Advances in the Evaluation and Management of Esophageal Disease of Systemic Sclerosis

  • Dustin A. Carlson
  • Monique Hinchcliff
  • John E. Pandolfino
Scleroderma (J Varga, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Scleroderma


Symptoms of heartburn and dysphagia as well as objective findings of abnormal esophageal acid exposure and esophageal dysmotility are common in patients with systemic sclerosis (SSc). Treatments for SSc esophageal disease are generally limited to gastroesophageal reflux disease (GERD) treatment with proton pump inhibitors. Progresses made in esophageal diagnostic testing offer the potential for improved clinical characterization of esophageal disease in SSc that may help direct management decisions. In addition to reviewing GERD management in patients with SSc, present and potential uses of endoscopy, reflux monitoring, manometry, impedance planimetry, and endoscopic ultrasound are discussed.


Systemic sclerosis GERD Esophageal reflux monitoring Manometry Impedance 



Barrett’s esophagus


Diffuse cutaneous systemic sclerosis




Esophagogastric junction


Esophageal pressure topography


High-resolution (impedance) manometry


Limited cutaneous systemic sclerosis


Lower esophageal sphincter


Multiple rapid swallows


Gastroesophageal reflux disease


Proton pump inhibitor


Small intestinal bacterial overgrowth


Systemic sclerosis


Upper esophageal sphincter



This work was supported by RO1 DK079902 (J.E.P.) and T32 DK101363-01 (J.E.P) from the Public Health Service. It was also supported in part by an NIH-NIAMS K23 AR059763 (M.H.) and a research award from the Scleroderma Research Foundation (MH).

Compliance with Ethics Guidelines

Conflict of Interest

Dustin A. Carlson and Monique Hinchcliff declare no conflict of interest.

John E. Pandolfino reports grants and personal fees from Given Imaging as well as personal fees from Astra Zeneca and Takeda, outside the submitted work.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    Abu-Shakra M, Guillemin F, Lee P. Gastrointestinal manifestations of systemic sclerosis. Semin Arthritis Rheum. 1994;24(1):29–39.PubMedCrossRefGoogle Scholar
  2. 2.
    Sjogren RW. Gastrointestinal motility disorders in scleroderma. Arthritis Rheum. 1994;37(9):1265–82.PubMedCrossRefGoogle Scholar
  3. 3.
    Ebert EC. Esophageal disease in scleroderma. J Clin Gastroenterol. 2006;40(9):769–75. doi: 10.1097/01.mcg.0000225549.19127.90.PubMedCrossRefGoogle Scholar
  4. 4.
    Treacy WL, Baggenstoss AH, Slocumb CH, et al. Scleroderma of the esophagus. A correlation of histologic and physiologic findings. Ann Intern Med. 1963;59:351–6.PubMedCrossRefGoogle Scholar
  5. 5.
    Roberts CG, Hummers LK, Ravich WJ, et al. A case-control study of the pathology of oesophageal disease in systemic sclerosis (scleroderma). Gut. 2006;55(12):1697–703. doi: 10.1136/gut.2005.086074.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Simeon-Aznar CP, Fonollosa-Pla V, Tolosa-Vilella C, et al. Registry of the Spanish network for systemic sclerosis: clinical pattern according to cutaneous subsets and immunological status. Semin Arthritis Rheum. 2012;41(6):789–800. doi: 10.1016/j.semarthrit.2011.10.004.PubMedCrossRefGoogle Scholar
  7. 7.
    Bassotti G, Battaglia E, Debernardi V, et al. Esophageal dysfunction in scleroderma: relationship with disease subsets. Arthritis Rheum. 1997;40(12):2252–9. doi: 10.1002/1529-0131(199712)40:12<2252::AID-ART21>3.0.CO;2-W.PubMedCrossRefGoogle Scholar
  8. 8.
    Roman S, Hot A, Fabien N, et al. Esophageal dysmotility associated with systemic sclerosis: a high-resolution manometry study. Dis Esophagus Off J Int Soc Dis Esophagus/ISDE. 2010. doi: 10.1111/j.1442-2050.2010.01150.x.Google Scholar
  9. 9.
    Savarino E, Bazzica M, Zentilin P, et al. Gastroesophageal reflux and pulmonary fibrosis in scleroderma: a study using pH-impedance monitoring. Am J Respir Crit Care Med. 2009;179(5):408–13. doi: 10.1164/rccm.200808-1359OC.PubMedCrossRefGoogle Scholar
  10. 10.
    Zhang XJ, Bonner A, Hudson M, et al. Association of gastroesophageal factors and worsening of forced vital capacity in systemic sclerosis. J Rheumatol. 2013;40(6):850–8. doi: 10.3899/jrheum.120705.PubMedCrossRefGoogle Scholar
  11. 11.
    Christmann RB, Wells AU, Capelozzi VL, et al. Gastroesophageal reflux incites interstitial lung disease in systemic sclerosis: clinical, radiologic, histopathologic, and treatment evidence. Semin Arthritis Rheum. 2010;40(3):241–9. doi: 10.1016/j.semarthrit.2010.03.002.PubMedCrossRefGoogle Scholar
  12. 12.
    Marie I, Dominique S, Levesque H, et al. Esophageal involvement and pulmonary manifestations in systemic sclerosis. Arthritis Rheum. 2001;45(4):346–54. doi: 10.1002/1529-0131(200108)45:4<346::AID-ART347>3.0.CO;2-L.PubMedCrossRefGoogle Scholar
  13. 13.
    Lock G, Pfeifer M, Straub RH, et al. Association of esophageal dysfunction and pulmonary function impairment in systemic sclerosis. Am J Gastroenterol. 1998;93(3):341–5. doi: 10.1111/j.1572-0241.1998.00341.x.PubMedCrossRefGoogle Scholar
  14. 14.
    Rubio-Rivas M, Royo C, Simeon CP, et al. Mortality and survival in systemic sclerosis: systematic review and meta-analysis. Semin Arthritis Rheum. 2014. doi: 10.1016/j.semarthrit.2014.05.010.PubMedGoogle Scholar
  15. 15.
    Kirchheiner J, Glatt S, Fuhr U, et al. Relative potency of proton-pump inhibitors-comparison of effects on intragastric pH. Eur J Clin Pharmacol. 2009;65(1):19–31. doi: 10.1007/s00228-008-0576-5.PubMedCrossRefGoogle Scholar
  16. 16.
    Pakozdi A, Wilson H, Black CM, et al. Does long term therapy with lansoprazole slow progression of oesophageal involvement in systemic sclerosis? Clin Exp Rheumatol. 2009;27(3 Suppl 54):5–8.PubMedGoogle Scholar
  17. 17.
    Hendel L, Hage E, Hendel J, et al. Omeprazole in the long-term treatment of severe gastro-oesophageal reflux disease in patients with systemic sclerosis. Aliment Pharmacol Ther. 1992;6(5):565–77.PubMedCrossRefGoogle Scholar
  18. 18.
    Muro Y, Sugiura K, Nitta Y, et al. Scoring of reflux symptoms associated with scleroderma and the usefulness of rabeprazole. Clin Exp Rheumatol. 2009;27(3 Suppl 54):15–21.PubMedGoogle Scholar
  19. 19.
    Boeckxstaens G, El-Serag HB, Smout AJ, et al. Symptomatic reflux disease: the present, the past and the future. Gut. 2014;63(7):1185–93. doi: 10.1136/gutjnl-2013-306393.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.•
    Kukulka M, Eisenberg C, Nudurupati S. Comparator pH study to evaluate the single-dose pharmacodynamics of dual delayed-release dexlansoprazole 60 mg and delayed-release esomeprazole 40 mg. Clin Exp Gastroenterol. 2011;4:213–20. doi: 10.2147/CEG.S24063. This single center, phase I, randomized, open label cross-over study that comparing gastric pH in healthy subjects receiving daily 60mg dexlansoprazole and 40mg esomeprazole. They demonstrated a higher mean gastric pH over 24 hours with dexlansoprazole, but similar gastric pH between the two groups at 0–12 hours.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.•
    Khan BA, Sodhi JS, Zargar SA, et al. Effect of bed head elevation during sleep in symptomatic patients of nocturnal gastroesophageal reflux. J Gastroenterol Hepatol. 2012;27(6):1078–82. doi: 10.1111/j.1440-1746.2011.06968.x. This open-label trial of patients with symptomatic nocturnal reflux and abnormal supine esophageal pH testing demonstrated reduced esophageal acid exposure and symptomatic improvement with head of the bed elevation.PubMedCrossRefGoogle Scholar
  22. 22.
    Wang Y, Pan T, Wang Q, et al. Additional bedtime H2-receptor antagonist for the control of nocturnal gastric acid breakthrough. Cochrane Database Syst Rev. 2009;4, CD004275. doi: 10.1002/14651858.CD004275.pub3.PubMedGoogle Scholar
  23. 23.
    Janiak P, Thumshirn M, Menne D, et al. Clinical trial: the effects of adding ranitidine at night to twice daily omeprazole therapy on nocturnal acid breakthrough and acid reflux in patients with systemic sclerosis—a randomized controlled, cross-over trial. Aliment Pharmacol Ther. 2007;26(9):1259–65. doi: 10.1111/j.1365-2036.2007.03469.x.PubMedCrossRefGoogle Scholar
  24. 24.
    Fackler WK, Ours TM, Vaezi MF, et al. Long-term effect of H2RA therapy on nocturnal gastric acid breakthrough. Gastroenterology. 2002;122(3):625–32.PubMedCrossRefGoogle Scholar
  25. 25.•
    Janarthanan S, Ditah I, Adler DG, et al. Clostridium difficile-associated diarrhea and proton pump inhibitor therapy: a meta-analysis. Am J Gastroenterol. 2012;107(7):1001–10. doi: 10.1038/ajg.2012.179. This meta-analysis of cohort and case–control studies demonstrated an increased incidence Clostridium difficile infection associated with PPI use.PubMedCrossRefGoogle Scholar
  26. 26.•
    Kwok CS, Arthur AK, Anibueze CI, et al. Risk of Clostridium difficile infection with acid suppressing drugs and antibiotics: meta-analysis. Am J Gastroenterol. 2012;107(7):1011–9. doi: 10.1038/ajg.2012.108. This meta-analysis of cohort and case–control studies demonstrated an increased risk of new and recurrent Clostridium difficile infection associated with PPI use.PubMedCrossRefGoogle Scholar
  27. 27.
    Eom CS, Jeon CY, Lim JW, et al. Use of acid-suppressive drugs and risk of pneumonia: a systematic review and meta-analysis. CMAJ Can Med Assoc J J Assoc Med Can. 2011;183(3):310–9. doi: 10.1503/cmaj.092129.CrossRefGoogle Scholar
  28. 28.
    Ngamruengphong S, Leontiadis GI, Radhi S, et al. Proton pump inhibitors and risk of fracture: a systematic review and meta-analysis of observational studies. Am J Gastroenterol. 2011;106(7):1209–18. doi: 10.1038/ajg.2011.113. quiz 19.PubMedCrossRefGoogle Scholar
  29. 29.
    Targownik LE, Lix LM, Leung S, et al. Proton-pump inhibitor use is not associated with osteoporosis or accelerated bone mineral density loss. Gastroenterology. 2010;138(3):896–904. doi: 10.1053/j.gastro.2009.11.014.PubMedCrossRefGoogle Scholar
  30. 30.•
    Targownik LE, Leslie WD, Davison KS, et al. The relationship between proton pump inhibitor use and longitudinal change in bone mineral density: a population-based study [corrected] from the Canadian Multicentre Osteoporosis Study (CaMos). Am J Gastroenterol. 2012;107(9):1361–9. doi: 10.1038/ajg.2012.200. This is a retrospective analysis of a large Canadian database of patients with bone mineral density testing at baseline, 5, and 10 years. They reported that while PPI use was associated with lower baseline bone mineral density, but was not associated with accelerated bone mineral density loss.PubMedCrossRefGoogle Scholar
  31. 31.
    Solomon DH, Diem SJ, Ruppert K, et al. Bone mineral density changes among women initiating proton pump inhibitors or H2 receptor antagonists: a SWAN cohort study. J Bone Miner Res Off J Am Soc Bone Miner Res. 2014. doi: 10.1002/jbmr.2344.Google Scholar
  32. 32.
    Lo WK, Chan WW. Proton pump inhibitor use and the risk of small intestinal bacterial overgrowth: a meta-analysis. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2013;11(5):483–90. doi: 10.1016/j.cgh.2012.12.011.Google Scholar
  33. 33.
    Jacobs C, Coss Adame E, Attaluri A, et al. Dysmotility and proton pump inhibitor use are independent risk factors for small intestinal bacterial and/or fungal overgrowth. Aliment Pharmacol Ther. 2013;37(11):1103–11. doi: 10.1111/apt.12304.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Mercado U, Arroyo de Anda R, Avendano L, et al. Metoclopramide response in patients with early diffuse systemic sclerosis. Effects on esophageal motility abnormalities. Clin Exp Rheumatol. 2005;23(5):685–8.PubMedGoogle Scholar
  35. 35.
    Johnson DA, Drane WE, Curran J, et al. Metoclopramide response in patients with progressive systemic sclerosis. Effect on esophageal and gastric motility abnormalities. Arch Intern Med. 1987;147(9):1597–601.PubMedCrossRefGoogle Scholar
  36. 36.
    Drane WE, Karvelis K, Johnson DA, et al. Scintigraphic detection of metoclopramide esophageal stimulation in progressive systemic sclerosis. J Nucl Med Off Publ Soc Nucl Med. 1987;28(5):810–5.Google Scholar
  37. 37.
    Ramirez-Mata M, Ibanez G, Alarcon-Segovia D. Stimulatory effect of metoclopramide on the esophagus and lower esophageal sphincter of patients of patients with PSS. Arthritis Rheum. 1977;20(1):30–4.PubMedCrossRefGoogle Scholar
  38. 38.
    Sallam H, McNearney TA, Chen JD. Systematic review: pathophysiology and management of gastrointestinal dysmotility in systemic sclerosis (scleroderma). Aliment Pharmacol Ther. 2006;23(6):691–712. doi: 10.1111/j.1365-2036.2006.02804.x.PubMedCrossRefGoogle Scholar
  39. 39.•
    Kessing BF, Smout AJ, Bennink RJ, et al. Prucalopride decreases esophageal acid exposure and accelerates gastric emptying in healthy subjects. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2014;26(8):1079–86. doi: 10.1111/nmo.12359. This double-blind, placebo-controlled, randomized cross-over study examined the effects of prucalopride, a 5-HT4 receptor agonist, on healthy volunteers. They found that prucalopride reduced esophageal acid exposure and gastric emptying, but did not affect esophageal motility.CrossRefGoogle Scholar
  40. 40.
    Poirier NC, Taillefer R, Topart P, et al. Antireflux operations in patients with scleroderma. Ann Thorac Surg. 1994;58(1):66–72. discussion −3.PubMedCrossRefGoogle Scholar
  41. 41.
    Orringer MB, Orringer JS, Dabich L, et al. Combined Collis gastroplasty–fundoplication operations for scleroderma reflux esophagitis. Surgery. 1981;90(4):624–30.PubMedGoogle Scholar
  42. 42.
    Mansour KA, Malone CE. Surgery for scleroderma of the esophagus: a 12-year experience. Ann Thorac Surg. 1988;46(5):513–4.PubMedCrossRefGoogle Scholar
  43. 43.
    Kent MS, Luketich JD, Irshad K, et al. Comparison of surgical approaches to recalcitrant gastroesophageal reflux disease in the patient with scleroderma. Ann Thorac Surg. 2007;84(5):1710–5. doi: 10.1016/j.athoracsur.2007.06.025. discussion 5–6.PubMedCrossRefGoogle Scholar
  44. 44.
    Pandolfino JE, Krishnan K. Do endoscopic antireflux procedures fit in the current treatment paradigm of gastroesophageal reflux disease? Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2014;12(4):544–54. doi: 10.1016/j.cgh.2013.06.012.Google Scholar
  45. 45.
    Arts J, Bisschops R, Blondeau K, et al. A double-blind sham-controlled study of the effect of radiofrequency energy on symptoms and distensibility of the gastro-esophageal junction in GERD. Am J Gastroenterol. 2012;107(2):222–30. doi: 10.1038/ajg.2011.395.PubMedCrossRefGoogle Scholar
  46. 46.
    Cohen LB, Johnson DA, Ganz RA, et al. Enteryx implantation for GERD: expanded multicenter trial results and interim postapproval follow-up to 24 months. Gastrointest Endosc. 2005;61(6):650–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Schwartz MP, Schreinemakers JR, Smout AJ. Four-year follow-up of endoscopic gastroplication for the treatment of gastroesophageal reflux disease. World J Gastrointest Pharmacol Ther. 2013;4(4):120–6. doi: 10.4292/wjgpt.v4.i4.120.PubMedCentralPubMedGoogle Scholar
  48. 48.
    Pleskow D, Rothstein R, Kozarek R, et al. Endoscopic full-thickness plication for the treatment of GERD: five-year long-term multicenter results. Surg Endosc. 2008;22(2):326–32. doi: 10.1007/s00464-007-9667-0.PubMedCrossRefGoogle Scholar
  49. 49.
    Ganz RA, Peters JH, Horgan S, et al. Esophageal sphincter device for gastroesophageal reflux disease. N Engl J Med. 2013;368(8):719–27. doi: 10.1056/NEJMoa1205544.PubMedCrossRefGoogle Scholar
  50. 50.
    Johnsson F, Joelsson B, Gudmundsson K, et al. Symptoms and endoscopic findings in the diagnosis of gastroesophageal reflux disease. Scand J Gastroenterol. 1987;22(6):714–8.PubMedCrossRefGoogle Scholar
  51. 51.
    Katz PO, Gerson LB, Vela MF. Guidelines for the diagnosis and management of gastroesophageal reflux disease. Am J Gastroenterol. 2013;108(3):308–28. doi: 10.1038/ajg.2012.444. quiz 29.PubMedCrossRefGoogle Scholar
  52. 52.•
    Thonhofer R, Siegel C, Trummer M, et al. Early endoscopy in systemic sclerosis without gastrointestinal symptoms. Rheumatol Int. 2012;32(1):165–8. doi: 10.1007/s00296-010-1595-y. This retrospective analysis of 13 asymptomatic SSc patients that underwent EGD within one year of SSc diagnosis found reflux esophagitis in 77%.PubMedCrossRefGoogle Scholar
  53. 53.
    Lundell LR, Dent J, Bennett JR, et al. Endoscopic assessment of oesophagitis: clinical and functional correlates and further validation of the Los Angeles classification. Gut. 1999;45(2):172–80.PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Kowal-Bielecka O, Landewe R, Avouac J, et al. EULAR recommendations for the treatment of systemic sclerosis: a report from the EULAR Scleroderma Trials and Research group (EUSTAR). Ann Rheum Dis. 2009;68(5):620–8. doi: 10.1136/ard.2008.096677.PubMedCrossRefGoogle Scholar
  55. 55.
    Marie I, Ducrotte P, Denis P, et al. Oesophageal mucosal involvement in patients with systemic sclerosis receiving proton pump inhibitor therapy. Aliment Pharmacol Ther. 2006;24(11–12):1593–601. doi: 10.1111/j.1365-2036.2006.03180.x.PubMedCrossRefGoogle Scholar
  56. 56.
    Sikkema M, de Jonge PJ, Steyerberg EW, et al. Risk of esophageal adenocarcinoma and mortality in patients with Barrett’s esophagus: a systematic review and meta-analysis. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2010;8(3):235–44. doi: 10.1016/j.cgh.2009.10.010. quiz e32.Google Scholar
  57. 57.
    Hvid-Jensen F, Pedersen L, Drewes AM, et al. Incidence of adenocarcinoma among patients with Barrett’s esophagus. N Engl J Med. 2011;365(15):1375–83. doi: 10.1056/NEJMoa1103042.PubMedCrossRefGoogle Scholar
  58. 58.
    Committee ASoP, Evans JA, Early DS, et al. The role of endoscopy in Barrett’s esophagus and other premalignant conditions of the esophagus. Gastrointest Endosc. 2012;76(6):1087–94. doi: 10.1016/j.gie.2012.08.004.PubMedCrossRefGoogle Scholar
  59. 59.
    American Gastroenterological A, Spechler SJ, Sharma P, et al. American Gastroenterological Association medical position statement on the management of Barrett’s esophagus. Gastroenterology. 2011;140(3):1084–91. doi: 10.1053/j.gastro.2011.01.030.CrossRefGoogle Scholar
  60. 60.
    Wang KK, Sampliner RE. Practice Parameters Committee of the American College of G. Updated guidelines 2008 for the diagnosis, surveillance and therapy of Barrett’s esophagus. Am J Gastroenterol. 2008;103(3):788–97. doi: 10.1111/j.1572-0241.2008.01835.x.PubMedCrossRefGoogle Scholar
  61. 61.•
    Wipff J, Coriat R, Masciocchi M, et al. Outcomes of Barrett’s oesophagus related to systemic sclerosis: a 3-year EULAR Scleroderma Trials and Research prospective follow-up study. Rheumatology (Oxford). 2011;50(8):1440–4. doi: 10.1093/rheumatology/ker110. This study that followed 50 SSc patients with Barrett’s esophagus (10 with and 40 without dysplasia) for 3 years reported a yearly progression rate of 0.7 per year when including all patients (slightly above the general population estimate). One patient with dysplasia and zero patients without dysplasia at baseline developed esophageal adenocarcinoma over the follow-up period.CrossRefGoogle Scholar
  62. 62.
    Landgren AM, Landgren O, Gridley G, et al. Autoimmune disease and subsequent risk of developing alimentary tract cancers among 4.5 million US male veterans. Cancer. 2011;117(6):1163–71. doi: 10.1002/cncr.25524.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Wong WM, Bautista J, Dekel R, et al. Feasibility and tolerability of transnasal/per-oral placement of the wireless pH capsule vs. traditional 24-h oesophageal pH monitoring--a randomized trial. Aliment Pharmacol Ther. 2005;21(2):155–63. doi: 10.1111/j.1365-2036.2005.02313.x.PubMedCrossRefGoogle Scholar
  64. 64.
    Pandolfino JE, Richter JE, Ours T, et al. Ambulatory esophageal pH monitoring using a wireless system. Am J Gastroenterol. 2003;98(4):740–9. doi: 10.1111/j.1572-0241.2003.07398.x.PubMedCrossRefGoogle Scholar
  65. 65.
    Wenner J, Johnsson F, Johansson J, et al. Wireless esophageal pH monitoring is better tolerated than the catheter-based technique: results from a randomized cross-over trial. Am J Gastroenterol. 2007;102(2):239–45. doi: 10.1111/j.1572-0241.2006.00939.x.PubMedCrossRefGoogle Scholar
  66. 66.
    Ahlawat SK, Novak DJ, Williams DC, et al. Day-to-day variability in acid reflux patterns using the BRAVO pH monitoring system. J Clin Gastroenterol. 2006;40(1):20–4.PubMedCrossRefGoogle Scholar
  67. 67.
    Hirano I, Zhang Q, Pandolfino JE, et al. Four-day Bravo pH capsule monitoring with and without proton pump inhibitor therapy. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2005;3(11):1083–8.Google Scholar
  68. 68.
    Scarpulla G, Camilleri S, Galante P, et al. The impact of prolonged pH measurements on the diagnosis of gastroesophageal reflux disease: 4-day wireless pH studies. Am J Gastroenterol. 2007;102(12):2642–7. doi: 10.1111/j.1572-0241.2007.01461.x.PubMedCrossRefGoogle Scholar
  69. 69.
    Andrews CN, Sadowski DC, Lazarescu A, et al. Unsedated peroral wireless pH capsule placement vs. standard pH testing: a randomized study and cost analysis. BMC Gastroenterol. 2012;12:58. doi: 10.1186/1471-230X-12-58.PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Charbel S, Khandwala F, Vaezi MF. The role of esophageal pH monitoring in symptomatic patients on PPI therapy. Am J Gastroenterol. 2005;100(2):283–9. doi: 10.1111/j.1572-0241.2005.41210.x.PubMedCrossRefGoogle Scholar
  71. 71.•
    Fisichella PM, Reder NP, Gagermeier J, et al. Usefulness of pH monitoring in predicting the survival status of patients with scleroderma awaiting lung transplantation. J Surg Res. 2014;189(2):232–7. doi: 10.1016/j.jss.2014.03.025. This retrospective analysis of 10 SSc patients with end-stage lung disease demonstrated that abnormal parameters of esophageal pH monitoring can predict survival duration as well or better than pulmonary function test measurements.PubMedCrossRefGoogle Scholar
  72. 72.
    Hershcovici T, Jha LK, Johnson T, et al. Systematic review: the relationship between interstitial lung diseases and gastro-oesophageal reflux disease. Aliment Pharmacol Ther. 2011;34(11–12):1295–305. doi: 10.1111/j.1365-2036.2011.04870.x.PubMedCrossRefGoogle Scholar
  73. 73.
    Gibson PG, Henry RL, Coughlan JL. Gastro-oesophageal reflux treatment for asthma in adults and children. Cochrane Database Syst Rev. 2003;2, CD001496. doi: 10.1002/14651858.CD001496.PubMedGoogle Scholar
  74. 74.
    Cantu 3rd E, Appel 3rd JZ, Hartwig MG, et al. Maxwell Chamberlain Memorial Paper. Early fundoplication prevents chronic allograft dysfunction in patients with gastroesophageal reflux disease. Ann Thorac Surg. 2004;78(4):1142–51. doi: 10.1016/j.athoracsur.2004.04.044. discussion −51.PubMedCrossRefGoogle Scholar
  75. 75.
    Hoppo T, Jarido V, Pennathur A, et al. Antireflux surgery preserves lung function in patients with gastroesophageal reflux disease and end-stage lung disease before and after lung transplantation. Arch Surg. 2011;146(9):1041–7. doi: 10.1001/archsurg.2011.216.PubMedCrossRefGoogle Scholar
  76. 76.
    Yarze JC, Varga J, Stampfl D, et al. Esophageal function in systemic sclerosis: a prospective evaluation of motility and acid reflux in 36 patients. Am J Gastroenterol. 1993;88(6):870–6.PubMedGoogle Scholar
  77. 77.
    Bredenoord AJ, Fox M, Kahrilas PJ et al. Chicago classification criteria of esophageal motility disorders defined in high resolution esophageal pressure topography. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2012.Google Scholar
  78. 78.
    Pandolfino JE, Ghosh SK, Rice J, et al. Classifying esophageal motility by pressure topography characteristics: a study of 400 patients and 75 controls. Am J Gastroenterol. 2008;103(1):27–37. doi: 10.1111/j.1572-0241.2007.01532.x.PubMedCrossRefGoogle Scholar
  79. 79.
    Tang DM, Pathikonda M, Harrison M, et al. Symptoms and esophageal motility based on phenotypic findings of scleroderma. Dis Esophagus Off J Int Soc Dis Esophagus/ISDE. 2013;26(2):197–203. doi: 10.1111/j.1442-2050.2012.01349.x.CrossRefGoogle Scholar
  80. 80.
    Tutuian R, Castell DO. Clarification of the esophageal function defect in patients with manometric ineffective esophageal motility: studies using combined impedance-manometry. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2004;2(3):230–6.Google Scholar
  81. 81.
    Lin Z, Imam H, Nicodeme F, et al. Flow time through esophagogastric junction derived during high-resolution impedance-manometry studies: a novel parameter for assessing esophageal bolus transit. Am J Physiol Gastrointest Liver Physiol. 2014;307(2):G158–63. doi: 10.1152/ajpgi.00119.2014. The bolus flow time is a new metric of esophageal function that utilizes high-resolution impedance manometry to measures the time of bolus flow through the EGJ.PubMedCrossRefGoogle Scholar
  82. 82.
    Cho YK, Lipowska AM, Nicodeme F, et al. Assessing bolus retention in achalasia using high-resolution manometry with impedance: a comparator study with timed barium esophagram. Am J Gastroenterol. 2014;109(6):829–35. doi: 10.1038/ajg.2014.61.PubMedCrossRefGoogle Scholar
  83. 83.•
    Lin Z, Yim B, Gawron A, et al. The four phases of esophageal bolus transit defined using high resolution impedance manometry and fluoroscopy. Am J Physiol Gastrointest Liver Physiol. 2014. doi: 10.1152/ajpgi.00148.2014. A novel paradigm of assessing esophageal function by identifying four distinct, functional phases of esophageal bolus transit is described.Google Scholar
  84. 84.
    Fornari F, Bravi I, Penagini R, et al. Multiple rapid swallowing: a complementary test during standard oesophageal manometry. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2009;21(7):718–e41. doi: 10.1111/j.1365-2982.2009.01273.x.CrossRefGoogle Scholar
  85. 85.•
    Shaker A, Stoikes N, Drapekin J, et al. Multiple rapid swallow responses during esophageal high-resolution manometry reflect esophageal body peristaltic reserve. Am J Gastroenterol. 2013;108(11):1706–12. doi: 10.1038/ajg.2013.289. Assessment of esophageal peristalsis following rapid multiple swallows during an esophageal manometry protocol is a measure of esophageal reserve and may help predict post-operative dysphagia following antireflux surgery.PubMedCentralPubMedCrossRefGoogle Scholar
  86. 86.
    Marjoux S, Roman S, Juget-Pietu F, et al. Impaired postoperative EGJ relaxation as a determinant of post laparoscopic fundoplication dysphagia: a study with high-resolution manometry before and after surgery. Surg Endosc. 2012;26(12):3642–9. doi: 10.1007/s00464-012-2388-z.PubMedCrossRefGoogle Scholar
  87. 87.
    Montenovo M, Tatum RP, Figueredo E, et al. Does combined multichannel intraluminal esophageal impedance and manometry predict postoperative dysphagia after laparoscopic Nissen fundoplication? Dis Esophagus Off J Int Soc Dis Esophagus/ISDE. 2009;22(8):656–63. doi: 10.1111/j.1442-2050.2009.00988.x.CrossRefGoogle Scholar
  88. 88.
    Strate U, Emmermann A, Fibbe C, et al. Laparoscopic fundoplication: nissen versus Toupet two-year outcome of a prospective randomized study of 200 patients regarding preoperative esophageal motility. Surg Endosc. 2008;22(1):21–30. doi: 10.1007/s00464-007-9546-8.PubMedCrossRefGoogle Scholar
  89. 89.
    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(1):8–15. doi: 10.1016/S1072-7515(03)00151-0.PubMedCrossRefGoogle Scholar
  90. 90.
    Broeders JA, Sportel IG, Jamieson GG, et al. Impact of ineffective oesophageal motility and wrap type on dysphagia after laparoscopic fundoplication. Br J Surg. 2011;98(10):1414–21. doi: 10.1002/bjs.7573.PubMedCrossRefGoogle Scholar
  91. 91.
    Kwiatek MA, Pandolfino JE, Hirano I, et al. Esophagogastric junction distensibility assessed with an endoscopic functional luminal imaging probe (EndoFLIP). Gastrointest Endosc. 2010;72(2):272–8. doi: 10.1016/j.gie.2010.01.069.PubMedCentralPubMedCrossRefGoogle Scholar
  92. 92.
    Rohof WO, Hirsch DP, Kessing BF, et al. Efficacy of treatment for patients with achalasia depends on the distensibility of the esophagogastric junction. Gastroenterology. 2012;143(2):328–35. doi: 10.1053/j.gastro.2012.04.048.PubMedCrossRefGoogle Scholar
  93. 93.
    Nicodeme F, Hirano I, Chen J, et al. Esophageal distensibility as a measure of disease severity in patients with eosinophilic esophagitis. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2013. doi: 10.1016/j.cgh.2013.03.020.Google Scholar
  94. 94.
    Kwiatek MA, Kahrilas K, Soper NJ, et al. Esophagogastric junction distensibility after fundoplication assessed with a novel functional luminal imaging probe. J Gastrointest Surg Off J Soc Surg Aliment Tract. 2010;14(2):268–76. doi: 10.1007/s11605-009-1086-1.CrossRefGoogle Scholar
  95. 95.
    Villadsen GE, Storkholm J, Zachariae H, et al. Oesophageal pressure-cross-sectional area distributions and secondary peristalsis in relation to subclassification of systemic sclerosis. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2001;13(3):199–210.CrossRefGoogle Scholar
  96. 96.•
    Gregersen H, Villadsen GE, Liao D. Mechanical characteristics of distension-evoked peristaltic contractions in the esophagus of systemic sclerosis patients. Dig Dis Sci. 2011;56(12):3559–68. doi: 10.1007/s10620-011-1777-9. A device that measures cross-sectional area and pressure during intraesophageal distension was utilized in 11 SSc patients and measured increased esophageal wall stiffness and impaired muscle function. These findings were associated with SSc disease duration.PubMedCrossRefGoogle Scholar
  97. 97.
    Krishnan K, Lin CY, Keswani R, et al. Endoscopic ultrasound as an adjunctive evaluation in patients with esophageal motor disorders subtyped by high-resolution manometry. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2014;26(8):1172–8. doi: 10.1111/nmo.12379.CrossRefGoogle Scholar
  98. 98.
    Zuber-Jerger I, Muller A, Kullmann F, et al. Gastrointestinal manifestation of systemic sclerosis—thickening of the upper gastrointestinal wall detected by endoscopic ultrasound is a valid sign. Rheumatology (Oxford). 2010;49(2):368–72. doi: 10.1093/rheumatology/kep381.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Dustin A. Carlson
    • 1
  • Monique Hinchcliff
    • 2
  • John E. Pandolfino
    • 1
  1. 1.Feinberg School of Medicine, Department of Medicine, Division of Gastroenterology and HepatologyNorthwestern UniversityChicagoUSA
  2. 2.Feinberg School of Medicine, Department of Medicine, Division of RheumatologyNorthwestern UniversityChicagoUSA

Personalised recommendations