Abstract
Background
Scleroderma is a systemic inflammatory disorder that can compromise the gastrointestinal tract in up to 90% of patients.
Aim
The purpose of this work is to characterize esophageal, gastric, and intestinal compromise in patients with scleroderma by means of minimally invasive methods and its association with symptoms and severity of their rheumatological condition.
Methods
Patients with systemic sclerosis were recruited according to the criteria of the American College of Rheumatology. The study of digestive involvement was carried out on four consecutive days: esophageal manometry was performed on the first day, intestinal manometry on the second day, surface electrogastrography on the third, and hydrogen breath test on the fourth. The Mann–Whitney test was used for quantitative variables and the chi-squared test for categorical variables (p < 0.05).
Results
A total of 30 patients were included, with an average age of 52.7 years and 93% women. Average disease evolution duration was 6.5 years, 70% with limited variety. Rodnan averaged 12 points, being higher in the diffuse variety. The main symptom was heartburn, followed by abdominal distension, with no differences between subtypes except for diffuse nausea; 80% had intestinal manometric compromise, 76% esophageal manometric compromise, and 30% electrogastrographic compromise. Bacterial overgrowth was evidenced in two-thirds (66%) of the patients, and 23% of the patients had simultaneous esophageal, gastric, and intestinal involvement, which correlated with greater skin involvement but not with gastrointestinal symptoms.
Conclusions
Gastrointestinal involvement in patients with scleroderma is frequent and is observed regardless of the symptoms and clinical characteristics of the latter, except for skin involvement.
Graphical Abstract
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References
Forbes A, Marie I. Gastrointestinal complications: the most frequent internal complications of systemic sclerosis. Rheumatology 2009;48:36–39.
McFarlane IM, Bhamra MS, Kreps A et al. Gastrointestinal manifestations of systemic sclerosis. Rheumatology (Sunnyvale). 2018;8:235.
Sjogren RW. Gastrointestinal features of scleroderma. Curr Opin Rheumatol 1996;8:569–575.
Cheah JX, Khanna D, McMahan ZH. Management of scleroderma gastrointestinal disease: lights and shadows. J Scleroderma Relat Disord. 2022;7:85–97.
Voulgaris TA, Karamanolis GP. Esophageal manifestation in patients with scleroderma. World J Clin Cases. 2021;9:5408–5419.
Kawaguchi Y, Nakamura Y, Matsumoto I et al. Muscarinic-3 acetylcholine receptor autoantibody in patients with systemic sclerosis: contribution to severe gastrointestinal tract dysmotility. Ann Rheum Dis 2009;68:710–714.
Kirby DF, Chatterjee S. Evaluation and management of gastrointestinal manifestations in scleroderma. Curr Opin Rheumatol 2014;26:621–629.
Cheah JX, Perin J, Volkmann ER, Hummers LK, Pasricha PJ, Wigley FM, McMahan ZH. Slow colonic transit in systemic sclerosis: an objective assessment of risk factors and clinical phenotype. Arthritis Care Res (Hoboken). 2021. https://doi.org/10.1002/acr.24767.
Assassi S, Fritzler MJ, Arnett FC et al. Primary biliary cirrhosis (PBC), PBC autoantibodies, and hepatic parameter abnormalities in a large population of systemic sclerosis patients. J Rheumatol 2009;36:2250–2256.
Van der Hoogen F, Khanna D, Franseen J et al. 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 2013;72:1747–1755.
Khanna D, Furst D, Clements P et al. Standardization of the modified Rodnan skin score for use in clinical trials of systemic sclerosis. Scleroderma Relat Disord. 2017;2:11–18.
Richter JE, Wu WC, Johns DN, Blackwell JN, Nelson JL, Castell JA, Castell DO. Esophageal manometry in 95 healthy adult volunteers. Dig Dis Sci 1987;32:583–592.
Defilippi C, Madrid A, Defilippi C. Cutaneous electrogastrography: a recently incorporated technique for the study of gastric motility. Rev Med Chile 2002;130:1209–1216.
Madrid A, Quera R, Defilippi C. Small intestinal manometry in gastrointestinal disorders. Rev Med Chile 1999;127:1176–1182.
Madrid A, Poniachik J, Quera R, Defilippi C. Small intestinal clustered contractions and bacterial overgrowth: a frequent finding in obese patients. Dig Dis Sci 2011;56:155–160.
Planzer M, Madrid A, Quera R, Defilippi CL, Defilippi C. Tiempo de transito Orocecal (TTOC): influencia del sexo, edad y el sobrecrecimiento bacteriano intestinal. Gastro Latam 2002;12:376.
Thonhofer R, Siegel C, Trummer M et al. Early endoscopy in systemic sclerosis without gastrointestinal symptoms. Rheumatol Int 2012;32:165–168.
Marabotto E, Savarino V, Savarino E. Towards a more precise classification of esophageal motility disorders in patients with systemic sclerosis. Neurogastroenterol Motil 2022;34:e14416.
Vettori S, Tolone S, Capocotta D, Chieffo R, Giacco V, Valentini G, Docimo L. Esophageal high-resolution impedance manometry alterations in asymptomatic patients with systemic sclerosis: prevalence, associations with disease features, and prognostic value. Clin Rheumatol. 2018;37:1239–1247.
Markus J, Pinto RMC, Matoso AGB, Ranza R. Esophageal manometry in systemic sclerosis: findings and association with clinical manifestations. Rev Assoc Med Bras 2020;66:48–54.
Carlson DA, Prescott JE, Germond E et al. Heterogeneity of primary and secondary peristalsis in systemic sclerosis: a new model of “scleroderma esophagus.” Neurogastroenterol Motil. 2022;34:e14284.
Fynne L, Liao D, Aksglaede K et al. Esophagogastric junction in systemic sclerosis: a study with the functional lumen imaging probe. Neurogastroenterol Motil. 2017. https://doi.org/10.1111/nmo.13073.
Adler B, Hummers LK, Pasricha PJ, McMahan ZH. Gastroparesis in systemic sclerosis: a detailed analysis using whole-gut scintigraphy. Rheumatology (Oxford). 2022. https://doi.org/10.1093/rheumatology/keac074.
Assad APL, Farias R, Gaspari CN, da Silva HC, Andrade DCO, Sampaio-Barros PD. Diagnosis and management of gastric antral vascular ectasia: experience in a large single cohort of patients with systemic sclerosis. J Clin Rheumatol. 2020;26:79–81.
McMahan ZH, Domsic RT, Zhu L, Medsger TA, Casciola-Rosen L, Shah AA. Anti-RNPC-3 (U11/U12) antibodies in systemic sclerosis in patients with moderate-to-severe gastrointestinal dysmotility. Arthritis Care Res (Hoboken). 2019;71:1164–1170.
DiRenzo D, Russell J, Bingham CO 3rd, McMahan Z. The relationship between autonomic dysfunction of the gastrointestinal tract and emotional distress in patients with systemic sclerosis. J Clin Rheumatol. 2021;27:11–17.
Jaovisidha K, Csuka ME, Almagro UA et al. Severe gastrointestinal involvement in systemic sclerosis: report of five cases and review of the literature. Semin Arthritis Rheum. 2005;34:689–702.
Szekanecz É, Szamosi S, Horváth Á et al. Malignancies associated with systemic sclerosis. Autoimmun Rev. 2012;11:852–855.
Snyder DL, Crowell MD, Kahn A, Griffing WL, Umar S, Ramirez FC. Prevalence of Barrett’s esophagus in female patients with scleroderma. Am J Gastroenterol. 2021;116:517–521.
Showalter K, Hoffmann A, Richardson C et al. Esophageal dilation and other clinical factors associated with pulmonary function decline in patients with systemic sclerosis. J Rheumatol. 2021;48:1830–1838.
Läubli J, Dobrota R, Maurer B, Jordan S, Misselwitz B, Fox M, Distler O. Impaired micronutrients and prealbumin in patients with established and very early systemic sclerosis. Clin Exp Rheumatol. 2020;125:120–126.
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CM was responsible for drafting the manuscript; LS and AMM for designing the study, collecting data, and drafting the manuscript; and CD and CD for collecting data.
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Patients of legal age who consented and signed an informed consent to participate in this study were included. The data obtained during the controls were entered into Excel without including the names of the patients to protect their confidentiality. This work has the approval of the Scientific Ethics Committee of the Clinical Hospital of the University of Chile.
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Appendix 1: Summary of Clinical Features, Symptoms, and Findings in Consecutive Studies of Patients
Appendix 1: Summary of Clinical Features, Symptoms, and Findings in Consecutive Studies of Patients
Sex; years | Subtype | Heartburn | Dysphagia | Chest pain | Bloating | Nausea | Diarrhea | Constipation | Esophagus | EGG | Small intestine | H2 breath test |
|---|---|---|---|---|---|---|---|---|---|---|---|---|
F; 54 | ScL | + | + | No | + | No | + | No | Abnormal | Abnormal | Abnormal | Normal |
F; 27 | ScL | + | No | No | + | No | No | No | Abnormal | Normal | Abnormal | Normal |
F; 62 | ScL | + | + | No | + | No | + | No | Normal | Normal | Abnormal | SIBO |
F; 35 | ScL | No | + | No | + | No | + | No | Normal | Normal | Abnormal | SIBO |
F; 52 | ScL | + | No | + | + | No | No | + | Normal | Normal | Normal | SIBO |
F; 50 | ScL | + | No | + | No | No | No | No | Abnormal | Normal | Abnormal | Normal |
F; 68 | ScL | + | + | No | + | No | No | No | Abnormal | Normal | Normal | SIBO |
F; 53 | ScL | + | + | No | No | No | No | No | Abnormal | Normal | Abnormal | Normal |
F; 58 | ScL | + | + | No | + | No | No | No | Abnormal | Abnormal | Abnormal | Normal |
F; 69 | ScL | No | No | + | No | No | No | No | Abnormal | Normal | Normal | SIBO |
F; 33 | ScL | + | + | No | + | No | No | No | Abnormal | Normal | Abnormal | SIBO |
F; 69 | ScL | + | + | No | + | No | No | No | Normal | Abnormal | Normal | Normal |
F; 38 | ScL | + | No | + | + | No | No | No | Normal | Normal | Normal | Normal |
F; 73 | ScL | + | + | No | No | No | + | No | Abnormal | Abnormal | Abnormal | SIBO |
F; 46 | ScL | + | No | No | + | + | + | No | Abnormal | Normal | Abnormal | Normal |
M; 21 | ScL | No | No | + | No | No | No | No | Abnormal | Abnormal | Abnormal | SIBO |
F; 51 | ScL | + | + | No | + | No | No | No | Abnormal | Abnormal | Abnormal | SIBO |
F; 46 | ScL | No | No | + | + | No | No | No | Normal | Normal | Abnormal | SIBO |
F; 47 | ScL | No | + | + | No | No | No | No | Abnormal | Normal | Abnormal | Normal |
F; 55 | ScL | + | + | No | + | No | + | No | Abnormal | Normal | Abnormal | SIBO |
F; 40 | ScL | + | + | No | No | No | No | No | Abnormal | Abnormal | Abnormal | SIBO |
F; 53 | ScD | + | + | No | + | No | + | No | Abnormal | Normal | Abnormal | SIBO |
F; 70 | ScD | No | + | + | No | + | + | No | Abnormal | Abnormal | Abnormal | SIBO |
F; 64 | ScD | + | No | No | No | + | No | + | Abnormal | Normal | Abnormal | SIBO |
F; 44 | ScD | + | No | + | No | + | No | No | Abnormal | Normal | Abnormal | SIBO |
F; 49 | ScD | + | + | No | + | + | No | No | Normal | Abnormal | Abnormal | SIBO |
F; 63 | ScD | + | + | No | No | No | No | No | Abnormal | Normal | Abnormal | Normal |
F; 56 | ScD | No | No | + | + | No | + | No | Abnormal | Normal | Normal | SIBO |
F; 68 | ScD | + | + | + | No | No | No | No | Abnormal | Normal | Abnormal | SIBO |
M; 69 | ScD | + | + | + | + | No | No | No | Abnormal | Normal | Abnormal | SIBO |
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von Mühlenbrock, C., Madrid, A., Defilippi, C. et al. Diffuse Gastrointestinal Motor Compromise in Patients with Scleroderma: Utility of Minimally Invasive Techniques. Dig Dis Sci 69, 191–199 (2024). https://doi.org/10.1007/s10620-023-08151-5
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DOI: https://doi.org/10.1007/s10620-023-08151-5