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CC BY-NC-ND 4.0 · Endosc Int Open 2019; 07(02): E282-E289
DOI: 10.1055/a-0799-9820
Original article
Owner and Copyright © Georg Thieme Verlag KG 2019

Diagnostic yield of capsule endoscopy for small bowel arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia: a systematic review and meta-analysis

Kevin Singh
1   Department of Internal Medicine, New York University School of Medicine, Woodhull Medical and Mental Health Center, Brooklyn, New York, United States
,
Ayla Zubair
1   Department of Internal Medicine, New York University School of Medicine, Woodhull Medical and Mental Health Center, Brooklyn, New York, United States
,
Andrew Prindle
1   Department of Internal Medicine, New York University School of Medicine, Woodhull Medical and Mental Health Center, Brooklyn, New York, United States
,
Ahmed Jamal Nadeem
2   Department of Hematology and Oncology, Lehigh Valley Health Network, Allentown, Pennsylvania, United States
,
Gulam Khan
3   Department of Gastroenterology and Hepatology, New York University School of Medicine, Woodhull Medical and Mental Health Center, Brooklyn, New York, United States
› Author Affiliations
Further Information

Publication History

submitted 04 July 2018

accepted after submission 02 October 2018

Publication Date:
30 January 2019 (online)

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Abstract

Background and study aims Small bowel arteriovenous malformations (AVMs) pose a bleeding risk and have traditionally been diagnosed by invasive enteroscopic procedures in patients with hereditary hemorrhagic telangiectasia (HHT). Capsule endoscopy (CE) is emerging as a safe and non-invasive alternative for small intestinal evaluation, but its diagnostic yield and utility in diagnosing small bowel AVMs in HHT patients are understudied. The aim of this study was to meta-analyze the utility of CE for diagnosing AVMs in HHT patients.

Methods A meta-analysis and systematic review of the literature on CE in HHT patients identified in the PubMed, EMBASE, Scopus, and Cochrane databases from inception to March 2018 were conducted. Summary effects were estimated using a random effects model.

Results After applying exclusion criteria, five studies (n = 124 patients) were eligible for meta-analysis. The pooled diagnostic yield for visualization of small bowel AVMs by CE was 77.0 % (95 % CI 65.8 – 85.4 %, P < 0.001).

Conclusions CE has a good diagnostic yield for small bowel AVMs in HHT. It can be regarded as a sufficient, noninvasive diagnostic modality for identifying small bowel AVMs in HHT patients.

 

  • References

  • 1 Garg N, Khunger M, Gupta A. et al. Optimal management of hereditary hemorrhagic telangiectasia. J Blood Med 2014; 5: 191-206
    PubMedGoogle Scholar
  • 2 Kjeldsen AD, Kjeldsen J. Gastrointestinal bleeding in patients with hereditary hemorrhagic telangiectasia. Am J Gastroenterol 2000; 95: 415-418
    CrossrefPubMedGoogle Scholar
  • 3 Gerson LB, Fidler JL, Cave DR. et al. ACG Clinical Guideline: Diagnosis and Management of Small Bowel Bleeding. Am J Gastroenterol 2015; 110: 1265-1287 quiz 1288
    CrossrefPubMedGoogle Scholar
  • 4 Canzonieri C, Centenara L, Ornati F. et al. Endoscopic evaluation of gastrointestinal tract in patients with hereditary hemorrhagic telangiectasia and correlation with their genotypes. Genet Med 2014; 16: 3-10
    Google Scholar
  • 5 Chamberlain SM, Patel J, Carter Balart J. et al. Evaluation of patients with hereditary hemorrhagic telangiectasia with video capsule endoscopy: a single-center prospective study. Endoscopy 2007; 39: 516-520
    Article in Thieme ConnectPubMedGoogle Scholar
  • 6 Greve E, Moussata D, Gaudin JL. et al. High diagnostic and clinical impact of small-bowel capsule endoscopy in patients with hereditary hemorrhagic telangiectasia with overt digestive bleeding and/or severe anemia. Gastrointest Endosc 2010; 71: 760-767
    CrossrefPubMedGoogle Scholar
  • 7 Ingrosso M, Sabba C, Pisani A. et al. Evidence of small-bowel involvement in hereditary hemorrhagic telangiectasia: a capsule-endoscopic study. Endoscopy 2004; 36: 1074-1079
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 van Tuyl SA, Letteboer TG, Rogge-Wolf C. et al. Assessment of intestinal vascular malformations in patients with hereditary hemorrhagic teleangiectasia and anemia. Eur J Gastroenterol Hepatol 2007; 19: 153-158
    CrossrefPubMedGoogle Scholar
  • 9 Cianci R, Urgesi R, Tortora A. et al. The role of capsule endoscopy and device assisted enteroscopy for small bowel lesions in hereditary hemorrhagic telangiectasia. Dig Liver Dis 2017; 25: pii: S1590-8658(17)30891-5
    PubMedGoogle Scholar
  • 10 Westermann CJJ, Rosina AF, De Vries V. et al. The prevalence and manifestations of hereditary hemorrhagic telangiectasia in the Afro-Caribbean population of the Netherlands Antilles: A family screening. Am J Med Genet 2003; 116A: 324-328
    CrossrefPubMedGoogle Scholar
  • 11 Govani FS, Shovlin CL. Hereditary haemorrhagic telangiectasia: a clinical and scientific review. Eur J Hum Genet 2009; 17: 860-871
    PubMedGoogle Scholar
  • 12 Johnson DW, Berg JN, Baldwin MA. et al. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet 1996; 13: 189-195
    CrossrefPubMedGoogle Scholar
  • 13 McAllister KA, Grogg KM, Johnson DW. et al. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 1994; 8: 345-351
    CrossrefPubMedGoogle Scholar
  • 14 Faughnan ME, Palda VA, Garcia-Tsao G. et al. International guidelines for the diagnosis and management of hereditary haemorrhagic telangiectasia. J Med Genet 2011; 48: 73-87
    CrossrefPubMedGoogle Scholar
  • 15 Plauchu H, de Chadarevian JP, Bideau A. et al. Age-related clinical profile of hereditary hemorrhagic telangiectasia in an epidemiologically recruited population. Am J Med Genet 1989; 32: 291-297
    CrossrefPubMedGoogle Scholar
  • 16 Longacre AV, Gross CP, Gallitelli M. et al. Diagnosis and management of gastrointestinal bleeding in patients with hereditary hemorrhagic telangiectasia. Am J Gastroenterol 2003; 98: 59-65
    CrossrefPubMedGoogle Scholar
  • 17 Committee AT, Chauhan SS, Manfredi MA. et al. Enteroscopy. Gastrointest Endosc 2015; 82: 975-990
    CrossrefPubMedGoogle Scholar
  • 18 Mourad FH, Leong RW. Role of hemostatic powders in the management of lower gastrointestinal bleeding: A review. J Gastroenterol Hepatol 2018; 2018: 1-9
    PubMedGoogle Scholar
  • 19 Nardone G, Compare D, Martino A. et al. Pharmacological treatment of gastrointestinal bleeding due to angiodysplasias: A position paper of the Italian Society of Gastroenterology (SIGE). Dig Liver Dis 2018; 50: 542-548
    CrossrefPubMedGoogle Scholar
  • 20 Sami SS, Al-Araji SA, Ragunath K. Review article: gastrointestinal angiodysplasia - pathogenesis, diagnosis and management. Aliment Pharmacol Ther 2014; 39: 15-34
    CrossrefPubMedGoogle Scholar
  • 21 Gunjan D, Sharma V, Rana SS. et al. Small bowel bleeding: a comprehensive review. Gastroenterol Rep (Oxf) 2014; 2: 262-275
    CrossrefPubMedGoogle Scholar
  • 22 Gostout CJ, Bowyer BA, Ahlquist DA. et al. Mucosal vascular malformations of the gastrointestinal tract: clinical observations and results of endoscopic neodymium: yttrium-aluminum-garnet laser therapy. Mayo Clin Proc 1988; 63: 993-1003
    CrossrefPubMedGoogle Scholar
  • 23 Sargeant IR, Loizou LA, Rampton D. et al. Laser ablation of upper gastrointestinal vascular ectasias: long term results. Gut 1993; 34: 470-475
    CrossrefPubMedGoogle Scholar
  • 24 Bown SG, Swain CP, Storey DW. et al. Endoscopic laser treatment of vascular anomalies of the upper gastrointestinal tract. Gut 1985; 26: 1338-1348
    CrossrefPubMedGoogle Scholar
  • 25 Szilagyi A, Ghali MP. Pharmacological therapy of vascular malformations of the gastrointestinal tract. Can J Gastroenterol 2006; 20: 171-178
    CrossrefPubMedGoogle Scholar
  • 26 American Society of Health-System Pharmacists. ed. AHFS Clinical Drug Information. 2018 Available at: http://www.ahfsdruginformation.com/ Accessed November 14, 2018
    PubMedGoogle Scholar
  • 27 Koch HJ, Escher GC, Lewis JS. Hormonal management of hereditary hemorrhagic telangiectasia. J Am Med Assoc 1952; 149: 1376-1380
    CrossrefPubMedGoogle Scholar
  • 28 Jackson CS, Gerson LB. Management of gastrointestinal angiodysplastic lesions (GIADs): a systematic review and meta-analysis. Am J Gastroenterol 2014; 109: 474-483
    CrossrefPubMedGoogle Scholar
  • 29 Nardone G, Compare D, Martino A. et al. Pharmacological treatment of gastrointestinal bleeding due to angiodysplasias: A position paper of the Italian Society of Gastroenterology (SIGE). Dig Liver Dis 2018; 50: 542-548
    CrossrefPubMedGoogle Scholar
  • 30 Epperla N, Hocking W. Blessing for the bleeder: bevacizumab in hereditary hemorrhagic telangiectasia. Clin Med Res 2015; 13: 32-35
    CrossrefPubMedGoogle Scholar
  • 31 Sehl ME, MGruber T, McWilliams JP. et al. Successful management of chronic gastrointestinal hemorrhage using bevacizumab in the setting of hereditary hemorrhagic telangiectasia. Am J Hematol 2015; 90: 561-563
    CrossrefPubMedGoogle Scholar
  • 32 Kochanowski J, Sobieszczańska M, Tubek S. et al. Successful therapy with bevacizumab in a case of hereditary hemorrhagic telangiectasia. Hum Vaccin Immunother 2015; 11: 680-681
    CrossrefPubMedGoogle Scholar
  • 33 Bennesser AlaouiH, Lehraiki M, Hamaz S. et al. Bevacizumab: a new success in hereditary hemorrhagic telangiectasia. Rev Med Internet 2015; 36: 623-625
    PubMedGoogle Scholar
  • 34 Wee JW, Jeon YW, Eun JY. et al. Hereditary hemorrhagic telangiectasia treated with low dose intravenous bevacizumab. Blood Res 2014; 49: 192-195
    CrossrefPubMedGoogle Scholar
  • 35 Epperla N, Kapke JT, Karafin M. et al. Effect of systemic bevacizumab in severe hereditary hemorrhagic telangiectasia associated with bleeding. Am J Hematol 2016; 91: E313-314
    CrossrefPubMedGoogle Scholar
  • 36 Ou G, Galorport C, Enns R. Bevacizumab and gastrointestinal bleeding in hereditary hemorrhagic telangiectasia. World J Gastrointest Surg 2016; 8: 792-795
    CrossrefPubMedGoogle Scholar
  • 37 Bertoli LF, Lee PL, Lallone L. et al. Intravenous bevacizumab therapy in a patient with hereditary hemorrhagic telangiectasia, ENG E137K, alcoholic cirrhosis, and portal hypertension. Case Rep Gastroenterol 2017; 11: 293-304
    CrossrefPubMedGoogle Scholar
  • 38 Guilhem A, Fargeton AE, Simon AC. et al. Intravenous bevacizumab in hereditary hemorrhagic telangiectasia (HHT): A retrospective study of 46 patients. PLoS One 2017; 12: 1-12
    CrossrefPubMedGoogle Scholar
  • 39 Bernardes C, Santos S, Loureiro R. et al. Bevacizumab for refractory gastrointestinal bleeding in Rendu-Osler-Weber disease. GE Port J Gastroenterol 2018; 25: 91-95
    CrossrefPubMedGoogle Scholar
  • 40 Al-Samkari H, Kritharis A, Rodriguez-Lopez JM. et al. systemic bevacizumab for the treatment of chronic bleeding in hereditary hemorrhagic telangiectasia. J Intern Med 2018; 1: 1-19
    PubMedGoogle Scholar
  • 41 Iyer VN, Apala DR, Pannu BS. et al. Intravenous bevacizumab for refractory hereditary hemorrhagic telangiectasia-related epistaxis and gastrointestinal bleeding. Mayo Clin Proc 2018; 93: 155-166
    CrossrefPubMedGoogle Scholar
  • 42 Kanellopoulou T, Alexopoulou A. Bevacizumab in the treatment of hereditary hemorrhagic telangiectasia. Expert Opin Biol Ther 2013; 13: 1315-1323
    CrossrefPubMedGoogle Scholar
  • 43 Lupu A, Stefanescu C, Treton X. et al. Bevacizumab as rescue treatment for severe recurrent gastrointestinal bleeding in hereditary hemorrhagic telangiectasia. J Clin Gastroenterol 2013; 47: 256-257
    CrossrefPubMedGoogle Scholar
  • 44 Lazaraki G, Akriviadis E, Pilpilidis I. et al. Low dose of bevacizumab is safe and effective in preventing bleeding episodes in hereditary hemorrhagic telangiectasia. Am J Gastroenterol 2011; 106: 2204-2206
    PubMedGoogle Scholar
  • 45 Bowcock SJ, Patrick HE. Lenalidomide to control gastrointestinal bleeding in hereditary haemorrhagic telangiectasia: potential implications for angiodysplasias?. Br J Haematol 2009; 146: 220-222
    CrossrefPubMedGoogle Scholar
  • 46 Haq AU, Glass J, Netchvolodoff CV. et al. Hereditary hemorrhagic telangiectasia and danazol. Ann Intern Med 1988; 109: 171
    PubMedGoogle Scholar
  • 47 Massoud OI, Youssef WI, Mullen KD. Resolution of hereditary hemorrhagic telangiectasia and anemia with prolonged alpha-interferon therapy for chronic hepatitis C. J Clin Gastroenterol 2004; 38: 377-379
    CrossrefPubMedGoogle Scholar
  • 48 Skaro AI, Marotta PJ, McAlister VC. Regression of cutaneous and gastrointestinal telangiectasia with sirolimus and aspirin in a patient with hereditary hemorrhagic telangiectasia. Ann Intern Med 2006; 144: 226-227
    PubMedGoogle Scholar
  • 49 Park JJ, Cheon JH, Kim HM. et al. Negative capsule endoscopy without subsequent enteroscopy does not predict lower long-term rebleeding rates in patients with obscure GI bleeding. Gastrointest Endosc 2010; 71: 990-997
    CrossrefPubMedGoogle Scholar
  • 50 Kim JB, Ye BD, Song Y. et al. Frequency of rebleeding events in obscure gastrointestinal bleeding with negative capsule endoscopy. J Gastroenterol Hepatol 2013; 28: 834-840
    CrossrefPubMedGoogle Scholar
  • 51 Pongprasobchai S, Chitsaeng S, Tanwandee T. et al. Yield, etiologies and outcomes of capsule endoscopy in Thai patients with obscure gastrointestinal bleeding. World J Gastrointest Endosc 2013; 5: 122-127
    CrossrefPubMedGoogle Scholar
  • 52 Min YW, Kim JS, Jeon SW. et al. Long-term outcome of capsule endoscopy in obscure gastrointestinal bleeding: a nationwide analysis. Endoscopy 2014; 46: 59-65
    Article in Thieme ConnectPubMedGoogle Scholar
  • 53 Saurin JC, Delvaux M, Vahedi K. et al. Clinical impact of capsule endoscopy compared to push enteroscopy: 1-year follow-up study. Endoscopy 2005; 37: 318-323
    Article in Thieme ConnectPubMedGoogle Scholar
  • 54 Hindryckx P, Botelberge T, De Vos M. et al. Clinical impact of capsule endoscopy on further strategy and long-term clinical outcome in patients with obscure bleeding. Gastrointest Endosc 2008; 68: 98-104
    CrossrefPubMedGoogle Scholar
  • 55 Leighton JA, Sharma VK, Hentz JG. et al. Capsule endoscopy versus push enteroscopy for evaluation of obscure gastrointestinal bleeding with 1-year outcomes. Dig Dis Sci 2006; 51: 891-899
    CrossrefPubMedGoogle Scholar
  • 56 Strate LL, Gralnek IM. ACG Clinical Guideline: Management of patients with acute lower gastrointestinal bleeding. Am J Gastroenterol 2016; 111: 755
    CrossrefPubMedGoogle Scholar
  • 57 Gralnek IM, Dumonceau JM, Kuipers EJ. et al. Diagnosis and management of nonvariceal upper gastrointestinal hemorrhage: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: a1-46
    Article in Thieme ConnectPubMedGoogle Scholar