Role of Obesity in the Pathogenesis and Progression of Barrett's Esophagus

Gastroenterology Clinics of North America

Volumn 44, Issue 2, 2015, Pages 249-264

  Chandar, Apoorva Krishna ^a   Iyer, Prasad G ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Adiponectin; Barrett's esophagus; Esophageal adenocarcinoma; Gastroesophageal reflux disease; Inflammation; Insulin resistance; Leptin; Obesity

Indexed keywords

ADIPOCYTOKINE; INSULIN; LEPTIN; METFORMIN; OMEGA 3 FATTY ACID; PLACEBO; POLYPHENOL DERIVATIVE; ADIPONECTIN;

ABDOMINAL FAT; ABDOMINAL OBESITY; BARIATRIC SURGERY; BARRETT ESOPHAGUS; BODY MASS; CANCER PREVENTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; DRUG DOSE TITRATION; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGUS DYSPLASIA; GASTROESOPHAGEAL REFLUX; HUMAN; INFLAMMATION; INSULIN RESISTANCE; INTESTINE METAPLASIA; MACROPHAGE; MALIGNANT TRANSFORMATION; NONHUMAN; OBESITY; PATHOGENESIS; REFLUX ESOPHAGITIS; REVIEW; WAIST CIRCUMFERENCE; BLOOD; COMPLICATION; HIATUS HERNIA; METABOLISM; OBESITY, ABDOMINAL;

ADIPONECTIN; BARRETT ESOPHAGUS; GASTROESOPHAGEAL REFLUX; HERNIA, HIATAL; HUMANS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; LEPTIN; OBESITY, ABDOMINAL;

EID: 84929963372     PISSN: 08898553     EISSN: 15581942     Source Type: Journal    
DOI: 10.1016/j.gtc.2015.03.001     Document Type: Review

References (84)

1. Kroep S., Lansdorp-Vogelaar I., Rubenstein J.H., et al. Comparing trends in esophageal adenocarcinoma incidence and lifestyle factors between the United States, Spain, and the Netherlands. Am J Gastroenterol 2014, 109:336-343. [quiz: 335, 344].
2. Blot W.J., McLaughlin J.K. The changing epidemiology of esophageal cancer. Semin Oncol 1999, 26:2-8.
3. Siegel R., Ma J., Zou Z., et al. Cancer statistics, 2014. CA Cancer J Clin 2014, 64:9-29.
4. Cook M.B., Greenwood D.C., Hardie L.J., et al. Asystematic review and meta-analysis of the risk of increasing adiposity on Barrett's esophagus. Am J Gastroenterol 2008, 103:292-300.
5. Kamat P., Wen S., Morris J., et al. Exploring the association between elevated body mass index and Barrett's esophagus: a systematic review and meta-analysis. Ann Thorac Surg 2009, 87:655-662.
6. Kaul S., Rothney M.P., Peters D.M., et al. Dual-energy X-ray absorptiometry for quantification of visceral fat. Obesity (Silver Spring) 2012, 20:1313-1318.
7. Houtkooper L.B., Lohman T.G., Going S.B., et al. Why bioelectrical impedance analysis should be used for estimating adiposity. Am J Clin Nutr 1996, 64:436S-448S.
8. Thrift A.P., Kramer J.R., Alsarraj A., et al. Fat mass by bioelectrical impedance analysis is not associated with increased risk of Barrett esophagus. JClin Gastroenterol 2014, 48:218-223.
9. Kramer J.R., Fischbach L.A., Richardson P., et al. Waist-to-hip ratio, but not body mass index, is associated with an increased risk of Barrett's esophagus in white men. Clin Gastroenterol Hepatol 2013, 11:373-381.e1.
10. Kendall B.J., Macdonald G.A., Hayward N.K., Study of Digestive Health, et al. The risk of Barrett's esophagus associated with abdominal obesity in males and females. Int J Cancer 2013, 132:2192-2199.
11. Singh S., Sharma A.N., Murad M.H., et al. Central adiposity is associated with increased risk of esophageal inflammation, metaplasia, and adenocarcinoma: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2013, 11:1399-1412.e7.
12. Kubo A., Cook M.B., Shaheen N.J., et al. Sex-specific associations between body mass index, waist circumference and the risk of Barrett's oesophagus: a pooled analysis from the international BEACON consortium. Gut 2013, 62:1684-1691.
13. El-Serag H.B., Hashmi A., Garcia J., et al. Visceral abdominal obesity measured by CT scan is associated with an increased risk of Barrett's oesophagus: a case-control study. Gut 2014, 63:220-229.
14. Nelsen E.M., Kirihara Y., Takahashi N., et al. Distribution of body fat and its influence on esophageal inflammation and dysplasia in patients with Barrett's esophagus. Clin Gastroenterol Hepatol 2012, 10:728-734. [quiz: e61-2].
15. Pandolfino J.E., El-Serag H.B., Zhang Q., et al. Obesity: a challenge to esophagogastric junction integrity. Gastroenterology 2006, 130:639-649.
16. Derakhshan M.H., Robertson E.V., Fletcher J., et al. Mechanism of association between BMI and dysfunction of the gastro-oesophageal barrier in patients with normal endoscopy. Gut 2012, 61:337-343.
17. Wu J.C., Mui L.M., Cheung C.M., et al. Obesity is associated with increased transient lower esophageal sphincter relaxation. Gastroenterology 2007, 132:883-889.
18. El-Serag H.B., Ergun G.A., Pandolfino J., et al. Obesity increases oesophageal acid exposure. Gut 2007, 56:749-755.
19. Andrici J., Tio M., Cox M.R., et al. Hiatal hernia and the risk of Barrett's esophagus. JGastroenterol Hepatol 2013, 28:415-431.
20. Taylor J.B., Rubenstein J.H. Meta-analyses of the effect of symptoms of gastroesophageal reflux on the risk of Barrett's esophagus. Am J Gastroenterol 2010, 105:1729-1737. [quiz: 1738].
21. El-Serag H.B., Tran T., Richardson P., et al. Anthropometric correlates of intragastric pressure. Scand J Gastroenterol 2006, 41:887-891.
22. Ma Y., Yang Y., Wang F., et al. Obesity and risk of colorectal cancer: a systematic review of prospective studies. PLoS One 2013, 8:e53916.
23. Gukovsky I., Li N., Todoric J., et al. Inflammation, autophagy, and obesity: common features in the pathogenesis of pancreatitis and pancreatic cancer. Gastroenterology 2013, 144:1199-1209.e4.
24. Lee B.C., Lee J. Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance. Biochim Biophys Acta 2014, 1842:446-462.
25. McNelis J.C., Olefsky J.M. Macrophages, immunity, and metabolic disease. Immunity 2014, 41:36-48.
26. Ryan A.M., Healy L.A., Power D.G., et al. Barrett esophagus: prevalence of central adiposity, metabolic syndrome, and a proinflammatory state. Ann Surg 2008, 247:909-915.
27. Olefsky J.M., Glass C.K. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010, 72:219-246.
28. Osborn O., Olefsky J.M. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012, 18:363-374.
29. Malhi H., Gores G.J., Katzka D.A., et al. Macrophage related inflammation andphenotype modulation in barrett's esophagus. Gastroenterology 2013, 144:S-688.
30. Friedman J.M., Halaas J.L. Leptin and the regulation of body weight in mammals. Nature 1998, 395:763-770.
31. Havel P.J., Kasim-Karakas S., Dubuc G.R., et al. Gender differences in plasma leptin concentrations. Nat Med 1996, 2:949-950.
32. Sierra-Honigmann M.R., Nath A.K., Murakami C., et al. Biological action of leptin as an angiogenic factor. Science 1998, 281:1683-1686.
33. Ogunwobi O., Mutungi G., Beales I.L. Leptin stimulates proliferation and inhibits apoptosis in Barrett's esophageal adenocarcinoma cells by cyclooxygenase-2-dependent, prostaglandin-E2-mediated transactivation of the epidermal growth factor receptor and c-Jun NH2-terminal kinase activation. Endocrinology 2006, 147:4505-4516.
34. Beales I.L., Ogunwobi O., Cameron E., et al. Activation of Akt is increased in the dysplasia-carcinoma sequence in Barrett's oesophagus and contributes to increased proliferation and inhibition of apoptosis: a histopathological and functional study. BMC Cancer 2007, 7:97.
35. Francois F., Roper J., Goodman A.J., et al. The association of gastric leptin with oesophageal inflammation and metaplasia. Gut 2008, 57:16-24.
36. Kendall B.J., Macdonald G.A., Hayward N.K., Study of Digestive Health, et al. Leptin and the risk of Barrett's oesophagus. Gut 2008, 57:448-454.
37. Rubenstein J.H., Morgenstern H., McConell D., et al. Associations of diabetes mellitus, insulin, leptin, and ghrelin with gastroesophageal reflux and Barrett's esophagus. Gastroenterology 2013, 145:1237-1244.e1-5.
38. Garcia J.M., Splenser A.E., Kramer J., et al. Circulating inflammatory cytokines and adipokines are associated with increased risk of Barrett's esophagus: a case-control study. Clin Gastroenterol Hepatol 2014, 12:229-238.e3.
39. Thompson O.M., Beresford S.A., Kirk E.A., et al. Serum leptin and adiponectin levels and risk of Barrett's esophagus and intestinal metaplasia of the gastroesophageal junction. Obesity (Silver Spring) 2010, 18:2204-2211.
40. Devanna S., Singh S., Dunagan K.T., et al. Association between serum adipokines, insulin and risk of Barrett's esophagus: a systematic review and meta-analysis. Gastroenterology 2014, 146:S-310.
41. Scherer P.E. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes 2006, 55:1537-1545.
42. Coppola A., Marfella R., Coppola L., et al. Effect of weight loss on coronary circulation and adiponectin levels in obese women. Int J Cardiol 2009, 134:414-416.
43. Wolf A.M., Wolf D., Rumpold H., et al. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004, 323:630-635.
44. Brakenhielm E., Veitonmaki N., Cao R., et al. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proc Natl Acad Sci USA 2004, 101:2476-2481.
45. Ogunwobi O.O., Beales I.L. Globular adiponectin, acting via adiponectin receptor-1, inhibits leptin-stimulated oesophageal adenocarcinoma cell proliferation. Mol Cell Endocrinol 2008, 285:43-50.
46. Suzuki S., Wilson-Kubalek E.M., Wert D., et al. The oligomeric structure of high molecular weight adiponectin. FEBS Lett 2007, 581:809-814.
47. Schober F., Neumeier M., Weigert J., et al. Low molecular weight adiponectin negatively correlates with the waist circumference and monocytic IL-6 release. Biochem Biophys Res Commun 2007, 361:968-973.
48. Konturek P.C., Burnat G., Rau T., et al. Effect of adiponectin and ghrelin on apoptosis of Barrett adenocarcinoma cell line. Dig Dis Sci 2008, 53:597-605.
49. Souza R.F., Shewmake K.L., Shen Y., et al. Differences in ERK activation in squamous mucosa in patients who have gastroesophageal reflux disease with and without Barrett's esophagus. Am J Gastroenterol 2005, 100:551-559.
50. Mokrowiecka A., Daniel P., Jasinska A., et al. Serum adiponectin, resistin, leptin concentration and central adiposity parameters in Barrett's esophagus patients with and without intestinal metaplasia in comparison to healthy controls and patients with GERD. Hepatogastroenterology 2012, 59:2395-2399.
51. Rubenstein J.H., Dahlkemper A., Kao J.Y., et al. Apilot study of the association of low plasma adiponectin and Barrett's esophagus. Am J Gastroenterol 2008, 103:1358-1364.
52. Rubenstein J.H., Kao J.Y., Madanick R.D., et al. Association of adiponectin multimers with Barrett's oesophagus. Gut 2009, 58:1583-1589.
53. Dvorakova K., Payne C.M., Ramsey L., et al. Increased expression and secretion of interleukin-6 in patients with Barrett's esophagus. Clin Cancer Res 2004, 10:2020-2028.
54. Schwartz M.W., Porte D. Diabetes, obesity, and the brain. Science 2005, 307:375-379.
55. Rubin R., Baserga R. Insulin-like growth factor-I receptor. Its role in cell proliferation, apoptosis, and tumorigenicity. Lab Invest 1995, 73:311-331.
56. Kooijman R. Regulation of apoptosis by insulin-like growth factor (IGF)-I. Cytokine Growth Factor Rev 2006, 17:305-323.
57. Greer K.B., Kresak A., Bednarchik B., et al. Insulin/insulin-like growth factor-1 pathway in Barrett's carcinogenesis. Clin Transl Gastroenterol 2013, 4:e31.
58. Siahpush S.H., Vaughan T.L., Lampe J.N., et al. Longitudinal study of insulin-like growth factor, insulin-like growth factor binding protein-3, and their polymorphisms: risk of neoplastic progression in Barrett's esophagus. Cancer Epidemiol Biomarkers Prev 2007, 16:2387-2395.
59. Clemons N.J., Phillips W.A., Lord R.V. Signaling pathways in the molecular pathogenesis of adenocarcinomas of the esophagus and gastroesophageal junction. Cancer Biol Ther 2013, 14:782-795.
60. Duggan C., Onstad L., Hardikar S., et al. Association between markers of obesity and progression from Barrett's esophagus to esophageal adenocarcinoma. Clin Gastroenterol Hepatol 2013, 11:934-943.
61. Yuan M., Konstantopoulos N., Lee J., et al. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 2001, 293:1673-1677.
62. Solinas G., Karin M. JNK1 and IKKbeta: molecular links between obesity and metabolic dysfunction. FASEB J 2010, 24:2596-2611.
63. Silha J.V., Krsek M., Skrha J.V., et al. Plasma resistin, adiponectin and leptin levels in lean and obese subjects: correlations with insulin resistance. Eur J Endocrinol 2003, 149:331-335.
64. Yadav A., Kataria M.A., Saini V., et al. Role of leptin and adiponectin in insulin resistance. Clin Chim Acta 2013, 417:80-84.
65. Kadowaki T., Yamauchi T., Kubota N., et al. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. JClin Invest 2006, 116:1784-1792.
66. Iyer P.G., Borah B.J., Heien H.C., et al. Association of Barrett's esophagus with type II diabetes mellitus: results from a large population-based case-control study. Clin Gastroenterol Hepatol 2013, 11:1108-1114.e5.
67. Leggett C.L., Nelsen E.M., Tian J., et al. Metabolic syndrome as a risk factor for Barrett esophagus: a population-based case-control study. Mayo Clin Proc 2013, 88(2):157-165.
68. Hsu C.S., Wang P.C., Chen J.H., et al. Increasing insulin resistance is associated with increased severity and prevalence of gastro-oesophageal reflux disease. Aliment Pharmacol Ther 2011, 34:994-1004.
69. Kubo A., Corley D.A. Body mass index and adenocarcinomas of the esophagus or gastric cardia: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev 2006, 15:872-878.
70. Thota P.N., Sanaka M.R., Singh P., et al. Influence of body mass index (BMI) on the prevalence of dysplasia in barrett's esophagus (BE). Gastroenterology 2014, 146(5):S-302.
71. Howard J.M., Beddy P., Ennis D., et al. Associations between leptin and adiponectin receptor upregulation, visceral obesity and tumour stage in oesophageal and junctional adenocarcinoma. Br J Surg 2010, 97:1020-1027.
72. Zhang H.Y., Zhang Q., Zhang X., et al. Cancer-related inflammation and Barrett's carcinogenesis: interleukin-6 and STAT3 mediate apoptotic resistance in transformed Barrett's cells. Am J Physiol Gastrointest Liver Physiol 2011, 300:G454-G460.
73. Tselepis C., Perry I., Dawson C., et al. Tumour necrosis factor-alpha in Barrett's oesophagus: a potential novel mechanism of action. Oncogene 2002, 21:6071-6081.
74. Kavanagh M.E., O'Sullivan K.E., O'Hanlon C., et al. The esophagitis to adenocarcinoma sequence; the role of inflammation. Cancer Lett 2014, 345:182-189.
75. Singh S., Devanna S., Edakkanambeth Varayil J., et al. Physical activity is associated with reduced risk of esophageal cancer, particularly esophageal adenocarcinoma: a systematic review and meta-analysis. BMC Gastroenterol 2014, 14:101.
76. Hilal J., Kramer J.R., Richardson P., et al. Physical activity and the risk of Barrett's esophagus. Gastroenterol 2014, 146:S-307-S-308.
77. Csendes A., Burgos A.M., Smok G., et al. Effect of gastric bypass on Barrett's esophagus and intestinal metaplasia of the cardia in patients with morbid obesity. JGastrointest Surg 2006, 10:259-264.
78. Nagi D.K., Yudkin J.S. Effects of metformin on insulin resistance, risk factors for cardiovascular disease, and plasminogen activator inhibitor in NIDDM subjects. A study of two ethnic groups. Diabetes Care 1993, 16:621-629.
79. Chak A., Buttar N.S., Foster N.R., Cancer Prevention Network, et al. Metformin does not reduce markers of cell proliferation in esophageal tissues of patients with Barrett's esophagus. Clin Gastroenterol Hepatol 2015, 13(4):665-672.
80. Oh da Y., Walenta E., Akiyama T.E., et al. AGpr120-selective agonist improves insulin resistance and chronic inflammation in obese mice. Nat Med 2014, 20:942-947.
81. Cockbain A.J., Toogood G.J., Hull M.A. Omega-3 polyunsaturated fatty acids for the treatment and prevention of colorectal cancer. Gut 2012, 61:135-149.
82. Kalupahana N.S., Claycombe K., Newman S.J., et al. Eicosapentaenoic acid prevents and reverses insulin resistance in high-fat diet-induced obese mice via modulation of adipose tissue inflammation. JNutr 2010, 140:1915-1922.
83. Mehta S.P., Boddy A.P., Cook J., et al. Effect of n-3 polyunsaturated fatty acids on Barrett's epithelium in the human lower esophagus. Am J Clin Nutr 2008, 87:949-956.
84. Siriwardhana N., Kalupahana N.S., Cekanova M., et al. Modulation of adipose tissue inflammation by bioactive food compounds. JNutr Biochem 2013, 24:613-623.