of esophageal eosinophilia is not increased in the summer months. Dysphagia 30(1):67–73.  https://doi.org/10.1007/s00455-014-9574-1 CrossRefPubMedGoogle Scholar
  23. 23.
    Elitsur Y, Aswani R, Lund V, Dementieva Y (2013) Seasonal distribution and eosinophilic esophagitis: the experience in children living in rural communities. J Clin Gastroenterol 47(3):287–288.  https://doi.org/10.1097/MCG.0b013e31826df861 CrossRefPubMedGoogle Scholar
  24. 24.
    Chadha M, Agarwal A, Agarwal N, Singh MK (2007) Solitary eosinophilic granuloma of the radius. An unusual differential diagnosis. Acta Orthop Belg 73(3):413–417PubMedGoogle Scholar
  25. 25.
    Sorser SA, Barawi M, Hagglund K, Almojaned M, Lyons H (2013) Eosinophilic esophagitis in children and adolescents: epidemiology, clinical presentation and seasonal variation. J Gastroenterol 48(1):81–85.  https://doi.org/10.1007/s00535-012-0608-x CrossRefPubMedGoogle Scholar
  26. 26.
    van Rhijn BD, Verheij J, Smout AJ, Bredenoord AJ (2013) Rapidly increasing incidence of eosinophilic esophagitis in a large cohort. Neurogastroenterol Motil 25(1):47–52.e45.  https://doi.org/10.1111/nmo.12009 CrossRefPubMedGoogle Scholar
  27. 27.
    Frederickson NW, Bayman L, Valestin J, Redd M, Lee YJ, Soubra M, Schey R (2014) Lack of seasonal variation in the incidence of eosinophilic oesophagitis in adolescent and adult non-PPI-responsive oesophageal eosinophilia midwestern US populations. United European Gastroenterol J 2(2):69–76.  https://doi.org/10.1177/2050640614525152 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Lucendo AJ, Arias Á, Redondo-González O, González-Cervera J (2015) Seasonal distribution of initial diagnosis and clinical recrudescence of eosinophilic esophagitis: a systematic review and meta-analysis. Allergy 70(12):1640–1650.  https://doi.org/10.1111/all.12767 CrossRefPubMedGoogle Scholar
  29. 29.
    Simon D, Straumann A, Wenk A, Spichtin H, Simon HU, Braathen LR (2006) Eosinophilic esophagitis in adults—no clinical relevance of wheat and rye sensitizations. Allergy 61(12):1480–1483.  https://doi.org/10.1111/j.1398-9995.2006.01224.x CrossRefPubMedGoogle Scholar
  30. 30.
    Sugnanam KK, Collins JT, Smith PK, Connor F, Lewindon P, Cleghorn G, Withers G (2007) Dichotomy of food and inhalant allergen sensitization in eosinophilic esophagitis. Allergy 62(11):1257–1260.  https://doi.org/10.1111/j.1398-9995.2007.01454.x CrossRefPubMedGoogle Scholar
  31. 31.
    Castro Jimenez A, Gomez Torrijos E, Garcia Rodriguez R, Feo Brito F, Borja Segade J, Galindo Bonilla PA, Rodriguez-Sanchez J, Guerra Pasadas F (2014) Demographic, clinical and allergological characteristics of eosinophilic esophagitis in a Spanish central region. Allergol Immunopathol (Madr) 42(5):407–414.  https://doi.org/10.1016/j.aller.2013.04.004 CrossRefGoogle Scholar
  32. 32.
    Rodrigues M, D'Amico MF, Patino FR, Barbieri D, Damiao AO, Sipahi AM (2013) Clinical manifestations, treatment, and outcomes of children and adolescents with eosinophilic esophagitis. J Pediatr 89(2):197–203.  https://doi.org/10.1016/j.jped.2013.03.001 CrossRefGoogle Scholar
  33. 33.
    Arias A, Gonzalez-Cervera J, Tenias JM, Lucendo AJ (2014) Efficacy of dietary interventions for inducing histologic remission in patients with eosinophilic esophagitis: a systematic review and meta-analysis. Gastroenterology 146(7):1639–1648.  https://doi.org/10.1053/j.gastro.2014.02.006 CrossRefPubMedGoogle Scholar
  34. 34.
    Mahdavinia M, Bishehsari F, Hayat W, Elhassan A, Tobin MC, Ditto AM (2017) Association of eosinophilic esophagitis and food pollen allergy syndrome. Ann Allergy Asthma Immunol 118(1):116–117.  https://doi.org/10.1016/j.anai.2016.10.012 CrossRefPubMedGoogle Scholar
  35. 35.
    Hill DA, Dudley JW, Spergel JM (2017) The prevalence of eosinophilic esophagitis in pediatric patients with IgE-mediated food allergy. J Allergy Clin Immunol Pract 5(2):369–375.  https://doi.org/10.1016/j.jaip.2016.11.020 CrossRefPubMedGoogle Scholar
  36. 36.
    van Rhijn BD, van Ree R, Versteeg SA, Vlieg-Boerstra BJ, Sprikkelman AB, Terreehorst I, Smout AJPM, Bredenoord AJ (2013) Birch pollen sensitization with cross-reactivity to food allergens predominates in adults with eosinophilic esophagitis. Allergy 68(11):1475–1481.  https://doi.org/10.1111/all.12257 CrossRefPubMedGoogle Scholar
  37. 37.
    van Rhijn BD, Vlieg-Boerstra BJ, Versteeg SA, Akkerdaas JH, van Ree R, Terreehorst I, Sprikkelman AB, Verheij J, Smout AJPM, Bredenoord AJ (2015) Evaluation of allergen-microarray–guided dietary intervention as treatment of eosinophilic esophagitis. J Allergy Clin Immunol 136(4):1095–1097.e1093.  https://doi.org/10.1016/j.jaci.2015.02.038 CrossRefPubMedGoogle Scholar
  38. 38.
    Miehlke S, Alpan O, Schröder S, Straumann A (2013) Induction of eosinophilic esophagitis by sublingual pollen immunotherapy. Case Rep Gastroenterol 7(3):363–368.  https://doi.org/10.1159/000355161 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Pesek RD, Rettiganti M, O'Brien E, Beckwith S, Daniel C, Luo C, Scurlock AM, Chandler P, Levy RA, Perry TT, Kennedy JL, Chervinskiy S, Vonlanthen M, Casteel H, Fiedorek SC, Gibbons T, Jones SM (2017) Effects of allergen sensitization on response to therapy in children with eosinophilic esophagitis. Ann Allergy Asthma Immunol 119(2):177–183.  https://doi.org/10.1016/j.anai.2017.06.006 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Spergel JM, Andrews T, Brown-Whitehorn TF, Beausoleil JL, Liacouras CA (2005) Treatment of eosinophilic esophagitis with specific food elimination diet directed by a combination of skin prick and patch tests. Ann Allergy Asthma Immunol 95(4):336–343.  https://doi.org/10.1016/s1081-1206(10)61151-9 CrossRefPubMedGoogle Scholar
  41. 41.
    Spergel JM, Brown-Whitehorn TF, Cianferoni A, Shuker M, Wang ML, Verma R, Liacouras CA (2012) Identification of causative foods in children with eosinophilic esophagitis treated with an elimination diet. J Allergy Clin Immunol 130(2):461–467.e465.  https://doi.org/10.1016/j.jaci.2012.05.021 CrossRefPubMedGoogle Scholar
  42. 42.
    Osterballe M, Andersen KE, Bindslev-Jensen C (2004) The diagnostic accuracy of the atopy patch test in diagnosing hypersensitivity to cow’s milk and hen’s egg in unselected children with and without atopic dermatitis. J Am Acad Dermatol 51(4):556–562.  https://doi.org/10.1016/j.jaad.2004.03.025 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jesus R. Guajardo
    • 1
  • Melissa A. Zegarra-Bustamante
    • 2
  • Edward G. Brooks
    • 2
  1. 1.Division of Pulmonary Medicine, Department of PediatricsUT Health San AntonioSan AntonioUSA
  2. 2.Division of Immunology and Infectious Disease, Department of PediatricsUT Health San AntonioSan AntonioUSA

Personalised recommendations