В настоящей статье освещены вопросы этиологии и патогенеза гастроэзофагеальной рефлюксной болезни, развивающейся у пациентов, страдающих сахарным диабетом 2-го типа. Гипергликемия приводит к опосредованному развитию нейропатии, что является базисом для возникновения дисмоторики пищевода, провоцируя появление гастроэзофагеального рефлюкса. В большинстве случаев у пациентов с сахарным диабетом отмечаются повышенный индекс массы тела и ожирение. Основными механизмами, индуцирующими возникновение патологических рефлюксов, у лиц с избыточной массой тела и ожирением являются высокое внутрибрюшное давление, низкое давление в области нижнего пищеводного сфинктера, повышенная частота спонтанных релаксаций нижнего пищеводного сфинктера. Помимо этого, у больных с ожирением уровень грелина снижен, что тормозит сократительную активность желудка и усиливает риск развития патологических рефлюксов.
This article covers a very important material about etiology and pathology of the gastroesophageal reflux disease with which most commonly suffer people with the diabetes mellitus type 2. It is well known fact that, on the one hand, hyperglycemia leads to the diabetic neuropathy. Neuropathy is the most common reason for motor disorders of the digestive system. On the other hand, patients who suffer from diabetes mellitus type 2 have an increased body mass index and obesity, which are associated with the increased abdominal pressure, the decreased lower esophageal sphincter pressure and increase of transient relaxation of the lower esophageal sphincter and lead to the pathophysiological reflux. In addition, such a decreased level of grelin in patients with obesity also leads to the pathophysiological reflux.
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3. El-Serag HB, Sweet S, Winchester CC, Dent J. Update on the epidemiology of gastro-esophageal reflux disease: a systematic review. Gut 2013; 5.
4. Bonatti H, Achem SR, Hinder RA. Impact of changing epidemiology of gastroesophageal reflux disease on its diagnosis and treatment. J Gastrointestinal Surg 2008; 12 (2): 373–81.
5. Bor S, Lazebnik LB, Kitapcioglu G et al. Prevalence of gastroesophageal reflux disease in Moscow. Dis Esophagus 2016; 29 (2): 159–65.
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8. Sun XM, Tan JC, Zhu Y, Lin L. Association between diabetes mellitus and gastroesophageal reflux disease: A meta-analysis. World J Gastroenterol 2015; 21 (10): 3085–92.
9. Iyer PG, Borah BJ, Heien HC et al. Association o fBarrett's esophagus with type II Diabetes Mellitus: results from a large population-based case-control study. Clin Gastroenterol Hepatol 2013; 11 (9): 1108-14e5.
10. Schwab A, Siddiqui A et al. Polyol pathway links glucose metabolism to the aggressivness of cancer cells. Cancer Res 2018.
11. Paawan Punjabi, Angela Hira Do , Shanti Prasad et al. Review of gastroesophageal reflux disease (GERD) in the diabetic patient. J Diabetes 2015; 7 (5): 599–609.
12. Wang X, Pitchumoni CS, Chandrarana K, Shah N. Increased prevalence of symptoms of gastroesophageal reflux diseases in type 2 diabetics with neuropathy. World J Gastroenterol 2008; 14 (5): 709–12.
13. Kinekawa F, Kubo F, Matsuda K et al. Esophageal function worsens with long duration of diabetes. J Gastroenterol 2008; 43 (5): 338–44.
14. Jorge JX, Panão EA, Simões MA et al. Esophageal body motility in people with diabetes: comparison with non-diabetic healthy individuals. Diabet Res Clin Pract 2012; 97 (1): 77–81.
15. Ahmed W, Vohra EA. Esophageal motility disorders in diabetics. J Pak Med Assoc 2004; 54 (12): 597–601.
16. Kinekawa F, Kubo F, Matsuda K et al. Relationship between esophageal dysfunction and neuropathy in diabetic patients. Am J Gastroenterol 2001; 96 (7): 2026-32.
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18. Sellin JH, Chang EB. Therapy Insight: gastrointestinal complications of diabetes-pathophysiology and management. Nature clinical practice. Gastroenterol Hepatol 2008; 5 (3): 162–71.
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20. 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.
21. Peeters A, Barendregt JJ, Willekens F et al. Obesity in adulthood and its consequences for life expectancy: a life-table analysis. Ann Internal Med 2003; 138 (1): 24–32.
22. Singh S, Sharma AN, Murad MH 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.
23. El-Serag HB, Graham DY, Satia JA et al. Obesity is an independent risk factor for GERD symptoms and erosive esophagitis. Am J Gastroenterol 2005; 100 (6): 1243–50.
24. 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): 872–8.
25. Hajar N, Castell DO, Ghomrawi H et al. Impedance pH confirms the relationship between GERD and BMI. Dig Dis Sci 2012; 57: 1875–9.
26. Nadaleto BF, Herbella FA, Patti MG. Gastroesophageal reflux disease in the obese: Pathophysiology and treatment. Surgery 2016; 159 (2): 475–86.
27. Alberti K, Zimmet P, Shaw J. Metabolic syndrome – a new world‐wide definition. A Consensus Statement from the International Diabetes Federation. Diabetic Med 2006; 23 (5): 469–80.
28. Niigaki M, Adachi K, Hirakawa K et al. Association between metabolic syndrome and prevalence of gastroesophageal reflux disease in a health screening facility in Japan. J Gastroenterol 2012: 1–10.
29. Chung SJ, Kim D, Park MJ et al. Metabolic syndrome and visceral obesity as risk factors for reflux oesophagitis: a cross-sectional case-control study of 7078 Koreans undergoing health check-ups. Gut 2008; 57 (10): 1360–5.
30. Moki F, Kusano M, Mizuide M et al. Association between reflux oesophagitis and features of the metabolic syndrome in Japan. Aliment Pharmacol Ther 2007; 26 (7): 1069–75.
31. Hirata A, Kishida K, Nakatsuji H et al. High prevalence of gastroesophageal reflux symptoms in type 2 diabetics with hypoadiponectinemia and metabolic syndrome. Nutr Metab 2012; 9 (1): 4.
32. Cummings DE, Purnell JQ, Frayo RS et al. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 2001; 50 (8): 1714–9.
33. Kawahara H, Kubota A, Hasegawa T et al. Effects of rikkunshito on the clinical symptoms and esophageal acid exposure in children with symptomatic gastroesophageal reflux. Pediatr Surg Int 2007; 23 (10): 1001–5.
34. Rubenstein JH, Morgenstern H, McConell D et al. Associations of Diabetes Mellitus, Insulin, Leptin, and Ghrelin With Gastroesophageal Reflux and Barrett's Esophagus. Gastroenterology 2013; 145 (6): 1237–44.e5.
35. Ohno T, Mochiki E, Kuwano H. The roles of motilin and ghrelin in gastrointestinal motility. Int J Pept 2010.
36. Perdikis G, Wilson P, Hinder RA et al. Gastroesophageal reflux disease is associated with enteric hormone abnormalities. Am J Surg 1994; 167 (1): 186–91; discussion 91-2.
37. Schmid R, Schusdziarra V, Allescher HD et al. Effect of motilin on gastric emptying in patients with diabetic gastroparesis. Diabetes Care 1991; 14 (1): 65–8.
38. McCallum RW, Cynshi O, TEAM UI. Efficacy of mitemcinal, a motilin agonist, on gastrointestinal symptoms in patients with symptoms suggesting diabetic gastropathy: a randomized, multi-center, placebo-controlled trial. Aliment Pharmacol Ther 2007; 26 (1): 107–16.
39. Okano H, Inui A, Ueno N et al. EM523L, a nonpeptide motilin agonist, stimulates gastric emptying and pancreatic polypeptide secretion. Peptides 1996; 17 (6): 895–900.
40. Nakanome C, Akai H, Hongo M et al. Disturbances of the alimentary tract motility and hypermotilinemia in the patients with diabetes mellitus. Tohoku J Exp Med 1983; 139 (2): 205–15.
41. Pendleton H, Ekman R, Olsson R et al. Motilin concentrations in relation to gastro intestinal dysmotility in diabetes mellitus. Eur J Intern Med 2009; 20 (6): 654–9.
42. Nies AT, Hofmann U, Resch C et al. Proton pump inhibitors inhibit metformin uptake by organic cation transporters (OCTs). PloS one 2011; 6 (7): e22163.
43. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest 2007; 117 (1): 13–23.
44. Dent J. Editorial: Better ammunition for use of weight loss in managing gastroesophageal reflux disease. Am J Gastroenterol 2013; 108 (3): 383–5.
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48. Crouch MA, Mefford IN, Wade EU. Proton pump inhibitor therapy associated with lower glycosylated hemoglobin levels in type 2 diabetes. J Am Board Family Med 2012; 25 (1): 50–4.
49. Mefford IN, Wade E.U. Proton pump inhibitors as a treatment method for type II diabetes. Medical Hypotheses 2009; 73 (1): 29–32.
50. Bodvarsdottir TB, Hove KD, Gotfredsen CF et al. Treatment with a proton pump inhibitor improves glycaemic control in Psam-momys obesus, a model of type 2 diabetes. Diabetologia 2010; 53 (10): 2220–3.
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[Maev I.V., Barkalova E.V., Ovsepian M.A. et al. Vozmozhnosti rn-impedansometrii i manometrii vysokogo razresheniia pri vedenii patsientov s refrakternoi gastroezofageal'noi refliuksnoi bolezn'iu. Therapeutic Archive. 2017; 89 (2): 76–83. (in Russian).]
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[Maev I.V., Barkalova E.V., Ovsepyan M.A. et al. Modern gastroenterology advances in esophageal tonus and motility disorders assessment. Consilium Medicum. 2018; 20 (8): 8–13. DOI: 10.26442/2075-1753_2018.8.8-13 (in Russian).]
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[Maev I.V., Dicheva D.T., Andreev D.N. et al. Terapevticheskaia rol' prokineticheskikh preparatov v lechenii gastroezofageal'noi refliuksnoi bolezni. Med. sovet. 2014; 4: 66–70 (in Russian).]
54. Holtmann G, Talley NJ, Liebregts T et al. A placebo-controlled trial of itopride in functional dyspepsia. N Engl J Med 2006; 354 (8): 832–40.
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[Dedov I.I. Endocrinology. National leadership. Moscow: GEOTAR-Media, 2016 (in Russian).]
________________________________________________
1. Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabet Res Clin Pract 2011; 94 (3): 311–21.
2. Maev I.V., Busarova G.A., Andreev D.N. Esophagus. Moscow: GEOTAR-Media, 2019 (in Russian).
3. El-Serag HB, Sweet S, Winchester CC, Dent J. Update on the epidemiology of gastro-esophageal reflux disease: a systematic review. Gut 2013; 5.
4. Bonatti H, Achem SR, Hinder RA. Impact of changing epidemiology of gastroesophageal reflux disease on its diagnosis and treatment. J Gastrointestinal Surg 2008; 12 (2): 373–81.
5. Bor S, Lazebnik LB, Kitapcioglu G et al. Prevalence of gastroesophageal reflux disease in Moscow. Dis Esophagus 2016; 29 (2): 159–65.
6. Maev I.V., Iurenev G.L., V'iuchnova E.S. et al. Gastroesophageal Reflux Disease. Moscow: GEOTAR-Media, 2019 (in Russian).
7. Nishida T, Tsuji S, Tsujii M et al. Gastroesophageal reflux disease related to diabetes: analysis of 241 cases with type 2 diabetes mellitus. J Gastroenterol Hepatol 2004; 19 (3): 258–65.
8. Sun XM, Tan JC, Zhu Y, Lin L. Association between diabetes mellitus and gastroesophageal reflux disease: A meta-analysis. World J Gastroenterol 2015; 21 (10): 3085–92.
9. Iyer PG, Borah BJ, Heien HC et al. Association o fBarrett's esophagus with type II Diabetes Mellitus: results from a large population-based case-control study. Clin Gastroenterol Hepatol 2013; 11 (9): 1108-14e5.
10. Schwab A, Siddiqui A et al. Polyol pathway links glucose metabolism to the aggressivness of cancer cells. Cancer Res 2018.
11. Paawan Punjabi, Angela Hira Do , Shanti Prasad et al. Review of gastroesophageal reflux disease (GERD) in the diabetic patient. J Diabetes 2015; 7 (5): 599–609.
12. Wang X, Pitchumoni CS, Chandrarana K, Shah N. Increased prevalence of symptoms of gastroesophageal reflux diseases in type 2 diabetics with neuropathy. World J Gastroenterol 2008; 14 (5): 709–12.
13. Kinekawa F, Kubo F, Matsuda K et al. Esophageal function worsens with long duration of diabetes. J Gastroenterol 2008; 43 (5): 338–44.
14. Jorge JX, Panão EA, Simões MA et al. Esophageal body motility in people with diabetes: comparison with non-diabetic healthy individuals. Diabet Res Clin Pract 2012; 97 (1): 77–81.
15. Ahmed W, Vohra EA. Esophageal motility disorders in diabetics. J Pak Med Assoc 2004; 54 (12): 597–601.
16. Kinekawa F, Kubo F, Matsuda K et al. Relationship between esophageal dysfunction and neuropathy in diabetic patients. Am J Gastroenterol 2001; 96 (7): 2026-32.
17. Fass R, McCallum RW, Parkman HP. Treatment Challenges in the Management of Gastroparesis-Related GERD. Gastroenterol Hepatol 2009; 5 (10; Suppl. 18): 4–16.
18. Sellin JH, Chang EB. Therapy Insight: gastrointestinal complications of diabetes-pathophysiology and management. Nature clinical practice. Gastroenterol Hepatol 2008; 5 (3): 162–71.
19. Promberger R, Spitzer A, Ott J et al. Quality of life in type 2 diabetics with gastroesophageal reflux disease: a case control study. Eur Surg 2013: 1–6.
20. 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.
21. Peeters A, Barendregt JJ, Willekens F et al. Obesity in adulthood and its consequences for life expectancy: a life-table analysis. Ann Internal Med 2003; 138 (1): 24–32.
22. Singh S, Sharma AN, Murad MH 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.
23. El-Serag HB, Graham DY, Satia JA et al. Obesity is an independent risk factor for GERD symptoms and erosive esophagitis. Am J Gastroenterol 2005; 100 (6): 1243–50.
24. 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): 872–8.
25. Hajar N, Castell DO, Ghomrawi H et al. Impedance pH confirms the relationship between GERD and BMI. Dig Dis Sci 2012; 57: 1875–9.
26. Nadaleto BF, Herbella FA, Patti MG. Gastroesophageal reflux disease in the obese: Pathophysiology and treatment. Surgery 2016; 159 (2): 475–86.
27. Alberti K, Zimmet P, Shaw J. Metabolic syndrome – a new world‐wide definition. A Consensus Statement from the International Diabetes Federation. Diabetic Med 2006; 23 (5): 469–80.
28. Niigaki M, Adachi K, Hirakawa K et al. Association between metabolic syndrome and prevalence of gastroesophageal reflux disease in a health screening facility in Japan. J Gastroenterol 2012: 1–10.
29. Chung SJ, Kim D, Park MJ et al. Metabolic syndrome and visceral obesity as risk factors for reflux oesophagitis: a cross-sectional case-control study of 7078 Koreans undergoing health check-ups. Gut 2008; 57 (10): 1360–5.
30. Moki F, Kusano M, Mizuide M et al. Association between reflux oesophagitis and features of the metabolic syndrome in Japan. Aliment Pharmacol Ther 2007; 26 (7): 1069–75.
31. Hirata A, Kishida K, Nakatsuji H et al. High prevalence of gastroesophageal reflux symptoms in type 2 diabetics with hypoadiponectinemia and metabolic syndrome. Nutr Metab 2012; 9 (1): 4.
32. Cummings DE, Purnell JQ, Frayo RS et al. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 2001; 50 (8): 1714–9.
33. Kawahara H, Kubota A, Hasegawa T et al. Effects of rikkunshito on the clinical symptoms and esophageal acid exposure in children with symptomatic gastroesophageal reflux. Pediatr Surg Int 2007; 23 (10): 1001–5.
34. Rubenstein JH, Morgenstern H, McConell D et al. Associations of Diabetes Mellitus, Insulin, Leptin, and Ghrelin With Gastroesophageal Reflux and Barrett's Esophagus. Gastroenterology 2013; 145 (6): 1237–44.e5.
35. Ohno T, Mochiki E, Kuwano H. The roles of motilin and ghrelin in gastrointestinal motility. Int J Pept 2010.
36. Perdikis G, Wilson P, Hinder RA et al. Gastroesophageal reflux disease is associated with enteric hormone abnormalities. Am J Surg 1994; 167 (1): 186–91; discussion 91-2.
37. Schmid R, Schusdziarra V, Allescher HD et al. Effect of motilin on gastric emptying in patients with diabetic gastroparesis. Diabetes Care 1991; 14 (1): 65–8.
38. McCallum RW, Cynshi O, TEAM UI. Efficacy of mitemcinal, a motilin agonist, on gastrointestinal symptoms in patients with symptoms suggesting diabetic gastropathy: a randomized, multi-center, placebo-controlled trial. Aliment Pharmacol Ther 2007; 26 (1): 107–16.
39. Okano H, Inui A, Ueno N et al. EM523L, a nonpeptide motilin agonist, stimulates gastric emptying and pancreatic polypeptide secretion. Peptides 1996; 17 (6): 895–900.
40. Nakanome C, Akai H, Hongo M et al. Disturbances of the alimentary tract motility and hypermotilinemia in the patients with diabetes mellitus. Tohoku J Exp Med 1983; 139 (2): 205–15.
41. Pendleton H, Ekman R, Olsson R et al. Motilin concentrations in relation to gastro intestinal dysmotility in diabetes mellitus. Eur J Intern Med 2009; 20 (6): 654–9.
42. Nies AT, Hofmann U, Resch C et al. Proton pump inhibitors inhibit metformin uptake by organic cation transporters (OCTs). PloS one 2011; 6 (7): e22163.
43. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest 2007; 117 (1): 13–23.
44. Dent J. Editorial: Better ammunition for use of weight loss in managing gastroesophageal reflux disease. Am J Gastroenterol 2013; 108 (3): 383–5.
45. Maev I.V., Kucheriavyi Iu.A., Andreev D.N. Obesity and comorbidity: a guide for doctors. Moscow: Prima Print, 2016 (In Russian).
46. Iurenev G.L., Mironova E.M., Andreev D.N., Iureneva-Tkhorzhevskaia T.V. Klinicheskie i patogeneticheskie paralleli gastroezofageal'noi refliuksnoi bolezni i ozhireniia. Farmateka. 2017; 13: 30–9 (In Russian).
47. Ivashkin V.T., Maev I.V., Trukhmanov A.S. i dr. Klinicheskie rekomendatsii Rossiiskoi gastroenterologicheskoi assotsiatsii po diagnostike i lecheniiu gastroezofageal'noi refliuksnoi bolezni. RZhGGK. 2017; 27 (4): 75–95 (In Russian).
48. Crouch MA, Mefford IN, Wade EU. Proton pump inhibitor therapy associated with lower glycosylated hemoglobin levels in type 2 diabetes. J Am Board Family Med 2012; 25 (1): 50–4.
49. Mefford IN, Wade E.U. Proton pump inhibitors as a treatment method for type II diabetes. Medical Hypotheses 2009; 73 (1): 29–32.
50. Bodvarsdottir TB, Hove KD, Gotfredsen CF et al. Treatment with a proton pump inhibitor improves glycaemic control in Psam-momys obesus, a model of type 2 diabetes. Diabetologia 2010; 53 (10): 2220–3.
51. Maev I.V., Barkalova E.V., Ovsepian M.A. et al. Vozmozhnosti rn-impedansometrii i manometrii vysokogo razresheniia pri vedenii patsientov s refrakternoi gastroezofageal'noi refliuksnoi bolezn'iu. Therapeutic Archive. 2017; 89 (2): 76–83. (in Russian).
52. Maev I.V., Barkalova E.V., Ovsepyan M.A. et al. Modern gastroenterology advances in esophageal tonus and motility disorders assessment. Consilium Medicum. 2018; 20 (8): 8–13. DOI: 10.26442/2075-1753_2018.8.8-13 (in Russian).
53. Maev I.V., Dicheva D.T., Andreev D.N. et al. Terapevticheskaia rol' prokineticheskikh preparatov v lechenii gastroezofageal'noi refliuksnoi bolezni. Med. sovet. 2014; 4: 66–70 (in Russian).
54. Holtmann G, Talley NJ, Liebregts T et al. A placebo-controlled trial of itopride in functional dyspepsia. N Engl J Med 2006; 354 (8): 832–40.
55. Dedov I.I. Endocrinology. National leadership. Moscow: GEOTAR-Media, 2016 (in Russian).
1 ФГБОУ ВО «Московский государственный медико-стоматологический университет им. А.И. Евдокимова» Минздрава России, Москва, Россия;
2 ФКУЗ «Главный клинический госпиталь Министерства внутренних дел Российской Федерации», Москва, Россия
*dna-mit8@mail.ru
________________________________________________
Elena I. Kuznetsova1, Ekaterina A. Rymareva2, Diana T. Dicheva1, Dmitrii N. Andreev*1
1 Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia;
2 Main Clinical Hospital of Ministry of Internal Affairs of the Russian Federation, Moscow, Russia
*dna-mit8@mail.ru