Advertisement

Increased risk of concurrent gastroesophageal reflux disease among patients with Sjögren's syndrome: A nationwide population-based study

  • Author Footnotes
    1 Chen-Shu Chang and Chun-Hui Liao contributed equally.
    Chen-Shu Chang
    Footnotes
    1 Chen-Shu Chang and Chun-Hui Liao contributed equally.
    Affiliations
    Department of Neurology, Changhua Christian Hospital, Changhua, Taiwan

    Department of Medical Laboratory Science and Biotechnology, and Medical Imaging and Radiological Sciences, Central Taiwan University of Science and Technology, Taichung, Taiwan
    Search for articles by this author
  • Author Footnotes
    1 Chen-Shu Chang and Chun-Hui Liao contributed equally.
    Chun-Hui Liao
    Footnotes
    1 Chen-Shu Chang and Chun-Hui Liao contributed equally.
    Affiliations
    Department of Psychiatry, China Medical University Hospital, Taichung, Taiwan

    Graduate Institute of Clinical Medicine Science and School of Medicine, College of Medicine, China Medical University, Taichung, Taiwan
    Search for articles by this author
  • Chih-Hsin Muo
    Affiliations
    Management Office for Health Data, China Medical University, Taichung, Taiwan

    School of Medicine, China Medical University, Taichung, Taiwan
    Search for articles by this author
  • Chia-Huang Kao
    Correspondence
    Corresponding author at: No. 2, Yuh-Der Road, Taichung 404, Taiwan. Tel: +886 4 22052121x7412; fax: +886 4 22336174.
    Affiliations
    Graduate Institute of Clinical Medicine Science and School of Medicine, College of Medicine, China Medical University, Taichung, Taiwan

    Department of Nuclear Medicine and PET Center, China Medical University Hospital, Taichung, Taiwan
    Search for articles by this author
  • Author Footnotes
    1 Chen-Shu Chang and Chun-Hui Liao contributed equally.
Published:February 04, 2016DOI:https://doi.org/10.1016/j.ejim.2016.01.014

      Highlights

      • The risk of GERD among SS patients was 2.41-fold greater than that for the general population.
      • The youngest SS patients had the highest risk and the lowest risk at age ≥65 years.
      • SS patients without comorbidity had a 2.87-fold risk higher than comparison cohort.

      Abstract

      Background

      Little data is available on the risk of gastroesophageal reflux disease in patients diagnosed with Sjögren's syndrome.

      Methods

      We identified 4650 Sjögren's syndrome patients between 2000 and 2011 from the National Health Insurance Research Database. Each Sjögren's syndrome patient was matched to 4 controls based on age, sex, and index year, and all subjects were followed up from the index date to December 31, 2011. Cox proportional hazards regression model was used to estimate the risk of gastroesophageal reflux disease.

      Results

      The risk of gastroesophageal reflux disease for Sjögren's syndrome patients was 2.41-fold greater than that for the comparison cohort after adjusting for age, sex, and comorbidities. In age stratified analyses, the youngest Sjögren's syndrome cohort (age: 20–44 years old) had the highest risk (HR = 3.02; 95% CI = 2.48–3.69) and the lowest risk at age ≥65 years (HR = 1.95; 95% CI = 1.61–2.36). Regardless of in subjects with and without comorbidity, Sjögren's syndrome patients had a higher risk than the controls. Sjögren's syndrome subjects with ischemic heart disease, hyperlipidemia and renal disease had the highest risk for gastroesophageal reflux disease compared with the comparison cohort without those diseases (HR = 7.67; 95% CI = 5.32–11.1).

      Conclusion

      Patients with Sjögren's syndrome have a significantly greater risk of developing subsequent gastroesophageal reflux disease than the general population.

      Abbreviations:

      ICD-9-CM (International Classification of Diseases, Ninth Revision, Clinical Modification), HR (hazard ratio), CI (confidence interval), NHIRD (National Health Insurance Research Database), LHID-CIP (longitudinal health insurance database for catastrophic illness patients), NHI (National Health Insurance), LHID (the longitudinal health insurance database), TBNHI (Taiwan Bureau of National Health Insurance), IRB (Institutional Review Board)

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to European Journal of Internal Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      1. Kasper D. Braunwald E. Fauci A. Hauser S. Longo D. Jameson L. Harrison's rheumatology. McGraw-Hill, New York2006
        • von Bultzinglowen I.
        • Sollecito T.
        • Fox P.
        • et al.
        Salivary dysfunction associated with systemic diseases: systematic review and clinical management recommendations.
        Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007; 103: e1-15
        • Kjellén G.
        • Fransson S.G.
        • Lindström F.
        • Sökjer H.
        • Tibbling L.
        Esophageal function, radiography, and dysphagia in Sjögren's syndrome.
        Dig Dis Sci. 1986; 31: 225-229
        • Volter F.
        • Fain O.
        • Mathieu E.
        • Thomas M.
        Esophageal function and Sjögren's syndrome.
        Dig Dis Sci. 2004; 49: 248-253
        • Boyce H.W.
        • Bakheet M.R.
        Sialorrhea: a review of a vexing, often unrecognized sign of oropharyngeal and esophageal disease.
        J Clin Gastroenterol. 2005; 39: 89-97
        • Sarosiek J.
        • McCallum R.W.
        What role do salivary inorganic components play in health and disease of the esophageal mucosa?.
        Digestion. 1995; 56: 24-31
        • Shafik A.
        • El-Sibai O.
        • Shafik A.A.
        • Mostafa R.
        Effect of topical esophageal acidification on salivary secretion: identification of the mechanism of action.
        J Gastroenterol Hepatol. 2005; 20: 1935-1939
        • Park K.
        • Haberberger R.V.
        • Gordon T.P.
        • Jackson M.W.
        Antibodies interfering with the type 3 muscarinic receptor pathway inhibit gastrointestinal motility and cholinergic neurotransmission in Sjögren's syndrome.
        Arthritis Rheum. 2011; 63: 1426-1434
        • De Giorgi F.
        • Palmiero M.
        • Esposito I.
        • Mosca F.
        • Cuomo R.
        Pathophysiology of gastro-oesophageal reflux disease.
        Acta Otorhinolaryngol Ital. 2006; 26: 241-246
        • Vakil N.
        • van Zanten S.V.
        • Kahrilas P.
        • Dent J.
        • Jones R.
        • Global Consensus Group
        The Montreal Definition and Classification of Gastroesophageal Reflux Disease: a global evidence-based consensus.
        Am J Gastroenterol. 2006; 101: 1900-1920
        • Abu-Shakra M.
        • Guillemin F.
        • Lee P.
        Gastrointestinal manifestations of systemic sclerosis.
        Semin Arthritis Rheum. 1994; 24: 29-39
        • Tsai M.C.
        • Lin H.L.
        • Lin C.C.
        • et al.
        Increased risk of concurrent asthma among patients with gastroesophageal reflux disease: a nationwide population-based study.
        Eur J Gastroenterol Hepatol. 2010; 22: 1169-1173
        • Wolfe F.
        • Hawley D.J.
        The comparative risk and predictors of adverse gastrointestinal events in rheumatoid arthritis and osteoarthritis: a prospective 13 year study of 2131 patients.
        J Rheumatol. 2000; 27: 1668-1673
        • Avidan B.
        • Sonnenberg A.
        • Schnell T.G.
        • Budiman-Mak E.
        • Sontag S.J.
        Risk factors of oesophagitis in arthritic patients.
        Eur J Gastroenterol Hepatol. 2001; 13: 1095-1099
        • Singh G.
        • Fries J.F.
        • Williams C.A.
        • Zatarain E.
        • Spitz P.
        • Bloch D.A.
        Toxicity profiles of disease modifying antirheumatic drugs in rheumatoid arthritis.
        J Rheumatol. 1991; 18: 188-194
        • Buchanan W.W.
        • Cox A.G.
        • Harden R.M.
        • Glen A.I.
        • Anderson J.R.
        • Gray K.G.
        Gastric studies in Sjögren's syndrome.
        Gut. 1966; 7: 351-354
        • Cheng T.M.
        Taiwan's new National Health Insurance program: genesis and experience so far.
        Health Aff (Millwood). 2003; 22: 61-76
        • Lu J.F.
        • Hsiao W.C.
        Does universal health insurance make health care unaffordable? Lessons from Taiwan.
        Health Aff (Millwood). 2003; 22: 77-88
        • Dent J.
        • El-Serag H.B.
        • Wallander M.A.
        • Johansson S.
        Epidemiology of gastro-esophageal reflux disease: a systematic review.
        Gut. 2005; 54: 710-717
        • Sharma P.
        • Wani S.
        • Romero Y.
        • Johnson D.
        • Hamilton F.
        Racial and geographic issues in gastroesophageal reflux disease.
        Am J Gastroenterol. 2008; 103: 2669-2680
        • Hung L.J.
        • Hsu P.I.
        • Yang C.Y.
        • Wang E.M.
        • Lai K.H.
        Prevalence of gastroesophageal reflux disease in a general population in Taiwan.
        J Gastroenterol Hepatol. 2011; 26: 1164-1168
        • Fujiwara Y.
        • Arakawa T.
        Epidemiology and clinical characteristics of GERD in the Japanese population.
        J Gastroenterol. 2009; 44: 518-534
        • Moraes-Filho J.P.
        • Navarro-Rodriguez T.
        • Eisig J.N.
        • Barbuti R.C.
        • Chinzon D.
        • Quigley E.M.
        Comorbidities are frequent in patients with gastroesophageal reflux disease in a tertiary health care hospital.
        Clinics (Sao Paulo). 2009; 64: 785-790
        • Cojocaru M.
        • Cojocaru I.M.
        • Silosi I.
        • Vrabie C.D.
        Gastrointestinal manifestations in systemic autoimmune diseases.
        Maedica (Buchar). 2011; 6: 45-51
        • Helmick C.G.
        • Felson D.T.
        • Lawrence R.C.
        • et al.
        Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part I.
        Arthritis Rheum. 2008; 58: 15-25
        • Weng M.Y.
        • Huang Y.T.
        • Liu M.F.
        • Lu T.H.
        Incidence and mortality of treated primary Sjogren's syndrome in Taiwan: a population-based study.
        J Rheumatol. 2011; 38: 706-708
        • Shahzad H.S.
        • Shaw-Stiffel T.A.
        The gastrointestinal manifestations of Sjögren's syndrome.
        Am J Gastroenterol. 1995; 90: 9-14
        • Anselmino M.
        • Zaninotto G.
        • Costantini M.
        • et al.
        Esophageal motor function in primary Sjogren's syndrome: correlation with dysphagia and xerostomia.
        Dig Dis Sci. 1997; 42: 113-118
        • Tsianos E.B.
        • Chiras C.D.
        • Drosos A.A.
        • Moutsopoulos H.M.
        Oesophageal dysfunction in patients with primary Sjogren's syndrome.
        Ann Rheum Dis. 1985; 44: 610-613
        • Ramirez-Mata M.
        • Pena Ancira F.F.
        • Alarcon-Segovia D.
        Abnormal esophageal motility in primary Sjogren's syndrome.
        J Rheumatol. 1976; 3: 63-69
        • Ebert E.C.
        Gastrointestinal and hepatic manifestations of Sjogren syndrome.
        J Clin Gastroenterol. 2012; 46: 25-30
        • Lapadula G.
        • Muolo P.
        • Semeraro F.
        • et al.
        Esophageal motility disorders in the rheumatic diseases: a review of 150 patients.
        Clin Exp Rheumatol. 1994; 12: 515-521
        • Asherson R.
        • Ramos-Casals M.
        • Rodes J.
        • et al.
        Digestive involvement in systemic autoimmune diseases.
        in: Handbook of systemic autoimmune diseases. 8. Elsevier Ltd, 2008: 1-295
        • Jiménez P.
        • Piazuelo E.
        • Sánchez M.T.
        • Ortego J.
        • Soteras F.
        • Lanas A.
        Free radicals and antioxidant systems in reflux esophagitis and Barrett's esophagus.
        World J Gastroenterol. 2005; 11: 2697-2703
        • Oh T.Y.
        • Lee J.S.
        • Ahn B.O.
        • et al.
        Oxidative damages are critical in pathogenesis of reflux esophagitis: implication of antioxidants in its treatment.
        Free Radic Biol Med. 2001; 30: 905-915
        • Isomoto H.
        • Wang A.
        • Mizuta Y.
        • et al.
        Elevated levels of chemokines in esophageal mucosa of patients with reflux esophagitis.
        Am J Gastroenterol. 2003; 98: 551-556
        • Isomoto H.
        • Nishi Y.
        • Wang A.
        • et al.
        Mucosal concentrations of proinflammatory cytokines and chemokines at gastric cardia: implication of Helicobacter pylori infection and gastroesophageal reflux.
        Am J Gastroenterol. 2004; 99: 1063-1068
        • Hinoki A.
        • Yoshimura K.
        • Fujita K.
        • et al.
        Suppression of proinflammatory cytokine production in macrophages by lansoprazole.
        Pediatr Surg Int. 2006; 22: 915-923
        • Capodicasa E.
        • De Bellis F.
        • Pelli M.A.
        Effect of lansoprazole on human leukocyte function.
        Immunopharmacol Immunotoxicol. 1999; 21: 357-377
        • Becker J.C.
        • Grosser N.
        • Waltke C.
        • et al.
        Beyond gastric acid reduction: proton pump inhibitors induce heme oxygenase-1 in gastric and endothelial cells.
        Biochem Biophys Res Commun. 2006; 345: 1014-1021
        • Giacomelli C.
        • Talarico R.
        • Baldini C.
        • Bazzichi L.
        Pain in Sjögren's syndrome.
        Reumatismo. 2014; 66: 39-43
        • Vitale C.
        • Palombi G.
        • Cataleta P.
        Treating Sjogren's syndrome: insights for the clinician.
        Ther Adv Musculoskelet Dis. 2010; 2: 155-166
        • Ruszniewski P.
        • Soufflet C.
        • Barthélémy P.
        Nonsteroidal anti-inflammatory drug use as a risk factor for gastro-oesophageal reflux disease: an observational study.
        Aliment Pharmacol Ther. 2008; 28: 1134-1139
        • Cryer B.
        • Luo X.
        • Assaf A.R.
        • Sands G.
        • Mardekian J.
        Persistence with non-selective NSAIDs and celecoxib among patients with gastroesophageal reflux disease and osteoarthritis or rheumatoid arthritis.
        Curr Med Res Opin. 2011; 27: 295-302