Advertisement

Genesis of Barrett’s Neoplasia: Current Concepts

  • Domenico Coppola
  • Nelly A. Nasir
  • Leslie Turner
Chapter
Part of the Cancer Growth and Progression book series (CAGP, volume 12)

Abstract

Barrett’esophagus is the replacement of the esophageal squamous epithelium with metaplastic columnar epithelium. This phenomenon, related to gastro-esophageal reflux, has increased in incidence over the last two decades, and with it there has been a similar increase in Barrett’s associated adenocarcinomas. In this chapter we describe the pathologic features of Barrett’s esophagus and of Barrett’s associated dysplasia and carcinoma. We address important aspects related to the clinical presentation, endoscopic findings, and differential diagnosis of Barrett’s esophagus. In addition, we present an overview of the molecular pathways involved in the genesis and progression of Barrett’s esophagus, and on the identification of potential molecular markers predictive of progression from normal esophageal mucosa to Barrett’s esophagus, to dysplasia, to carcinoma. Finally, we briefly review the use of recent technologies including cDNA microarray, micro-RNA, and proteomics to improve the diagnosis of Barrett’s associated dysplasia, and to identify gene or protein signatures predictive of progression in Barrett’s esophagus.

Keywords

Intestinal Metaplasia Esophageal Adenocarcinoma Duodenogastric Reflux Heterotopic Gastric Mucosa Columnar Crypt 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Spechler SJ, Goyal RK. Barrett’s esophagus. N Engl J Med. 1986;315:362–71.PubMedCrossRefGoogle Scholar
  2. 2.
    Pohl H, Welch HG. The role of overdiagnosis and reclassification in the marked increase of esophageal adenocarcinoma incidence. J Natl Cancer Inst. 2005;97:142–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Gamliel Z, Krasna MJ. Multimodality treatment of esophageal cancer. Surg Clin North Am. 2005;85:621–30.PubMedCrossRefGoogle Scholar
  4. 4.
    Dent J, Bremner CG, Collen MJ, et al. Barrett’s oesophagus. J Gastroenterol Hepatol. 1991;6:1–22.PubMedCrossRefGoogle Scholar
  5. 5.
    Collen MJ, Lewis JH, Benjamin SB. Gastric acid hypersecretion in refractory gastroesophageal reflux disease. Gastroenterology. 1990;98:654–61.PubMedGoogle Scholar
  6. 6.
    Mulholland MW, Reid BJ, Levine DS, et al. Elevated gastric acid secretion in patients with Barrett’s metaplastic epithelium. Dig Dis Sci. 1989;34:1329–34.PubMedCrossRefGoogle Scholar
  7. 7.
    Meyer W, Vollmar F, Bar W. Barrett-esophagus following total gastrectomy: a contribution to its pathogenesis. Endoscopy. 1979;11:121–6.PubMedCrossRefGoogle Scholar
  8. 8.
    Othersen HB Jr, Ocampo RJ, Parker EF, et al. Barrett’s esophagus in children: diagnosis and management. Ann Surg. 1993;217:676–80.PubMedCrossRefGoogle Scholar
  9. 9.
    Rector LE, Connerley ML. Aberrant mucosa in the esophagus in infants and children. Arch Pathol. 1941;31:285–94.Google Scholar
  10. 10.
    Hamilton SR. Pathogenesis of columnar cell-lined (Barrett’s) esophagus. In: Spechler SJ, Goyal RK, eds. Barrett’s Esophagus: Pathophysiology, Diagnosis and Management. New York: Elsevier Science; 1985:29–37.Google Scholar
  11. 11.
    Woolf GM, Riddell RH, Irvine EJ, et al. A study to examine agreement between endoscopy and histology for the diagnosis of columnar-lined (Barrett’s) esophagus. Gastrointest Endosc. 1989;35:541–4.PubMedCrossRefGoogle Scholar
  12. 12.
    Paull A, Trier JS, Dalton MD, et al. The histologic spectrum of Barrett’s esophagus. N Engl J Med. 1976;295:476–80.PubMedCrossRefGoogle Scholar
  13. 13.
    Hameeteman W, Tytgat GN, Houthoff HJ, et al. Barrett’s esophagus: development of dysplasia and adenocarcinoma. Gastroenterology. 1989;96:1249–56.PubMedGoogle Scholar
  14. 14.
    Haggitt RC. Barrett’s esophagus, dysplasia, and adenocarcinoma. Hum Pathol. 1994;25:982–93.PubMedCrossRefGoogle Scholar
  15. 15.
    Blot WJ, Devesa SS, Kneller RW, et al. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA. 1991;265:1287–89.PubMedCrossRefGoogle Scholar
  16. 16.
    Pera M, Cameron AJ, Trastek VF, et al. Increasing incidence of adenocarcinoma of the esophagus and esophagogastric junction. Gastroenterology. 1993;104:510–3.PubMedGoogle Scholar
  17. 17.
    Spechler SJ, Goyal RK. The columnar-lined esophagus, intestinal metaplasia, and Norman Barrett. Gastroenterology. 1996;110:614–21.PubMedCrossRefGoogle Scholar
  18. 18.
    Hamilton SR, Smith RR, Cameron JL. Prevalence and characteristics of Barrett esophagus in patients with adenocarcinoma of the esophagus or esophagogastric junction. Hum Pathol. 1988;19:942–8.PubMedCrossRefGoogle Scholar
  19. 19.
    McArdle JE, Lewin KJ, Randall G, et al. Distribution of dysplasias and early invasive carcinoma in Barrett’s esophagus. Hum Pathol. 1992;23:479–82.PubMedCrossRefGoogle Scholar
  20. 20.
    Hamilton SR. Reflux esophagitis and Barrett’s esophagus. In: Goldman H, Appelman HD, Kaufman N, eds. Gastrointestinal Pathology. Baltimore, MD: Williams & Wilkins; 1990:11–68.Google Scholar
  21. 21.
    Riddell RH, Goldman H, Ransohoff DF, et al. Dysplasia in inflammatory bowel disease: standardized classification with provisional clinical implications. Hum Pathol. 1983;14:931–68.PubMedCrossRefGoogle Scholar
  22. 22.
    Hamilton SR. Adenocarcinoma in Barrett’s esophagus. In: Whitehead R, ed. Gastrointestinal and Esophageal Pathology. Edinburgh, Scotland: Churchill Livingstone; 1989;683–706.Google Scholar
  23. 23.
    Antonioli DA. Esophagus. In: Henson DE, Albores-Saavedra J, eds. Pathology of Incipient Neoplasia. Philadelphia, PA: WB Saunders Co; 1993;64–84.Google Scholar
  24. 24.
    Reid BJ, Weinstein WM, Lewin KJ, et al. Endoscopic biopsy can detect high-grade dysplasia or early adenocarcinoma in Barrett’s esophagus without grossly recognizable neoplastic lesions. Gastroenterology. 1988;94:81–90.PubMedGoogle Scholar
  25. 25.
    Smith RR, Hamilton SR, Boitnott JK, et al. The spectrum of carcinoma arising in Barrett’s esophagus: a clinicopathologic study of 26 patients. Am J Surg Pathol. 1984;8:563–73.PubMedCrossRefGoogle Scholar
  26. 26.
    Levine DS, Haggitt RC, Blount PL, et al. An endoscopic biopsy protocol can differentiate high-grade dysplasia from early adenocarcinoma in Barrett’s esophagus. Gastroenterology. 1993;105:40–50.PubMedGoogle Scholar
  27. 27.
    Sharma P. Recent advances in Barrett’s esophagus: short-segment Barrett’s esophagus and carida intestinal metaplasia. Semin Gastrointest Dis. 1999;10:93–102PubMedGoogle Scholar
  28. 28.
    Sharma P, Sampliner RE. Short segment Barrett’s esophagus and intestinal metaplasia of the cardia – it’s not all symantics!! Am J Gastroenterol. 1998;93:2303–4.PubMedGoogle Scholar
  29. 29.
    Sharma P, Weston AP, Morales T, et al. Relative risk of dysplasia for patients with intestinal metaplasia in the distal oesophagus and in the gastric cardia. Gut. 2000;46:9–13.PubMedCrossRefGoogle Scholar
  30. 30.
    Sampliner RE. Practice guidelines on the diagnosis, surveillance, and therapy of Barrett’s esophagus. The Practice Parameters Committee of the American College of Gastroenterology. Am J Gastroenterol. 1998;93:1028–32.PubMedCrossRefGoogle Scholar
  31. 31.
    Srivastava A, Odze RD, Lauwers GY, Redston M, Antonioli DA, Glickman JN. Morphologic features are useful in distinguishing Barrett esophagus from carditis with intestinal meatplasia. Am J Surg Pathol. 2007;31:1733–41.PubMedCrossRefGoogle Scholar
  32. 32.
    Borhan-Manesh F, Farnum JB. Incidence of heterotopic gastric mucosa in the upper oesophagus. Gut. 1991;32:968–72.PubMedCrossRefGoogle Scholar
  33. 33.
    Wang HH, Zeroogian JM, Spechler SJ, Goyal RK, Antonioli DA. Prevalence and significance of pancreatic acinar metaplaisa at the gastroesophageal junction. Am J Surg Pathol. 1996;20:1507–10.PubMedCrossRefGoogle Scholar
  34. 34.
    Reid BJ, Blount PL, Rubin CE, et al. Flow-cytometric and histological progression to malignancy in Barrett’s esophagus: prospective endoscopic surveillance of a cohort. Gastroenterology. 1992;102:1212–9.PubMedGoogle Scholar
  35. 35.
    Geisinger KR. Endoscopic biopsies and cytologic brushings of the esophagus are diagnostically complementary. Am J Clin Pathol. 1995;103:295–9.PubMedGoogle Scholar
  36. 36.
    Chittajallu RS, Falk GW, Goldblum JR et al. Balloon cytology for the detection and surveillance of Barrett’s esophagus. Gastroenterology. 1995;108:71A.Google Scholar
  37. 37.
    Bani-Hani K, Martin IG, Hardie LJ, Mapstone N, Briggs JA, Forman D, Wild CP. Prospective study of Cyclin D1 overexpression in Barrett’s esophagus: association with increased risk of adenocarcinoma. J Natl Cancer Inst. 2000;92:1316–21.PubMedCrossRefGoogle Scholar
  38. 38.
    Geddert H, Heep H, Gabbert H, Sarbia M. Expression of Cyclin B1 in the metaplasia-dysplasia-carcinoma sequence of Barrett esophagus. Cancer. 2002;94:212–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Barrett MT, Sanchez CA, Galipeau PC, et al. Allelic loss of 9p21 and mutation of the CDKN2/p16 gene develop as early lesions during neoplastic progression in Barrett’s esophagus. Oncogene. 1996;13:1867–73.PubMedGoogle Scholar
  40. 40.
    Nakamura T, Nekarda H, Hoelscher AH, et al. Prognostic value of DNA ploidy and c-erbB-2 oncoprotein overexpression in adenocarcinoma of Barrett’s esophagus. Cancer. 1994;73:1785–94.PubMedCrossRefGoogle Scholar
  41. 41.
    Fennerty MB, Sampliner RE, Way D, et al. Discordance between flow cytometric abnormalities and dysplasia in Barrett’s esophagus. Gastroenterology. 1989;97:815–20.PubMedGoogle Scholar
  42. 42.
    Al-Kasspooles M, Moore JH, Orringer MB, et al. Amplification and over-expression of the EGFR and erbB-2 genes in human esophageal adenocarcinomas. Int J Cancer. 1993;4:213–19.CrossRefGoogle Scholar
  43. 43.
    Kumble S, Omary MB, Cartwright CA, et al. Src activation in malignant and premalignant epithelia of Barrett’s esophagus. Gastroenterology. 1997;112:348–56.PubMedCrossRefGoogle Scholar
  44. 44.
    Swami S, Kumble S, Triadafilopoulos G, et al. E-cadherin expression in gastroesophageal reflux disease, Barrett’s esophagus, and esophageal adenocarcinoma: an immunohistochemical and immunoblot study. Am J Gastroenterol. 1995;90:1808–13.PubMedGoogle Scholar
  45. 45.
    Bian YS, Osterheld MC, Bosman FT, Fontolliet C, Benhattar J. Nuclear accumulation of beta-Catenin is a common and early event during neoplastic progression of Barrett esophagus. Am J Clin Pathol. 2000;114:583–90.PubMedCrossRefGoogle Scholar
  46. 46.
    Betkas N, Donner A, Wirtz C, Heep H, Gabbert HE, Sarbia M. Allelic loss involving the tumor suppressor genes APC and MCC and expression of the APC protein in the development of dysplasia and carcinoma in Barrett’s esophagus. Am J Clin Pathol. 2000;114:890–5.CrossRefGoogle Scholar
  47. 47.
    Osterheld MC, Bian YS, Bosman FT, Benhattar J, Fontolliet C. Beta-catenin expression and its association with prognostic factors in adenocarcinoma developed in Barrett esophagus. Am J Clin Pathol. 2002;117:451–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Tselepis C, Perry I, Dawson C, Hardy R, Darnton SJ, Mc Conkey C, Stuart RC, Wright N, Harrison R, Jankowski JAZ. Tumour necrosis factor-α in Barrett’s oesophagus: a potential novel mechanism of action. Oncogene. 2002;21:6071–81.PubMedCrossRefGoogle Scholar
  49. 49.
    Montgomery E, Mamelak AJ, Gibson M, Maitra A, Sheikh S, Amr S, et al. Overexpression of claudin proteins in esophageal adenocarcinoma and its precursor lesions. Appl Immunohistochem Mol Morphol. 2006;14:24–30.PubMedCrossRefGoogle Scholar
  50. 50.
    Soslow RA, Petersen CG, Remotti H, Altorki N. Acidic fibroblast growth factor is expressed sequentially in the progression from Barrett’s esophagus to esophageal adenocarcinoma. Dis Esophag. 2001;14:23–7.CrossRefGoogle Scholar
  51. 51.
    Hammoud ZT, Badve S, Saxena R, Kesler KA, Rieger K, Malkas L, et al. A novel biomarker for the detection of esophageal adenocarcinoma. J Thorac Cardiovasc Surg. 2007;133:82–7.PubMedCrossRefGoogle Scholar
  52. 52.
    Ray GS, Lee JR, Nwokeji K, et al. Increased immunoreactivity for Rab11, a small GTP-binding protein, in low-grade dysplastic Barrett’s epithelia. Lab Invest. 1997;77:503–11.PubMedGoogle Scholar
  53. 53.
    Coppola D, Schreiber RH, Mora L, et al. Significance of Fas and Rb protein expression during the progression of Barrett’s metaplasia to adenocarcinoma: platform presentation at the 51st Annual Cancer Symposium of the Society of Surgical Oncology, San Diego, CA, March 26–29, 1998. Ann Surg Oncol. 1998;In press.Google Scholar
  54. 54.
    Casson AG, Kerkvliet N, O’Malley F. Prognostic value of p53 protein in esophageal adenocarcinoma. J Surg Oncol. 1995;60:5–11.PubMedCrossRefGoogle Scholar
  55. 55.
    Hollstein MC, Metcalf RA, Welsh JA, et al. Frequent mutation of the p53 gene in human esophageal cancer. Proc Natl Acad Sci USA. 1990;87:9958–61.PubMedCrossRefGoogle Scholar
  56. 56.
    Blount PL, Ramel S, Raskind WH, et al. 17p allelic deletions and p53 protein overexpression in Barrett’s adenocarcinoma. Cancer Res. 1991;51:5482–6.PubMedGoogle Scholar
  57. 57.
    Ramel S, Reid BJ, Sanchez CA, et al. Evaluation of p53 protein expression in Barrett’s esophagus by two-parameter flow cytometry. Gastroenterology. 1992;102:1220–8.PubMedGoogle Scholar
  58. 58.
    Younes M, Lebovitz RM, Lechago LV, et al. p53 protein accumulation in Barrett’s metaplasia, dysplasia and adenocarcinoma: a follow-up study. Gastroenterology. 1993;105:1637–42.PubMedGoogle Scholar
  59. 59.
    Chatelain D, Flejou JF. High-grade dysplasia and superficial adenocarcinoma in Barrett’s esophagus: histological mapping and expression of p53, p21 and Bcl-2 oncoproteins. Virchows Arch. 2003;442:18–24.PubMedGoogle Scholar
  60. 60.
    Younes M, Lechago J, Chakraborty S, Ostrowski M, Bridges M, Meriano F, et al. Relationship between dysplasia, p53 protein accumulation, DNA ploidy, and Glut1 overexpression in Barrett metaplasia. Scand J Gastroenterol. 2000;2:131–7.Google Scholar
  61. 61.
    Weston AP, Banerjee SK, Sharma P, Tran TM, Richards R, Cherian R. p53 Protein overexpression in low grade dysplasia (LGD) in Barrett’s esophagus: immunohistochemical marker predictive of progression. Am J Gastroenterology. 2001;96(5);1355–62.CrossRefGoogle Scholar
  62. 62.
    Bian YS, Osterheld MC, Bosman FT, Benhattar J, Fontolliet C. p53 Gene mutation and protein accumulation during neoplastic progression in Barrett’s esophagus. Mod Pathol. 2001;14(5);397–403.PubMedCrossRefGoogle Scholar
  63. 63.
    Flejou JF, Potet F, Muzeau F, et al. Overexpression of p53 protein in Barrett’s syndrome with malignant transformation. J Clin Pathol. 1993;46:330–3.PubMedCrossRefGoogle Scholar
  64. 64.
    Younes M, Ertan A, Lechago LV, et al. p53 Protein accumulation is a specific marker of malignant potential in Barrett’s metaplasia. Dig Dis Sci. 1997;42:697–701.PubMedCrossRefGoogle Scholar
  65. 65.
    Glickman JN, Yang A, Shahsafaei A, McKeon F, Odze R. Expression of p53-related protein p63 in the gastrointestinal tract and in esophageal metaplastic and neoplastic disorders. Hum Pathol. 2001;32(11);1157–65.PubMedCrossRefGoogle Scholar
  66. 66.
    Hall PA, Woodman AC, Campbell SJ, Shepherd NA. Expression of the p53 homologue p63α and ▵Np63α in the neoplastic sequence of Barrett’s oesophagus: correlation with morphology and p53 protein. Gut. 2001;49:618–23.PubMedCrossRefGoogle Scholar
  67. 67.
    Hughes SJ, Nambu Y, Soldes OS, et al. Fas/APO-1(CD95) is not translocated to the cell membrane in esophageal adenocarcinoma. Cancer Res. 1997;57:5571–8.PubMedGoogle Scholar
  68. 68.
    Van Der Woude CJ, Jansen PLM, Tiebosch ATGM, Beuving A, Homan M, Kleibeuker JH, et al. Expression of apoptosis-related proteins in Barrett’s metaplasia-dysplasia-carcinoma sequence: a switch to a more resistant phenotype. Hum Pathol. 2002;33(7);686–92.PubMedCrossRefGoogle Scholar
  69. 69.
    Raouf AA, Evoy DA, Carton E, Mulligan E, Griffin MM, Reynolds JV. Loss of Bcl-2 expression in Barrett’s dysplasia and adenocarcinoma is associated with tumor progression and worse survival but not with response to neoadjuvant chemoradiation. Dis Esophag. 2003;16:17–23.CrossRefGoogle Scholar
  70. 70.
    Kuester D, Dar AA, Moskaluk CC, Krueger S, Meyer F, Hartig R, et al. Early involvement of death-associated protein kinase promoter hypermethylation in the carinogenesis of Barrett’s esophageal adenocarcinoma and its association with clinical progression. Neoplasia. 2007;9:236–45.PubMedCrossRefGoogle Scholar
  71. 71.
    Li Y, Wo JM, Cai Lu, Zhou Z, Rosenbaum D, Mendez C, et al. Association of metallothionein expression and lack of apoptosis with progression of carcinogenesis in Barrett’s esophagus. Exp Biol Med. 2003;228:286–92.Google Scholar
  72. 72.
    Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature. 1989;339:58–61.PubMedCrossRefGoogle Scholar
  73. 73.
    Bossi P, Viale G, Lee AK, Alfano R, Coggi G, Bosari S. Angiogenesis in colorectal tumors: microvessel quantitation in adenoma and carcinomas with clinicopathological correlations. Cancer Res. 1995;55:5049–53.PubMedGoogle Scholar
  74. 74.
    Bosari S, Lee AK, DeLellis RA, Wiley BD, Heatley GJ, Silverman ML. Microvessel quantitation and prognosis in invasive breast carcinoma. Hum Pathol. 1992;23:755–61.PubMedCrossRefGoogle Scholar
  75. 75.
    Millikan KW, Mall JW, Myers JA, Hollinger EF, Doolas A, Saclarides TJ. Do angiogenesis and growth factor expression predict prognosis of esophageal cancer? Am Surg. 2000;66:401–5;405–6 (discussion).PubMedGoogle Scholar
  76. 76.
    Torres C, Wang H, Turner J, Shahsafaei A, Odze RD. Prognostic significance and effect of chemoradiotherapy on microvessel density (angiogenesis) in esophageal Barrett’s esophagus-associated adenocarcinoma and squamous cell carcinoma. Hum Pathol. 1999;30:753–8.PubMedCrossRefGoogle Scholar
  77. 77.
    Couvelard A, Paraf F, Gratio V, Scoazec JY, Henin D, Degott C, et al. Angiogenesis in the neoplastic sequence of Barrett’s oesophagus. Correlation with VEGF expression. J Pathol. 2000;192:14–8.PubMedCrossRefGoogle Scholar
  78. 78.
    Lord RVN, Park JM, Wickramasinghe K, DeMeester SR, Oberg S, Salonga D, et al. Vascular endothelial growth factor and basic fibroblast growth factor expression in esophageal adenocarcinoma and Barrett esophagus. J Thorac Cardiovasc Surg. 2003;125:246–53.PubMedCrossRefGoogle Scholar
  79. 79.
    Dubois RN, Gupta RA. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat Rev Cancer. 2001;1:11–21.PubMedCrossRefGoogle Scholar
  80. 80.
    Sawaoka H, Tsuji S, Tsujii M, Gunawan ES, Sasaki Y, Kawano S, Hori. Cyclooxygenase inhibitors suppress angiogenesis and reduce tumor growth in vivo. Lab Invest. 1999;79:1469–77.PubMedGoogle Scholar
  81. 81.
    Cheong E, Igali L, Harvey I, Mole M, Lund E, Johnson IT, et al. Cyclo-oxygenase-2 expression in Barrett’s oesophageal carcinogenesis: an immunohitochemical study. Aliment Pharmacol Ther. 2003;17:379–86.PubMedCrossRefGoogle Scholar
  82. 82.
    Lagorce C, Paraf F, Vidaud D, Couvelard A, Wendum D, Martin A, et al. Cyclooxygenase-2 is expressed frequently and early in Barrett’s oesophagus and associated adenocarcinoma. Histopathology. 2003;42:457–65.PubMedCrossRefGoogle Scholar
  83. 83.
    Buskens CJ, Van Rees BP, Sivula A, Reitsma JB, Haglund C, Bosma P, et al. Prognostic significance of elevated cyclooxygenase 2 expression in patients with adenocarcinoma of the esophagus. Gastroenterology. 2002;122:1800–7.PubMedCrossRefGoogle Scholar
  84. 84.
    Wilson KT. Angiogenic markers, neovascularization and malignant deformation of Barrett’s esophagus. Dis Esophag. 2002;15:16–21.CrossRefGoogle Scholar
  85. 85.
    Kulke MH, Thakore KS, Thomas G, Wang H, Loda M, Eng C, Odze RD. Microsatellite instability and hMLH1/hMSH2 expression in Barrett esophagus-associated adenocarcinoma. Cancer. 2001; 91:1451–7.PubMedCrossRefGoogle Scholar
  86. 86.
    Reichelt U, Duesedau P, Tsourlakis MCh, et al. Frequent homogeneous HER-2 amplification in primary and metastatic adenocarcinoma of the esophagus. Mod Pathol. 2007;20:120–9.PubMedCrossRefGoogle Scholar
  87. 87.
    Rauser S, Weis R, Braselmann H, Feith M, Stein HJ, Langer R, et al. Significance of HER2 low-level copy gain in Barrett’s cancer: implications for florescence in situ hybridization testing in tissues. Clin Cancer Res. 2007;13:5115–23.PubMedCrossRefGoogle Scholar
  88. 88.
    Lin J, Raoof DA, Thomas DG, Greenson JK, Giordano TJ, Robinson GS, et al. L-type amino acid transporter-1 overexpression and melphalan sensitivity in Barrett’s adenocarcinoma. Neoplasia. 2004;6:74–84.PubMedCrossRefGoogle Scholar
  89. 89.
    Lin J, Lin L, Thomas DG, Greenson JK, Giordano TJ, Robinson GS, et al. Melanoma-associated antigens in esophageal adenocarcinoma: identification of novel MAGE-A10 splice variants. Clin Cancer Res. 2004;10:5708–16.PubMedCrossRefGoogle Scholar
  90. 90.
    Brabender J, Lord RV, Wickramasinghe K, Metzger R, Schneider PM, Park JM, Holscher AH, DeMeester TR, Danenberg KD, Danenberg PV. Glutathione S-transferase-Pi expression is downregulated in patients with Barrett’s esophagus and esophageal adenocarcinoma. J Gastrointest Surg. 2002;6:359–67.PubMedCrossRefGoogle Scholar
  91. 91.
    Xu Y, Selaru F, Yin J, Zou TT, Shustova V, Mori Y, et al. Artificial neural networks and gene filtering distinguish between global gene expression profiles of Barrett’s esophagus and esophageal cancer. Cancer Res. 2002;62:3493–7.PubMedGoogle Scholar
  92. 92.
    Selaru FM, Zou T, Xu Y, Shustova V, Yin J, Mori Y, et al. Global gene expression profiling in Barrett’s esophagus and esophageal cancer: a comparative analysis using cDNA microarrays. Oncogene. 2002;21:475–8.PubMedCrossRefGoogle Scholar
  93. 93.
    Wang S, Zhan M, Yin J, Abraham JM, Mori Y, Sato F, et al. Transcriptional profiling suggests that Barrett’s metaplasia is an early intermediate stage in esophageal adenocarinogenesis. Oncogene. 2006;25:3346–56.PubMedCrossRefGoogle Scholar
  94. 94.
    Brabender J, Marjoram P, Salonga D, Metzger R, Schneider PM, Park JM, et al. A multigene expression panel for the molecular diagnosis of Barrett’s esophagus and Barrett’s adenocarcinoma of the esophagus. Oncogene. 2004;23:4780–8.PubMedCrossRefGoogle Scholar
  95. 95.
    Morgan C, Alazawi W, Sirieix P, Freeman T, Coleman N, Fitzgerald R. In vitro acid exposure has a differential effect on apoptotic and proliferative pathways in a Barrett’s adenocarcinoma cell line. Am J Gastroenterol. 2004;218–24.Google Scholar
  96. 96.
    Cheng P, Gong J, Wang T, Jie C, Liu GS, Zhang R. Gene expression in Barrett’s esophagus and reflux esophagitis induced by gastroduodenoesophageal refulux in rats. World J Gastroeneterol. 2005;11(21);3277–80.Google Scholar
  97. 97.
    Cheng P, Gong J, Wang T, Jie C, Liu GS, Zhang R. Gene expression in rats with Barrett’s esophagus and esophageal adenocarcinoma induced by gastroduodenoesophageal reflux. World J Gastroenterol. 2005;11(33);5117–22.PubMedGoogle Scholar
  98. 98.
    Helm J, Enkemann S, Coppola D, Barthel JS, Kelley ST, Yeatman TJ. Dedifferentiation precedes invasion in the progression from Barrett’s metaplasia to esophageal adenocarcinoma. Clin Cancer Res. 2005;11(7);2478–85.PubMedCrossRefGoogle Scholar
  99. 99.
    Sui G, Zhou S, Wang J, Canto M, Eshleman ER, Montgomery EA, et al. Mitochondrial DNA mutations in preneoplastic lesions of the gastrointestinal tract: a biomarker for the early detection of cancer. Mol Cancer. 2006;5:73.PubMedCrossRefGoogle Scholar
  100. 100.
    Feber A, Xi L, Luketich J, Pennathur A, Landreneau RJ, Wu M, et al. MicroRNA expression profiles of esophageal cancer. J Thorac Cardiovasc Surg. 2008;135:255–60.PubMedCrossRefGoogle Scholar
  101. 101.
    Feldman A, Espina V, Petricoin EF, Liotta LA, Rosenblatt KP. Use of proteomic patterns to screen for gastrointestinal malignancies. Surgery. 2004;135(3);243–7.PubMedCrossRefGoogle Scholar
  102. 102.
    Zhao J, Chang AC, Li C, Shedden KA, Thomas DG, Misek DE, Manoharan AP, Giordano TJ, Beer DG, Lubman DM. Comparative proteomics analysis of Barrett metaplasia and esophageal adenocarcinoma using two-dimensional liquid mass mapping. Mol Cell Proteomics. 2007;6:987–99.PubMedCrossRefGoogle Scholar
  103. 103.
    Ostrowski J, Mikula M, Karezmarski J, Rubel T, Wyrwicz LS, Bragoszewski P, Gaj P, Dadlez M, Butruk E, Regula J. Molecular defense mechanisms of Barrett’s metaplasia estimated by an integrative genomics. J Mol Med. 2007;85(7);733–43.PubMedCrossRefGoogle Scholar
  104. 104.
    Peng D, Sheta EA, Powell SM, Moskaluk CA, Washington K, Goldknopf IL, et al. Alterations in Barrett’s-related adenocarcinomas: a proteomic approach. Int J Cancer. 2008;122(6);1303–10.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Domenico Coppola
    • 1
    • 2
  • Nelly A. Nasir
    • 1
    • 2
    • 3
  • Leslie Turner
    • 1
    • 2
  1. 1.Department of Anatomic PathologyMoffitt Cancer Center and Research InstituteTampaUSA
  2. 2.Department of Anatomic PathologyCollege of Medicine, University of South FloridaTampaUSA
  3. 3.Department of PathologySir Mortimer Jewish General Hospital, McGill UniversityMontrealUSA

Personalised recommendations