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Bleeding Lesion of the Small Bowel: an Extensive Update Leaving No Stone Unturned

  • Cedric Van de Bruaene
  • Pieter Hindryckx
  • Laurens Van de Bruaene
  • Danny De Looze
Small Intestine (D Sachar, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Small Intestine

Abstract

Purpose of Review

Gastrointestinal bleeding originating from the small bowel (SB) poses a challenge to the treating gastroenterologist. Once diagnosed, management is not a walk in the park either. This review intends to summarize the current state-of-the-art evidence in a complete way with special attention for vascular and ulcerative lesions, to provide the reader with a clinical guide and flow chart towards SB bleeding.

Recent Findings

Absence of SB bleeding lesions on CE does not directly yield better prognosis; although having a lower rebleeding rate the first 2 years, rebleeding in the long term is high. Push enteroscopy can play an early role in patients with SB bleeding if suspicion of angioectasia is high, since these lesions tend to be located in the proximal SB. Endoscopic management of angioectasia is, however, difficult and shows poor results.

Summary

Capsule endoscopy (CE) or device-assisted enteroscopy (DAE) remain the diagnostic mainstay in SB bleeding, choosing one over the other based upon patient characteristics and expected lesions.

Keywords

Small bowel Gastrointestinal bleeding Midgut bleeding Capsule endoscopy Small bowel imaging Endoscopic treatment 

Notes

Compliance with Ethical Standards

Conflict of Interest

Danny De Looze, Cedric Van de Bruaene, and Laurens Van de Bruaene declare no conflict of interest.

Pieter Hindryckx reports receiving reimbursement for travel accommodations from Y-ECCO; personal fees from Abbvie, Takeda, and Janssen for work as a consultant; personal fees from Ferring as a lecturer; and is a board member of the Yount Flemisch Society of Gastroenterology.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Peery AF, Crockett SD, Barritt AS, Dellon ES, Eluri S, Gangarosa LM, et al. Burden of gastrointestinal, liver, and pancreatic diseases in the United States. Gastroenterology. 2015;149(7):1731–41 e1733.  https://doi.org/10.1053/j.gastro.2015.08.045.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Kim BS, Li BT, Engel A, Samra JS, Clarke S, Norton ID, et al. Diagnosis of gastrointestinal bleeding: a practical guide for clinicians. World J Gastrointest Pathophysiol. 2014;5(4):467–78.  https://doi.org/10.4291/wjgp.v5.i4.467.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Sharara AI, Rockey DC. Gastroesophageal variceal hemorrhage. N Engl J Med. 2001;345(9):669–81.  https://doi.org/10.1056/NEJMra003007.PubMedCrossRefGoogle Scholar
  4. 4.
    Okazaki H, Fujiwara Y, Sugimori S, Nagami Y, Kameda N, Machida H, et al. Prevalence of mid-gastrointestinal bleeding in patients with acute overt gastrointestinal bleeding: multi-center experience with 1,044 consecutive patients. J Gastroenterol. 2009;44(6):550–5.  https://doi.org/10.1007/s00535-009-0039-5.PubMedCrossRefGoogle Scholar
  5. 5.
    Committee ASoP, Gurudu SR, Bruining DH, Acosta RD, Eloubeidi MA, Faulx AL, et al. The role of endoscopy in the management of suspected small-bowel bleeding. Gastrointest Endosc. 2017;85(1):22–31.  https://doi.org/10.1016/j.gie.2016.06.013.CrossRefGoogle Scholar
  6. 6.
    Zhang BL, Chen CX, Li YM. Capsule endoscopy examination identifies different leading causes of obscure gastrointestinal bleeding in patients of different ages. Turk J Gastroenterol. 2012;23(3):220–5.  https://doi.org/10.4318/tjg.2012.0338.PubMedCrossRefGoogle Scholar
  7. 7.
    Yung DE, Rondonotti E, Giannakou A, Avni T, Rosa B, Toth E, et al. Capsule endoscopy in young patients with iron deficiency anaemia and negative bidirectional gastrointestinal endoscopy. United European Gastroenterol J. 2017;5(7):974–81.  https://doi.org/10.1177/2050640617692501.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Li L, Chen C, Li Y, Zhang B. The role of capsule endoscopy in the diagnosis and treatment of obscure gastrointestinal bleeding in older individuals. Eur J Gastroenterol Hepatol. 2016;28(12):1425–30.  https://doi.org/10.1097/MEG.0000000000000737.PubMedCrossRefGoogle Scholar
  9. 9.
    • Bosch X, Montori E, Guerra-Garcia M, Costa-Rodriguez J, Quintanilla MH, Tolosa-Chapasian PE, et al. A comprehensive evaluation of the gastrointestinal tract in iron-deficiency anemia with predefined hemoglobin below 9mg/dL: a prospective cohort study. Digestive Liver Dis. 2017;49(4):417–26.  https://doi.org/10.1016/j.dld.2016.12.013. This large study confirms the importance of diffuse angioectasia as disease entity, as it is, just like GI cancer, correlated with the lowest hemoglobin values in GI bleeding.CrossRefGoogle Scholar
  10. 10.
    Hosoe N, Matsukawa S, Kanno Y, Naganuma M, Imaeda H, Ida Y, et al. Cross-sectional small intestinal surveillance of maintenance hemodialysis patients using video capsule endoscopy: SCHEMA study. Endosc Int Open. 2016;4(5):E589–96.  https://doi.org/10.1055/s-0042-105203.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    • Draper KV, Huang RJ, Gerson LB. GI bleeding in patients with continuous-flow left ventricular assist devices: a systematic review and meta-analysis. Gastrointestinal Endoscopy. 2014;80(3):435–446 e431.  https://doi.org/10.1016/j.gie.2014.03.040. This systematic review and meta-analysis creates awareness of GI bleeding due to GI angioectasia in patients with Left Ventricular Assist Devices.PubMedCrossRefGoogle Scholar
  12. 12.
    •• Sakai E, Endo H, Taniguchi L, Hata Y, Ezuka A, Nagase H, et al. Factors predicting the presence of small bowel lesions in patients with obscure gastrointestinal bleeding. Dig Endoscopy. 2013;25(4):412–20.  https://doi.org/10.1111/den.12002. This study emphasizes the impact of nonsteroidal anti-inflammatory drugs, low-dose aspirin, and proton-pump inhibitor use on GI bleeding.CrossRefGoogle Scholar
  13. 13.
    Okamoto J, Tominaga K, Sugimori S, Kato K, Minamino H, Ominami M, et al. Comparison of risk factors between small intestinal ulcerative and vascular lesions in occult versus overt obscure gastrointestinal bleeding. Dig Dis Sci. 2016;61(2):533–41.  https://doi.org/10.1007/s10620-015-3904-5.PubMedCrossRefGoogle Scholar
  14. 14.
    Nagata N, Niikura R, Yamada A, Sakurai T, Shimbo T, Kobayashi Y, et al. Acute middle gastrointestinal bleeding risk associated with NSAIDs, antithrombotic drugs, and PPIs: a multicenter case-control study. PLoS One. 2016;11(3):e0151332.  https://doi.org/10.1371/journal.pone.0151332.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    • Van de Bruaene C, Hindryckx P, Snauwaert C, Dooremont D, Vanduyfhuys B, Vandenabeele L, et al. The predictive value of negative capsule endoscopy for the indication of Obscure Gastrointestinal Bleeding: no reassurance in the long term. Acta Gastroenterol Belg. 2016;79(4):405–13. Our recently published study shows the outcome of negative capsule endoscopies in patients with gastrointestinal bleeding. High rebleeding rates were found in the long term and negative capsule endoscopy should not reassure the treating gastroenterologist. PubMedGoogle Scholar
  16. 16.
    Hoedemaker RA, Westerhof J, Weersma RK, Koornstra JJ. Non-small-bowel abnormalities identified during small bowel capsule endoscopy. World J Gastroenterol WJG. 2014;20(14):4025–9.  https://doi.org/10.3748/wjg.v20.i14.4025.PubMedCrossRefGoogle Scholar
  17. 17.
    Fry LC, Bellutti M, Neumann H, Malfertheiner P, Monkemuller K. Incidence of bleeding lesions within reach of conventional upper and lower endoscopes in patients undergoing double-balloon enteroscopy for obscure gastrointestinal bleeding. Aliment Pharmacol Ther. 2009;29(3):342–9.  https://doi.org/10.1111/j.1365-2036.2008.03888.x.PubMedCrossRefGoogle Scholar
  18. 18.
    Pennazio M, Spada C, Eliakim R, Keuchel M, May A, Mulder CJ, et al. Small-bowel capsule endoscopy and device-assisted enteroscopy for diagnosis and treatment of small-bowel disorders: European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline. Endoscopy. 2015;47(4):352–86.  https://doi.org/10.1055/s-0034-1391855.PubMedCrossRefGoogle Scholar
  19. 19.
    • Van de Bruaene C, De Looze D, Hindryckx P. Small bowel capsule endoscopy: where are we after almost 15 years of use? World J Gastrointest Endosc. 2015;7(1):13–36.  https://doi.org/10.4253/wjge.v7.i1.13. This review encompasses every possible aspect of capsule endoscopy in-depth.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Ou G, Shahidi N, Galorport C, Takach O, Lee T, Enns R. Effect of longer battery life on small bowel capsule endoscopy. World J Gastroenterol: WJG. 2015;21(9):2677–82.  https://doi.org/10.3748/wjg.v21.i9.2677.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Monteiro S, de Castro FD, Carvalho PB, Moreira MJ, Rosa B, Cotter J. PillCam((R)) SB3 capsule: does the increased frame rate eliminate the risk of missing lesions? World J Gastroenterol: WJG. 2016;22(10):3066–8.  https://doi.org/10.3748/wjg.v22.i10.3066.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Koulaouzidis A, Rondonotti E, Giannakou A, Plevris JN. Diagnostic yield of small-bowel capsule endoscopy in patients with iron-deficiency anemia: a systematic review. Gastrointest Endosc. 2012;76(5):983–92.  https://doi.org/10.1016/j.gie.2012.07.035.PubMedCrossRefGoogle Scholar
  23. 23.
    Shahidi NC, Ou G, Svarta S, Law JK, Kwok R, Tong J, et al. Factors associated with positive findings from capsule endoscopy in patients with obscure gastrointestinal bleeding. Clin Gastroenterol Hepatol. 2012;10(12):1381–5.  https://doi.org/10.1016/j.cgh.2012.08.035.PubMedCrossRefGoogle Scholar
  24. 24.
    Nennstiel S, Machanek A, von Delius S, Neu B, Haller B, Abdelhafez M, et al. Predictors and characteristics of angioectasias in patients with obscure gastrointestinal bleeding identified by video capsule endoscopy. United European Gastroenterol J. 2017;5(8):1129–35.  https://doi.org/10.1177/2050640617704366.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Sulbaran M, de Moura E, Bernardo W, Morais C, Oliveira J, Bustamante-Lopez L, et al. Overtube-assisted enteroscopy and capsule endoscopy for the diagnosis of small-bowel polyps and tumors: a systematic review and meta-analysis. Endosc Int Open. 2016;4(2):E151–63.  https://doi.org/10.1055/s-0041-108261.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Rahman M, Akerman S, DeVito B, Miller L, Akerman M, Sultan K. Comparison of the diagnostic yield and outcomes between standard 8 h capsule endoscopy and the new 12 h capsule endoscopy for investigating small bowel pathology. World J Gastroenterol. 2015;21(18):5542–7.  https://doi.org/10.3748/wjg.v21.i18.5542.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Pioche M, Gaudin JL, Filoche B, Jacob P, Lamouliatte H, Lapalus MG, et al. Prospective, randomized comparison of two small-bowel capsule endoscopy systems in patients with obscure GI bleeding. Gastrointest Endosc. 2011;73(6):1181–8.  https://doi.org/10.1016/j.gie.2011.02.011.PubMedCrossRefGoogle Scholar
  28. 28.
    Pioche M, Vanbiervliet G, Jacob P, Duburque C, Gincul R, Filoche B, et al. Prospective randomized comparison between axial- and lateral-viewing capsule endoscopy systems in patients with obscure digestive bleeding. Endoscopy. 2014;46(6):479–84.  https://doi.org/10.1055/s-0033-1358832.PubMedGoogle Scholar
  29. 29.
    •• Tontini GE, Wiedbrauck F, Cavallaro F, Koulaouzidis A, Marino R, Pastorelli L, et al. Small-bowel capsule endoscopy with panoramic view: results of the first multicenter, observational study (with videos). Gastrointest Endosc. 2017;85(2):401–408 e402.  https://doi.org/10.1016/j.gie.2016.07.063. In this study, the diagnostic yield and safety of 360° panoramic-view cameras was found to be similar to forward-viewing capsules.PubMedCrossRefGoogle Scholar
  30. 30.
    Lepileur L, Dray X, Antonietti M, Iwanicki-Caron I, Grigioni S, Chaput U, et al. Factors associated with diagnosis of obscure gastrointestinal bleeding by video capsule enteroscopy. Clin Gastroenterol Hepatol. 2012;10(12):1376–80.  https://doi.org/10.1016/j.cgh.2012.05.024.PubMedCrossRefGoogle Scholar
  31. 31.
    Sidhu R, Sanders DS, Kapur K, Leeds JS, McAlindon ME. Factors predicting the diagnostic yield and intervention in obscure gastrointestinal bleeding investigated using capsule endoscopy. J Gastrointest Liver Dis. 2009;18(3):273–8.Google Scholar
  32. 32.
    Kim SH, Keum B, Chun HJ, Yoo IK, Lee JM, Lee JS, et al. Efficacy and implications of a 48-h cutoff for video capsule endoscopy application in overt obscure gastrointestinal bleeding. Endosc Int Open. 2015;3(4):E334–8.  https://doi.org/10.1055/s-0034-1391852.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Sung JJ, Tang RS, Ching JY, Rainer TH, Lau JY. Use of capsule endoscopy in the emergency department as a triage of patients with GI bleeding. Gastrointest Endosc. 2016;84(6):907–13.  https://doi.org/10.1016/j.gie.2016.04.043.PubMedCrossRefGoogle Scholar
  34. 34.
    Maeda Y, Moribata K, Deguchi H, Inoue I, Maekita T, Iguchi M, et al. Video capsule endoscopy as the initial examination for overt obscure gastrointestinal bleeding can efficiently identify patients who require double-balloon enteroscopy. BMC Gastroenterol. 2015;15:132.  https://doi.org/10.1186/s12876-015-0362-7.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Chalazan B, Gostout CJ, Song LM, Enders FT, Rajan E. Use of capsule small bowel transit time to determine the optimal enteroscopy approach. Gastroenterol Res. 2012;5(2):39–44.  https://doi.org/10.4021/gr404w.Google Scholar
  36. 36.
    • Rezapour M, Amadi C, Gerson LB. Retention associated with video capsule endoscopy: systematic review and meta-analysis. Gastrointestinal Endoscopy. 2017;85(6):1157–1168 e1152.  https://doi.org/10.1016/j.gie.2016.12.024. This systematic review and meta-analysis focuses on the retention of capsules in patients with small bowel bleeding undergoing capsule endoscopy, being ~ 2%. Retention rates can be decreased by 50% using patency capsules or CT enterography.PubMedCrossRefGoogle Scholar
  37. 37.
    Bouchard S, Ibrahim M, Van Gossum A. Video capsule endoscopy: perspectives of a revolutionary technique. World J Gastroenterol. 2014;20(46):17330–44.  https://doi.org/10.3748/wjg.v20.i46.17330.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Laine L, Sahota A, Shah A. Does capsule endoscopy improve outcomes in obscure gastrointestinal bleeding? Randomized trial versus dedicated small bowel radiography. Gastroenterology. 2010;138(5):1673–1680 e1671; quiz e1611–1672.  https://doi.org/10.1053/j.gastro.2010.01.047.PubMedCrossRefGoogle Scholar
  39. 39.
    Segarajasingam DS, Hanley SC, Barkun AN, Waschke KA, Burtin P, Parent J, et al. Randomized controlled trial comparing outcomes of video capsule endoscopy with push enteroscopy in obscure gastrointestinal bleeding. Can J Gastroenterol Hepatol. 2015;29(2):85–90.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Holleran GE, Barry SA, Thornton OJ, Dobson MJ, McNamara DA. The use of small bowel capsule endoscopy in iron deficiency anaemia: low impact on outcome in the medium term despite high diagnostic yield. Eur J Gastroenterol Hepatol. 2013;25(3):327–32.  https://doi.org/10.1097/MEG.0b013e32835b7d3a.PubMedCrossRefGoogle Scholar
  41. 41.
    Chen WG, Shan GD, Zhang H, Yang M, L L, Yue M, et al. Double-balloon enteroscopy in small bowel diseases: eight years single-center experience in China. Medicine (Baltimore). 2016;95(42):e5104.  https://doi.org/10.1097/MD.0000000000005104.CrossRefGoogle Scholar
  42. 42.
    Aniwan S, Viriyautsahakul V, Rerknimitr R, Angsuwatcharakon P, Kongkam P, Treeprasertsuk S, et al. Urgent double balloon endoscopy provides higher yields than non-urgent double balloon endoscopy in overt obscure gastrointestinal bleeding. Endosc Int Open. 2014;2(2):E90–5.  https://doi.org/10.1055/s-0034-1365543.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Lipka S, Rabbanifard R, Kumar A, Brady P. Single versus double balloon enteroscopy for small bowel diagnostics: a systematic review and meta-analysis. J Clin Gastroenterol. 2015;49(3):177–84.  https://doi.org/10.1097/MCG.0000000000000274.PubMedCrossRefGoogle Scholar
  44. 44.
    Teshima CW, Kuipers EJ, van Zanten SV, Mensink PB. Double balloon enteroscopy and capsule endoscopy for obscure gastrointestinal bleeding: an updated meta-analysis. J Gastroenterol Hepatol. 2011;26(5):796–801.  https://doi.org/10.1111/j.1440-1746.2010.06530.x.PubMedCrossRefGoogle Scholar
  45. 45.
    Aniwan S, Viriyautsahakul V, Angsuwatcharakon P, Kongkam P, Treeprasertsuk S, Rerknimitr R, et al. Comparison of urgent video capsule endoscopy and urgent double-balloon endoscopy in massive obscure gastrointestinal bleeding. Hepato-Gastroenterology. 2014;61(135):1990–4.PubMedGoogle Scholar
  46. 46.
    Pinto-Pais T, Pinho R, Rodrigues A, Fernandes C, Ribeiro I, Fraga J, et al. Emergency single-balloon enteroscopy in overt obscure gastrointestinal bleeding: efficacy and safety. United Eur Gastroenterol J. 2014;2(6):490–6.  https://doi.org/10.1177/2050640614554850.CrossRefGoogle Scholar
  47. 47.
    • Nelson KK, Lipka S, Davis-Yadley AH, Rodriguez AC, Doraiswamy V, Rabbanifard R, et al. Timing of single balloon enteroscopy: significant or not? Endosc Int Open. 2016;4(7):E761–6.  https://doi.org/10.1055/s-0042-108189. Diagnostic and therapeutic yield of SBE within or after 24 hours were similar, yet hospital stay was significantly shorter if SBE was performed early.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Rahmi G, Samaha E, Vahedi K, Ponchon T, Fumex F, Filoche B, et al. Multicenter comparison of double-balloon enteroscopy and spiral enteroscopy. J Gastroenterol Hepatol. 2013;28(6):992–8.  https://doi.org/10.1111/jgh.12188.PubMedCrossRefGoogle Scholar
  49. 49.
    Despott EJ, Murino A, Bourikas L, Nakamura M, Ramachandra V, Fraser C. A prospective comparison of performance during back-to-back, anterograde manual spiral enteroscopy and double-balloon enteroscopy. Digest Liver Dis. 2015;47(5):395–400.  https://doi.org/10.1016/j.dld.2015.02.003.CrossRefGoogle Scholar
  50. 50.
    •• Baniya R, Upadhya S, Subedi SC, Khan J, Sharma P, Mohammed TS, et al. Balloon enteroscopy versus spiral enteroscopy for small-bowel disorders: a systematic review and meta-analysis. Gastrointest Endosc. 2017;  https://doi.org/10.1016/j.gie.2017.06.015. This recently published systematic review and meta-analysis shows no difference in balloon enteroscopy and spiral enteroscopy, regarding diagnostic and therapeutic outcomes. However, spiral enteroscopy is associated with shorter procedure times.
  51. 51.
    Foutch PG, Sawyer R, Sanowski RA. Push-enteroscopy for diagnosis of patients with gastrointestinal bleeding of obscure origin. Gastrointest Endosc. 1990;36(4):337–41.  https://doi.org/10.1016/S0016-5107(90)71060-7.PubMedCrossRefGoogle Scholar
  52. 52.
    • Plotkin E, Imaeda A. mall intestinal angioectasias are not randomly distributed in the small bowel and most may be reached by push enteroscopy. J Clin Gastroenterol. 2016;50(7):561–5.  https://doi.org/10.1097/MCG.0000000000000425. Although more and more replaced by balloon-assisted endoscopy, push enteroscopy might be of use in patients at risk of bleeding GI angioectasia, since these lesions were found to be located in the proximal part of the small bowel.PubMedCrossRefGoogle Scholar
  53. 53.
    Douard R, Wind P, Berger A, Maniere T, Landi B, Cellier C, et al. Role of intraoperative enteroscopy in the management of obscure gastointestinal bleeding at the time of video-capsule endoscopy. Am J Surg. 2009;198(1):6–11.  https://doi.org/10.1016/j.amjsurg.2008.06.036.PubMedCrossRefGoogle Scholar
  54. 54.
    Bonnet S, Douard R, Malamut G, Cellier C, Wind P. Intraoperative enteroscopy in the management of obscure gastrointestinal bleeding. Digest Liver Dis. 2013;45(4):277–84.  https://doi.org/10.1016/j.dld.2012.07.003.CrossRefGoogle Scholar
  55. 55.
    Wang Z, Chen JQ, Liu JL, Qin XG, Huang Y. CT enterography in obscure gastrointestinal bleeding: a systematic review and meta-analysis. J Med Imaging Radiat Oncol. 2013;57(3):263–73.  https://doi.org/10.1111/1754-9485.12035.PubMedCrossRefGoogle Scholar
  56. 56.
    Limsrivilai J, Srisajjakul S, Pongprasobchai S, Leelakusolvong S, Tanwandee T. A prospective blinded comparison of video capsule endoscopy versus computed tomography enterography in potential small bowel bleeding: clinical utility of computed tomography enterography. J Clin Gastroenterol. 2016;  https://doi.org/10.1097/MCG.0000000000000639.
  57. 57.
    Heo HM, Park CH, Lim JS, Lee JH, Kim BK, Cheon JH, et al. The role of capsule endoscopy after negative CT enterography in patients with obscure gastrointestinal bleeding. Eur Radiol. 2012;22(6):1159–66.  https://doi.org/10.1007/s00330-011-2374-1.PubMedCrossRefGoogle Scholar
  58. 58.
    He B, Gong S, Hu C, Fan J, Qian J, Huang S, et al. Obscure gastrointestinal bleeding: diagnostic performance of 64-section multiphase CT enterography and CT angiography compared with capsule endoscopy. Br J Radiol. 2014;87(1043):20140229.  https://doi.org/10.1259/bjr.20140229.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Van Weyenberg SJ, Bouman K, Jacobs MA, Halloran BP, Van der Peet DL, Mulder CJ, et al. Comparison of MR enteroclysis with video capsule endoscopy in the investigation of small-intestinal disease. Abdom Imaging. 2013;38(1):42–51.  https://doi.org/10.1007/s00261-012-9892-4.PubMedCrossRefGoogle Scholar
  60. 60.
    Wiarda BM, Heine DG, Mensink P, Stolk M, Dees J, Hazenberg HJ, et al. Comparison of magnetic resonance enteroclysis and capsule endoscopy with balloon-assisted enteroscopy in patients with obscure gastrointestinal bleeding. Endoscopy. 2012;44(7):668–73.  https://doi.org/10.1055/s-0032-1309386.PubMedCrossRefGoogle Scholar
  61. 61.
    Tseng CM, Lin IC, Chang CY, Wang HP, Chen CC, Mo LR, et al. Role of computed tomography angiography on the management of overt obscure gastrointestinal bleeding. PLoS One. 2017;12(3):e0172754.  https://doi.org/10.1371/journal.pone.0172754.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Wildgruber M, Wrede CE, Zorger N, Muller-Wille R, Hamer OW, Zeman F, et al. Computed tomography versus digital subtraction angiography for the diagnosis of obscure gastrointestinal bleeding. Eur J Radiol. 2017;88:8–14.  https://doi.org/10.1016/j.ejrad.2016.12.029.PubMedCrossRefGoogle Scholar
  63. 63.
    Grady E. Gastrointestinal bleeding scintigraphy in the early 21st century. J Nucl Med. 2016;57(2):252–9.  https://doi.org/10.2967/jnumed.115.157289.PubMedCrossRefGoogle Scholar
  64. 64.
    Gerson L, Kamal A. Cost-effectiveness analysis of management strategies for obscure GI bleeding. Gastrointest Endosc. 2008;68(5):920–36.  https://doi.org/10.1016/j.gie.2008.01.035.PubMedCrossRefGoogle Scholar
  65. 65.
    Marmo R, Rotondano G, Rondonotti E, de Franchis R, D’Inca R, Vettorato MG, et al. Capsule enteroscopy vs. other diagnostic procedures in diagnosing obscure gastrointestinal bleeding: a cost-effectiveness study. Eur J Gastroenterol Hepatol. 2007;19(7):535–42.  https://doi.org/10.1097/MEG.0b013e32812144dd.PubMedCrossRefGoogle Scholar
  66. 66.
    Somsouk M, Gralnek IM, Inadomi JM. Management of obscure occult gastrointestinal bleeding: a cost-minimization analysis. Clin Gastroenterol Hepatol. 2008;6(6):661–70.  https://doi.org/10.1016/j.cgh.2008.02.033.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Albert JG, Nachtigall F, Wiedbrauck F, Dollinger MM, Gittinger FS, Hollerbach S, et al. Minimizing procedural cost in diagnosing small bowel bleeding: comparison of a strategy based on initial capsule endoscopy versus initial double-balloon enteroscopy. Eur J Gastroenterol Hepatol. 2010;22(6):679–88.PubMedGoogle Scholar
  68. 68.
    Palimaka S, Blackhouse G, Goeree R. Capsule endoscopy in the assessment of obscure gastrointestinal bleeding: an economic analysis. Ont Health Technol Assess Ser. 2015;15(2):1–32.Google Scholar
  69. 69.
    Jackson CS, Gerson LB. Management of gastrointestinal angiodysplastic lesions (GIADs): a systematic review and meta-analysis. Am J Gastroenterol. 2014;109(4):474–83; quiz 484.  https://doi.org/10.1038/ajg.2014.19.PubMedCrossRefGoogle Scholar
  70. 70.
    Sakai E, Endo H, Taguri M, Kawamura H, Taniguchi L, Hata Y, et al. Frequency and risk factors for rebleeding events in patients with small bowel angioectasia. BMC Gastroenterol. 2014;14:200.  https://doi.org/10.1186/s12876-014-0200-3.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Pinho R, Ponte A, Rodrigues A, Pinto-Pais T, Fernandes C, Ribeiro I, et al. Long-term rebleeding risk following endoscopic therapy of small-bowel vascular lesions with device-assisted enteroscopy. Eur J Gastroenterol Hepatol. 2016;28(4):479–85.  https://doi.org/10.1097/MEG.0000000000000552.PubMedGoogle Scholar
  72. 72.
    Shinozaki S, Yamamoto H, Yano T, Sunada K, Hayashi Y, Shinhata H, et al. Favorable long-term outcomes of repeat endotherapy for small-intestine vascular lesions by double-balloon endoscopy. Gastrointest Endosc. 2014;80(1):112–7.  https://doi.org/10.1016/j.gie.2013.11.029.PubMedCrossRefGoogle Scholar
  73. 73.
    Romagnuolo J, Brock AS, Ranney N. Is endoscopic therapy effective for angioectasia in obscure gastrointestinal bleeding?: a systematic review of the literature. J Clin Gastroenterol. 2015;49(10):823–30.  https://doi.org/10.1097/MCG.0000000000000266.PubMedCrossRefGoogle Scholar
  74. 74.
    Bauditz J. Effective treatment of gastrointestinal bleeding with thalidomide—chances and limitations. World J Gastroenterol. 2016;22(11):3158–64.  https://doi.org/10.3748/wjg.v22.i11.3158.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    • Chen H, Fu S, Feng N, Chen H, Gao Y, Zhao Y, et al. Bleeding recurrence in patients with gastrointestinal vascular malformation after thalidomide. Medicine (Baltimore). 2016;95(33):e4606.  https://doi.org/10.1097/MD.0000000000004606. This retrospective study showed the efficacy of Thalidomide as treatment of GI angioectasia. An 80% response rate and 20% recurrence rate were found, confirming its relevance in patients at risk of vascular malformations. However, in 60% of patients, adverse events were observed.CrossRefGoogle Scholar
  76. 76.
    Nardone G, Compare D, Scarpignato C, Rocco A. Long acting release-octreotide as “rescue” therapy to control angiodysplasia bleeding: a retrospective study of 98 cases. Digest Liver Dis. 2014;46(8):688–94.  https://doi.org/10.1016/j.dld.2014.04.011.CrossRefGoogle Scholar
  77. 77.
    • Holleran G, Hall B, Breslin N, McNamara D. Long-acting somatostatin analogues provide significant beneficial effect in patients with refractory small bowel angiodysplasia: results from a proof of concept open label mono-centre trial. United European Gastroenterol J. 2016;4(1):70–6.  https://doi.org/10.1177/2050640614559121. In this small study of 20 patients with small bowel angioectasia, long-acting somatostatin analogues proved to be effective in 90% of patients, significantly increasing hemoglobin values and reducing further transfusion need. However, adverse events were present in ~ 30%.PubMedCrossRefGoogle Scholar
  78. 78.
    Grooteman KV, van Geenen EJ, Drenth JP. Multicentre, open-label, randomised, parallel-group, superiority study to compare the efficacy of octreotide therapy 40 mg monthly versus standard of care in patients with refractory anaemia due to gastrointestinal bleeding from small bowel angiodysplasias: a protocol of the OCEAN trial. BMJ Open. 2016;6(9):e011442.  https://doi.org/10.1136/bmjopen-2016-011442.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Hongsakul K, Pakdeejit S, Tanutit P. Outcome and predictive factors of successful transarterial embolization for the treatment of acute gastrointestinal hemorrhage. Acta Radiol. 2014;55(2):186–94.  https://doi.org/10.1177/0284185113494985.PubMedCrossRefGoogle Scholar
  80. 80.
    Bua-Ngam C, Norasetsingh J, Treesit T, Wedsart B, Chansanti O, Tapaneeyakorn J, et al. Efficacy of emergency transarterial embolization in acute lower gastrointestinal bleeding: a single-center experience. Diagn Interv Imaging. 2017;98(6):499–505.  https://doi.org/10.1016/j.diii.2017.02.005.PubMedCrossRefGoogle Scholar
  81. 81.
    Manatsathit W, Khrucharoen U, Jensen DM, Hines OJ, Kovacs T, Ohning G, Jutabha R, Ghassemi K, Dulai GS, Machicado G. Laparotomy and intraoperative enteroscopy for obscure gastrointestinal bleeding before and after the era of video capsule endoscopy and deep enteroscopy: a tertiary center experience. Am J Surg. 2017.  https://doi.org/10.1016/j.amjsurg.2017.05.018
  82. 82.
    Frydman J, Bahouth H, Leiderman M, Ofer A, Kluger Y. Methylene Blue injection via superior mesenteric artery microcatheter for focused enterectomy in the treatment of a bleeding small intestinal arteriovenous malformation. World J Emerg Surg. 2014;9(1):17.  https://doi.org/10.1186/1749-7922-9-17.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Tziatzios G, Gkolfakis P, Dimitriadis GD, Triantafyllou K. Long-term effects of video capsule endoscopy in the management of obscure gastrointestinal bleeding. Ann Transl Med. 2017;5(9):196.  https://doi.org/10.21037/atm.2017.03.80.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Hindryckx P, Botelberge T, De Vos M, De Looze D. Clinical impact of capsule endoscopy on further strategy and long-term clinical outcome in patients with obscure bleeding. Gastrointest Endosc. 2008;68(1):98–104.  https://doi.org/10.1016/j.gie.2007.09.042.PubMedCrossRefGoogle Scholar
  85. 85.
    •• Niikura R, Yamada A, Nagata N, Kobayashi Y, Okamoto M, Mitsuno Y, et al. New predictive model of rebleeding during follow-up of patents with obscure gastrointestinal bleeding: a multicenter cohort study. J Gastroenterol Hepatol. 2016;31(4):752–60.  https://doi.org/10.1111/jgh.13201. This study provides the reader with an interesting prognostic model, which is not only able to predict rebleeding, but also future transfusion needs, length of hospital stay, and mortality rates, based on the presence of 5 risk factors: female gender, liver cirrhosis, warfarin use, overt bleeding, and positive capsule endoscopy findings.PubMedCrossRefGoogle Scholar
  86. 86.
    Rahmi G, Samaha E, Vahedi K, Delvaux M, Gay G, Lamouliatte H, et al. Long-term follow-up of patients undergoing capsule and double-balloon enteroscopy for identification and treatment of small-bowel vascular lesions: a prospective, multicenter study. Endoscopy. 2014;46(7):591–7.  https://doi.org/10.1055/s-0034-1365514.PubMedCrossRefGoogle Scholar
  87. 87.
    Ribeiro I, Pinho R, Rodrigues A, Silva J, Ponte A, Rodrigues J, et al. What is the long-term outcome of a negative capsule endoscopy in patients with obscure gastrointestinal bleeding? Rev Esp Enferm Dig. 2015;107(12):753–8.PubMedGoogle Scholar
  88. 88.
    Tan W, Ge ZZ, Gao YJ, Li XB, Dai J, Fu SW, et al. Long-term outcome in patients with obscure gastrointestinal bleeding after capsule endoscopy. J Dig Dis. 2015;16(3):125–34.  https://doi.org/10.1111/1751-2980.12222.PubMedCrossRefGoogle Scholar
  89. 89.
    Min YW, Kim JS, Jeon SW, Jeen YT, Im JP, Cheung DY, et al. Long-term outcome of capsule endoscopy in obscure gastrointestinal bleeding: a nationwide analysis. Endoscopy. 2014;46(1):59–65.  https://doi.org/10.1055/s-0033-1358803.PubMedGoogle Scholar
  90. 90.
    Ormeci A, Akyuz F, Baran B, Gokturk S, Ormeci T, Pinarbasi B, et al. What is the impact of capsule endoscopy in the long term period? World J Gastrointest Endosc. 2016;8(7):344–8.  https://doi.org/10.4253/wjge.v8.i7.344.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Matsumura T, Arai M, Saito K, Okimoto K, Saito M, Minemura S, Oyamada A, Maruoka D, Nakagawa T, Watabe H, Katsuno T, Yokosuka O. Predictive factor of re-bleeding after negative capsule endoscopy for obscure gastrointestinal bleeding: over 1-year follow-up study. Digest Endosc. 2014.  https://doi.org/10.1111/den.12257
  92. 92.
    Mai SH, Chao DC, Liao SY, Jackson CS. Nonisolated small bowel gastrointestinal angiodysplasias are associated with higher rebleeding rates when compared with isolated small bowel gastrointestinal angiodysplasia on video capsule endoscopy. J Clin Gastroenterol. 2017;  https://doi.org/10.1097/MCG.0000000000000836.
  93. 93.
    Shinozaki S, Yano T, Sakamoto H, Sunada K, Hayashi Y, Sato H, et al. Long-term outcomes in patients with overt obscure gastrointestinal bleeding after negative double-balloon endoscopy. Dig Dis Sci. 2015;60(12):3691–6.  https://doi.org/10.1007/s10620-015-3792-8.PubMedCrossRefGoogle Scholar
  94. 94.
    •• Yung DE, Koulaouzidis A, Avni T, Kopylov U, Giannakou A, Rondonotti E, et al. Clinical outcomes of negative small-bowel capsule endoscopy for small-bowel bleeding: a systematic review and meta-analysis. Gastrointest Endosc. 2017;85(2):305–317 e302.  https://doi.org/10.1016/j.gie.2016.08.027. This large systematic review and meta-analysis showed that negative capsule endoscopies were associated with low rebleeding rates. However, this protective effect was only observed for a period of 2 years.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Cedric Van de Bruaene
    • 1
  • Pieter Hindryckx
    • 1
  • Laurens Van de Bruaene
    • 2
  • Danny De Looze
    • 1
  1. 1.Department of GastroenterologyGhent University HospitalGhentBelgium
  2. 2.Department of Internal MedicineGhent University HospitalGhentBelgium

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