Skip to main content

Advertisement

Log in

Dietary Therapy for Eosinophilic Esophagitis: Elimination and Reintroduction

  • Published:
Clinical Reviews in Allergy & Immunology Aims and scope Submit manuscript

Abstract

Eosinophilic esophagitis (EoE) is a food antigen-mediated disorder of the esophagus characterized by eosinophil predominant inflammation and symptoms of esophageal dysfunction. Dietary antigen elimination induces clinical and histological remission in patients with EoE. The most restrictive of elimination diets (the elemental diet) removes all possible food antigens while empiric elimination diets remove all (or a subset) of food antigens most commonly reported to cause esophageal eosinophilia and food allergies (milk, egg, wheat, soy, peanuts, tree nuts, fish, or legumes). Elimination diets are effective treatments for EoE but pose psychosocial and financial challenges to patients and consequently may impair quality of life. Foods that are commonly eliminated, especially milk, are also nutrient-dense and therefore their elimination may result in inadequate nutrient intake or deficiencies without careful diet planning to include nutritionally comparable and safe food substitutes. After remission is achieved with elimination diets, foods can be reintroduced sequentially to identify specific food triggers, but this reintroduction is not standardized. Food elimination and food reintroductions should consider the patient’s lifestyle, nutrition needs, and skills and ideally be managed by a team with knowledge of eosinophilic gastrointestinal disorders and nutrition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Liacouras CA, Furuta GT, Hirano I, Atkins D, Attwood SE, Bonis PA et al (2011) Eosinophilic esophagitis: updated consensus recommendations for children and adults. J Allergy Clin Immunol 128(1):3–20 e6; quiz 1-2

    Article  PubMed  Google Scholar 

  2. Kelly KJ, Lazenby AJ, Rowe PC, Yardley JH, Perman JA, Sampson HA (1995) Eosinophilic esophagitis attributed to gastroesophageal reflux: improvement with an amino acid-based formula. Gastroenterology 109(5):1503–1512

    Article  PubMed  CAS  Google Scholar 

  3. Kagalwalla AF, Sentongo TA, Ritz S, Hess T, Nelson SP, Emerick KM et al (2006) Effect of six-food elimination diet on clinical and histologic outcomes in eosinophilic esophagitis. Clin Gastroenterol Hepatol 4(9):1097–1102

    Article  PubMed  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. Peterson KA, Byrne KR, Vinson LA, Ying J, Boynton KK, Fang JC, Gleich GJ, Adler DG, Clayton F (2013) Elemental diet induces histologic response in adult eosinophilic esophagitis. Am J Gastroenterol 108(5):759–766. https://doi.org/10.1038/ajg.2012.468

    Article  PubMed  CAS  Google Scholar 

  6. Warners MJ, Vlieg-Boerstra BJ, Verheij J, van Rhijn BD, Van Ampting MT, Harthoorn LF et al (2017) Elemental diet decreases inflammation and improves symptoms in adult eosinophilic oesophagitis patients. Aliment Pharmacol Ther 45(6):777–787. https://doi.org/10.1111/apt.13953

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Henderson CJ, Abonia JP, King EC, Putnam PE, Collins MH, Franciosi JP, Rothenberg ME (2012) Comparative dietary therapy effectiveness in remission of pediatric eosinophilic esophagitis. J Allergy Clin Immunol 129(6):1570–1578. https://doi.org/10.1016/j.jaci.2012.03.023

    Article  PubMed  PubMed Central  Google Scholar 

  8. Al-Hussaini A, Al-Idressi E, Al-Zahrani M (2013) The role of allergy evaluation in children with eosinophilic esophagitis. J Gastroenterol 48(11):1205–1212

    Article  PubMed  CAS  Google Scholar 

  9. De Agustin JC, Sanz N, Canals MJ, Alvarez E, Morales JL, Soler J et al (2002) Successful medical treatment of two patients with eosinophilic oesophagitis. J Pediatr Surg 37(2):207–213

    Article  PubMed  Google Scholar 

  10. Kagalwalla AF, Amsden K, Shah A, Ritz S, Manuel-Rubio M, Dunne K, Nelson SP, Wershil BK, Melin-Aldana H (2012) Cow’s milk elimination: a novel dietary approach to treat eosinophilic esophagitis. J Pediatr Gastroenterol Nutr 55(6):711–716. https://doi.org/10.1097/MPG.0b013e318268da40

    Article  PubMed  CAS  Google Scholar 

  11. Liacouras CA, Spergel JM, Ruchelli E, Verma R, Mascarenhas M, Semeao E, Flick J, Kelly J, Brown–Whitehorn T, Mamula P, Markowitz JE (2005) Eosinophilic esophagitis: a 10-year experience in 381 children. Clin Gastroenterol Hepatol 3(12):1198–1206. https://doi.org/10.1016/S1542-3565(05)00885-2

    Article  PubMed  Google Scholar 

  12. Lucendo AJ, Arias A, Gonzalez-Cervera J, Yague-Compadre JL, Guagnozzi D, Angueira T et al (2013) Empiric 6-food elimination diet induced and maintained prolonged remission in patients with adult eosinophilic esophagitis: a prospective study on the food cause of the disease. J Allergy Clin Immunol 131(3):797–804. https://doi.org/10.1016/j.jaci.2012.12.664

    Article  PubMed  Google Scholar 

  13. Gonsalves N, Yang GY, Doerfler B, Ritz S, Ditto AM, Hirano I (2012) Elimination diet effectively treats eosinophilic esophagitis in adults; food reintroduction identifies causative factors. Gastroenterology 142(7):1451–9 e1 quiz e14–5

    Article  PubMed  Google Scholar 

  14. Wolf WA, Jerath MR, Sperry SL, Shaheen NJ, Dellon ES (2014) Dietary elimination therapy is an effective option for adults with eosinophilic esophagitis. Clin Gastroenterol Hepatol 12(8):1272–1279. https://doi.org/10.1016/j.cgh.2013.12.034

    Article  PubMed  PubMed Central  Google Scholar 

  15. Rodriguez-Sanchez J, Gomez Torrijos E, Lopez Viedma B, de la Santa Belda E, Martin Davila F, Garcia Rodriguez C et al (2014) Efficacy of IgE-targeted vs empiric six-food elimination diets for adult eosinophilic oesophagitis. Allergy 69(7):936–942. https://doi.org/10.1111/all.12420

    Article  PubMed  CAS  Google Scholar 

  16. Philpott H, Nandurkar S, Royce SG, Thien F, Gibson PR (2016) A prospective open clinical trial of a proton pump inhibitor, elimination diet and/or budesonide for eosinophilic oesophagitis. Aliment Pharmacol Ther 43(9):985–993. https://doi.org/10.1111/apt.13576

    Article  PubMed  CAS  Google Scholar 

  17. Kagalwalla AF, Shah A, Li BU, Sentongo TA, Ritz S, Manuel-Rubio M et al (2011) Identification of specific foods responsible for inflammation in children with eosinophilic esophagitis successfully treated with empiric elimination diet. J Pediatr Gastroenterol Nutr 53(2):145–149. https://doi.org/10.1097/MPG.0b013e31821cf503

    Article  PubMed  CAS  Google Scholar 

  18. Molina-Infante J, Arias A, Barrio J, Rodriguez-Sanchez J, Sanchez-Cazalilla M, Lucendo AJ (2014) Four-food group elimination diet for adult eosinophilic esophagitis: a prospective multicenter study. J Allergy Clin Immunol 134(5):1093–1099 e1

    Article  PubMed  Google Scholar 

  19. Kagalwalla AF, Wechsler JB, Amsden K, Schwartz S, Makhija M, Olive A, Davis CM, Manuel-Rubio M, Marcus S, Shaykin R, Sulkowski M, Johnson K, Ross JN, Riffle ME, Groetch M, Melin-Aldana H, Schady D, Palac H, Kim KYA, Wershil BK, Collins MH, Chehade M (2017) Efficacy of a 4-food elimination diet for children with eosinophilic esophagitis. Clin Gastroenterol Hepatol 15(11):1698–1707.e7. https://doi.org/10.1016/j.cgh.2017.05.048

    Article  PubMed  Google Scholar 

  20. Molina-Infante J, Arias A, Alcedo J, Garcia-Romero R, Casabona-Frances S, Prieto-Garcia A, Modolell I, Gonzalez-Cordero PL, Perez-Martinez I, Martin-Lorente JL, Guarner-Argente C, Masiques ML, Vila-Miravet V, Garcia-Puig R, Savarino E, Sanchez-Vegazo CT, Santander C, Lucendo AJ (2017) Step-up empiric elimination diet for pediatric and adult eosinophilic esophagitis: the 2-4-6 study. J Allergy Clin Immunol. https://doi.org/10.1016/j.jaci.2017.08.038

  21. Kruszewski PG, Russo JM, Franciosi JP, Varni JW, Platts-Mills TA, Erwin EA (2016) Prospective, comparative effectiveness trial of cow’s milk elimination and swallowed fluticasone for pediatric eosinophilic esophagitis. Dis Esophagus 29(4):377–384. https://doi.org/10.1111/dote.12339

    Article  PubMed  CAS  Google Scholar 

  22. Spergel JM, Beausoleil JL, Mascarenhas M, Liacouras CA (2002) The use of skin prick tests and patch tests to identify causative foods in eosinophilic esophagitis. J Allergy Clin Immunol 109(2):363–368. https://doi.org/10.1067/mai.2002.121458

    Article  PubMed  Google Scholar 

  23. Simon D, Cianferoni A, Spergel JM, Aceves S, Holbreich M, Venter C, Rothenberg ME, Terreehorst I, Muraro A, Lucendo AJ, Schoepfer A, Straumann A, Simon HU (2016) Eosinophilic esophagitis is characterized by a non-IgE-mediated food hypersensitivity. Allergy 71(5):611–620. https://doi.org/10.1111/all.12846

    Article  PubMed  CAS  Google Scholar 

  24. 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 e3. https://doi.org/10.1016/j.jaci.2015.02.038

    Article  PubMed  Google Scholar 

  25. 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

    Article  PubMed  CAS  Google Scholar 

  26. Wilson JM, Schuyler AJ, Tripathi A, Erwin EA, Commins SP, Platts-Mills TAE (2016) IgG4 component allergens are preferentially increased in eosinophilic esophagitis as compared to patients with milk anaphylaxis or galactose-alpha-1,3-galactose allergy. J Allergy Clin Immunol. Presented AAAAI 2016

  27. Venter C, Fleischer DM (2016) Diets for diagnosis and management of food allergy: the role of the dietitian in eosinophilic esophagitis in adults and children. Ann Allergy Asthma Immunol 117(5):468–471. https://doi.org/10.1016/j.anai.2016.08.003

    Article  PubMed  Google Scholar 

  28. Liacouras CA, Wenner WJ, Brown K, Ruchelli E (1998) Primary eosinophilic esophagitis in children: successful treatment with oral corticosteroids. J Pediatr Gastroenterol Nutr 26(4):380–385

    Article  PubMed  CAS  Google Scholar 

  29. Aceves SS, Dohil R, Newbury RO, Bastian JF (2005) Topical viscous budesonide suspension for treatment of eosinophilic esophagitis. J Allergy Clin Immunol 116(3):705–706

    Article  PubMed  CAS  Google Scholar 

  30. Konikoff MR, Noel RJ, Blanchard C, Kirby C, Jameson SC, Buckmeier BK, Akers R, Cohen MB, Collins MH, Assa’ad AH, Aceves SS, Putnam PE, Rothenberg ME (2006) A randomized, double-blind, placebo-controlled trial of fluticasone propionate for pediatric eosinophilic esophagitis. Gastroenterology 131(5):1381–1391. https://doi.org/10.1053/j.gastro.2006.08.033

    Article  PubMed  CAS  Google Scholar 

  31. Ahmet A, Benchimol EI, Goldbloom EB, Barkey JL (2016) Adrenal suppression in children treated with swallowed fluticasone and oral viscous budesonide for eosinophilic esophagitis. Allergy Asthma Clin Immunol 12:49

    Article  PubMed  PubMed Central  Google Scholar 

  32. Golekoh MC, Hornung LN, Mukkada VA, Khoury JC, Putnam PE, Backeljauw PF (2016) Adrenal insufficiency after chronic swallowed glucocorticoid therapy for eosinophilic esophagitis. J Pediatr 170:240–245. https://doi.org/10.1016/j.jpeds.2015.11.026

    Article  PubMed  CAS  Google Scholar 

  33. Turpeinen M, Pelkonen AS, Nikander K, Sorva R, Selroos O, Juntunen-Backman K, Haahtela T (2010) Bone mineral density in children treated with daily or periodical inhaled budesonide: the Helsinki early intervention childhood asthma study. Pediatr Res 68(2):169–173. https://doi.org/10.1203/PDR.0b013e3181e69e36

    Article  PubMed  CAS  Google Scholar 

  34. Pedersen S (2006) Clinical safety of inhaled corticosteroids for asthma in children: an update of long-term trials. Drug Saf 29(7):599–612

    Article  PubMed  CAS  Google Scholar 

  35. Wolf WA, Cotton CC, Green DJ, Hughes JT, Woosley JT, Shaheen NJ, Dellon ES (2015) Predictors of response to steroid therapy for eosinophilic esophagitis and treatment of steroid-refractory patients. Clin Gastroenterol Hepatol 13(3):452–458. https://doi.org/10.1016/j.cgh.2014.07.034

    Article  PubMed  Google Scholar 

  36. Leung J, Hundal NV, Katz AJ, Shreffler WG, Yuan Q, Butterworth CA et al (2013) Tolerance of baked milk in patients with cow’s milk-mediated eosinophilic esophagitis. J Allergy Clin Immunol 132(5):1215–1216 e1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Groetch M, Henry M, Feuling MB, Kim J (2013) Guidance for the nutrition management of gastrointestinal allergy in pediatrics. J Allergy Clin Immunol Pract 1(4):323–331. https://doi.org/10.1016/j.jaip.2013.05.002

    Article  PubMed  Google Scholar 

  38. Burks AW, Jones SM, Boyce JA, Sicherer SH, Wood RA, Assa’ad A et al (2011) NIAID-sponsored 2010 guidelines for managing food allergy: applications in the pediatric population. Pediatrics 128(5):955–965

    Article  PubMed  PubMed Central  Google Scholar 

  39. Singhal S, Baker RD, Baker SS (2017) A comparison of the nutritional value of cow’s milk and nondairy beverages. J Pediatr Gastroenterol Nutr 64(5):799–805. https://doi.org/10.1097/MPG.0000000000001380

    Article  PubMed  CAS  Google Scholar 

  40. Fiocchi A, Schunemann HJ, Brozek J, Restani P, Beyer K, Troncone R et al (2010) Diagnosis and Rationale for Action Against Cow’s Milk Allergy (DRACMA): a summary report. J Allergy Clin Immunol 126(6):1119–1128 e12

    Article  PubMed  Google Scholar 

  41. Carvalho NF, Kenney RD, Carrington PH, Hall DE (2001) Severe nutritional deficiencies in toddlers resulting from health food milk alternatives. Pediatrics 107(4):E46

    Article  PubMed  CAS  Google Scholar 

  42. Kliewer KL, Venter C, Cassin AM, Abonia JP, Aceves SS, Bonis PA et al (2016) Should wheat, barley, rye, and/or gluten be avoided in a 6-food elimination diet? J Allergy Clin Immunol 137(4):1011–1014

    Article  PubMed  CAS  Google Scholar 

  43. Doerfler B, Bryce P, Hirano I, Gonsalves N (2015) Practical approach to implementing dietary therapy in adults with eosinophilic esophagitis: the Chicago experience. Dis Esophagus 28(1):42–58

    Article  PubMed  CAS  Google Scholar 

  44. Hernando A, Mujico JR, Mena MC, Lombardia M, Mendez E (2008) Measurement of wheat gluten and barley hordeins in contaminated oats from Europe, the United States and Canada by Sandwich R5 ELISA. Eur J Gastroenterol Hepatol 20(6):545–554. https://doi.org/10.1097/MEG.0b013e3282f46597

    Article  PubMed  Google Scholar 

  45. Marketsandmarkets.com. Gluten-free products market by type, sales channel and geography: global trends and forecasts to 2018. Available at http://www.marketsandmarkets.com/MarketReports/gluten-free-products-market-738.html2013

  46. Awazuhara H, Kawai H, Baba M, Matsui T, Komiyama A (1998) Antigenicity of the proteins in soy lecithin and soy oil in soybean allergy. Clin Exp Allergy 28(12):1559–1564. https://doi.org/10.1046/j.1365-2222.1998.00431.x

    Article  PubMed  CAS  Google Scholar 

  47. Groetch M, Venter C, Skypala I, Vlieg-Boerstra B, Grimshaw K, Durban R, Cassin A, Henry M, Kliewer K, Kabbash L, Atkins D, Nowak-Węgrzyn A, Holbreich M, Chehade M, Eosinophilic Gastrointestinal Disorders Committee of the American Academy of Allergy, Asthma and Immunology (2017) Dietary therapy and nutrition management of eosinophilic esophagitis: a work group report of the American Academy of Allergy, Asthma, and Immunology. J Allergy Clin Immunol Pract 5(2):312–324 e29. https://doi.org/10.1016/j.jaip.2016.12.026

    Article  PubMed  Google Scholar 

  48. Borneo R, Aguirre A, Leon AE (2010) Chia (Salvia hispanica L) gel can be used as egg or oil replacer in cake formulations. J Am Diet Assoc 110(6):946–949

    Article  PubMed  CAS  Google Scholar 

  49. Leonard SA, Nowak-Wegrzyn AH (2016) Baked milk and egg diets for milk and egg allergy management. Immunol Allergy Clin N Am 36(1):147–159. https://doi.org/10.1016/j.iac.2015.08.013

    Article  Google Scholar 

  50. Assa'ad AH, Putnam PE, Collins MH, Akers RM, Jameson SC, Kirby CL et al (2007) Pediatric patients with eosinophilic esophagitis: an 8-year follow-up. J Allergy Clin Immunol 119(3):731–738

    Article  PubMed  Google Scholar 

  51. Teuber SS, Brown RL, Haapanen LA (1997) Allergenicity of gourmet nut oils processed by different methods. J Allergy Clin Immunol 99(4):502–507

    Article  PubMed  CAS  Google Scholar 

  52. Stutius LM, Sheehan WJ, Rangsithienchai P, Bharmanee A, Scott JE, Young MC, Dioun AF, Schneider LC, Phipatanakul W (2010) Characterizing the relationship between sesame, coconut, and nut allergy in children. Pediatr Allergy Immunol 21(8):1114–1118. https://doi.org/10.1111/j.1399-3038.2010.00997.x

    Article  PubMed  PubMed Central  Google Scholar 

  53. Fiocchi A, Bouygue GR, Sarratud T, Terracciano L, Martelli A, Restani P (2004) Clinical tolerance of processed foods. Ann Allergy Asthma Immunol 93(5 Suppl 3):S38–S46. https://doi.org/10.1016/S1081-1206(10)61731-0

    Article  PubMed  Google Scholar 

  54. United States Food and Drug Administration CfFSaAN. Food Allergen Labeling and Consumer Protection Act of 2004 (Title II of Public Law 108e282). August 2004 ed2004

  55. Allen KJ, Turner PJ, Pawankar R, Taylor S, Sicherer S, Lack G, Rosario N, Ebisawa M, Wong G, Mills EN, Beyer K, Fiocchi A, Sampson HA (2014) Precautionary labelling of foods for allergen content: are we ready for a global framework? World Allergy Organ J 7(1):10. https://doi.org/10.1186/1939-4551-7-10

    Article  PubMed  PubMed Central  Google Scholar 

  56. Turner PJ, Kemp AS, Campbell DE (2011) Advisory food labels: consumers with allergies need more than “traces” of information. BMJ 343(oct13 2):d6180. https://doi.org/10.1136/bmj.d6180

    Article  PubMed  Google Scholar 

  57. Ford LS, Taylor SL, Pacenza R, Niemann LM, Lambrecht DM, Sicherer SH (2010) Food allergen advisory labeling and product contamination with egg, milk, and peanut. J Allergy Clin Immunol 126(2):384–385. https://doi.org/10.1016/j.jaci.2010.05.034

    Article  PubMed  Google Scholar 

  58. Taft TH, Ballou S, Keefer L (2012) Preliminary evaluation of maternal caregiver stress in pediatric eosinophilic gastrointestinal disorders. J Pediatr Psychol 37(5):523–532

    Article  PubMed  PubMed Central  Google Scholar 

  59. Menard-Katcher C, Henry M, Furuta GT, Atkins D, Maune NC, Haas AM (2014) Significance of feeding dysfunction in eosinophilic esophagitis. World J Gastroenterol 20(31):11019–11022

    Article  PubMed  PubMed Central  Google Scholar 

  60. Haas AM, Maune NC (2009) Clinical presentation of feeding dysfunction in children with eosinophilic gastrointestinal disease. Immunol Allergy Clin N Am 29(1):65–75 ix

    Article  Google Scholar 

  61. Mukkada VA, Haas A, Maune NC, Capocelli KE, Henry M, Gilman N et al (2010) Feeding dysfunction in children with eosinophilic gastrointestinal diseases. Pediatrics 126(3):e672–e677

    Article  PubMed  Google Scholar 

  62. Pentiuk S, Putnam PE, Collins MH, Rothenberg ME (2009) Dissociation between symptoms and histological severity in pediatric eosinophilic esophagitis. J Pediatr Gastroenterol Nutr 48(2):152–160. https://doi.org/10.1097/MPG.0b013e31817f0197

    Article  PubMed  PubMed Central  Google Scholar 

  63. 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

    Article  PubMed  CAS  Google Scholar 

  64. 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

    Article  PubMed  Google Scholar 

  65. Ram G, Lee J, Ott M, Brown-Whitehorn TF, Cianferoni A, Shuker M, Wang ML, 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 e1. https://doi.org/10.1016/j.anai.2015.07.004

    Article  PubMed  Google Scholar 

  66. Broussard JL, Devkota S (2016) The changing microbial landscape of Western society: diet, dwellings and discordance. Mol Metab 5(9):737–742. https://doi.org/10.1016/j.molmet.2016.07.007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Tamburini S, Shen N, HC W, Clemente JC (2016) The microbiome in early life: implications for health outcomes. Nat Med 22(7):713–722

    Article  PubMed  CAS  Google Scholar 

  68. Jensen ET, Kuhl JT, Martin LJ, Rothenberg ME, Dellon ES (2017) Prenatal, intrapartum, and postnatal factors are associated with pediatric eosinophilic esophagitis. J Allergy Clin Immunol

  69. Benitez AJ, Hoffmann C, Muir AB, Dods KK, Spergel JM, Bushman FD, Wang ML (2015) Inflammation-associated microbiota in pediatric eosinophilic esophagitis. Microbiome 3(1):23. https://doi.org/10.1186/s40168-015-0085-6

    Article  PubMed  PubMed Central  Google Scholar 

  70. Harris JK, Fang R, Wagner BD, Choe HN, Kelly CJ, Schroeder S, Moore W, Stevens MJ, Yeckes A, Amsden K, Kagalwalla AF, Zalewski A, Hirano I, Gonsalves N, Henry LN, Masterson JC, Robertson CE, Leung DY, Pace NR, Ackerman SJ, Furuta GT, Fillon SA (2015) Esophageal microbiome in eosinophilic esophagitis. PLoS One 10(5):e0128346. https://doi.org/10.1371/journal.pone.0128346

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Markowitz JE, Spergel JM, Ruchelli E, Liacouras CA (2003) Elemental diet is an effective treatment for eosinophilic esophagitis in children and adolescents. Am J Gastroenterol 98(4):777–782

    Article  PubMed  CAS  Google Scholar 

  72. Wechsler JB, Schwartz S, Amsden K, Kagalwalla AF (2014) Elimination diets in the management of eosinophilic esophagitis. J Asthma Allergy 7:85–94. https://doi.org/10.2147/JAA.S47243

    Article  PubMed  PubMed Central  Google Scholar 

  73. Miles MV, Putnam PE, Miles L, Tang PH, DeGrauw AJ, Wong BL, Horn PS, Foote HL, Rothenberg ME (2011) Acquired coenzyme Q10 deficiency in children with recurrent food intolerance and allergies. Mitochondrion 11(1):127–135. https://doi.org/10.1016/j.mito.2010.08.010

    Article  PubMed  CAS  Google Scholar 

  74. Lucendo AJ, Arias A, Gonzalez-Cervera J, Mota-Huertas T, Yague-Compadre JL (2013) Tolerance of a cow’s milk-based hydrolyzed formula in patients with eosinophilic esophagitis triggered by milk. Allergy 68(8):1065–1072

    Article  PubMed  CAS  Google Scholar 

  75. Delaney AL, Arvedson JC (2008) Development of swallowing and feeding: prenatal through first year of life. Dev Disabil Res Rev 14(2):105–117. https://doi.org/10.1002/ddrr.16

    Article  PubMed  Google Scholar 

  76. Davis BP, Rothenberg ME (2013) Emerging concepts of dietary therapy for pediatric and adult eosinophilic esophagitis. Expert Rev Clin Immunol 9(4):285–287

    Article  PubMed  CAS  Google Scholar 

  77. Pelz BJ, Wechsler JB, Amsden K, Johnson K, Singh AM, Wershil BK, Kagalwalla AF, Bryce PJ (2016) IgE-associated food allergy alters the presentation of paediatric eosinophilic esophagitis. Clin Exp Allergy 46(11):1431–1440. https://doi.org/10.1111/cea.12776

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Colson D, Kalach N, Soulaines P, Vannerom Y, Campeotto F, Talbotec C, Chatenoud L, Hankard R, Dupont C (2014) The impact of dietary therapy on clinical and biologic parameters of pediatric patients with eosinophilic esophagitis. J Allergy Clin Immunol Pract 2(5):587–593. https://doi.org/10.1016/j.jaip.2014.05.012

    Article  PubMed  Google Scholar 

  79. Berry MJ, Adams J, Voutilainen H, Feustel PJ, Celestin J, Jarvinen KM (2015) Impact of elimination diets on growth and nutritional status in children with multiple food allergies. Pediatr Allergy Immunol 26(2):133–138

    Article  PubMed  Google Scholar 

  80. Meyer R, De Koker C, Dziubak R, Venter C, Dominguez-Ortega G, Cutts R, Yerlett N, Skrapak AK, Fox AT, Shah N (2014) Malnutrition in children with food allergies in the UK. J Hum Nutr Diet 27(3):227–235. https://doi.org/10.1111/jhn.12149

    Article  PubMed  CAS  Google Scholar 

  81. Flammarion S, Santos C, Guimber D, Jouannic L, Thumerelle C, Gottrand F et al (2011) Diet and nutritional status of children with food allergies. Pediatr Allergy Immunol 22(2):161–165

    Article  PubMed  Google Scholar 

  82. Thomassen RA, Kvammen JA, Eskerud MB, Juliusson PB, Henriksen C, Rugtveit J (2017) Iodine status and growth in 0-2-year-old infants with cow’s milk protein allergy. J Pediatr Gastroenterol Nutr 64(5):806–811. https://doi.org/10.1097/MPG.0000000000001434

    Article  PubMed  CAS  Google Scholar 

  83. Tuokkola J, Luukkainen P, Nevalainen J, Ahonen S, Toppari J, Ilonen J, Veijola R, Knip M, Virtanen SM, Kaila M (2017) Eliminating cows' milk, but not wheat, barley or rye, increases the risk of growth deceleration and nutritional inadequacies. Acta Paediatr 106(7):1142–1149. https://doi.org/10.1111/apa.13846

    Article  PubMed  CAS  Google Scholar 

  84. Berni Canani R, Leone L, D'Auria E, Riva E, Nocerino R, Ruotolo S et al (2014) The effects of dietary counseling on children with food allergy: a prospective, multicenter intervention study. J Acad Nutr Diet 114(9):1432–1439

    Article  PubMed  Google Scholar 

  85. Robbins KA, Wood RA, Keet CA (2014) Milk allergy is associated with decreased growth in US children. J Allergy Clin Immunol 134(6):1466–1468 e6. https://doi.org/10.1016/j.jaci.2014.08.037

    Article  PubMed  PubMed Central  Google Scholar 

  86. Christie L, Hine RJ, Parker JG, Burks W (2002) Food allergies in children affect nutrient intake and growth. J Am Diet Assoc 102(11):1648–1651

    Article  PubMed  Google Scholar 

  87. Jarvinen KM, Konstantinou GN, Pilapil M, Arrieta MC, Noone S, Sampson HA et al (2013) Intestinal permeability in children with food allergy on specific elimination diets. Pediatr Allergy Immunol 24(6):589–595. https://doi.org/10.1111/pai.12106

    Article  PubMed  PubMed Central  Google Scholar 

  88. Sova C, Feuling MB, Baumler M, Gleason L, Tam JS, Zafra H et al (2013) Systematic review of nutrient intake and growth in children with multiple IgE-mediated food allergies. Nutr Clin Pract 28(6):669–675

    Article  PubMed  Google Scholar 

  89. Kabbani TA, Goldberg A, Kelly CP, Pallav K, Tariq S, Peer A et al (2012) Body mass index and the risk of obesity in coeliac disease treated with the gluten-free diet. Aliment Pharmacol Ther 35(6):723–729

    Article  PubMed  CAS  Google Scholar 

  90. Ohlund K, Olsson C, Hernell O, Ohlund I (2010) Dietary shortcomings in children on a gluten-free diet. J Hum Nutr Diet 23(3):294–300. https://doi.org/10.1111/j.1365-277X.2010.01060.x

    Article  PubMed  CAS  Google Scholar 

  91. Wild D, Robins GG, Burley VJ, Howdle PD (2010) Evidence of high sugar intake, and low fibre and mineral intake, in the gluten-free diet. Aliment Pharmacol Ther 32(4):573–581. https://doi.org/10.1111/j.1365-2036.2010.04386.x

    Article  PubMed  CAS  Google Scholar 

  92. Murray JA, Watson T, Clearman B, Mitros F (2004) Effect of a gluten-free diet on gastrointestinal symptoms in celiac disease. Am J Clin Nutr 79(4):669–673

    Article  PubMed  CAS  Google Scholar 

  93. Innis SM (2008) Dietary omega 3 fatty acids and the developing brain. Brain Res 1237:35–43

    Article  PubMed  CAS  Google Scholar 

  94. De Caterina R (2011) N-3 fatty acids in cardiovascular disease. N Engl J Med 364(25):2439–2450. https://doi.org/10.1056/NEJMra1008153

    Article  PubMed  Google Scholar 

  95. Aldamiz-Echevarria L, Bilbao A, Andrade F, Elorz J, Prieto JA, Rodriguez-Soriano J (2008) Fatty acid deficiency profile in children with food allergy managed with elimination diets. Acta Paediatr 97(11):1572–1576

    Article  PubMed  CAS  Google Scholar 

  96. Kim SH, Lee JH, Ly SY (2016) Children with atopic dermatitis in Daejeon, Korea: individualized nutrition intervention for disease severity and nutritional status. Asia Pac J Clin Nutr 25(4):716–728. https://doi.org/10.6133/apjcn.092015.31

    Article  PubMed  CAS  Google Scholar 

  97. Paassilta M, Kuusela E, Korppi M, Lemponen R, Kaila M, Nikkari ST (2014) Food allergy in small children carries a risk of essential fatty acid deficiency, as detected by elevated serum mead acid proportion of total fatty acids. Lipids Health Dis 13(1):180. https://doi.org/10.1186/1476-511X-13-180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Meyer R, De Koker C, Dziubak R, Godwin H, Dominguez-Ortega G, Chebar Lozinsky A, Skrapac AK, Gholmie Y, Reeve K, Shah N (2016) The impact of the elimination diet on growth and nutrient intake in children with food protein induced gastrointestinal allergies. Clin Transl Allergy. 6(1):25. https://doi.org/10.1186/s13601-016-0115-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Pasiakos SM, Agarwal S, Lieberman HR, Fulgoni VL 3rd (2015) Sources and amounts of animal, dairy, and plant protein intake of US adults in 2007-2010. Nutrients 7(8):7058–7069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. van Vliet S, Burd NA, van Loon LJ (2015) The skeletal muscle anabolic response to plant- versus animal-based protein consumption. J Nutr 145(9):1981–1991

    Article  PubMed  Google Scholar 

  101. Dietary protein quality evaluation in human nutrition (2013). Report of an FAQ Expert Consultation. FAO Food Nutr Pap 92:1–66

  102. Saturni L, Ferretti G, Bacchetti T (2010) The gluten-free diet: safety and nutritional quality. Nutrients 2(1):16–34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Pellegrini N, Agostoni C (2015) Nutritional aspects of gluten-free products. J Sci Food Agric 95(12):2380–2385. https://doi.org/10.1002/jsfa.7101

    Article  PubMed  CAS  Google Scholar 

  104. Martin J, Geisel T, Maresch C, Krieger K, Stein J (2013) Inadequate nutrient intake in patients with celiac disease: results from a German dietary survey. Digestion 87(4):240–246

    Article  PubMed  CAS  Google Scholar 

  105. Missbach B, Schwingshackl L, Billmann A, Mystek A, Hickelsberger M, Bauer G, König J (2015) Gluten-free food database: the nutritional quality and cost of packaged gluten-free foods. PeerJ 3:e1337. https://doi.org/10.7717/peerj.1337

    Article  PubMed  PubMed Central  Google Scholar 

  106. JH W, Neal B, Trevena H, Crino M, Stuart-Smith W, Faulkner-Hogg K et al (2015) Are gluten-free foods healthier than non-gluten-free foods? An evaluation of supermarket products in Australia. Br J Nutr 114(3):448–454

    Article  Google Scholar 

  107. Miranda J, Lasa A, Bustamante MA, Churruca I, Simon E (2014) Nutritional differences between a gluten-free diet and a diet containing equivalent products with gluten. Plant Foods Hum Nutr 69(2):182–187. https://doi.org/10.1007/s11130-014-0410-4

    Article  PubMed  CAS  Google Scholar 

  108. Anderson JW, Baird P, Davis RH Jr, Ferreri S, Knudtson M, Koraym A et al (2009) Health benefits of dietary fiber. Nutr Rev 67(4):188–205. https://doi.org/10.1111/j.1753-4887.2009.00189.x

    Article  PubMed  Google Scholar 

  109. Golden NH, Abrams SA (2014) Committee on N. Optimizing bone health in children and adolescents. Pediatrics 134(4):e1229–e1243. https://doi.org/10.1542/peds.2014-2173

    Article  PubMed  Google Scholar 

  110. Pludowski P, Holick MF, Pilz S, Wagner CL, Hollis BW, Grant WB, Shoenfeld Y, Lerchbaum E, Llewellyn DJ, Kienreich K, Soni M (2013) Vitamin D effects on musculoskeletal health, immunity, autoimmunity, cardiovascular disease, cancer, fertility, pregnancy, dementia and mortality—a review of recent evidence. Autoimmun Rev 12(10):976–989. https://doi.org/10.1016/j.autrev.2013.02.004

    Article  PubMed  CAS  Google Scholar 

  111. Prasad AS (2008) Zinc in human health: effect of zinc on immune cells. Mol Med 14(5–6):353–357. https://doi.org/10.2119/2008-00033.Prasad

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Prado EL, Dewey KG (2014) Nutrition and brain development in early life. Nutr Rev 72(4):267–284. https://doi.org/10.1111/nure.12102

    Article  PubMed  Google Scholar 

  113. Kim J, Kwon J, Noh G, Lee SS (2013) The effects of elimination diet on nutritional status in subjects with atopic dermatitis. Nutr Res Pract 7(6):488–494. https://doi.org/10.4162/nrp.2013.7.6.488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Meyer R, De Koker C, Dziubak R, Skrapac AK, Godwin H, Reeve K, Chebar-Lozinsky A, Shah N (2015) A practical approach to vitamin and mineral supplementation in food allergic children. Clin Transl Allergy 5(1):11. https://doi.org/10.1186/s13601-015-0054-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Meyer R, De Koker C, Dziubak R, Godwin H, Dominguez-Ortega G, Shah N (2014) Dietary elimination of children with food protein induced gastrointestinal allergy—micronutrient adequacy with and without a hypoallergenic formula? Clin Transl Allergy 4(1):31

    Article  PubMed  PubMed Central  Google Scholar 

  116. Moore CE, Radcliffe JD, Liu Y, Vitamin D (2014) Intakes of children differ by race/ethnicity, sex, age, and income in the United States, 2007 to 2010. Nutr Res 34(6):499–506. https://doi.org/10.1016/j.nutres.2014.06.002

    Article  PubMed  CAS  Google Scholar 

  117. Bailey RL, Dodd KW, Goldman JA, Gahche JJ, Dwyer JT, Moshfegh AJ, Sempos CT, Picciano MF (2010) Estimation of total usual calcium and vitamin D intakes in the United States. J Nutr 140(4):817–822. https://doi.org/10.3945/jn.109.118539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Molina-Infante J, Katzka DA, Gisbert JP (2013) Review article: proton pump inhibitor therapy for suspected eosinophilic oesophagitis. Aliment Pharmacol Ther 37(12):1157–1164

    Article  PubMed  CAS  Google Scholar 

  119. Jung SB, Nagaraja V, Kapur A, Eslick GD (2015) Association between vitamin B12 deficiency and long-term use of acid-lowering agents: a systematic review and meta-analysis. Intern Med J 45(4):409–416

    Article  PubMed  CAS  Google Scholar 

  120. Freedberg DE, Kim LS, Yang YX (2017) The risks and benefits of long-term use of proton pump inhibitors: expert review and best practice advice from the American Gastroenterological Association. Gastroenterology 152(4):706–715. https://doi.org/10.1053/j.gastro.2017.01.031

    Article  PubMed  CAS  Google Scholar 

  121. do Nascimento AB, Fiates GM, Dos Anjos A, Teixeira E (2013) Analysis of ingredient lists of commercially available gluten-free and gluten-containing food products using the text mining technique. Int J Food Sci Nutr 64(2):217–222. https://doi.org/10.3109/09637486.2012.718744

    Article  PubMed  CAS  Google Scholar 

  122. deCastro BR, Caldwell KL, Jones RL, Blount BC, Pan Y, Ward C, Mortensen ME (2014) Dietary sources of methylated arsenic species in urine of the United States population, NHANES 2003-2010. PLoS One 9(9):e108098. https://doi.org/10.1371/journal.pone.0108098

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Bulka CM, Davis MA, Karagas MR, Ahsan H, Argos M (2017) The unintended consequences of a gluten-free diet. Epidemiology 28(3):e24–ee5. https://doi.org/10.1097/EDE.0000000000000640

    Article  PubMed  PubMed Central  Google Scholar 

  124. Raehsler SL, Choung RS, Marietta EV, Murray JA (2017) Accumulation of heavy metals in people on a gluten-free diet. Clin Gastroenterol Hepatol. https://doi.org/10.1016/j.cgh.2017.01.034

  125. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. EXS 101:133–164. https://doi.org/10.1007/978-3-7643-8340-4_6

    Article  PubMed  PubMed Central  Google Scholar 

  126. De Geest S, Sabate E (2003) Adherence to long-term therapies: evidence for action. Eur J Cardiovasc Nurs 2(4):323. https://doi.org/10.1016/S1474-5151(03)00091-4

    Article  PubMed  Google Scholar 

  127. Hommel KA, Franciosi JP, Hente EA, Ahrens A, Rothenberg ME (2012) Treatment adherence in pediatric eosinophilic gastrointestinal disorders. J Pediatr Psychol 37(5):533–542

    Article  PubMed  Google Scholar 

  128. Franciosi JP, Hommel KA, Greenberg AB, DeBrosse CW, Greenler AJ, Abonia JP, Rothenberg ME, Varni JW (2012) Development of the pediatric quality of life inventory eosinophilic esophagitis module items: qualitative methods. BMC Gastroenterol 12(1):135. https://doi.org/10.1186/1471-230X-12-135

    Article  PubMed  PubMed Central  Google Scholar 

  129. Leffler DA, Edwards-George J, Dennis M, Schuppan D, Cook F, Franko DL et al (2008) Factors that influence adherence to a gluten-free diet in adults with celiac disease. Dig Dis Sci 53(6):1573–1581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. MacCulloch K, Rashid M (2014) Factors affecting adherence to a gluten-free diet in children with celiac disease. Paediatr Child Health 19(6):305–309. https://doi.org/10.1093/pch/19.6.305

    Article  PubMed  PubMed Central  Google Scholar 

  131. Singh J, Whelan K (2011) Limited availability and higher cost of gluten-free foods. J Hum Nutr Diet 24(5):479–486. https://doi.org/10.1111/j.1365-277X.2011.01160.x

    Article  PubMed  CAS  Google Scholar 

  132. McMahon EJ, Campbell KL, Mudge DW, Bauer JD (2012) Achieving salt restriction in chronic kidney disease. Int J Nephrol 2012:720429

    Article  PubMed  PubMed Central  Google Scholar 

  133. Whitaker JK, West J, Holmes GK, Logan RF (2009) Patient perceptions of the burden of coeliac disease and its treatment in the UK. Aliment Pharmacol Ther 29(10):1131–1136. https://doi.org/10.1111/j.1365-2036.2009.03983.x

    Article  PubMed  CAS  Google Scholar 

  134. Schulman-Green D, Jaser SS, Park C, Whittemore R (2016) A metasynthesis of factors affecting self-management of chronic illness. J Adv Nurs 72(7):1469–1489

    Article  PubMed  PubMed Central  Google Scholar 

  135. Wang R, Hirano I, Doerfler B, Zalewski A, Gonsalves N, Taft T (2017) Assessing adherence and barriers to long term dietary elimination therapy in patients with eosinophilic esophagitis (EOE). Gastroenterology 152(5):S864

    Article  Google Scholar 

  136. Asher Wolf W, Huang KZ, Durban R, Iqbal ZJ, Robey BS, Khalid FJ et al (2016) The six-food elimination diet for eosinophilic esophagitis increases grocery shopping cost and complexity. Dysphagia 31(6):765–770

    Article  PubMed  CAS  Google Scholar 

  137. Roma E, Roubani A, Kolia E, Panayiotou J, Zellos A, Syriopoulou VP (2010) Dietary compliance and life style of children with coeliac disease. J Hum Nutr Diet 23(2):176–182. https://doi.org/10.1111/j.1365-277X.2009.01036.x

    Article  PubMed  CAS  Google Scholar 

  138. Giovannini M, D'Auria E, Caffarelli C, Verduci E, Barberi S, Indinnimeo L, Iacono I, Martelli A, Riva E, Bernardini R (2014) Nutritional management and follow up of infants and children with food allergy: Italian Society of Pediatric Nutrition/Italian Society of Pediatric Allergy and Immunology Task Force Position Statement. Ital J Pediatr 40(1):1. https://doi.org/10.1186/1824-7288-40-1

    Article  PubMed  PubMed Central  Google Scholar 

  139. Harris RF, Menard-Katcher C, Atkins D, Furuta GT, Klinnert MD (2013) Psychosocial dysfunction in children and adolescents with eosinophilic esophagitis. J Pediatr Gastroenterol Nutr 57(4):500–505. https://doi.org/10.1097/MPG.0b013e31829ce5ad

    Article  PubMed  Google Scholar 

  140. Webb D, Byrd-Bredbenner C (2015) Overcoming consumer inertia to dietary guidance. Adv Nutr 6(4):391–396

    Article  PubMed  PubMed Central  Google Scholar 

  141. Henry ML, Atkins D, Fleischer D, Pan Z, Ruybal J, Furuta GT (2012) Factors contributing to adherence to dietary treatment of eosinophilic gastrointestinal diseases. J Pediatr Gastroenterol Nutr 54(3):430–432. https://doi.org/10.1097/MPG.0b013e3182407aee

    Article  PubMed  Google Scholar 

Download references

Funding

There is no funding source for this review.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kara L. Kliewer.

Ethics declarations

Conflict of Interest

KK declares no conflicts of interest. AC has received honoraria from Nutricia and Abbott Nutrition. CV has received honoraria from Danone, Nestle, Mead Johnson, and DBV Technologies.

Ethical Approval and Informed Consent

This article does not contain any studies with human participants or animals performed by any of the authors. The present article is a review; therefore, no informed consent was required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kliewer, K.L., Cassin, A.M. & Venter, C. Dietary Therapy for Eosinophilic Esophagitis: Elimination and Reintroduction. Clinic Rev Allerg Immunol 55, 70–87 (2018). https://doi.org/10.1007/s12016-017-8660-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12016-017-8660-1

Keywords

Navigation