Relationship between esophageal motility abnormalities and skin or lung involvements in patients with systemic sclerosis

  • Shiko KuribayashiEmail author
  • Sei-ichiro Motegi
  • Kenichiro Hara
  • Yasuyuki Shimoyama
  • Hiroko Hosaka
  • Akiko Sekiguchi
  • Kouichi Yamaguchi
  • Osamu Kawamura
  • Takeshi Hisada
  • Osamu Ishikawa
  • Motoyasu Kusano
  • Toshio Uraoka
Original Article—Alimentary Tract



Esophageal motility abnormalities (EMAs) and interstitial lung diseases (ILDs) are often seen in patients with systemic sclerosis (SSc). Gastroesophageal reflux disease (GERD) could be associated with ILDs, but it is not fully understood if ILDs are caused by GERD or SSc itself.


A total of 109 patients with SSc who underwent high-resolution manometry were enrolled. Esophageal motility was diagnosed with the Chicago classification v3.0. The severity of skin thickness was evaluated by the modified Rodnan total skin thickness score (mRSS). The severity of ILDs was assessed with the chest high-resolution computer tomography (HRCT) scoring system. Relationships between EMAs, GERD, autoantibodies, skin thickness and ILDs were evaluated.


44 patients had normal esophageal motility, eight had esophago-gastric junction outflow obstruction, one had distal esophageal spasm, 27 had ineffective esophageal motility and 29 had absent contractility (AC). Patients with AC had more GERD than those with normal esophageal motility (p < 0.05). The mRSS score in patients with AC was significantly higher than that in those with normal esophageal motility (p < 0.05). The HRCT score in patients with AC tended to be higher than that in those with normal esophageal motility (p = 0.05). A multivariable analysis showed that severe skin thickness was a significant predictor of AC. GERD was not a significant predictor for ILDs.


There were significant correlations between EMAs and severe skin thickness. GERD is not an etiology of ILDs.


Systemic sclerosis Esophageal motility abnormalities Gastroesophageal reflux disease Interstitial lung disease 



The authors thank Prof. Kunihiko Hayashi and Prof. Mitsuo Uchida who contributed statistical analyses. The English language was reviewed by a native English speaker (NAI Inc., Tokyo, Japan).

Author contributions

SK is responsible for study concept and design, acquisition of data, analysis and interpretation of data, drafting of the manuscript, statistical analysis, obtained funding. SM and KH are responsible for study concept and design, acquisition of data, interpretation of data, and critical revision of the manuscript. YS, HH, AS and KY are responsible for acquisition of data. OK, MK, TH, OI and TU are responsible for study supervision.


This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI for Early Career Scientists Grant Number JP18K15772.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (DOCX 19 kb)
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Supplementary material 2 (DOCX 18 kb)
535_2019_1578_MOESM3_ESM.docx (18 kb)
Supplementary material 3 (DOCX 17 kb)


  1. 1.
    Matsuzaki T, Sugiyama T, Sekiguchi T, et al. Reflux esophagitis in progressive systemic sclerosis. (1) Nocturnal gastroesophageal motility in recumbent position. Nihon Shokakibyo Gakkai zasshi Jpn J Gastroenterol. 1983;80:2329–38.Google Scholar
  2. 2.
    Marie I, Dominique S, Levesque H, et al. Esophageal involvement and pulmonary manifestations in systemic sclerosis. Arthritis Rheum. 2001;45:346–54.CrossRefGoogle Scholar
  3. 3.
    Matsuzaki T, Sugiyama T, Sekiguchi T, et al. A study on reflux esophagitis in progressive systemic sclerosis (PSS): second report. Nocturnal gastroesophageal motility and esophageal pH in supine position. Nihon Shokakibyo Gakkai zasshi Jpn J Gastroenterol. 1985;82:1300–7.Google Scholar
  4. 4.
    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;24:1593–601.CrossRefGoogle Scholar
  5. 5.
    Roman S, Hot A, Fabien N, et al. Esophageal dysmotility associated with systemic sclerosis: a high-resolution manometry study. Dis Esophagus. 2011;24:299–304.CrossRefGoogle Scholar
  6. 6.
    Tang DM, Pathikonda M, Harrison M, et al. Symptoms and esophageal motility based on phenotypic findings of scleroderma. Dis Esophagus. 2013;26:197–203.CrossRefGoogle Scholar
  7. 7.
    Crowell MD, Umar SB, Griffing WL, et al. Esophageal motor abnormalities in patients with scleroderma: heterogeneity, risk factors, and effects on quality of life. Clin Gastroenterol Hepatol. 2017;15(207–13):e1.Google Scholar
  8. 8.
    Kimmel JN, Carlson DA, Hinchcliff M, et al. The association between systemic sclerosis disease manifestations and esophageal high-resolution manometry parameters. Neurogastroenterol Motil. 2016;28:1157–65.CrossRefGoogle Scholar
  9. 9.
    Lahcene M, Oumnia N, Matougui N, et al. Esophageal involvement in scleroderma: clinical, endoscopic, and manometric features. ISRN Rheumatol. 2011;2011:325826.CrossRefGoogle Scholar
  10. 10.
    Garrett JM, Winkelmann RK, Schlegel JF, et al. Esophageal deterioration in scleroderma. Mayo Clin Proc. 1971;46:92–6.Google Scholar
  11. 11.
    Harrison NK, Myers AR, Corrin B, et al. Structural features of interstitial lung disease in systemic sclerosis. Am Rev Respir Dis. 1991;144:706–13.CrossRefGoogle Scholar
  12. 12.
    Young RH, Mark GJ. Pulmonary vascular changes in scleroderma. Am J Med. 1978;64:998–1004.CrossRefGoogle Scholar
  13. 13.
    Yousem SA. The pulmonary pathologic manifestations of the CREST syndrome. Hum Pathol. 1990;21:467–74.CrossRefGoogle Scholar
  14. 14.
    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;179:408–13.CrossRefGoogle Scholar
  15. 15.
    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;45:172–80.CrossRefGoogle Scholar
  16. 16.
    Kahrilas PJ, Bredenoord AJ, Fox M, et al. The Chicago classification of esophageal motility disorders, v3.0. Neurogastroenterol Motil. 2015;27:160–74.CrossRefGoogle Scholar
  17. 17.
    Kuribayashi S, Iwakiri K, Kawada A, et al. Variant parameter values-as defined by the Chicago Criteria-produced by ManoScan and a new system with Unisensor catheter. Neurogastroenterol Motil. 2015;27:188–94.CrossRefGoogle Scholar
  18. 18.
    LeRoy EC, Black C, Fleischmajer R, et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol. 1988;15:202–5.Google Scholar
  19. 19.
    Clements PJ, Lachenbruch PA, Seibold JR, et al. Skin thickness score in systemic sclerosis: an assessment of interobserver variability in 3 independent studies. J Rheumatol. 1993;20:1892–6.Google Scholar
  20. 20.
    Ooi GC, Mok MY, Tsang KW, et al. Interstitial lung disease in systemic sclerosis. Acta Radiol. 2003;44:258–64.Google Scholar
  21. 21.
    Galie N, Hoeper MM, Humbert M, et al. Guidelines for the diagnosis and treatment of pulmonary hypertension: the task force for the diagnosis and treatment of pulmonary hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS), endorsed by the International Society of Heart and Lung Transplantation (ISHLT). Eur Heart J. 2009;30:2493–537.CrossRefGoogle Scholar
  22. 22.
    Lee SW, Choi EY, Jung SY, et al. E/E’ ratio is more sensitive than E/A ratio for detection of left ventricular diastolic dysfunction in patients with systemic sclerosis. Clin Exp Rheumatol. 2010;28:S12–7.Google Scholar
  23. 23.
    Carlson DA, Crowell MD, Kimmel JN, et al. Loss of peristaltic reserve, determined by multiple rapid swallows, is the most frequent esophageal motility abnormality in patients with systemic sclerosis. Clin Gastroenterol Hepatol. 2016;14:1502–6.CrossRefGoogle Scholar
  24. 24.
    Fernandez Morales A, Iniesta N, Fernandez-Codina A, et al. Cardiac tamponade and severe pericardial effusion in systemic sclerosis: report of nine patients and review of the literature. Int J Rheum Dis. 2017;20:1582–92.CrossRefGoogle Scholar

Copyright information

© Japanese Society of Gastroenterology 2019

Authors and Affiliations

  • Shiko Kuribayashi
    • 1
    • 2
    Email author
  • Sei-ichiro Motegi
    • 3
  • Kenichiro Hara
    • 4
  • Yasuyuki Shimoyama
    • 2
  • Hiroko Hosaka
    • 2
  • Akiko Sekiguchi
    • 3
  • Kouichi Yamaguchi
    • 4
  • Osamu Kawamura
    • 2
  • Takeshi Hisada
    • 4
  • Osamu Ishikawa
    • 3
  • Motoyasu Kusano
    • 2
  • Toshio Uraoka
    • 2
  1. 1.Clinical Investigation and Research UnitGunma University HospitalMaebashiJapan
  2. 2.Division of Gastroenterology and Hepatology, Integrative Center of Internal MedicineGunma University HospitalMaebashiJapan
  3. 3.Department of DermatologyGunma University Graduate School of MedicineMaebashiJapan
  4. 4.Allergy and Respiratory Medicine, Integrative Center of Internal MedicineGunma University HospitalMaebashiJapan

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