Skip to main content
SpringerLink
Log in

The impact of reflux composition on mucosal injury and esophageal function

  • 2005 SSAT Annual Meeting
  • Published:
Journal of Gastrointestinal Surgery

Abstract

The components of refluxed gastric juice are known to cause mucosal injury, but their effect on esophageal function is less appreciated. Our aim was to determine the effect of acid and/or bile on mucosal injury and esophageal function. From 1993–2004, 402 patients with reflux symptoms had 24-hour pH and Bilitec monitoring, manometry, and endoscopy with biopsies. Mucosal injury (esophagitis or Barrett’s esophagus) and esophageal function (lower esophageal sphincter [LES] characteristics and body contractility) in patients with acid reflux, bile reflux, or both were compared with patients without reflux. Reflux was present in 273/402 patients; of these, 37 (13.5%) had increased exposure to bile, 82 (30.0%) had increased exposure to acid, and 154 (56.4%) had increased exposure to both. Mucosal injury was most common with increased mixed acid and bile exposure, followed by acid alone, and was uncommon with bile alone (P<0.0001). Functional deterioration paralleled mucosal injury (P<0.0001). Mixed acid and bile exposure was present in more than half of patients with reflux and was associated with the most severe mucosal injury and the greatest deterioration of esophageal function. This suggests that composition of gastric juice is the primary determinant of inflammatory mucosal injury and subsequent loss of esophageal function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  1. Locke GR 3rd, Talley NJ, Fett SL, Zinsmeister AR, Melton LJ 3rd. Prevalence and clinical spectrum of gastroesophageal reflux: A population-based study in Olmsted County, Minnesota. Gastroenterology 1997;112:1448–1456.

    Article  PubMed  Google Scholar 

  2. Sandler RS, Everhart JE, Donowitz M, et al. The burden of selected digestive diseases in the United States. Gastroenterology 2002;122:1500–1511.

    Article  PubMed  Google Scholar 

  3. IMS Health. Available at: http://www.imshealth.com. Accessed March, 2005.

  4. Orlando RC. Pathogenesis of reflux esophagitis and Barrett’s esophagus. Med Clin North Am 2005;89:219–241.

    Article  PubMed  Google Scholar 

  5. Prach AT, MacDonald TA, Hopwood DA, Johnston DA. Increasing incidence of Barrett’s oesophagus: Education, enthusiasm, or epidemiology? Lancet 1997;350:933.

    Article  PubMed  CAS  Google Scholar 

  6. Pohl H, Welch HG. The role of overdiagnosis and reclassification in the marked increase of esophageal adenocarcinoma incidence. J Natl Cancer Inst 2005;97:142–146.

    Article  PubMed  Google Scholar 

  7. van Blankenstein M, Looman CWN, Johnston BJ, Caygill CPJ. Age and sex distribution of the prevalence of Barrett’s esophagus found in a primary referral endoscopy center. American J Gastroenterol 2005;100:568–576.

    Article  Google Scholar 

  8. Blot WJ, McLaughlin JK. The changing epidemiology of esophageal cancer. Semin Oncol 1999;26(5 Suppl 15):2–8.

    PubMed  CAS  Google Scholar 

  9. Gillison EW, De Castro VA, Nyhus LM, Kusakarik K, Bombeck CT. The significance of bile in reflux esophagitis. Surg Gynecol Obstet 1972;134:419–424.

    PubMed  CAS  Google Scholar 

  10. Bremner CG. The columnar-lined (Barrett’s) esophagus. Surg Annu 1977;9:103–123.

    PubMed  CAS  Google Scholar 

  11. Bechi P, Pucciani F, Baldini F, et al. Long-term ambulatory enterogastric reflux monitoring. Validation of a new fiberoptic technique. Dig Dis Sci 1993;38:1297–1306.

    Article  PubMed  CAS  Google Scholar 

  12. Kauer WK, Burdiles P, Ireland AP, et al. Does duodenal juice reflux into the esophagus of patients with complicated GERD? Evaluation of a fiberoptic sensor for bilirubin [comment]. Am J Surg 1995;169:98–103.

    Article  PubMed  CAS  Google Scholar 

  13. Kauer WK, Peters JH, DeMeester TR, Ireland AP, Bremner CG, Hagen JA. Mixed reflux of gastric and duodenal juices is more harmful to the esophagus than gastric juice alone. The need for surgical therapy re-emphasized [comment]. Ann Surg 1995;222:525–531.

    Article  PubMed  CAS  Google Scholar 

  14. Fein M, Ireland AP, Ritter MP, et al. Duodenogastric reflux potentiates the injurious effects of gastroesophageal reflux. J Gastrointest Surg 1997;1:27–33.

    Article  PubMed  CAS  Google Scholar 

  15. Jamieson JR, Stein HJ, DeMeester TR, et al. Ambulatory 24-h esophageal pH monitoring: Normal values, optimal thresholds, specificity, sensitivity, and reproducibility, [comment]. Am J Gastroenterol 1992;87:1102–1111.

    PubMed  CAS  Google Scholar 

  16. DeMeester SR, DeMeester TR. Columnar mucosa and intestinal metaplasia of the esophagus: Fifty years of controversy. Ann Surg 2000;231:303–321.

    Article  PubMed  CAS  Google Scholar 

  17. Bremner CG Bremner DT, Bremner RM. Esophageal Motility Testing Made Easy. St. Louis: Quality Medical Publishing, 2001.

    Google Scholar 

  18. Zaninotto G, DeMeester TR, Schwizer W, Johansson KE, Cheng SC. The lower esophageal sphincter in health and disease. Am J Surg 1988;155:104–111.

    Article  PubMed  CAS  Google Scholar 

  19. Henderson RD, Mugashe F, Jeejeebhoy KN, et al. The role of bile and acid in the production of esophagitis and the motor defect of esophagitis. Ann Thorac Surg 1972;14:465–473.

    Article  PubMed  CAS  Google Scholar 

  20. Paterson WG, Kolyn DM. Esophageal shortening induced by short-term intraluminal acid perfusion in opossum: A cause for hiatus hernia? Gastroenterology 1994;107:1736–1740.

    PubMed  CAS  Google Scholar 

  21. Wells RW, Morris GP, Blennerhassett MG, Paterson WG. Effects of acid-induced esophagitis on esophageal smooth muscle. Can J Physiol Pharmacol 2003;81:451–458.

    Article  PubMed  CAS  Google Scholar 

  22. Shirazi S, Schulze-Delrieu K, Custer-Hagen T, Brown CK, Ren J. Motility changes in opossum esophagus from experimental esophagitis. Dig Dis Sci 1989;34:1668–1676.

    Article  PubMed  CAS  Google Scholar 

  23. Koek GH, Vos R, Sifrim D, Cuomo R, Janssens J, Tack J. Mechanisms underlying duodeno-gastric reflux in man. Neurogastroenterol Motil 2005;17:191–199.

    Article  PubMed  CAS  Google Scholar 

  24. Fuchs KH, Fein M, Maroske J, Heimbucher J, Freys SM. The role of 24-hr gastric pH-monitoring in the interpretation of 24-hr gastric bile monitoring for duodenogastric reflux. Hepatogastroenterology 1999;46:60–65.

    PubMed  CAS  Google Scholar 

  25. Keane FB, Dimagno EP, Malagelada JR. Duodenogastric reflux in humans: Its relationship to fasting antroduodenal motility and gastric, pancreatic, and biliary secretion. Gastroenterology 1981;81:726–731.

    PubMed  CAS  Google Scholar 

  26. Kauer WK, Peters JH, DeMeester TR, et al. Composition and concentration of bile acid reflux into the esophagus of patients with gastroesophageal reflux disease. Surgery 1997;122:874–881.

    Article  PubMed  CAS  Google Scholar 

  27. Harmon JW, Johnson LF, Maydonovitch CL. Effects of acid and bile salts on the rabbit esophageal mucosa. Dig Dis Sci 1981;26:65–72.

    Article  PubMed  CAS  Google Scholar 

  28. Schweitzer EJ, Bass BL, Batzri S, Harmon JW. Bile acid accumulation by rabbit esophageal mucosa. Dig Dis Sci 1986;31:1105–1113.

    Article  PubMed  CAS  Google Scholar 

  29. Lillemoe KD, Gadacz TR, Harmon JW. Bile absorption occurs during disruption of the esophageal mucosal barrier. J Surg Res 1983;35:57–62.

    Article  PubMed  CAS  Google Scholar 

  30. Theisen J, Peters JH, Fein M, et al. The mutagenic potential of duodenoesophageal reflux. Ann Surg 2005;241:63–68.

    PubMed  Google Scholar 

  31. Silverman SJ, Andrews AW. Bile acids: Co-mutagenic activity in the Salmonella-mammalian-microsome mutagenicity test: Brief communication. J Natl Cancer Inst 1977;59:1557–1559.

    PubMed  CAS  Google Scholar 

  32. Bernstein H, Bernstein C, Payne CM, Dvorakova K, Garewel H. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 2005;589:47–65.

    Article  PubMed  CAS  Google Scholar 

  33. DeMeester TR, Peters JH, Bremner CG, Chandrasoma P. Biology of gastroesophageal reflux disease: Pathophysiology relating to medical and surgical treatment. Annu Rev Med 1999;50:469–506.

    Article  PubMed  CAS  Google Scholar 

  34. Ireland AP, Peters JH, Smyrk TC, et al. Gastric juice protects against the development of esophageal adenocarcinoma in the rat. Ann Surg 1996;224:358–370.

    Article  PubMed  CAS  Google Scholar 

  35. Hunt RH. Importance of pH control in the management of GERD. Arch Intern Med 1999;159:649–657.

    Article  PubMed  CAS  Google Scholar 

  36. Blum RA, Shi H, Karol MD, Greski-Rose PA, Hunt RH. The comparative effects of lansoprazole, omeprazole, and ranitidine in suppressing gastric acid secretion. Clin Ther 1997;19:1013–1023.

    Article  PubMed  CAS  Google Scholar 

  37. Katzka DA, Castell DO. Successful elimination of reflux symptoms does not insure adequate control of acid reflux in patients with Barrett’s esophagus [comment]. Am J Gastroenterol 1994;89:989–991.

    PubMed  CAS  Google Scholar 

  38. Tamhankar AP, Peters JH, Portale G, et al. Omeprazole does not reduce gastroesophageal reflux: New insights using multichannel intraluminal impedance technology. J Gastrointest Surg 2004;8:890–897.

    Article  PubMed  Google Scholar 

  39. Jackson C-CA, DeMeester SR. Surgical therapy for Barrett’s esophagus. Thorac Surg Clin 2005;15:429–436.

    Article  PubMed  Google Scholar 

  40. Stein HJ, Kauer WK, Feussner H, Siewert JR. Bile reflux in benign and malignant Barrett’s esophagus: Effect of medical acid suppression and Nissen fundoplication. J Gastrointest Surg 1998;2:333–341.

    Article  PubMed  CAS  Google Scholar 

  41. Oleynikov D, Eubanks TR, Oelschlager BK, Pellegrini CA. Total fundoplication is the operation of choice for patients with gastroesophageal reflux and defective peristalsis. Surg Endosc 2002;16:909–913.

    Article  PubMed  CAS  Google Scholar 

  42. Chrysos E, Tsiaoussis J, Zoras OJ, et al. Laparoscopic surgery for gastroesophageal reflux disease patients with impaired esophageal peristalsis: Total or partial fundoplication? J Am Coll Surg 2003;197:8–15.

    Article  PubMed  Google Scholar 

  43. Munitiz V, Ortiz A, Martinez de Haro LF, Molina J, Parrilla P. Ineffective oesophageal motility does not affect the clinical outcome of open Nissen fundoplication. Br J Surg 2004;91:1010–1014.

    Article  PubMed  CAS  Google Scholar 

  44. Scheffer RCH, Samsom M, Frakking TG, Smout AJPM, Gooszen HG. Long-term effect of fundoplication on motility of the oesophagus and oesophagogastric junction. Br J Surg 2004;91:1466–1472.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Keck School of Medicine, University of Southern California, 1510 San Pablo Street, Suite 514, 90033, Los Angeles, CA

    Daniel S. Oh M.D., Jeffrey A. Hagen M.D., Martin Fein M.D., Cedric G. Bremner M.D., Christy M. Dunst M.D., Steven R. DeMeester M.D., John Lipham M.D. & Tom R. DeMeester M.D. (Professor and Chairman)

Authors
  1. Daniel S. Oh M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey A. Hagen M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Fein M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cedric G. Bremner M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christy M. Dunst M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Steven R. DeMeester M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John Lipham M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tom R. DeMeester M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tom R. DeMeester M.D..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oh, D.S., Hagen, J.A., Fein, M. et al. The impact of reflux composition on mucosal injury and esophageal function. J Gastrointest Surg 10, 787–797 (2006). https://doi.org/10.1016/j.gassur.2006.02.005

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.gassur.2006.02.005

Key words

Search

Navigation