Gastroenterology
Volume 122, Issue 5 , Pages 1216-1225 , May 2002

Eosinophilic esophagitis in children: Immunopathological analysis and response to fluticasone propionate

  • Jonathan E. Teitelbaum

      Affiliations

    • Combined Program in Pediatric Gastroenterology and Nutrition
    • ,
  • Victor L. Fox

      Affiliations

    • Combined Program in Pediatric Gastroenterology and Nutrition
    • ,
  • Frank J. Twarog

      Affiliations

    • Division of Allergy and Immunology, Children's Hospital, Harvard Medical School, Boston, Massachusetts
    • ,
  • Samuel Nurko

      Affiliations

    • Combined Program in Pediatric Gastroenterology and Nutrition
    • ,
  • Don Antonioli

      Affiliations

    • Department of Pathology
    • ,
  • Gerald Gleich

      Affiliations

    • Department of Dermatology, University of Utah, Salt Lake City, Utah
    • ,
  • Kamran Badizadegan

      Affiliations

    • Department of Pathology
    • ,
  • Glenn T. Furuta

      Affiliations

    • Combined Program in Pediatric Gastroenterology and Nutrition

Received 11 October 2001 ,Accepted 3 January 2002.

References 

  1. Attwood SEA, Smyrk TC, Demeester TR, Jones JB. Esophageal eosinophilia with dysphagia: a distinct clinicopathologic syndrome. Dig Dis Sci. 1993;38:109–116
  2. Faubion WA, Perrault J, Burgart LJ, Zein NN, Clawson M, Freese DK. Treatment of eosinophilic esophagitis with inhaled corticosteroids. J Pediatr Gastroenterol Nutr. 1998;27:90–93
  3. Kelly KJ, Lazenby AJ, Rowe PC, Yardley JH, Perman JA, Sampson HA. Eosinophilic esophagitis attributed to gastroesophageal reflux: improvement with an amino acid-based formula. Gastoenterology. 1995;109:1503–1512
  4. Liacouras CA, Wenner WJ, Brown K, Ruchelli E. Primary eosinophilic esophagitis in children: successful treatment with oral corticosteroids. J Pediatr Gastroenterol Nutr. 1998;26:380–385
  5. Orenstein SR, Shalaby TM, DiLorenzo C, Putnam PE, Sigurdsson L, Kocoshis SA. The spectrum of pediatric eosinophilic esophagitis beyond infancy: a clinical series of 30 children. Am J Gastroenterol. 2000;95:1422–1430
  6. Siafakas CG, Ryan CK, Brown MR, Miller TL. Multiple esophageal rings: an association with eosinophilic esophagitis. Am J Gastroenterol. 2000;95:1572–1575
  7. Walsh SV, Antonioli DA, Goldman H, Fox VL, Bousvaros A, Leichtner AM, et al. Allergic esophagitis in children: a clinicopathological entity. Am J Surg Pathol. 1999;23:390–396
  8. Gupta SK, Fitzgerald JF, Chong SKF, Croffie JM, Collins MH. Vertical lines in distal esophageal mucosa (VLEM): a true endoscopic manifestation of esophagitis in children?. Gastrointest Endosc. 1997;45:485–489
  9. Mishra A, Hogan S, Brandt E, Rothenberg M. An etiological role for aeroallergens and eosinophils in experimental esophagitis. J Clin Invest. 2001;107:83–90
  10. Harding S. The human pharmacology of fluticasone propionate. Respir Med. 1990;84(Suppl A):25–29
  11. Kahrilas P, Quigley E. Clinical esophageal pH recording: a technical review for practice guideline development. Gastroenterology. 1996;110:1982–1996
  12. Biller JA, Winter HS, Grand RJ, Allred EN. Are endoscopic changes predictive of histologic esophagitis in children?. J Pediatr. 1983;103:215–218
  13. Shub MD, Ulshen MH, Hargrove CB, Siegal GP, Groben PA, Askin FB. Esophagitis: a frequent consequence of gastroesophageal reflux in infancy. J Pediatr. 1985;107:881–884
  14. Wilcox CM. Esophagitis in the immunocompromised host. In:  Castell DO,  Richter JE editor. The esophagus. Philadelphia: Lippincott Williams and Wilkins; 1999;p. 539–555
  15. Till S, Jacobson M, O'Brien F, Durham SR, KleinJan A, Fokkens WJ, et al. Recruitment of CD1a+ Langerhans cells to the nasal mucosa in seasonal allergic rhinitis and effects of topical corticosteroids. Allergy. 2001;56:126–131
  16. Lambrecht B, DeVeerman M, Coyle A, Gutierrez-Ramos J, Thielemans K, Pauwels R. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J Clin Invest. 2000;106:551–559
  17. Leiferman KM. Eosinophils in atopic dermatitis. J Allergy Clin Immunol. 1994;94:1310–1317
  18. Akdis M, Simon H, Weigl L, Kreyden O, Blaser K, Akdis C. Skin homing (cutaneous lymphocyte-associated antigen-positive) CD8+ T cells respond to superantigen and contribute to eosinophilia and IgE production in atopic dermatitis. J Immunol. 1999;163:466–475
  19. Wang HH, Mangano MM, Antonioli DA. Evaluation of T-lymphocytes in esophageal mucosal biopsies. Mod Pathol. 1994;7:55–58
  20. Yassin T, Toner P. Langerhans cells in the human oesophagus. J Anat. 1976;122:435–445
  21. Terris B, Potet F. Structure and role of Langerhans cells in the human oesophageal epithelium. Digestion. 1995;56:9–14
  22. Mangano M, Antonioli D, Schnitt S, Wang H. Nature and significance of cells with irregular nuclear contours in esophageal mucosal biopsies. Mod Pathol. 1992;5:191–196
  23. Charton-Bain M, Terris B, Dauge M, Marche C, Walker F, Bouchaud O, et al. Reduced numbers of Langerhans cells in oesophageal mucosa from AIDS patients. Histopathology. 1999;34:399–404
  24. Abbas A, Murphy K, Sher A. Functional diversity of helper T lymphocytes. Nature. 1996;383:787–793
  25. Schwarze J, Cielewicz G, Joetham A, Ikemura T, Hamelmann E, Gelfand E. CD8 T cells are essential in the development of respiratory syncytial virus-induced lung eosinophilia and airways hyperresponsiveness. J Immunol. 1999;162:4207–4211
  26. Schwarze J, Makela M, Cieslewicz G, Dakhama A, Lahn M, Ikemura T, et al. Transfer of enhancing effect of respiratory syncytial virus infection on subsequent allergic airway sensitization by T lymphocytes. J Immunol. 1999;163:5729–5734
  27. Ying S, Humbert M, Barkans J, Corrigan CJ, Pfister R, Menz G, et al. Expression of IL-4 and IL-5 mRNA and protein product by CD4+ and CD8+ T cells, eosinophils, and mast cells in bronchial biopsies obtained from atopic and nonatopic asthmatics. J Immunol. 1997;158:3539–3944
  28. Lambrecht B, Salomon B, Klatzmann D, Pauwels R. Dendritic cells are required for the development of chronic eosinophilia airway inflammation in response to inhaled antigen in sensitized mice. J Immunol. 1998;160:4090–4097
  29. Hogan S, Mishra A, Brandt E, Foster P, Rothenberg M. A critical role for eotaxin in experimental oral antigen-induced eosinophilic gastrointestinal allergy. Proc Natl Acad Sci U S A. 2000;97:6681–6686
  30. Hogan S, Mishra A, Brandt E, Royalty MP, Pope SM, Zimmermann N, et al. A pathological function for eotaxin and eosinophils in eosinophilic gastrointestinal inflammation. Nat Immunol. 2001;2:353–360
  31. Bousquet J, Chanez P, Lacoste JY, Barneon G, Ghavanian N, Enander I, et al. Eosinophilic inflammation in asthma. N Engl J Med. 1990;323:1033–1039
  32. Levy A, Gleich G, Sandborn W, Tremaine W, Steiner B, Phillips S. Increased eosinophil granule proteins in gut lavage fluid from patients with inflammatory bowel diseases. Mayo Clin Proc. 1997;72:117–123
  33. Dvorak AM, Monahan RA, Osage JE, Dickersin GR. Crohn's disease: transmission electron microscopic studies-immunologic inflammatory response. Alterations of mast cells, basophils, eosinophils, and the microvasculature. Hum Pathol. 1980;11:606–619
  34. Haskell M, Moy J, Gleich G, Thomas L. Analysis of signaling events associated with activation of neutrophil superoxide anion production by eosinophil granule major basic protein. Blood. 1995;86:4627–4637
  35. Flavahan NA, Slifman NR, Gleich GJ, Vanhoutte PM. Human eosinophil major basic protein causes hyperactivity of respiratory smooth muscle. Am Rev Respir Dis. 1988;138:685–688
  36. Furuta GT, Ackerman SJ, Williams RE, Wershil BK. Eosinophil major basic protein induces the release of TNF-alpha and arachidonic acid mediators from mouse bone marrow derived mast cells grown in stem cell factor. Blood. 1998;92:1055–1061
  37. Furuta GT, Ackerman SJ, Varga J, Spiess AM, Wang MY, Wershil BK. Eosinophil granule-derived major basic protein induces IL-8 expression in human intestinal myofibroblasts. Clin Exp Immunol. 2000;122:35–40
  38. Kita H, Abu-Ghazaleh RA, Sur S, Gleich GJ. Eosinophil major basic protein induces degranulation and IL-8 production by human eosinophils. J Immunol. 1995;154:4749–4758
  39. Landres R, Kuster G, Strum W. Eosinophilic esophagitis in a patient with vigorous achalasia. Gastroenterology. 1978;74:1298–1301
  40. Kelly K. Eosinophilic gastroenteritis. J Pediatr Gastroenterol Nutr. 2000;30:S28–S35
  41. Sondheimer J. What are the roles of eosinophils in esophagitis?. J Pediatr Gastroenterol Nutr. 1998;27:90–93
  42. Liacouras CA, Markowitz JE, Spergel J. Eosinophilic esophagitis in children: a 5 year review. J Pediatr Gastroenterol Nutr. 2001;33:418
  43. Akdis M, Simon HU, Weigl L, Kreyden O, Blaser K, Akdis CA. Skin homing (cutaneous lymphocyte-associated antigen-positive) CD8+ T cells respond to superantigen and contribute to eosinophilia and IgE production in atopic dermatitis. J Immunol. 1999;163:466–475
  44. Sharek P, Bergman D. The effect of inhaled steroids on the linear growth of children with asthma: a meta-analysis. Pediatrics. 2000;106:E8
  45. Ventura M, Piccinni T, Matino M, Giuliano G, Di Corato R, Di Napoli P, et al. Retrospective study on fluticasone propionate aqueous nasal spray efficacy in patients with allergic rhinitis: evaluation of clinical and laboratory parameters. Allergy. 2001;56:29–34
  46. Johnson M. Development of fluticasone propionate and comparison with other inhaled corticosteroids. J Allergy Clin Immunol. 1998;101:S434–S439
  47. Hoogsteden H, Berhoeven G, Lambrecht B, Prins J. Airway inflammation in asthma and chronic obstructive pulmonary disease with special emphasis on the antigen presenting dendritic cell: influence of treatment with fluticasone proprionate. Clin Exp Allergy. 1999;29:116–124
  48. Liu MC, Proud D, Lichtenstein LM, Hubbard WC, Bochner BS, Stealey BA, et al. Effects of prednisone on the cellular responses and release of cytokines and mediators after segmental allergen challenge of asthmatic subjects. J Allergy Clin Immunol. 2001;108:29–38
  49. Feczko PJ, Halpert RD, Zonca M. Radiographic abnormalities in eosinophilic esohagitis. Gastrointest Radiol. 1985;10:321–324
  50. Mahajan L, Wyllie R, Petras R, Steffan R, Kay M. Idiopathic eosinophilic esophagitis with stricture formation in a patient with long-standing eosinophilic gastroenteritis. Gastrointest Endosc. 1997;46:557–560
  51. Vitellas KM, Bennett WF, Bova JG, Johnston JC, Caldwell JH, Mayle JE. Idiopathic eosinophilic esophagitis. Radiology. 1993;186:789–793

☆ Address requests for reprints to: Glenn T. Furuta, M.D., 300 Longwood Avenue, Hunnewell Ground Floor, Boston, Massachusetts 02115. e-mail: gfuruta@zeus.bwh.harvard.edu; fax: (617) 739-5871.

☆☆ Supported by grants K08 DK 02564 and P30 DK40561 (to G.T.F.).

PII: S0016-5085(02)12378-X

Gastroenterology
Volume 122, Issue 5 , Pages 1216-1225 , May 2002

Article Tools

* Image Usage & Resolution