Have a personal or library account? Click to login
Digestive Dysbiosis in Systemic Scleroderma: a Review Cover

Digestive Dysbiosis in Systemic Scleroderma: a Review

Open Access
|Jul 2021

References

  1. 1. McMahan ZH, Hummers LK. Gastrointestinal involvement in systemic sclerosis: diagnosis and management. Curr Opin Rheumatol. 2018;30:533-540.10.1097/BOR.000000000000054530234725
  2. 2. Denaxas K, Ladas SD, Karamanolis GP. Evaluation and management of esophageal manifestations in systemic sclerosis. Ann Gastroenterol. 2018;31:1-6.10.20524/aog.2018.0228582594629507463
  3. 3. Tétreault MP, Kahrilas P. GI Manifestations With a Focus on the Esophagus: Recent Progress in Understanding Pathogenesis. Curr Rheumatol Rep. 2019;21;42.10.1007/s11926-019-0841-x885283831270707
  4. 4. Miller JB, Gandhi N, Clarke J, McMahan Z. Gastrointestinal Involvement in Systemic Sclerosis: An Update. J Clin Rheumatol. 2018;24:328-337.10.1097/RHU.0000000000000626611037729095721
  5. 5. Schmeiser T, Saar P, Jin D, et al. Profile of gastrointestinal involvement in patients with systemic sclerosis. Rheumatol Int. 2012;32:2471-2478.10.1007/s00296-011-1988-621769490
  6. 6. Ferreli C, Gasparini G, Parodi A, Cozzani E, Rongioletti F, Atzori L. Cutaneous Manifestations of Scleroderma and Scleroderma-Like Disorders: a Comprehensive Review. Clinic Rev Allerg Immunol. 2017;53:306-336.10.1007/s12016-017-8625-428712039
  7. 7. Anton E. Current management of the gastrointestinal complications of systemic sclerosis. Nat Rev Gastroenterol Hepatol. 2016;13:461-472.10.1038/nrgastro.2016.9927381075
  8. 8. Lynch S, Pedersen O. The Human Intestinal Microbiome in Health and Disease. N Engl J Med. 2016;375:2369-2379.10.1056/NEJMra160026627974040
  9. 9. Vogelzang A, Guerrini MM, Minato N, Fagarasan S. Microbiota – an amplifier of autoimmunity. Curr Opin Immunol. 2018;55:15-21.10.1016/j.coi.2018.09.00330248521
  10. 10. Tallota R, Atzeni F, Ditto MC, Gerardi MC, Sarzi-Puttini P. The Microbiome in Connective Tissue Diseases and Vasculitides: An Update Narrative Review. J Immunol Res. 2017; 2017:6836498.10.1155/2017/6836498555660928835902
  11. 11. Tong Y, Marion T, Schett G, Luo Y, Liu Y. Microbiota and metabolites in rheumatic diseases. Autoimmun Rev. 2020;19:102530.10.1016/j.autrev.2020.102530
  12. 12. Konig MF. The microbiome in autoimmune rheumatic disease. Best Pract Res Clin Rheumatol. 2020;34:101473.10.1016/j.berh.2019.101473
  13. 13. Asano Y. The Pathogenesis of Systemic Sclerosis: An Understanding Based on a Common Pathologic Cascade across Multiple Organs and Additional Organ-Specific Pathologies. J Clin Med. 2020;9:2687.10.3390/jcm9092687
  14. 14. Frantz C, Avouac J, Distler O, et al. Impaired quality of life in systemic sclerosis and patient perception of the disease: A large international survey. Semin Arthritis Rheum. 2016;46:115-123.10.1016/j.semarthrit.2016.02.005
  15. 15. Smirani R, Poursac N, Naveau A, Schaeverbeke T, Devillard R, Truchetet ME. Orofacial consequences of systemic sclerosis: A systematic review. J Scleroderma Relat Disord. 2018;3:88-90.10.1177/2397198317746966
  16. 16. Hadj Said M, Foletti J, Graillon N, Guyot L, Chossegros C. Orofacial manifestations of scleroderma. A literature review. Rev Stomatol Chir Maxillofac Chir Orale. 2016;117:322-326.
  17. 17. Jung S, Martin T, Schmittbuhl M, Huck O. The spectrum of orofacial manifestations in systemic sclerosis: a challenging management. Oral Dis. 2017;23:424-439.10.1111/odi.12507
  18. 18. Gomes da Silva G, Maymone de Melo M, Leão J, et al. Oral features of systemic sclerosis: A case control study. Oral Dis. 2019;25:1995-2002.10.1111/odi.13174
  19. 19. 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;53:1386-1394.10.1093/rheumatology/ket441
  20. 20. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366:1809-1820.10.1016/S0140-6736(05)67728-8
  21. 21. Isola G, Williams RC, Lo Gullo A, et al. Risk association between scleroderma disease characteristics, periodontitis, and tooth loss. Clin Rheumatol. 2017;36:2733-2741.10.1007/s10067-017-3861-928988297
  22. 22. Cheng Z, Meade J, Mankia K, Emery P, Devine DA. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2017;31:1-12.10.1016/j.berh.2017.08.00129221594
  23. 23. Kobak S, Oskel F, Aksu K, Kabasakal Y. The frequency of sicca symptoms and Sjogren’s syndrome in patients with systemic sclerosis. Int J Rheum Dis. 2013;16:88-92.10.1111/j.1756-185X.2012.01810.x23441777
  24. 24. Denaxas K, Ladas SD, Karamanolis GP. Evaluation and management of esophageal manifestations in systemic sclerosis. Ann Gastroenterol. 2018;31:165-170.10.20524/aog.2018.0228582594629507463
  25. 25. Roberts CGP, Hummers LK, Ravich WJ, Wigley FM, Hutchins GM. A case-control study of the pathology of oesophageal disease in systemic sclerosis (scleroderma). Gut. 2006;55:1697-1703.10.1136/gut.2005.086074185646216527835
  26. 26. Kumar S, Singh J, Rattan S, DiMarino A, Cohen S, Jimenez S. Review article: pathogenesis and clinical manifestations of gastrointestinal involvement in systemic sclerosis. Aliment Pharmacol Ther. 2017;45:883-898.10.1111/apt.13963557644828185291
  27. 27. Lee JS, Kim HS, Moon JR, et al. Esophageal involvement and Determinants of Perception of Esophageal Symptoms Among South Koreans With Systemic Sclerosis. J Neurogastroenterol Motil. 2020;26:477-485.10.5056/jnm19148754719632989185
  28. 28. Arana-Guajardo AC, Barrera-Torres G, Villarreal-Alarcón MÁ, Vega-Morales D, Esquivel-Valerio JA. Esophageal symptoms and their lack of association with high-resolution manometry in systemic sclerosis patients. Reumatol Clin. 2017;15:165-169.10.1016/j.reuma.2017.09.00529258795
  29. 29. Crowell MD, Umar SB, Griffing LW, DiBase JK, Lacy BE, Vela MF. Esophageal Motor Abnormalities in Patients With Scleroderma: Heterogeneity, Risk Factors, and Effects on Quality of Life. Clin Gastroenterol Hepatol. 2017;15:207-213.10.1016/j.cgh.2016.08.03427613260
  30. 30. De Carlan M, Lescoat A, Brochard C, et al. Association between clinical manifestations of systemic sclerosis and esophageal dysmotility assessed by high-resolution manometry. J Scleroderma Relat Disord. 2017;2:50-56.10.5301/jsrd.5000233
  31. 31. Nicola S, Rolla G, Bucca C, et al. Gastric Juice Expression of Th-17 and T-Reg Related Cytokines in Scleroderma Esophageal Involvement. Cells. 2020;19;2106.10.3390/cells9092106756448032947843
  32. 32. 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. 2020;116:517-521.10.14309/ajg.000000000000110933657040
  33. 33. Petcu A, Ghib LJ, Grad SM, et al. Upper gastrointestinal involvement in systemic sclerosis: Findings in a real-life setting. Exp Ther Med. 2019;18:5095-5100.10.3892/etm.2019.8125688039531798729
  34. 34. Grusell NE, Dahlén G, Ruth M, et al. Bacterial flora of the human oral cavity, and the upper and lower esophagus. Dis Esophagus. 2012;53:650-656.
  35. 35. D’Souza SM, Cundra LB, Yoo BS, Parekh PJ, Johnson DA. Microbiome and Gastroesophageal Disease: Pathogenesis and Implications for Therapy. Ann Clin Gastroenterol Hepatol. 2020;4:020-033.10.29328/journal.acgh.1001018
  36. 36. Espinoza M, Mehta BK, Wang Y, et al. Characterization of the Esophageal Microbiome in Patients with Systemic Sclerosis (SSc). Arthritis Rheumatol. 2018;Suppl70.
  37. 37. Hong BY, Giang R, Mbuagbaw L, Larche M, Thabane L. Factors associated with development of gastrointestinal problems in patients with scleroderma: a systematic review. Syst Rev. 2015;4:188.10.1186/s13643-015-0176-2469731826718896
  38. 38. Radić M. Role of Helicobacter pylori infection in autoimmune systemic rheumatic diseases. World J Gastroenterol. 2014;20:12839-12846.10.3748/wjg.v20.i36.12839417746625278681
  39. 39. Yong W, 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): S168-S174.
  40. 40. Radić M, Kaliterna MD, Bonacin D, et al. Is Helicobacter pylori infection a risk factor for disease severity in systemic sclerosis? Rheumatol Int. 2013;33:2943-2948.
  41. 41. Yamaguchi K, Iwakiri R, Hara M, et al. Reflux Esophagitis and Helicobacter pylori Infection in Patients with Scleroderma. Inter Med. 2008;47:1555-1559.10.2169/internalmedicine.47.112818797112
  42. 42. Ram M, Barzilai O, Shapira Y, et al. Helicobacter pylori serology in autoimmune diseases: fact or fiction? Clin Chem Lab Med. 2013;51:1075-1082.
  43. 43. Bilgin H, Kocabaș H, Keșli R. The prevalence of infectious agents in patients with systemic sclerosis. Turk J Med Sci. 2015;45:1192-1197.10.3906/sag-1404-150
  44. 44. Balaji C, Bhuvanesh M, Saranya C, Ramesh R, Saravanan M, Rajeswari S. Helicobacter Pylori infection in Systemic Sclerosis and Its Association with Upper Gastrointestinal Dysfunction. Indian J Rheumatol. 2017;12:204-208.10.4103/injr.injr_62_17
  45. 45. Efthymiou G, Liaskos C, Siamopoulou T, et al. Antigen-specific humoral responses against Helicobacter pylori in patients with systemic sclerosis. Immunol Res. 2020;68:39-47.10.1007/s12026-020-09124-w32253703
  46. 46. Quigley EM. Small Intestinal Dysmotility, Its Role in Irritable Bowel Syndrome and Small Intestinal Bacterial Overgrowth: Assessment and Management. Front Gastrointest Res Basel Karger. 2014;33:55-64.10.1159/000356743
  47. 47. Rawn S, Pitman N, Beattie K, Bazzaz A, Larche M. Small Intestinal Bacterial Overgrowth in Patients with Systemic Sclerosis. Indian J Rheumatol. 2017;12:S167-S170.10.4103/0973-3698.219077
  48. 48. Feng X, Li XQ, Jiang Z. Prevalence and predictors of small intestinal bacterial overgrowth in systemic sclerosis: a systematic review and meta-analysis. Clin Rheumatol. 2021 January. [Epub ahead of print]10.1007/s10067-020-05549-833426631
  49. 49. Marie I, Ducrotté P, Denis P, Menard JF, Levesque H. Small Intestinal bacterial overgrowth in systemic sclerosis. Rheumatology. 2009;48:1314-1319.10.1093/rheumatology/kep22619696066
  50. 50. Polkowska-Pruszyńska B, Gerkowicz A, Rawicz-Pruszyński K, Krasowska D. The Role of Fecal Calprotectin in Patients with Systemic Sclerosis and Small Intestinal Bacterial Overgrowth (SIBO). Diagnostics. 2020;10:587.10.3390/diagnostics10080587745988232823752
  51. 51. Preis E, Franz K, Siegert E, et al. The impact of malnutrition on quality of life in patients with systemic sclerosis. Eur J Clin Nutr. 2018;72:504-510.10.1038/s41430-018-0116-z29520082
  52. 52. Zou H, De Palma G, Bercik P, Verdu E, Beattie K, Larche M. Distinct Characteristics of the Gut Microbiome of Patients with Systemic Sclerosis and Small Intestinal Bacterial Overgrowth [abstract]. Arthritis Rheumatol. 2019;71(suppl10).
  53. 53. Parodi A, Sessarego M, Greco A, et al. Small Intestinal Bacterial Overgrowth in Patients Suffering From Scleroderma: Clinical Effectiveness of Its Eradication. Am J Gastroenetrol. 2008;103: 1257-1262.10.1111/j.1572-0241.2007.01758.x18422815
  54. 54. Fynne L, Worsøe J, Gregersen T, Schalageter V, Laurberg S, Krogh K. Gastrointestinal transit in patients with systemic sclerosis. Scand J Gastroenterol. 2011;46:1187-1193.10.3109/00365521.2011.60315821815862
  55. 55. Gemignani L, Savarino V, Ghio M, et al. Lactulose Breath Test to Assess Orocecal Transit Delay and Estimate Esophageal Dysmotility in Scleroderma Patients. Semin Arthritis Rheum. 2013;42:522-529.10.1016/j.semarthrit.2012.09.00423352249
  56. 56. Savarino E, Mei F, Parodi A, et al. Gastrointestinal motility disorder assessment in systemic sclerosis. Rheumatology. 2013;52:1095-1100.10.1093/rheumatology/kes42923382360
  57. 57. Tauber M, Avouac J, Benahmed A, et al. Prevalence and predictors of small intestinal bacterial overgrowth in systemic sclerosis patients with gastrointestinal symptoms. Clin Exp Rheumatol. 2014;32:S82-S87.
  58. 58. Soukup T, Cyrany J, Kopacova M, Tacheci I, Bures J. Small intestinal bacterial overgrowth in patients with systemic sclerosis, clinical data relevance [abstract]. Clin and Exp Rheumatol. 2014;32:S132.
  59. 59. Marie I, Leroi A, Menard J, Levesque H, Quillard M, Ducrotte P. Fecal calprotectin in systemic sclerosis and review of the literature. Autoimmun Rev. 2015;14:547-554.10.1016/j.autrev.2015.01.01825661980
  60. 60. Adarsh M, Sharma S, Sinha S, et al. Gastrointestinal Dysmotility and Infections in Systemic Sclerosis – An Indian Scenario. Curr Rheumatol Rev. 2017;13.
  61. 61. Cruz-Dominguez M, Garcia-Collinot G, Madrigal-Santillan E, et al. Small intestinal bacterial overgrowth in relation to gastrointestinal symptoms in systemic sclerosis [abstract]. Ann Rheum Dis. 2017;103:1282.
  62. 62. 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;22:695-699.10.1111/1756-185X.1349530729669
  63. 63. García-Collinot G, Madrigal-Santillán EO, Martínez-Benzomo MA, et al. Effectiveness of Saccharomyces boulardii and Metronidazole for Small Intestinal Bacterial Overgrowth in Systemic Sclerosis. Dig Dis Sci. 2020;65:1134-1143.10.1007/s10620-019-05830-031549334
  64. 64. Zhang X, Chen Bd, Zhao Ld, Li H. The Gut Microbiota: Emerging Evidence in Autoimmune Diseases. Trends Mol Med. 2020;26:862-873.10.1016/j.molmed.2020.04.00132402849
  65. 65. Volkmann E, Chang Y, Barroso N, et al. Association of Systemic Sclerosis With a Unique Colonic Microbial Consortium. Arthritis Rheumatol. 2016;68:1483-1492.10.1002/art.39572556166626749064
  66. 66. Andrnasson K, Alrawi Z, Persson A, Jonsson G, Marsal J. Intestinal dysbiosis is common in systemic sclerosis and associated with gastrointestinal and extraintestinal features of disease. Arthritis Res Ther. 2016;18:278.10.1186/s13075-016-1182-z512698627894337
  67. 67. Bosello S, Paroni Sterbini F, Natalello G, et al. The intestinal involvement in systemic sclerosis is characterized by a peculiar gut microbiota [abstract]. Arthritis Rheumatol. 2016;68.
  68. 68. Volkmann E, Hoffman-Vold A, Chang Y, et al. Systemic sclerosis is associated with alterations in gastrointestinal microbiota in two independent cohorts. BMJ Open Gastroenterol. 2017;4: e000134.10.1136/bmjgast-2017-000134550863628761687
  69. 69. Patrone V, Puglisi E, Cardinali M, et al. Gut microbiota profile in systemic sclerosis patients with and without clinical evidence of gastrointestinal involvement. Sci Rep. 2017;7:14874.10.1038/s41598-017-14889-6566591229093509
  70. 70. Bellocchi C, Fernandez-Ochoa A, Montanelli G, et al. Microbial and metabolic multi-omic correlations in systemic sclerosis patients. Ann N Y Acad Sci. 2018;1421:97-109.10.1111/nyas.1373629749635
  71. 71. Natalello G, Bosello S, Paroni Sterbini F, et al. Gut microbiota analysis in systemic sclerosis according to disease characteristics and nutritional status. Clin Exp Rheumatol. 2020;38(Suppl. 125).
  72. 72. Bellocchi C, Volkmann ER. Update on the Gastrointestinal Microbiome in Systemic Sclerosis. Curr Rheumatol Rep. 2018;20:49.10.1007/s11926-018-0758-929943234
DOI: https://doi.org/10.2478/jim-2021-0018 | Journal eISSN: 2501-8132 | Journal ISSN: 2501-5974
Language: English
Page range: 53 - 59
Submitted on: Mar 30, 2021
Accepted on: Apr 15, 2021
Published on: Jul 17, 2021
Published by: Asociatia Transilvana de Terapie Transvasculara si Transplant KARDIOMED
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2021 Ioana Bratoiu, Alexandra Burlui, Patricia Richter, Anca Cardoneanu, Ciprian Rezus, Elena Rezus, published by Asociatia Transilvana de Terapie Transvasculara si Transplant KARDIOMED
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.