Abstract
Background and aim
Double-balloon enteroscopy (DBE) performed to investigate overt small bowel bleeding can miss the source of bleeding. We investigated the clinical outcomes of patients with negative DBE results for suspected overt small bowel bleeding, which is defined in the current guidelines as obscure gastrointestinal bleeding.
Methods
We reviewed the prospectively collected medical records of patients who underwent DBE at our hospital between May 1, 2004 and April 30, 2016. During this period, 297 patients underwent DBE for suspected overt small bowel bleeding. The first DBE yielded negative results for 83 patients (27.9%). Written interviews, telephone interviews, and medical records of these patients were reviewed in April 2017. Follow-up data were collected for 63 patients (75.9%).
Results
During a mean follow-up period of 83.5 months, re-bleeding occurred in 21 of 63 patients (33.3%) after a mean of 23.0 months after the first DBE yielded negative results. The bleeding source was identified in 19 of 21 patients (90.5%). In 15 of these 19 patients (78.9%), the source was the small intestine. Among these 15 patients, 14 (93.3%) had bleeding sites within reach of the first DBE and 3 (20%) experienced their first incidence of re-bleeding more than 3 years after the first DBE. The need for transfusion for the first bleeding episode was a predictor of re-bleeding (odds ratio 7.5; 95% confidence interval 1.7–33.0).
Conclusions
False-negative DBE results for overt small bowel bleeding are not rare, and the first re-bleeding episode can occur 3 years later. Repeat DBE when re-bleeding occurs should be considered, even if the first DBE results were negative.
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References
Okazaki H, Fujiwara Y, Sugimori S, Nagami Y, Kameda N, Machida H, Yamagami H, Tanigawa T, Shiba M, Watanabe K, Tominaga K, Watanabe T, Oshitani N, Arakawa T (2009) Prevalence of mid-gastrointestinal bleeding in patients with acute overt gastrointestinal bleeding: multi-center experience with 1,044 consecutive patients. J Gastroenterol 44:550–555
Longstreth GF (1997) Epidemiology and outcome of patients hospitalized with acute lower gastrointestinal hemorrhage: a population-based study. Am J Gastroenterol 92:419–424
Gerson LB, Fidler JL, Cave DR, Leighton JA (2015) ACG clinical guideline: diagnosis and management of small bowel bleeding. Am J Gastroenterol 110:1265–1287
ASGE Standards of Practice Committee, Gurudu SR, Bruining DH, Acosta RD, Eloubeidi MA, Faulx AL, Khashab MA, Kothari S, Lightdale JR, Muthusamy VR, Yang J, DeWitt JM (2017) The role of endoscopy in the management of suspected small-bowel bleeding. Gastrointest Endosc 85:22–31
Yamamoto H, Sekine Y, Sato Y, Higashizawa T, Miyata T, Iino S, Ido K, Sugano K (2001) Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc 53:216–220
Shinozaki S, Yamamoto H, Yano T, Sunada K, Miyata T, Hayashi Y, Arashiro M, Sugano K (2010) Long-term outcome of patients with obscure gastrointestinal bleeding investigated by double-balloon endoscopy. Clin Gastroenterol Hepatol 8:151–158
Yamamoto H, Kita H, Sunada K, Hayashi Y, Sato H, Yano T, Iwamoto M, Sekine Y, Miyata T, Kuno A, Ajibe H, Ido K, Sugano K (2004) Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases. Clin Gastroenterol Hepatol 2:1010–1016
Teshima CW, Kuipers EJ, van Zanten SV, Mensink PB (2011) Double balloon enteroscopy and capsule endoscopy for obscure gastrointestinal bleeding: an updated meta-analysis. J Gastroenterol Hepatol 26:796–801
Xin L, Liao Z, Jiang YP, Li ZS (2011) Indications, detectability, positive findings, total enteroscopy, and complications of diagnostic double-balloon endoscopy: a systematic review of data over the first decade of use. Gastrointest Endosc 74:563–570
Fry LC, Bellutti M, Neumann H, Malfertheiner P, Mönkemüller K (2009) 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 29:342–349
Tee HP, Kaffes AJ (2010) Non-small-bowel lesions encountered during double-balloon enteroscopy performed for obscure gastrointestinal bleeding. World J Gastroenterol 16:1885–1889
Wadhwa V, Sethi S, Tewani S, Garg SK, Pleskow DK, Chuttani R, Berzin TM, Sethi N, Sawhney MS (2015) A meta-analysis on efficacy and safety: single-balloon vs. double-balloon enteroscopy. Gastroenterol Rep (Oxford) 3:148–155
Shinozaki S, Yamamoto H, Yano T, Sunada K, Hayashi Y, Shinhata H, Sato H, Despott EJ, Sugano K (2014) Favorable long-term outcomes of repeat endotherapy for small-intestine vascular lesions by double-balloon endoscopy. Gastrointest Endosc 80:112–117
Rahmi G, Samaha E, Vahedi K, Delvaux M, Gay G, Lamouliatte H, Filoche B, Saurin JC, Ponchon T, Rhun ML, Coumaros D, Bichard P, Manière T, Lenain E, Chatellier G, Cellier C (2014) Long-term follow-up of patients under-going capsule and double-balloon enteroscopy for identification and treatment of small-bowel vascular lesions: a prospective, multicenter study. Endoscopy 46:591–597
Samaha E, Rahmi G, Landi B, Lorenceau-Savale C, Malamut G, Canard JM, Bloch F, Jian R, Chatellier G, Cellier C (2012) Long-term outcome of patients treated with double balloon enteroscopy for small bowel vascular lesions. Am J Gastroenterol 107:240–246
May A, Friesing-Sosnik T, Manner H, Pohl K, Ell C (2011) Long-term outcome after argon plasma coagulation of small-bowel lesions using double-balloon enteroscopy in patients with mid-gastrointestinal bleeding. Endoscopy 43:759–765
Jeon SR, Byeon JS, Jang HJ, Park SJ, Im JP, Kim ER, Koo JS, Ko BM, Chang DK, Kim JO, Park SY (2017) Clinical outcome after enteroscopy for small bowel angioectasia bleeding: a Korean Association for the Study of Intestinal Disease (KASID) multicenter study. J Gastroenterol Hepatol 32:388–394
Pinho R, Mascarenhas-Saraiva M, Mão-de-Ferro S, Ferreira S, Almeida N, Figueiredo P, Rodrigues A, Cardoso H, Marques M, Rosa B, Cotter J, Vilas-Boas G, Cardoso C, Salgado M, Marcos-Pinto R (2016) Multicenter survey on the use of device-assisted enteroscopy in Portugal. United Eur Gastroenterol J 4:264–274
Sun B, Rajan E, Cheng S, Shen R, Zhang C, Zhang S, Wu Y, Zhong J (2006) Diagnostic yield and therapeutic impact of double-balloon enteroscopy in a large cohort of patients with obscure gastrointestinal bleeding. Am J Gastroenterol 101:2011–2015
Gerson LB, Batenic MA, Newsom SL, Ross A, Semrad CE (2009) Long-term outcomes after double-balloon enteroscopy for obscure gastrointestinal bleeding. Clin Gastroenterol Hepatol 7:664–669
Shinozaki S, Yano T, Sakamoto H, Sunada K, Hayashi Y, Sato H, Lefor AK, Yamamoto H (2015) Long-term outcomes in patients with overt obscure gastrointestinal bleeding after negative double-balloon endoscopy. Dig Dis Sci 60:3691–3696
Yano T, Yamamoto H, Sunada K, Miyata T, Iwamoto M, Hayashi Y, Arashiro M, Sugano K (2008) Endoscopic classification of vascular lesions of the small intestine (with videos). Gastrointest Endosc 67:169–172
Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48:452–458
Hashimoto R, Chonan A (2017) Duodenal diverticular bleeding missed repeatedly at endoscopy. Clin Gastroenterol Hepatol 15:e79
Aniwan S, Viriyautsahakul V, Rerknimitr R, Angsuwatcharakon P, Kongkam P, Treeprasertsuk S, Kullavanijaya P (2014) Urgent double balloon endoscopy provides higher yields than non-urgent double balloon endoscopy in overt obscure gastrointestinal bleeding. Endosc Int Open 2:E90–E95
Pinto-Pais T, Pinho R, Rodrigues A, Fernandes C, Ribeiro I, Fraga J, Carvalho J (2014) Emergency single-balloon enteroscopy in overt obscure gastrointestinal bleeding: efficacy and safety. United Eur Gastroenterol J 2:490–496
Monkemuller K, Neumann H, Meyer F, Kuhn R, Malfertheiner P, Fry LC (2009) A retrospective analysis of emergency double-balloon enteroscopy for small-bowel bleeding. Endoscopy 41:715–717
Chu Y, Wu S, Qian Y, Wang Q, Li J, Tang Y, Bai T, Wang L (2016) Complimentary imaging modalities for investigating obscure gastrointestinal bleeding: capsule endoscopy, double-balloon enteroscopy, and computed tomographic enterography. Gastroenterol Res Pract 2016:8367519
Agrawal JR, Travis AC, Mortele KJ, Silverman SG, Maurer R, Reddy SI, Saltzman JR (2012) Diagnostic yield of dual-phase computed tomography enterography in patients with obscure gastrointestinal bleeding and a non-diagnostic capsule endoscopy. J Gastroenterol Hepatol 27:751–759
Wu LM, Xu JR, Yin Y, Qu XH (2010) Usefulness of CT angiography in diagnosing acute gastrointestinal bleeding: a meta-analysis. World J Gastroenterol 16:3957–3963
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Study conception and design: RH, TM, MN; Data analysis and interpretation: RH, TM; Drafting of the article: RH; Critical revision: TM, MN; Final approval of the article: TM.
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Drs. Rintaro Hashimoto, Tomoki Matsuda, and Masato Nakahori have no conflicts of interest or financial ties to disclose.
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Hashimoto, R., Matsuda, T. & Nakahori, M. False-negative double-balloon enteroscopy in overt small bowel bleeding: long-term follow-up after negative results. Surg Endosc 33, 2635–2641 (2019). https://doi.org/10.1007/s00464-018-6561-x
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DOI: https://doi.org/10.1007/s00464-018-6561-x