Gastro-oesophageal reflux disease in type 2 diabetics: symptom load and pathophysiologic aspects - a retro-pro study

BMC Gastroenterology

Christoph Neumayer²  Michael Gadenstätter⁵  Franz Martin Riegler¹  Johannes Ott³  Wolf Hans Eilenberg¹  Gernot Seebacher⁵  Otto Riedl⁴  Johannes Lenglinger¹  Regina Promberger¹ 

[1] Division of General Surgery, Department of Surgery, Medical University of Vienna, Vienna, Austria;Division of Vascular Surgery, Department of Surgery, Medical University of Vienna, Vienna, Austria;Department of Gynecology and Obstetrics, Medical University of Vienna, Vienna, Austria;Division of Plastic and Reconstructive Surgery, Department of Surgery, Medical University of Vienna, Vienna, Austria;Karl Landsteiner Institute for Clinical Surgery, General Hospital of Krems, Krems, Austria

关键词: Hiatal hernia;    Heartburn;    Dysphagia;    GERD;    Diabetes;   

Others  :  857657
DOI  :  10.1186/1471-230X-13-132

 received in 2013-03-21, accepted in 2013-08-14,  发布年份 2013

【 摘 要 】

Background

Information about gastro-oesophageal reflux disease (GERD) in patients with Diabetes mellitus type 2 (T2D) is scarce, although the incidence of both disorders is increasing.

We aimed to determine GERD symptoms and their underlying pathophysiologic characteristics in T2D patients.

Methods

This “retro-pro” study compared 65 T2D patients to a control group of 130 age- and sex-matched non-diabetics. GERD was confirmed by gastroscopy, manometry, pH-metry and barium swallow.

Results

In patients with T2D compared to controls, dysphagia (32.3% vs. 13.1%; p = 0.001) and globus sensation (27.7% vs. 13.8%; p = 0.021) were found more frequently, whereas heartburn (76.9% vs. 88.5%; p = 0.046) and regurgitation (47.7% vs. 72.3%; p = 0.001) were predominant in non-diabetics. Despite higher body mass indices (31.1 ± 5.2 vs. 27.7 ± 3.7 kg/m²; p < 0.001), hiatal hernia was less frequent in T2D patients compared to controls (60.0% vs. 90.8%, p < 0.001). Lower oesophageal sphincter (LES) pressure was higher in patients with T2D (median 10.0 vs. 7.2 mmHg, p = 0.016). DeMeester scores did not differ between the groups. Helicobacter pylori infections were more common in T2D patients (26.2% vs. 7.7%, p = 0.001). Barrett metaplasia (21.5% vs. 17.7%), as well as low- (10.8% vs. 3.8%) and high-grade dysplasia (1.5% vs. 0%) were predominant in T2D patients.

Conclusions

T2D patients exhibit different GERD symptoms, higher LES pressures and a decreased prevalence of hiatal hernia than non-diabetics, which may be related to worse oesophageal motility and, thus, a more functional rather than anatomical cause of GERD. Low-grade dysplasia was more than twice as high in T2D than in non-diabetics patients.

Trial registration

Ethics committee of the Medical University of Vienna, IRB number 720/2011.

【 授权许可】

   
2013 Promberger et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Moayyedi P, Talley NJ: Gastro-oesophageal reflux disease. Lancet 2006, 367:2086-2100.
• [2]Shaw JE, Sicree RA, Zimmet PZ: Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010, 87:4-14.
• [3]Nishida T, Tsuji S, Tsujii M, Arimitsu S, Sato T, Haruna Y, Miyamoto T, Kanda T, Kawano S, Hori M: Gastroesophageal reflux disease related to diabetes: analysis of 241 cases with type 2 diabetes mellitus. J Gastroenterol Hepatol 2004, 19:258-265.
• [4]Wang X, Pitchumoni CS, Chandrarana K, Shah N: Increased prevalence of symptoms of gastrooesophageal reflux diseases in type 2 diabetics with neuropathy. World J Gastroenterol 2008, 14:709-712.
• [5]Ariizumi K, Koike T, Ohara S, Inomata Y, Abe Y, Iijima K, Imatani A, Oka T, Shimosegawa T: Incidence of reflux esophagitis and H pylori infection in diabetic patients. World J Gastroenterol 2008, 14:3212-3217.
• [6]Horikawa A, Ishii-Nozawa R, Ohguro M, Takagi S, Ohtuji M, Yamada M, Kuzuya N, Ujihara N, Ujihara M, Takeuchi K: Prevalence of GORD (gastro-ooesophageal reflux disease) in type 2 diabetes and a comparison of clinical profiles between diabetic patients with and without GORD. Diabet Med 2009, 26:228-233.
• [7]Niigaki M, Adachi K, Hirakawa K, Furuta K, Kinoshita Y: Association between metabolic syndrome and prevalence of gastrooesophageal reflux disease in a health screening facility in Japan. J Gastroenterol 2012. Sep 14. [Epub ahead of print]
• [8]Promberger R, Gadenstätter M, Ciovica R, Schwab G, Neumayer C: Gastrooesophageal reflux disease in diabetic patients: a systematic review. Eur Surg 2007, 39:340-354.
• [9]Kase H, Hattori Y, Sato N, Banba N, Kasai K: Symptoms of gastrooesophageal reflux in diabetes patients. Diabetes Res Clin Pract 2008, 79:6-7.
• [10]Holub JL, Silberg DG, Michaels LC, Williams JL, Morris CD, Eisen G: Acid-related upper endoscopy findings in patients with diabetes versus non-diabetic patients. Dig Dis Sci 2010, 55:2853-2859.
• [11]Hall JC, Hall JL: Emergence of ‘retropro’ studies in the surgical literature. ANZ J Surg 2008, 78:411-413.
• [12]American Diabetes Association: Standards of medical care in diabetes–2006. Diabetes Care 2006, 29:S4-S42.
• [13]Ollyo JB, Fontolliet C, Lang BF: La nouvelle classification de savary des oesophagites de reflux. Acta Endosc 1992, 22:307-320.
• [14]Riddell RH: The biopsy diagnosis of gastrooesophageal reflux disease, “carditis,” and Barrett’s esophagus, and sequelae of therapy. Am J Surg Pathol 1996, 20:S31-S50.
• [15]Zaninotto G, DeMeester TR, Schwizer W, Johansson KE, Cheng SC: The lower oesophageal sphincter in health and disease. Am J Surg 1988, 155:104-111.
• [16]Kaul BK, DeMeester TR, Oka M, Ball CS, Stein HJ, Kim CB, Cheng SC: The cause of dysphagia in uncomplicated sliding hiatal hernia and its relief by hiatal herniorrhaphy. A roentgenographic, manometric, and clinical study. Ann Surg 1990, 211:406-410.
• [17]Richter JE, Wu WC, Johns DN, Blackwell JN, Nelson JL 3rd, Castell JA, Castell DO: Oesophageal manometry in 95 healthy adult volunteers. Variability of pressures with age and frequency of “abnormal” contractions. Dig Dis Sci 1987, 32:583-592.
• [18]DeMeester TR, Wang CI, Wernly JA, Pellegrini CA, Little AG, Klementschitsch P, Bermudez G, Johnson LF, Skinner DB: Technique, indications, and clinical use of 24 hour oesophageal pH monitoring. J Thorac Cardiovasc Surg 1980, 79:656-670.
• [19]Hsu CS, Wang PC, Chen JH, Su WC, Tseng TC, Chen HD, Hsiao TH, Wang CC, Lin HH, Shyu RY, Chao YC: Increasing insulin resistance is associated with increased severity and prevalence of gastro-oesophageal reflux disease. Aliment Pharmacol Ther 2011, 34:994-1004.
• [20]Ahuja V, Yencha MW, Lassen LF: Head and neck manifestations of gastrooesophageal reflux disease. Am Fam Physician 1999, 60:873-886.
• [21]Said A, Brust DJ, Gaumnitz EA, Reichelderfer M: Predictors of early recurrence of benign oesophageal strictures. Am J Gastroenterol 2003, 98:1252-1256.
• [22]GadEl-Hak NA, Mostafa M, AbdelHamid Hussein Haleem M: Hypertensive lower oesophageal sphincter (HLES): prevalence, symptoms genesis and effect of pneumatic balloon dilatation. Saudi Gastroenterol 2006, 12:77-82.
• [23]Bonatti H, Achem SR, Hinder RA: Impact of changing epidemiology of gastrooesophageal reflux disease on its diagnosis and treatment. J Gastrointest Surg 2008, 12:373-381.
• [24]Rosanowski F, Eysholdt U: ENT manifestations of gastrooesophageal reflux. Internist (Berl) 2003, 44:63-67.
• [25]Hill J, Stuart RC, Fung HK, Ng EK, Cheung FM, Chung CS, van Hasselt CA: Gastrooesophageal reflux, motility disorders, and psychological profiles in the etiology of globus pharyngis. Laryngoscope 1997, 107:1373.
• [26]Martín-Merino E, Ruigómez A, García Rodríguez LA, Wallander MA, Johansson S: Depression and treatment with antidepressants are associated with the development of gastro-ooesophageal reflux disease. Aliment Pharmacol Ther 2010, 31:1132-1140.
• [27]Rakshit R, de Caestecker J: Globus: are we any nearer to understanding it? Am J Gastroenterol 2009, 104:299-301.
• [28]Kwiatek MA, Mirza F, Kahrilas PJ, Pandolfino JE: Hyperdynamic upper oesophageal sphincter pressure: a manometric observation in patients reporting globus sensation. Am J Gastroenterol 2009, 104:289-298.
• [29]Wang KK, Sampliner RE: Practice parameters committee of the American college of gastroenterology. Updated guidelines 2008 for the diagnosis, surveillance and therapy of Barrett’s esophagus. Am J Gastroenterol 2008, 103:788-797.
• [30]Hüppe D, Tegenthoff M, Faig J, Brunke F, Depka S, Stuhldreier M, Micklefield G, Gillissen A, May B: Oesophageal dysfunction in diabetes mellitus: is there a relation to clinical manifestation of neuropathy? Clin Investig 1992, 70:740-747.
• [31]Petersen H, Johannessen T, Sandvik AK, Kleveland PM, Brenna E, Waldum H, Dybdahl JD: Relationship between endoscopic hiatus hernia and gastroesophageal reflux symptoms. Scand J Gastroenterol 1991, 26:921-926.
• [32]Xia HH, Talley NJ, Kam EP, Young LJ, Hammer J, Horowitz M: Helicobacter pylori infection is not associated with diabetes mellitus, nor with upper gastrointestinal symptoms in diabetes mellitus. Am J Gastroenterol 2001, 96:1039-1046.
• [33]Labenz J: Facts and fantasies in extra-ooesophageal symptoms in GORD. Best Pract Res Clin Gastroenterol 2010, 24:893-904.
• [34]Chang AB, Lasserson TJ, Gaffney J, Connor FL, Garske LA: Gastro-ooesophageal reflux treatment for prolonged non-specific cough in children and adults. Cochrane Database Syst Rev 2011., 1CD004823
• [35]Ciovica R, Gadenstätter M, Klingler A, Neumayer C, Schwab GP: Laparoscopic antireflux surgery provides excellent results and quality of life in gastrooesophageal reflux disease patients with respiratory symptoms. J Gastrointest Surg 2005, 9:633-637.
• [36]Giovannucci E, Harlan DM, Archer MC, Bergenstal RM, Gapstur SM, Habel LA, Pollak M, Regensteiner JG, Yee D: Diabetes and cancer: a consensus report. Diabetes Care 2010, 33:1674-1685.
• [37]Li Q, Zhang J, Zhou Y, Qiao L: Obesity and gastric cancer. Front Biosci 2012, 17:2383-2390.
• [38]Tian T, Zhang LQ, Ma XH, Zhou JN, Shen J: Diabetes mellitus and incidence and mortality of gastric cancer: a meta-analysis. Exp Clin Endocrinol Diabetes 2012, 120:217-223.
• [39]Nozu T, Komiyama H: Clinical characteristics of asymptomatic esophagitis. J Gastroenterol 2008, 43:27-31.
• [40]Promberger R, Spitzer A, Ott J, Lenglinger J, Eilenberg W, Gadenstätter M, Neumayer C: Quality of life in type 2 diabetics with gastroesophageal reflux disease: a case control study. Eur Surg 2013, 45:194-199.
• [41]Clouse RE, Lustman PF: Gastrointestinal symptoms in diabetic patients: lack of associationwith neuropathy. Am J Gastroenterol 1989, 84:868-872.
• [42]Lee SD, Keum B, Chun HJ, Bak YT: Gastrooesophageal reflux disease in type II diabetes mellitus with or without peripheral neuropathy. J Neurogastroenterol Motil 2011, 17:274-278.
• [43]Sellin JH, Chang EB: Therapy insight: gastrointestinal complications of diabetes–pathophysiology and management. Nat Clin Pract Gastroenterol Hepatol 2008, 5:162-171.
• [44]Neumayer C, Ciovica R, Gadenstätter M, Erd G, Leidl S, Lehr S, Schwab G: Significant weight loss after laparoscopic Nissen fundoplication. Surg Endosc 2005, 19:15-20.
• [45]Friedenberg FK, Xanthopoulos M, Foster GD, Richter JE: The association between gastrooesophageal reflux disease and obesity. Am J Gastroenterol 2008, 103:2111-2122.
• [46]Lauffer A, Forcelini CM, Ruas LO, Madalosso CA, Fornari F: Gastrooesophageal reflux disease is inversely related with glycemic control in morbidly obese patients. Obes Surg 2011, 21:864-870.
• [47]Stacher G, Lenglinger J, Bergmann H, Schneider C, Brannath W, Festa A, Meghdadi S, Stacher-Janotta G: Impaired gastric emptying and altered intragastric meal distribution in diabetes mellitus related to autonomic neuropathy? Dig Dis Sci 2003, 48:1027-1034.
• [48]Scheffer RC, Bredenoord AJ, Hebbard GS, Smout AJ, Samsom M: Effect of proximal gastric volume on hiatal hernia. Neurogastroenterol Motil 2010, 22:552-556.
• [49]Choi CW, Kim GH, Song CS, Wang SG, Lee BJ IH, Kang DH, Song GA: Is obesity associated with gastropharyngeal reflux disease? World J Gastroenterol 2008, 14:265-271.
• [50]Nelsen EM, Kirihara Y, Takahashi N, Shi Q, Lewis JT, Namasivayam V, Buttar NS, Dunagan KT, Prasad GA: 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.
• [51]Ko GT, Chan FK, Chan WB, Sung JJ, Tsoi CL, To KF, Lai CW, Cockram CS: Helicobacter pylori infection in Chinese subjects with type 2 diabetes. Endocr Res 2001, 27:171-177.
• [52]Quadri R, Rossi C, Catalfamo E, Masoero G, Lombardo L, Della Monica P, Rovera L, Pera A, Cavello Perin P: Helicobacter pylori infection in type 2 diabetic patients. Nutr Metab Cardiovasc Dis 2000, 10:263-266.
• [53]Lluch I, Ascaso JF, Mora F, Minguez M, Peña A, Hernandez A, Benages A: Gastrooesophageal reflux in diabetes mellitus. Am J Gastroenterol 1999, 94:919-924.