Risk factors and progression predictors of Barrett´s oesophagus to adenocarcinoma

Czech version

Authors: Pavel Svoboda ^1,2; Petr Dítě ^1,2; Pavel Klvaňa ^1,2; Tomáš Kupka ²; Martina Bojková ²; Jana Žmolíková ^3,4,5; Irena Urbanovská ^3,4,6; Magdalena Uvírová ^3,4,6; Petr Buzrla ^7,8; Jana Dvořáčková ^5,7,8
Authors‘ workplace: Katedra interních oborů LF OU Ostrava, vedoucí katedry MUDr. Ivo Valkovský, Ph. D. ¹; Interní klinika LF OU a FN Ostrava, přednosta doc. MUDr. Arnošt Martínek., CSc. ²; Vědecký a výzkumný institut Agel, pobočka Ostrava-Vítkovice, CGB laboratoř, ředitelka společnosti RNDr. Magdalena Uvírová ³; Katedra biomedicínských oborů LF OU Ostrava, vedoucí katedry doc. RNDr. Kristian Šafarčík, Ph. D. ⁴; Ústav biologie LF UP Olomouc, přednosta ústavu doc. RNDr. Vladimír Divoký, Ph. D. ⁵; Ústav molekulární a translační medicíny LF UP Olomouc, ředitel doc. MUDr. Marián Hajdúch, Ph. D. ⁶; Ústav patologie LF OU, vedoucí ústavu doc. MUDr. Jaroslav Horáček, CSc. ⁷; Ústav patologie FN Ostrava, vedoucí ústavu doc. MUDr. Jana Dvořáčková, Ph. D. ⁸
Published in: Vnitř Lék 2014; 60(5-6): 467-473
Category: Review

Overview

Gastroesophageal reflux disease is a quite common disorder, and the condition affects some 40 per cent of population in the course of their lifetime. Fortunately, about half of the patients examined due to clear symptoms do not manifest macroscopic damage of the oesophageal mucosa, and serious endoscopic findings (Barrett's oesophagus) are observed in only a small percentage of patients (10%). Barrett's oesophagus is a serious complication – precancerous condition with a 30-fold higher risk of development of oesophageal adenocarcinoma when compared with patients without this condition. The article presents risk factors and predictors of progression of the Barrett's oesophagus into the stage of adenocarcinoma. The main risk factors associated with oesophageal adenocarcinoma are male sex, white race, gastroesophageal reflux.

Key words:
aetiology – Barrett's oesophagus – oesophageal adenocarcinoma – reflux

Sources

1. Barrett NR. Chronic peptic ulcer of the oesophagus and “oesophagitis”. Br J Surg 1950; 38(150): 175–182.

2. Allison PR, Johnstone AS. The oesophagus lined with gastric mucous membrane. Thorax 1953; 8(2): 87–101.

3. Naef AP, Savary M, Ozzello L. Columnar-lined lower esophagus: an acquired lesion with malignant predisposition. Report on 140 cases of Barrett`s esophagus with 12 adenocarcinomas. J Thorac Cardiovasc Surg 1975; 70(5): 826–835.

4. Devesa SS, Blot WJ, Fraumeni jr. JF Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer 1998; 83(10): 2049–2453.

5. Hvid-Jensen F, Pedersen L, Drewes AM et al. Incidence of adenocarcinoma among patients with Barrett`s esophagus. N Engl J Med 2011; 365(15): 1375–1383.

6. Martínek J, Beneš M, Brandtl P et al. Low incidence of adenocarcinoma and high-grade intraepithelial neoplasia in patients with Barrett's esophagus: a prospective cohort study. Endoscopy 2008; 40(9): 711–716.

7. Voltaggio L, Montgomery EA, Lam-Himlin D. A clinical and histopathologic focus on Barrett esophagus and Barrett-related dysplasia. Arch Pathol Lab Med 2011; 135(10): 1249–1260.

8. Shepherd NA, Warren BF et al (edts). Morson and Dawson´s Gastrointestinal Pathology. 5th ed. Wiley-Blackwell: Hoboken (NJ) 2013. ISBN 978–1-4051–9943–8.

9. Lisovsky M, Srivastava A. Barrett Esophagus: Evolving Concepts in Diagnosis and Neoplastic Progression. Surgical Pathology Clinics 2013; 6(3): 475–496.

10. Řešení Barrettova jícnu. Lékařské listy 2010; 11 (Suppl). Dostupné on-line: <http://zdravi.e15.cz/clanek/priloha-lekarske-listy/reseni-barrettova-jicnu-452135>.

11. Montgomery EA, Voltaggio L. Biopsy Interpretation of the Gastrointestinal Mucosa, Volume 2: Neoplastic. 2nd ed. Lippincott Williams and Wilkins: Philadelphia 2012. ISBN 9781451109597.

12. Curvers WL, Kate FJ, Krishnadath KK et al. Low-grade dysplasia in Barrett`s esophagus: overdiagnosed and undereestimated. Am J Gastroenterol 2010; 105: 1523–1530.

13. Pech O, Vieth M, Schmitz D et al. Conclusion from the histological diagnosis of low.grade intraepithelial neoplasia in Barrett`s oesophagus. Scand J Gastroenterol 2007; 42(6): 682–688.

14. Phoa KN, van Vilsteren RE, Pouw BL et al. Surveillance vs RFA for Barrett`s esophagus with confirmed low grade dysplasia: a european Multicenter randomized controlled trial. DDW 2013, abstract No. 1004.

15. Hamamoto Y, Endo T, Nosho K et al. Usefulness of narrow-band imaging endoscopy for diagnosis of Barrett`s esophagus. J Gastroenterol 2004; 39(1): 14–20.

16. Stefanová M, Zavoral M, Závada F et al. Přínos autofluorescence v diagnostice lehké intraepiteliální neoplazie u pacientů s Barrettovým jícnem. Gastroent Hepatol 2011; 65(5): 249–254.

17. Curvers WL, Herrero LA, Wallace MB et al. Endoscopic tri-modal imaging is more effective than standard endoscopy in identifying early-stage neoplasie in Barrett`s esophagus. Gasrteonterology 2010; 139(4): 1106–1114.

18. Mannath JJ, Subramanian V, Hawkey CJ et al. Narrow band imaging for characterization of high grade dysplasia and specialized intestinal metaplasia in Barrett`s esophagus: a meta-analysis. Endoscopy 2010; 42(5): 351–359.

19. Kara MA, Bergman JJ. Autofluorescence imaging and narrow-band imaging for the detection of early neoplasia in patients with Barret`s esophagus. Endoscopy 2006; 38(6): 627–631.

20. Wang KK, Okoro N, Prasad G et al. Endoscopic evaluation and advanced imaging of Barrett`s esophagus. Gastrointest Endosc Clin N Am 2011; 21(1): 39–51.

21. Stefanová M, Tučková I, Malušková J et al. Biopsie nejsou dostatečné pro přesnou diagnostiku neoplazie u pacientů s Barrettovám jícnem. Gastroent Hepatol 2013; 67(4): 264–270.

22. Hull MJ, Mino-Kenudson M, Nishioka NS et al. Endoscopoc mucosal resection: an improved diagnostic procedur for early gastroesophageal epithelial neoplasms. Am J Surg Pathol 2006; 30(1): 114–118.

23. Spechler SJ, Sharma P, Souza RF et al. American Gastroenterological Association medical position statement on the management of Barrett`s esophagus. Gastroenterology 2011; 140(3): 1084–1091.

24. Ell C, May A, Gossner L et al. Endoscopic mucosal resection of early cancer and high-grade dysplasia in Barrett`s esophagus. Gastroenterology 2000; 118(4): 670–677.

25. Vakil N, van Zanten SV, Kahrilas P et al. The Montreal definition and classiffication of gastroesophageal reflux disease: a global evidence-based consensus. Am J Gastroenterol 2006; 101(8): 1900–1920.

26. Overholt BF, Lightdale CJ, Wang KK et al. Photodynamic therapy with porfimer sodium for ablativ of high-grade dysplasia in Barrett`s esophagus: international, partially blinded, randomized phase III trial. Gastrointest Endosc 2005; 62(4): 488–498.

27. Lagergren J, Bergstrom R, Lindgren A et al. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med 1999; 340(11): 825–831.

28. Fitzgerald RC, Omary MB, Triadafilopoulos G. Dynamic effects of acid on Barrett`s esophagus. An ex vivo proliferation and differentiation model. J Clin Invest 1996; 98(9): 2120–2128.

29. Haigh CR, Attwood SE, Thompson DG et al. Gastrin induces proliferation in Barrett`s metabplasia through activation of the CCK2 receptor. Gastroenterology 2003; 124(3): 615–625.

30. Chang EY, Morris CD, Seltman AK et al. The effect of antireflux surgery on esophageal carcinogenesis in patients with Barrett esophagus: a systematic review. Ann Surg 2007; 246(1): 11–21.

31. Weston AP, Badr AS, Hassanein RS. Prospective multivariate analysis of factors predictive of complete regression of Barrett`s esophagus. Am J Gastroenterol 1999; 94(12): 3420–3426.

32. Weston AP, Sharma P, Mathur S et al. Risk stratification of Barrett’s esophagus: updated prospective multivariate analysis. Am J Gastroenterol 2004; 99(9): 1657–1666.

33. Buttar NS, Wang KK, Sebo TJ et al. Extent of high-grade dysplasia in Barrett’s esophagus correlates with risk of adenocarcinoma. Gastroenterology 2001; 120(7): 1630–1639.

34. Montgomery E, Bronner MP, Greenson JK et al. Are ulcers a marker for invasive carcinoma in Barrett’s esophagus? Data from a diagnostic variability study with clinical follow-up. Am J Gastroenterol 2002; 97(1): 27–31.

35. Wani S, Puli SR, Shaheen NJ et al. Esophageal adenocarcinoma in Barrett’s esophagus after endoscopic ablative therapy: a meta-analysis and systematic review. Am J Gastroenterol 2009; 104(2): 502–513.

36. Hampel H, Abraham NS, El-Serag HB. Meta-analysis: obesity and the risk for gastroesophageal reflux disease and its complications. Ann Intern Med 2005; 143(3): 199–211.

37. Kubo A, Corley DA. Body mass index and adenocarcinomas of the esophagus or gastric cardia: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev 2006; 15(5): 872–878.

38. Cook MB, Greenwood DC, Hardie LJ et al. A systematic review and meta-analysis of the risk of increasing adiposity on Barrett‘ s esophagus. Am J Gastroenterol 2008; 103(2): 292–300.

39. Edelstein ZR, Farrow DC, Bronner MP et al. Central adiposity and risk of Barrett’s esophagus. Gastroenterology 2007; 133(2): 403–411.

40. Ye W, Held M, Lagergren J et al. Helicobacter pylori infection and gastric atrophy: risk of adenocarcinoma and squamous-cell carcinoma of the esophagus and adenocarcinoma of the gastric cardia. J Natl Cancer Inst 2004; 96(5): 388–396.

41. Whiteman DC, Parmar P, Fahey P et al. Association of Helicobacter pylori infection with reduced risk for esophageal cancer is independent of environmental and genetic modifiers. Gastroenterology 2010; 139(1): 73–83.

42. Chow WH, Blaser MJ, Blot WJ et al. An inverse relation between cagA+ strains of Helicobacter pylori infection and risk of esophageal and gastric cardia adenocarcinoma. Cancer Res 1998; 58(4): 588–590.

43. Whiteman DC, Sadeghi S, Pandeya N et al. Combined effects of obesity, acid reflux and smoking on the risk of adenocarcinomas of the oesophagus. Gut 2008; 57(2): 173–180.

44. Lukáš K. Je hiátová hernie synonynem pro refluxní chorobu jícnu? Čes a Slov Gastroent a Hepatol 2004; 58(3): 110–115.

45. Kamangar F, Chow WH, Abnet CC et al. Environmental causes of esophageal cancer. Gastroenterol Clin North Am 2009; 38(1): 27–57.

46. Avidan B, Sonnenberg A, Schnell TG et al. Hiatal hernia size, Barrett’s length, and severity of acid reflux are all risk factors for esophageal adenocarcinoma. Am J Gastroenterol 2002; 97(8): 1930–1936.

47. Menke-Pluymers MB, Hop WC, Dees J et al. Risk factors for the development of an adenocarcinoma in columnar-lined (Barrett) esophagus. The Rotterdam Esophageal Tumor Study Group. Cancer 1993; 72(4): 1155–1158.

48. Gray MR, Donnelly RJ, Kingsnorth AN. The role of smoking and alcohol in metaplasia and cancer risk in Barrett’s columnar lined oesophagus. Gut 1993; 34(6): 727–731.

49. Freedman ND, Abnet CC, Leitzmann MF et al. A prospective study of tobacco, alcohol, and the risk of oesophageal and gastric cancer subtypes. Am J Epidemiol 2007; 165(12): 1424–1433.

50. Wu AH, Wan P, Bernstein L. A multiethnic population-based study of smoking, alcohol and body size and risk of adenocarcinomas of the stomach and esophagus (United States). Cancer Causes Control 2001; 12(8): 721–732.

51. Veugelers PJ, Porter GA, Guernsey DL et al. Obesity and lifestyle risk factors for gastroesophageal reflux disease, Barrett esophagus and esophageal adenocarcinoma. Dis Esophagus 2006; 19(5): 321–328.

52. Chen Z, Yang G, Zhou M et al. Body mass index and mortality from ischaemic heart disease in a lean population: 10 year prospective study of 220,000 adult men. Int J Epidemiol 2006; 35(1): 141–150.

53. Gammon MD, Schoenberg JB, Ahsan H et al. Tobacco, alcohol, and socioeconomic status and adenocarcinomas of the esophagus and gastric cardia. J Natl Cancer Inst 1997; 89(17): 1277–1284.

54. Bani-Hani KE, Bani-Hani BK, Martin IG Characteristics of patients with columnar-lined Barrett’s esophagus and risk factors for progression to esophageal adenocarcinoma. World J Gastroenterol 2005; 11(43): 6807–6814.

55. Avidan B, Sonnenberg A, Schnell TG et al. Hiatal hernia size, Barrett’s length, and severity of acid reflux are all risk factors for esophageal adenocarcinoma. Am J Gastroenterol 2002; 97(8): 1930–1936.

56. Prasad GA, Bansal A, Sharma P et al. Predictors of progression in Barrett`s esophagus: current knowledge and future directions. Am J Gastrolenterol 2010; 105(7): 1490–1502.

57. Yousef F, Cardwell C, Cantwell MM et al. The incidence of esophageal cancer and high-grade dysplasia in Barrett’s esophagus: a systematic review and meta-analysis. Am J Epidemiol 2008; 168(3): 237–249.

58. de Jonge PJ, Steyerberg EW, Kuipers EJ et al. Risk factors for the development of esophageal adenocarcinoma in Barrett’s esophagus. Am J Gastroenterol 2006; 101(7): 1421–1429.

59. Mehta S, Johnson IT, Rhodes M. Systematic review: the chemoprevention of oesophageal adenocarcinoma. Aliment Pharmacol Ther 2005; 22(9): 759–768.

60. Dong LM, Kristal AR, Peters U et al. Dietary supplement use and risk of neoplastic progression in esophageal adenocarcinoma: a prospective study. Nutr Cancer 2008; 60(1): 39–48.

61. Guo W, Blot WJ, Li JY et al. A nested case- control study of oesophageal and stomach cancers in the Linxian nutrition intervention trial. Int J Epidemiol 1994; 23(3): 444–450.

62. Gonzalez CA, Pera G, Agudo A et al. Fruit and vegetable intake and the risk of stomach and oesophagus adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer 2006; 118(10): 2559–2566.

63. Sapkota A, Hsu CC, Zaridze D et al. Dietary risk factors for squamous cell carcinoma of the upper aerodigestive tract in central and eastern Europe. Cancer Causes Control 2008; 19(10): 1161–1170.

64. Riboli E, Norat T. Epidemiologic evidence of the protective effect of fruit and vegetables on cancer risk. Am J Clin Nutr 2003; 78(Suppl 3): S559-S569.

65. Jansson C, Johansson AL, Bergdahl IA et al. Occupational exposures and risk of esophageal and gastric cardia cancers among male Swedish construction workers. Cancer Causes Control 2005; 16(6): 755–764.

66. Engel LS, Vaughan TL, Gammon MD et al. Occupation and risk of esophageal and gastric cardia adenocarcinoma. Am J Ind Med 2002; 42(1): 11–22.

67. Jansson C, Jeding K, Lagergren J. Job strain and risk of esophageal and cardia cancers. Cancer Epidemiol 2009; 33(6): 473–475.

68. Leeuwenburgh I, Haringsma J, Van Dekken H et al. Long-term risk of oesophagitis, Barrett‘s oesophagus and oesophageal cancer in achalasia patients. Scand J Gastroenterol Suppl 2006; (243): 7–10.

69. Zendehdel K, Nyrén O, Edberg A et al. Risk of esophageal adenocarcinoma in achalasia patients, a retrospective cohort study in Sweden. Am J Gastroenterol 2011; 106(1): 57–61.

70. Corley DA, Kerlikowske K, Verma R et al. Protective association of aspirin/NSAIDs and esophageal cancer: a systematic review and meta-analysis. Gastroenterology 2003; 124(1): 47–56.

71. Rothwell PM, Wilson M, Elwin CE et al. Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials. Lancet 2010; 376 (9754): 1741–1750.

72. Smith M, Zhou M, Whitlock G et al. Esophageal cancer and body mass index: results from a prospective study of 220,000 men in China and a meta-analysis of published studies. Int J Cancer 2008; 122(7): 1604–1610.

73. Krishnadath KK, Hugo WT, van Blankenstein M et al. Accumulation of Genetic Abnormalities during neoplastic Progression in Barrett´s Esophagus. Cancer Res 1995; 55(9): 1971–1976.

74. Jankowski JA, Wright NA, Meltzter SJ et al. Molecular evolution of the metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am J Pathol 1999; 154(4): 965–973.

75. Maley CC, Galipeau PC, Li X et al. Selectively advantageous mutations and hitchhikers in neoplasms: p16 lesions are selected in Barrett´s espohagus. Cancer Res 2004; 64(10): 3414–3427.

76. Rauser S, Weis R, Braselmann H et al. Significance of HER2 low-level copy gain in Barrett´s cancer: implications for fluorescence in situ hybridization testing in tissues. Clin Cancer Res 2007; 13(17): 5115–5123.

77. Illig R, Klieser E, Kiesslich T et al. GERD-Barrett-Adenocarcinoma: Do We Have Suitable Prognostic and Predictive Molecular Markers? Gastroenterol Res Pract 2013; 2013: 643084.

78. Brankley SM, Fritcher EG, Smyrk TC et al. Fluorescence in situ hybridization mapping of esophagectomy specimens from patients with Barrett's esophagus with high-grade dysplasia or adenocarcinoma. Hum Pathol 2012; 43(2): 172–179.

79. Saito H, Tsujitani S, Oka S at al. The expression of murine double minute 2 is a favorable prognostic marker in esophageal squamous cell carcinoma without p53 protein accumulation. Ann Surg Oncol 2002; 9(5): 450–456.

80. Sanjeev S, Shaomeng W. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy. Annu Rev Pharmacol Toxicol 2009; 49: 223–241.

81. Ellsworth E, Jackson SA, Thakkar SJ et al. Correlation of the presence and extend of los sof heterozygosity mutations with histological classifications of Barrett´s esofagus. BMC Gastroenterol 2012; 12: 181. Dostupné z DOI: <http://doi: 10.1186/1471–230X-12–181>.

82. Rygiel AM, van Baal JWPM, Milano F et al. Efficient automated assessment of genetic abnormalities detected by fluorescence in situ hybridization on brush cytology in a Barrett esophagus surveillance population. Cancer 2007; 109(10): 1980–1988.

83. Bian YS, Osterheld MC, Fontolliet C et al. p16 inactivation by methylation of the CDKN2A promoter occurs early during neoplastic progression in Barrett´s esofagus. Gastroenterology 2002; 122(4): 1113–1121.

84. Brankley SM, Fritcher EG, Smyrk TC et al. Fluorescence in situ hybridization mapping of esophagectomy specimens from patients with Barrett's esophagus with high-grade dysplasia or adenocarcinoma. Hum Pathol 2012; 43(2): 172–179.

85. Croxtall JD, McKeage K. Trastuzumab: in HER2-positive metastatic gastrin cancer. Drugs 2010; 70(17): 2259–2267.

86. Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med 2009; 60: 167–179.

87. Luzna P, Gregar J, Uberall I et al. Changes of microRNAs-192,196a adn 203 correlate with Barrett´s esofagus diagnosis and its progression compared to normal healthy individuals. Diagn Pathol 2011; 6: 114. Dostupné z DOI: <http://doi: 10.1186/1746–1596–6-114>.

88. Saini S, Majid S, Yamamura S et al. Regulatory role of miR-203 in prostate cancer progression and metastasis. Clin Cancer Res 2011; 17(16): 5287–5298.