Skip to main content

Advertisement

SpringerLink
Log in

The role of high-resolution manometry in the assessment of upper gastrointestinal involvement in systemic sclerosis: a systematic review

  • Review Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Systemic sclerosis (SSc) affects the upper gastrointestinal (GI) system in 90% of patients. High-resolution manometry (HRM) assesses esophageal dysmotility, but its role in diagnosis and follow-up remains unclear. The objectives of this systematic review were to investigate the role of HRM in the assessment of SSc-associated upper GI involvement and to evaluate the correlation between HRM abnormalities and clinical characteristics and the effects of therapeutic interventions on HRM findings. Fifteen articles were included. Most (11/15) studies were of very good or good quality. Most studies assessed correlations between esophageal symptoms and esophageal dysmotility. Two studies assessed the effectiveness of buspirone and reported HRM findings. Studies assessing upper GI symptoms using validated questionnaires, such as the University of California Scleroderma Clinical Trial Consortium Gastrointestinal Tract 2.0 or Gastrointestinal Symptoms Severity Index score, found an association between absent contractility on HRM and upper GI symptoms, but even asymptomatic patients often have esophageal body dysmotility on HRM. Esophageal dysmotility positively correlates with the presence of interstitial lung disease on high-resolution computed tomography and reduced diffusion capacity (< 0.8 of predicted value). Trials investigating the effect of buspirone demonstrate both increased lower esophageal sphincter resting pressure and reduced upper GI symptoms. Most studies report on limited patient numbers and retrospective data. Potential bias was minimized using quality appraisal. HRM findings correlate to upper GI symptoms when assessed by validated questionnaires and can detect response to therapy in buspirone trials. Esophageal body dysmotility on HRM positively correlates with the presence of interstitial lung disease.

Key Points

• Esophageal body dysmotility on HRM correlates with presence of ILD.

• HRM findings seem to correspond to clinical symptom alleviation in interventional trials, but data are still limited.

• At present HRM, a procedure with a high negative burden to the patient, offers little to no role in the therapeutic strategy.

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

Fig. 1

Similar content being viewed by others

References

  1. Varga J, Trojanowska M, Kuwana M (2017) Pathogenesis of systemic sclerosis: recent insights of molecular and cellular mechanisms and therapeutic opportunities. J Scleroderma Relat Disord 2(3):137–152. https://doi.org/10.5301/jsrd.5000249

    Article  Google Scholar 

  2. Volkmann ER, Tashkin DP, Sim M et al (2018) Determining progression of scleroderma-related interstitial lung disease. J Scleroderma Relat Disord. https://doi.org/10.1177/23971983188169153

  3. Thoua NM, Bunce C, Brough G, Forbes A, Emmanuel AV, Denton CP (2010) Assessment of gastrointestinal symptoms in patients with systemic sclerosis in a UK tertiary referral centre. Rheumatology 49:1770–1775. https://doi.org/10.1093/rheumatology/keq147

    Article  PubMed  Google Scholar 

  4. Schmeiser T, Saar P, Jin D, Noethe M, Müller A, Soydan N, Hardt PD, Jaeger C, Distler O, Roeb E, Bretzel RG, Müller-Ladner U (2012) Profile of gastrointestinal involvement in patients with systemic sclerosis. Rheumatol Int 32:2471–2478. https://doi.org/10.1007/s00296-011-1988-6

    Article  CAS  PubMed  Google Scholar 

  5. Pandolfino JE (2010) High-resolution manometry: is it better for detecting esophageal disease? Gastroenterol Hepatol (N Y) 6:632–634

    Google Scholar 

  6. Carlson DA, Pandolfino JE (2015) High-resolution manometry in clinical practice. Gastroenterol Hepatol (N Y) 11:374–384

    Google Scholar 

  7. Kahrilas PJ, Bredenoord AJ, Fox M, Gyawali CP, Roman S, Smout AJ, Pandolfino JE, International High Resolution Manometry Working Group (2015) The Chicago classification of esophageal motility disorders, v3.0. Neurogastroenterol Motil 27:160–174. https://doi.org/10.1111/nmo.12477

    Article  CAS  PubMed  Google Scholar 

  8. Ogliari C, Sed NPO, Vecchi M (2017) High resolution manometry in scleroderma patients. Clin Gastroenterol Hepatol 15:1640–1641. https://doi.org/10.1016/J.CGH.2017.05.030

    Article  PubMed  Google Scholar 

  9. Forbes A, Marie I (2009) Gastrointestinal complications: the most frequent internal complications of systemic sclerosis. Rheumatology 48:iii36–iii39. https://doi.org/10.1093/rheumatology/ken485

    Article  PubMed  Google Scholar 

  10. Omair MA, Lee P (2012) Effect of gastrointestinal manifestations on quality of life in 87 consecutive patients with systemic sclerosis. J Rheumatol 39:992–996. https://doi.org/10.3899/jrheum.110826

    Article  PubMed  Google Scholar 

  11. Bodukam V, Hays RD, Maranian P et al (2011) Association of gastrointestinal involvement and depressive symptoms in patients with systemic sclerosis. Rheumatology. https://doi.org/10.1093/rheumatology/keq296

    Article  Google Scholar 

  12. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6:e1000100. https://doi.org/10.1371/journal.pmed.1000100

    Article  PubMed  PubMed Central  Google Scholar 

  13. (1980) Subcommittee for scleroderma criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 23:581–90

  14. Van Den Hoogen F, Khanna D, Fransen J et al (2013) 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. https://doi.org/10.1002/art.38098

    Article  Google Scholar 

  15. Lo CK-L, Mertz D, Loeb M (2014) Newcastle-Ottawa Scale: comparing reviewers’ to authors’ assessments. BMC Med Res Methodol 14:45. https://doi.org/10.1186/1471-2288-14-45

    Article  PubMed  PubMed Central  Google Scholar 

  16. Sterne JA, Hernán MA, Reeves BC et al (2016) ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 355:i4919. https://doi.org/10.1136/bmj.i4919

    Article  PubMed  PubMed Central  Google Scholar 

  17. Roman S, Hot A, Fabien N et al (2011) Esophageal dysmotility associated with systemic sclerosis: a high-resolution manometry study. Dis Esophagus. https://doi.org/10.1111/j.1442-2050.2010.01150.x

    Article  Google Scholar 

  18. Tang DM, Pathikonda M, Harrison M et al (2013) Symptoms and esophageal motility based on phenotypic findings of scleroderma. Dis Esophagus. https://doi.org/10.1111/j.1442-2050.2012.01349.x

    Article  Google Scholar 

  19. Kimmel JN, Carlson DA, Hinchcliff M et al (2016) The association between systemic sclerosis disease manifestations and esophageal high-resolution manometry parameters. Neurogastroenterol Motil. https://doi.org/10.1111/nmo.12813

    Article  CAS  Google Scholar 

  20. Carlson DA, Crowell MD, Kimmel JN et al (2016) Loss of peristaltic reserve, determined by multiple rapid swallows, is the most frequent esophageal motility abnormality in patients with systemic sclerosis. Clin Gastroenterol Hepatol. https://doi.org/10.1016/j.cgh.2016.03.039

    Article  Google Scholar 

  21. Luciano L, Granel B, Bernit E et al (2016) Oesophageal and anorectal involvement in systemic sclerosis: a systematic assessment high resolution manometry. Clin Exp Rheumatol

  22. de Carlan M, Lescoat A, Brochard C et al (2017) Association between clinical manifestations of systemic sclerosis and esophageal dysmotility assessed by high-resolution manometry. J Scleroderma Relat Disord. https://doi.org/10.5301/jsrd.5000233

    Article  Google Scholar 

  23. Crowell MD, Umar SB, Griffing WL et al (2017) Esophageal motor abnormalities in patients with scleroderma: heterogeneity, risk factors, and effects on quality of life. Clin Gastroenterol Hepatol. https://doi.org/10.1016/j.cgh.2016.08.034

    Article  Google Scholar 

  24. Abozaid HSM, Imam HMK, Abdelaziz MM et al (2017) High-resolution manometry compared with the University of California, Los Angeles Scleroderma Clinical Trials Consortium GIT 2.0 in Systemic Sclerosis. Semin Arthritis Rheum. https://doi.org/10.1016/j.semarthrit.2017.05.005

    Article  Google Scholar 

  25. Karamanolis GP, Denaxas K, Panopoulos S et al (2017) Severe oesophageal disease and its associations with systemic sclerosis. Clin Exp Rheumatol

  26. Arana-Guajardo AC, Barrera-Torres G, Villarreal-Alarcón MÁ et al (2019) Esophageal symptoms and their lack of association with high-resolution manometry in systemic sclerosis patients. Reumatol Clin. https://doi.org/10.1016/j.reuma.2017.09.005

    Article  Google Scholar 

  27. Aggarwal N, Lopez R, Gabbard S et al (2017) Spectrum of esophageal dysmotility in systemic sclerosis on high-resolution esophageal manometry as defined by Chicago classification. Dis Esophagus. https://doi.org/10.1093/dote/dox067

    Article  CAS  Google Scholar 

  28. Stern EK, Carlson DA, Falmagne S et al (2018) Abnormal esophageal acid exposure on high-dose proton pump inhibitor therapy is common in systemic sclerosis patients. Neurogastroenterol Motil. https://doi.org/10.1111/nmo.13247

    Article  Google Scholar 

  29. Vettori S, Tolone S, Capocotta D, Chieffo R, Giacco V, Valentini G, Docimo L (2018) Esophageal high-resolution impedance manometry alterations in asymptomatic patients with systemic sclerosis: prevalence, associations with disease features, and prognostic value. Clin Rheumatol 37:1239–1247. https://doi.org/10.1007/s10067-018-4026-1

    Article  PubMed  Google Scholar 

  30. Karamanolis GP, Panopoulos S, Karlaftis A et al (2015) Beneficial effect of the 5-HT1A receptor agonist buspirone on esophageal dysfunction associated with systemic sclerosis: a pilot study. United European Gastroenterol J. https://doi.org/10.1177/2050640614560453

    Article  Google Scholar 

  31. Karamanolis GP, Panopoulos S, Denaxas K, Karlaftis A, Zorbala A, Kamberoglou D, Ladas SD, Sfikakis PP (2016) The 5-HT1A receptor agonist buspirone improves esophageal motor function and symptoms in systemic sclerosis: a 4-week, open-label trial. Arthritis Res Ther 18:1–6. https://doi.org/10.1186/s13075-016-1094-y

    Article  CAS  Google Scholar 

  32. Peoples C, Medsger TA, Lucas M et al (2016) Gender differences in systemic sclerosis: relationship to clinical features, serologic status and outcomes. J Scleroderma Relat Disord. https://doi.org/10.5301/jsrd.5000209

    Article  Google Scholar 

  33. Di Stefano M, Papathanasopoulos A, Blondeau K et al (2012) Effect of buspirone, a 5-HT1A receptor agonist, on esophageal motility in healthy volunteers. Dis Esophagus. https://doi.org/10.1111/j.1442-2050.2011.01275.x

    Article  Google Scholar 

  34. Airo P, Della CD, Danieli E et al (2005) Oesophageal manometry in early and definite systemic sclerosis. Clin Rheumatol 24:370–376. https://doi.org/10.1007/s10067-004-1049-6

    Article  PubMed  Google Scholar 

  35. Carlson DA, Kahrilas PJ, Lin Z et al (2016) Evaluation of esophageal motility utilizing the functional lumen imaging probe (FLIP). Am J Gastroenterol. https://doi.org/10.1038/ajg.2016.454

    Article  Google Scholar 

  36. Pitrez EH, Bredemeier M, Xavier RM et al (2006) Oesophageal dysmotility in systemic sclerosis: comparison of HRCT and scintigraphy. Br J Radiol. https://doi.org/10.1259/bjr/17000205

    Article  CAS  Google Scholar 

  37. Sallam H, McNearney TA, Chen JDZ (2006) Systematic review: pathophysiology and management of gastrointestinal dysmotility in systemic sclerosis (scleroderma). Aliment Pharmacol Ther

  38. Hempfling C, Neuhuber WL, Wörl J (2012) Serotonin-immunoreactive neurons and mast cells in the mouse esophagus suggest involvement of serotonin in both motility control and neuroimmune interactions. Neurogastroenterol Motil. https://doi.org/10.1111/j.1365-2982.2011.01797.x

    Article  Google Scholar 

Download references

Funding

Jean-Baptiste Vulsteke holds an FWO SB fellowship and has received support from the Fund Joël Hurlet.

Author information

Author notes

  1. Wouter Schutyser and Ludovic Cruyt contributed equally to this work.

Authors and Affiliations

  1. Faculty of Medicine, KU Leuven, Leuven, Belgium

    Wouter Schutyser & Ludovic Cruyt

  2. Division of Rheumatology, University Hospitals Leuven, Leuven, Belgium

    Jean-Baptiste Vulsteke, Jan L. Lenaerts & Ellen De Langhe

  3. Skeletal Biology and Engineering Research Center, Department of Development and Regeneration, KU Leuven, 3000, Leuven, Belgium

    Jean-Baptiste Vulsteke & Ellen De Langhe

Authors
  1. Wouter Schutyser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ludovic Cruyt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-Baptiste Vulsteke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan L. Lenaerts
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ellen De Langhe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ellen De Langhe.

Ethics declarations

Disclosures

None.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schutyser, W., Cruyt, L., Vulsteke, JB. et al. The role of high-resolution manometry in the assessment of upper gastrointestinal involvement in systemic sclerosis: a systematic review. Clin Rheumatol 39, 149–157 (2020). https://doi.org/10.1007/s10067-019-04794-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-019-04794-w

Keywords

Search

Navigation