Clinical Assessment of Gastrointestinal Involvement in Patients with Systemic Sclerosis Approach to gastrointestinal disease in scleroderma

Main Article Content

Timothy Kaniecki, MD Tsion Abdi, MD Zsuzsanna H. McMahan, MD, MHS

Abstract

Systemic sclerosis (SSc) is an autoimmune connective tissue disease that negatively impacts the function of the skin and internal organs. The gastrointestinal (GI) tract is the most commonly affected internal organ in SSc, though GI complications may also arise indirectly when infections occur in the setting of immunosuppression or concurrent disease processes arise for which patients with SSc are found to be at higher risk.  In this review, we provide a systematic approach for the clinical assessment of GI complications in SSc from the oropharynx to the anorectum to guide both general internists and rheumatologists caring for this complex patient population. It is organized so that each component of the luminal GI tract has its own specified section, beginning with a review of a clinical approach to diagnosis, followed by a more detailed discussion of the literature surrounding approaches for an objective GI evaluation. A focused discussion early in the manuscript addressing what is known about pathogenesis, and later about in the manuscript about the assessment for GI bleeding are also included.

Keywords: systemic sclerosis, scleroderma, clinical, gastrointestinal

Article Details

How to Cite
KANIECKI, Timothy; ABDI, Tsion; MCMAHAN, Zsuzsanna H.. Clinical Assessment of Gastrointestinal Involvement in Patients with Systemic Sclerosis. Medical Research Archives, [S.l.], v. 8, n. 10, oct. 2020. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/2252>. Date accessed: 23 apr. 2024. doi: https://doi.org/10.18103/mra.v8i10.2252.
Section
Research Articles

References

1. Yang H, Xu D, Li MT, et al. Gastrointestinal manifestations on impaired quality of life in systemic sclerosis. J Dig Dis. 2019;20(5):256-261.
2. Kroner PT, Tolaymat OA, Bowman AW, Abril A, Lacy BE. Gastrointestinal manifestations of rheumatological diseases. Am J Gastroenterol. 2019;114(9):1441-1454.
3. Kowal-Bielecka O, Fransen J, Avouac J, et al. Update of EULAR recommendations for the treatment of systemic sclerosis. Ann Rheum Dis. 2017;76(8):1327-1339.
4. Shreiner AB, Murray C, Denton C, Khanna D. Gastrointestinal manifestations of systemic sclerosis. J Scleroderma Relat Disord. 2016;1(3):247-256.
5. Gyger G, Baron M. Systemic sclerosis: Gastrointestinal disease and its management. Rheum Dis Clin North Am. 2015;41(3):459-473.
6. Kumar S, Singh J, Rattan S, DiMarino AJ, Cohen S, Jimenez SA. Review article: Pathogenesis and clinical manifestations of gastrointestinal involvement in systemic sclerosis. Aliment Pharmacol Ther. 2017;45(7):883-898.
7. Roberts CG, Hummers LK, Ravich WJ, Wigley FM, Hutchins GM. A case-control study of the pathology of oesophageal disease in systemic sclerosis (scleroderma). Gut. 2006;55(12):1697-1703.
8. Pattanaik D, Brown M, Postlethwaite BC, Postlethwaite AE. Pathogenesis of systemic sclerosis. Front Immunol. 2015;6:272.
9. Distler O, Assassi S, Cottin V, et al. Predictors of progression in systemic sclerosis patients with interstitial lung disease. Eur Respir J. 2020;55(5):1902026. doi: 10.1183/13993003.02026-2019. Print 2020 May.
10. Goldblatt F, Gordon TP, Waterman SA. Antibody-mediated gastrointestinal dysmotility in scleroderma. Gastroenterology. 2002;123(4):1144-1150.
11. Rose S, Young MA, Reynolds JC. Gastrointestinal manifestations of scleroderma. Gastroenterol Clin North Am. 1998;27(3):563-594.
12. Cohen S, Fisher R, Lipshutz W, Turner R, Myers A, Schumacher R. The pathogenesis of esophageal dysfunction in scleroderma and raynaud's disease. J Clin Invest. 1972;51(10):2663-2668.
13. Willerson JT, Thompson RH, Hookman P, Herdt J, Decker JL. Reserpine in raynaud's disease and phenomenon. short-term response to intra-arterial injection. Ann Intern Med. 1970;72(1):17-27.
14. Shah AA, Wigley FM. Often forgotten manifestations of systemic sclerosis. Rheum Dis Clin North Am. 2008;34(1):221-38; ix.
15. Malandrini A, Selvi E, Villanova M, et al. Autonomic nervous system and smooth muscle cell involvement in systemic sclerosis: Ultrastructural study of 3 cases. J Rheumatol. 2000;27(5):1203-1206.
16. Bali V, Dabra S, Behl AB, Bali R. A rare case of hidebound disease with dental implications. Dent Res J (Isfahan). 2013;10(4):556-561.
17. McFarlane IM, Bhamra MS, Kreps A, et al. Gastrointestinal manifestations of systemic sclerosis. Rheumatology (Sunnyvale). 2018;8(1):10.4172/2161-1149.1000235. Epub 2018 Mar 30.
18. Wood RE, Lee P. Analysis of the oral manifestations of systemic sclerosis (scleroderma). Oral Surg Oral Med Oral Pathol. 1988;65(2):172-178.
19. Avouac J, Sordet C, Depinay C, et al. Systemic sclerosis-associated sjogren's syndrome and relationship to the limited cutaneous subtype: Results of a prospective study of sicca syndrome in 133 consecutive patients. Arthritis Rheum. 2006;54(7):2243-2249.
20. Eversole LR, Jacobsen PL, Stone CE. Oral and gingival changes in systemic sclerosis (scleroderma). J Periodontol. 1984;55(3):175-178.
21. Baron M, Hudson M, Tatibouet S, et al. Relationship between disease characteristics and orofacial manifestations in systemic sclerosis: Canadian systemic sclerosis oral health study III. Arthritis Care Res (Hoboken). 2015;67(5):681-690.
22. Zalewska A, Knaś M, Gińdzieńska-Sieśkiewicz E, et al. Salivary antioxidants in patients with systemic sclerosis. J Oral Pathol Med. 2014;43(1):61-68.
23. Isola G, Williams RC, Lo Gullo A, et al. Risk association between scleroderma disease characteristics, periodontitis, and tooth loss. Clin Rheumatol. 2017;36(12):2733-2741.
24. Baron M, Hudson M, Tatibouet S, et al. The canadian systemic sclerosis oral health study: Orofacial manifestations and oral health-related quality of life in systemic sclerosis compared with the general population. Rheumatology (Oxford). 2014;53(8):1386-1394.
25. Andonopoulos AP, Drosos AA, Skopouli FN, Moutsopoulos HM. Sjögren's syndrome in rheumatoid arthritis and progressive systemic sclerosis. A comparative study. Clin Exp Rheumatol. 1989;7(2):203-205.
26. Yuen HK, Hant FN, Hatfield C, Summerlin LM, Smith EA, Silver RM. Factors associated with oral hygiene practices among adults with systemic sclerosis. Int J Dent Hyg. 2014;12(3):180-186.
27. Pizzo G, Scardina GA, Messina P. Effects of a nonsurgical exercise program on the decreased mouth opening in patients with systemic scleroderma. Clin Oral Investig. 2003;7(3):175-178.
28. Yuen HK, Nelson SL. Test--retest reliability of oral health impact profile (OHIP-49) in adults with systemic sclerosis. Spec Care Dentist. 2014;34(1):27-33.
29. Salliot C, Mouthon L, Ardizzone M, et al. Sjogren's syndrome is associated with and not secondary to systemic sclerosis. Rheumatology (Oxford). 2007;46(2):321-326.
30. Paik JJ. Muscle disease in scleroderma. Curr Opin Rheumatol. 2018;30(6):576-580.
31. Suresh E, Wimalaratna S. Proximal myopathy: Diagnostic approach and initial management. Postgrad Med J. 2013;89(1054):470-477.
32. Zivković SA, Medsger TA,Jr. Myasthenia gravis and scleroderma: Two cases and a review of the literature. Clin Neurol Neurosurg. 2007;109(4):388-391.
33. Bohlmeyer TJ, Wu AH, Perryman MB. Evaluation of laboratory tests as a guide to diagnosis and therapy of myositis. Rheum Dis Clin North Am. 1994;20(4):845-856.
34. Shapiro J, Martin S, DeGirolami U, Goyal R. Inflammatory myopathy causing pharyngeal dysphagia: A new entity. Ann Otol Rhinol Laryngol. 1996;105(5):331-335.
35. Tetreault MP, Kahrilas P. GI manifestations with a focus on the esophagus: Recent progress in understanding pathogenesis. Curr Rheumatol Rep. 2019;21(8):42-019-0841-x.
36. Denaxas K, Ladas SD, Karamanolis GP. Evaluation and management of esophageal manifestations in systemic sclerosis. Ann Gastroenterol. 2018;31(2):165-170.
37. Abonia JP, Wen T, Stucke EM, et al. High prevalence of eosinophilic esophagitis in patients with inherited connective tissue disorders. J Allergy Clin Immunol. 2013;132(2):378-386.
38. Frech TM, Boynton K, Downs-Kelly E, Jones B, Kriesel JD, Peterson K. Eosinophilic esophagitis in two patients with systemic sclerosis. Case Rep Rheumatol. 2016;2016:6410421.
39. Domsic R, Fasanella K, Bielefeldt K. Gastrointestinal manifestations of systemic sclerosis. Dig Dis Sci. 2008;53(5):1163-1174.
40. 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.
41. Abu-Shakra M, Guillemin F, Lee P. Gastrointestinal manifestations of systemic sclerosis. Semin Arthritis Rheum. 1994;24(1):29-39.
42. Maddern GJ, Horowitz M, Jamieson GG, Chatterton BE, Collins PJ, Roberts-Thomson P. Abnormalities of esophageal and gastric emptying in progressive systemic sclerosis. Gastroenterology. 1984;87(4):922-926.
43. Marie I, Levesque H, Ducrotté P, et al. Gastric involvement in systemic sclerosis: A prospective study. Am J Gastroenterol. 2001;96(1):77-83.
44. Rocha GA, Queiroz DM, Mendes EN, Barbosa AJ, Lima Júnior GF, Oliveira CA. Helicobacter pylori acute gastritis: Histological, endoscopical, clinical, and therapeutic features. Am J Gastroenterol. 1991;86(11):1592-1595.
45. Yuan W, Li Y, Yang K, et al. Iron deficiency anemia in helicobacter pylori infection: Meta-analysis of randomized controlled trials. Scand J Gastroenterol. 2010;45(6):665-676.
46. Mwafy SN, Afana WM. Hematological parameters, serum iron and vitamin B(12) levels in hospitalized palestinian adult patients infected with helicobacter pylori: A case-control study. Hematol Transfus Cell Ther. 2018;40(2):160-165.
47. Yong WC, Upala S, Sanguankeo A. Helicobacter pylori infection in systemic sclerosis: A systematic review and meta-analysis of observational studies. Clin Exp Rheumatol. 2018;36 Suppl 113(4):168-174.
48. Radić M, Martinović Kaliterna D, Bonacin D, Morović Vergles J, Radić J. Correlation between helicobacter pylori infection and systemic sclerosis activity. Rheumatology (Oxford). 2010;49(9):1784-1785.
49. Magen E, Delgado JS. Helicobacter pylori and skin autoimmune diseases. World J Gastroenterol. 2014;20(6):1510-1516.
50. Iwakiri K, Kinoshita Y, Habu Y, et al. Evidence-based clinical practice guidelines for gastroesophageal reflux disease 2015. J Gastroenterol. 2016;51(8):751-767.
51. Carlson DA, Hinchcliff M, Pandolfino JE. Advances in the evaluation and management of esophageal disease of systemic sclerosis. Curr Rheumatol Rep. 2015;17(1):475-014-0475-y.
52. Thonhofer R, Siegel C, Trummer M, Graninger W. Early endoscopy in systemic sclerosis without gastrointestinal symptoms. Rheumatol Int. 2012;32(1):165-168.
53. Marie I, Ducrotte P, Denis P, Hellot MF, Levesque H. Oesophageal mucosal involvement in patients with systemic sclerosis receiving proton pump inhibitor therapy. Aliment Pharmacol Ther. 2006;24(11-12):1593-1601.
54. Wang KK, Sampliner RE, Practice Parameters Committee of the American College of Gastroenterology. Updated guidelines 2008 for the diagnosis, surveillance and therapy of barrett's esophagus. Am J Gastroenterol. 2008;103(3):788-797.
55. Gyawali CP, Azagury DE, Chan WW, et al. Nonerosive reflux disease: Clinical concepts. Ann N Y Acad Sci. 2018;1434(1):290-303.
56. Fisichella PM, Reder NP, Gagermeier J, Kovacs EJ. Usefulness of pH monitoring in predicting the survival status of patients with scleroderma awaiting lung transplantation. J Surg Res. 2014;189(2):232-237.
57. Gyawali CP, de Bortoli N, Clarke J, et al. Indications and interpretation of esophageal function testing. Ann N Y Acad Sci. 2018;1434(1):239-253.
58. Savarino E, de Bortoli N, Bellini M, et al. Practice guidelines on the use of esophageal manometry - A GISMAD-SIGE-AIGO medical position statement. Dig Liver Dis. 2016;48(10):1124-1135.
59. Khashab MA, Vela MF, Thosani N, et al. ASGE guideline on the management of achalasia. Gastrointest Endosc. 2020;91(2):213-227.e6.
60. Liu LWC, Andrews CN, Armstrong D, et al. Clinical practice guidelines for the assessment of uninvestigated esophageal dysphagia. J Can Assoc Gastroenterol. 2018;1(1):5-19.
61. Jung HK, Hong SJ, Lee OY, et al. 2019 seoul consensus on esophageal achalasia guidelines. J Neurogastroenterol Motil. 2020;26(2):180-203.
62. Fox MR, Bredenoord AJ. Oesophageal high-resolution manometry: Moving from research into clinical practice. Gut. 2008;57(3):405-423.
63. Klingler PJ, Hinder RA, Wetscher GJ, et al. Accurate placement of the esophageal pH electrode for 24-hour pH monitoring using a combined pH/manometry probe. Am J Gastroenterol. 2000;95(4):906-909.
64. Carlson DA, Kahrilas PJ, Lin Z, et al. Evaluation of esophageal motility utilizing the functional lumen imaging probe. Am J Gastroenterol. 2016;111(12):1726-1735.
65. 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(8):1157-1165.
66. Aggarwal N, Lopez R, Gabbard S, Wadhwa N, Devaki P, Thota PN. Spectrum of esophageal dysmotility in systemic sclerosis on high-resolution esophageal manometry as defined by chicago classification. Dis Esophagus. 2017;30(12):1-6.
67. Luciano L, Granel B, Bernit E, et al. Esophageal and anorectal involvement in systemic sclerosis: A systematic assessment with high resolution manometry. Clin Exp Rheumatol. 2016;34 Suppl 100(5):63-69.
68. Roman S, Hot A, Fabien N, et al. Esophageal dysmotility associated with systemic sclerosis: A high-resolution manometry study. Dis Esophagus. 2011;24(5):299-304.
69. Raja J, Ng CT, Sujau I, Chin KF, Sockalingam S. High-resolution oesophageal manometry and 24-hour impedance-pH study in systemic sclerosis patients: Association with clinical features, symptoms and severity. Clin Exp Rheumatol. 2016;34 Suppl 100(5):115-121.
70. Ogliari C, Piazza O Sed N, Vecchi M. High resolution manometry in scleroderma patients. Clin Gastroenterol Hepatol. 2017;15(10):1640-1641.
71. Camilleri M, Parkman HP, Shafi MA, Abell TL, Gerson L, American College of Gastroenterology. Clinical guideline: Management of gastroparesis. Am J Gastroenterol. 2013;108(1):18-37; quiz 38.
72. Miller JB, Gandhi N, Clarke J, McMahan Z. Gastrointestinal involvement in systemic sclerosis: An update. J Clin Rheumatol. 2018;24(6):328-337.
73. Ghoos YF, Maes BD, Geypens BJ, et al. Measurement of gastric emptying rate of solids by means of a carbon-labeled octanoic acid breath test. Gastroenterology. 1993;104(6):1640-1647.
74. Reinauer S, Goerz G, Ruzicka T, Susanto F, Humfeld S, Reinauer H. Helicobacter pylori in patients with systemic sclerosis: Detection with the 13C-urea breath test and eradication. Acta Derm Venereol. 1994;74(5):361-363.
75. Wang YK, Kuo FC, Liu CJ, et al. Diagnosis of helicobacter pylori infection: Current options and developments. World J Gastroenterol. 2015;21(40):11221-11235.
76. Marie I, Levesque H, Ducrotté P, et al. Manometry of the upper intestinal tract in patients with systemic sclerosis: A prospective study. Arthritis Rheum. 1998;41(10):1874-1883.
77. Chander Roland B, Mullin GE, Passi M, et al. A prospective evaluation of ileocecal valve dysfunction and intestinal motility derangements in small intestinal bacterial overgrowth. Dig Dis Sci. 2017;62(12):3525-3535.
78. Sawadpanich K, Soison P, Chunlertrith K, et al. Prevalence and associated factors of small intestinal bacterial overgrowth among systemic sclerosis patients. Int J Rheum Dis. 2019;22(4):695-699.
79. Sakkas LI, Simopoulou T, Daoussis D, Liossis SN, Potamianos S. Intestinal involvement in systemic sclerosis: A clinical review. Dig Dis Sci. 2018;63(4):834-844.
80. Sjogren RW. Gastrointestinal motility disorders in scleroderma. Arthritis Rheum. 1994;37(9):1265-1282.
81. Marie I, Ducrotté P, Denis P, Hellot MF, Levesque H. Outcome of small-bowel motor impairment in systemic sclerosis--a prospective manometric 5-yr follow-up. Rheumatology (Oxford). 2007;46(1):150-153.
82. Rao SS, Camilleri M, Hasler WL, et al. Evaluation of gastrointestinal transit in clinical practice: Position paper of the american and european neurogastroenterology and motility societies. Neurogastroenterol Motil. 2011;23(1):8-23.
83. Quigley EM. Small intestinal bacterial overgrowth: What it is and what it is not. Curr Opin Gastroenterol. 2014;30(2):141-146.
84. Shah SC, Day LW, Somsouk M, Sewell JL. Meta-analysis: Antibiotic therapy for small intestinal bacterial overgrowth. Aliment Pharmacol Ther. 2013;38(8):925-934.
85. Quigley EM, Murray JA, Pimentel M. AGA clinical practice update on small intestinal bacterial overgrowth: Expert review. Gastroenterology. 2020.
86. Caimmi C, Caramaschi P, Venturini A, et al. Malnutrition and sarcopenia in a large cohort of patients with systemic sclerosis. Clin Rheumatol. 2018;37(4):987-997.
87. Baron M, Hudson M, Steele R, Canadian Scleroderma Research Group. Malnutrition is common in systemic sclerosis: Results from the canadian scleroderma research group database. J Rheumatol. 2009;36(12):2737-2743.
88. Stratton RJ, Hackston A, Longmore D, et al. Malnutrition in hospital outpatients and inpatients: Prevalence, concurrent validity and ease of use of the 'malnutrition universal screening tool' ('MUST') for adults. Br J Nutr. 2004;92(5):799-808.
89. Codullo V, Cereda E, Crepaldi G, et al. Disease-related malnutrition in systemic sclerosis: Evidences and implications. Clin Exp Rheumatol. 2015;33(4 Suppl 91):S190-4.
90. Rosato E, Gigante A, Gasperini ML, et al. Nutritional status measured by BMI is impaired and correlates with left ventricular mass in patients with systemic sclerosis. Nutrition. 2014;30(2):204-209.
91. Krause L, Becker MO, Brueckner CS, et al. Nutritional status as marker for disease activity and severity predicting mortality in patients with systemic sclerosis. Ann Rheum Dis. 2010;69(11):1951-1957.
92. Cederholm T, Barazzoni R, Austin P, et al. ESPEN guidelines on definitions and terminology of clinical nutrition. Clin Nutr. 2017;36(1):49-64.
93. Dupont R, Longué M, Galinier A, et al. Impact of micronutrient deficiency & malnutrition in systemic sclerosis: Cohort study and literature review. Autoimmun Rev. 2018;17(11):1081-1089.
94. Emmanuel A. Current management of the gastrointestinal complications of systemic sclerosis. Nat Rev Gastroenterol Hepatol. 2016;13(8):461-472.
95. Baron M, Bernier P, Côté LF, et al. Screening and therapy for malnutrition and related gastro-intestinal disorders in systemic sclerosis: Recommendations of a north american expert panel. Clin Exp Rheumatol. 2010;28(2 Suppl 58):S42-6.
96. Brandler JB, Sweetser S, Khoshbin K, Babameto M, Prokop LJ, Camilleri M. Colonic manifestations and complications are relatively under-reported in systemic sclerosis: A systematic review. Am J Gastroenterol. 2019;114(12):1847-1856.
97. Vischio J, Matlyuk-Urman Z, Lakshminarayanan S. Benign spontaneous pneumoperitoneum in systemic sclerosis. J Clin Rheumatol. 2010;16(8):379-381.
98. Wu LL, Yang YS, Dou Y, Liu QS. A systematic analysis of pneumatosis cystoids intestinalis. World J Gastroenterol. 2013;19(30):4973-4978.
99. Morris MS, Gee AC, Cho SD, et al. Management and outcome of pneumatosis intestinalis. Am J Surg. 2008;195(5):679-82; discussion 682-3.
100. Kaneko M, Sasaki S, Teruya S, et al. Pneumatosis cystoides intestinalis in patients with systemic sclerosis: A case report and review of 39 japanese cases. Case Rep Gastrointest Med. 2016;2016:2474515.
101. Wang SJ, Lan JL, Chen DY, Chen YH, Hsieh TY, Lin WY. Colonic transit disorders in systemic sclerosis. Clin Rheumatol. 2001;20(4):251-254.
102. Rao SS, Rattanakovit K, Patcharatrakul T. Diagnosis and management of chronic constipation in adults. Nat Rev Gastroenterol Hepatol. 2016;13(5):295-305.
103. Staller K, Barshop K, Ananthakrishnan AN, Kuo B. Number of retained radiopaque markers on a colonic transit study does not correlate with symptom severity or quality of life in chronic constipation. Neurogastroenterol Motil. 2018;30(5):e13269.
104. Sattar B, Chokshi RV. Colonic and anorectal manifestations of systemic sclerosis. Curr Gastroenterol Rep. 2019;21(7):33-019-0699-0.
105. Trezza M, Krogh K, Egekvist H, Bjerring P, Laurberg S. Bowel problems in patients with systemic sclerosis. Scand J Gastroenterol. 1999;34(4):409-413.
106. Heyt GJ, Oh MK, Alemzadeh N, et al. Impaired rectoanal inhibitory response in scleroderma (systemic sclerosis): An association with fecal incontinence. Dig Dis Sci. 2004;49(6):1040-1045.
107. Thoua NM, Abdel-Halim M, Forbes A, Denton CP, Emmanuel AV. Fecal incontinence in systemic sclerosis is secondary to neuropathy. Am J Gastroenterol. 2012;107(4):597-603.
108. Jorge JM, Wexner SD. Anorectal manometry: Techniques and clinical applications. South Med J. 1993;86(8):924-931.
109. Deen KI, Premaratna R, Fonseka MM, De Silva HJ. The recto-anal inhibitory reflex: Abnormal response in diabetics suggests an intrinsic neuroenteropathy. J Gastroenterol Hepatol. 1998;13(11):1107-1110.
110. Zhang HW, Han XD, Wang Y, Zhang P, Jin ZM. Anorectal functional outcome after repeated transanal endoscopic microsurgery. World J Gastroenterol. 2012;18(40):5807-5811.
111. Wald A. Clinical practice. fecal incontinence in adults. N Engl J Med. 2007;356(16):1648-1655.
112. Yamaguchi K, Iwakiri R, Hara M, et al. Reflux esophagitis and helicobacter pylori infection in patients with scleroderma. Intern Med. 2008;47(18):1555-1559.
113. Fuccio L, Mussetto A, Laterza L, Eusebi LH, Bazzoli F. Diagnosis and management of gastric antral vascular ectasia. World J Gastrointest Endosc. 2013;5(1):6-13.
114. Marie I, Ducrotte P, Antonietti M, Herve S, Levesque H. Watermelon stomach in systemic sclerosis: Its incidence and management. Aliment Pharmacol Ther. 2008;28(4):412-421.
115. Hung EW, Mayes MD, Sharif R, et al. Gastric antral vascular ectasia and its clinical correlates in patients with early diffuse systemic sclerosis in the SCOT trial. J Rheumatol. 2013;40(4):455-460.
116. Parrado RH, Lemus HN, Coral-Alvarado PX, Quintana López G. Gastric antral vascular ectasia in systemic sclerosis: Current concepts. Int J Rheumatol. 2015;2015:762546.
117. Ingraham KM, O'Brien MS, Shenin M, Derk CT, Steen VD. Gastric antral vascular ectasia in systemic sclerosis: Demographics and disease predictors. J Rheumatol. 2010;37(3):603-607.
118. Khanlou H, Malhotra A, Friedenberg F, Rothstein K. Jejunal telangiectasias as a cause of massive bleeding in a patient with scleroderma. Rev Rhum Engl Ed. 1999;66(2):119-121.
119. Marie I, Antonietti M, Houivet E, et al. Gastrointestinal mucosal abnormalities using videocapsule endoscopy in systemic sclerosis. Aliment Pharmacol Ther. 2014;40(2):189-199.
120. Ko CW, Siddique SM, Patel A, et al. AGA clinical practice guidelines on the gastrointestinal evaluation of iron deficiency anemia. Gastroenterology. 2020.
121. Otani K, Watanabe T, Shimada S, et al. Clinical utility of capsule endoscopy and double-balloon enteroscopy in the management of obscure gastrointestinal bleeding. Digestion. 2018;97(1):52-58.