{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T15:32:55Z","timestamp":1790263975624,"version":"4.1.0"},"reference-count":44,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2019,12,28]],"date-time":"2019-12-28T00:00:00Z","timestamp":1577491200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004587","name":"Instituto de Salud Carlos III","doi-asserted-by":"publisher","award":["PI17\/00669"],"award-info":[{"award-number":["PI17\/00669"]}],"id":[{"id":"10.13039\/501100004587","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Background: We aimed to describe risk factors for gastrointestinal (GI) bleeding and endoscopic findings in patients with hereditary hemorrhagic telangiectasia (HHT). Methods: This is a prospective study from a referral HHT unit. Endoscopic tests were performed when there was suspicion of GI bleeding, and patients were divided as follows: with, without, and with unsuspected GI involvement. Results: 67 (27.9%) patients with, 28 (11.7%) patients without, and 145 (60.4%) with unsuspected GI involvement were included. Age, tobacco use, endoglin (ENG) mutation, and hemoglobin were associated with GI involvement. Telangiectases were mostly in the stomach and duodenum, but 18.5% of patients with normal esophagogastroduodenoscopy (EGD) had GI involvement in video capsule endoscopy (VCE). Telangiectases \u2264 3 mm and \u226410 per location were most common. Among patients with GI disease, those with hemoglobin &lt; 8 g\/dL or transfusion requirements (65.7%) were older and had higher epistaxis severity score (ESS) and larger telangiectases (&gt;3 mm). After a mean follow-up of 34.2 months, patients with GI involvement required more transfusions and more emergency department and hospital admissions, with no differences in mortality. Conclusions: Risk factors for GI involvement have been identified. Patients with GI involvement and severe anemia had larger telangiectases and higher ESS. VCE should be considered in patients with suspicion of GI bleeding, even if EGD is normal.<\/jats:p>","DOI":"10.3390\/jcm9010082","type":"journal-article","created":{"date-parts":[[2019,12,30]],"date-time":"2019-12-30T05:49:41Z","timestamp":1577684981000},"page":"82","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Gastrointestinal Bleeding in Patients with Hereditary Hemorrhagic Telangiectasia: Risk Factors and Endoscopic Findings"],"prefix":"10.3390","volume":"9","author":[{"given":"Jos\u00e9 Mar\u00eda","family":"Mora-Luj\u00e1n","sequence":"first","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Internal Medicine Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adriana","family":"Iriarte","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Internal Medicine Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Esther","family":"Alba","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Radiology Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miguel \u00c1ngel","family":"S\u00e1nchez-Corral","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Cardiology Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Berrozpe","sequence":"additional","affiliation":[{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Gastroenterolgy Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pau","family":"Cerd\u00e0","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Internal Medicine Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesc","family":"Cruellas","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Otorhinolaringology Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jes\u00fas","family":"Ribas","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Pneumology Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jose","family":"Castellote","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Gastroenterolgy Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9411-804X","authenticated-orcid":false,"given":"Antoni","family":"Riera-Mestre","sequence":"additional","affiliation":[{"name":"HHT Unit, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Internal Medicine Department, Hospital Universitari de Bellvitge, 08907 Barcelona, Spain"},{"name":"Bellvitge Biomedical Research Institute (IDIBELL), L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"},{"name":"Clinical Sciences Department, Faculty of Medicine and Health Sciences, Universitat de Barcelona, L\u2019Hospitalet de Llobregat, 08907 Barcelona, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,12,28]]},"reference":[{"key":"ref_1","unstructured":"(2019, July 22). The Portal for Rare Diseases and Orphan Drugs. Available online: https:\/\/www.orpha.net\/consor\/cgi-bin\/index.php."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fgene.2015.00001","article-title":"Hereditary hemorrhagic telangiectasia: Genetics and molecular diagnostics in a new era","volume":"6","author":"McDonald","year":"2015","journal-title":"Front. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1136\/thoraxjnl-2013-203720","article-title":"The UK prevalence of hereditary haemorrhagic telangiectasia and its association with sex, socioeconomic status and region of residence: A population-based study","volume":"69","author":"Donaldson","year":"2014","journal-title":"Thorax"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1136\/jmg.2009.069013","article-title":"HHT Foundation International Guidelines Working Group. International guidelines for the diagnosis and management of hereditary haemorrhagic telangiectasia","volume":"48","author":"Faughnan","year":"2011","journal-title":"J. Med. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1002\/(SICI)1096-8628(20000306)91:1<66::AID-AJMG12>3.0.CO;2-P","article-title":"Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu- Osler-Weber syndrome)","volume":"91","author":"Shovlin","year":"2000","journal-title":"Am. J. Med. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1186\/s13023-018-0850-2","article-title":"European Reference Network for Rare Vascular Diseases (VASCERN) Outcome measures for Hereditary Haemorrhagic Telangiectasia (HHT)","volume":"13","author":"Shovlin","year":"2018","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1136\/jmg.2005.030833","article-title":"Hereditary haemorrhagic telangiectasia: Current views on genetics and mechanisms of disease","volume":"43","author":"Abdalla","year":"2006","journal-title":"J. Med. Genet."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1016\/S0140-6736(04)15732-2","article-title":"A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4)","volume":"363","author":"Gallione","year":"2004","journal-title":"Lancet"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1097\/GIM.0b013e31802d8373","article-title":"French-Italian-Rendu-Osler Network. Genotype-phenotype correlations in hereditary hemorrhagic telangiectasia: Data from the French-Italian HHT network","volume":"9","author":"Lesca","year":"2007","journal-title":"Genet. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"456","DOI":"10.3389\/fgene.2014.00456","article-title":"Emerging roles of BMP9 and BMP10 in hereditary hemorrhagic telangiectasia","volume":"5","author":"Tillet","year":"2015","journal-title":"Front. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1111\/1523-1747.ep12555569","article-title":"Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia","volume":"95","author":"Braverman","year":"1990","journal-title":"J. Investig. Dermatol."},{"key":"ref_12","first-page":"468","article-title":"Computerized registry of patients with hemorrhagic hereditary telangiectasia (RiHHTa Registry) in Spain: Objectives, methods, and preliminary results","volume":"218","author":"Cabeza","year":"2018","journal-title":"Rev. Clin. Esp."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/gim.2013.62","article-title":"Endoscopic evaluation of gastrointestinal tract in patients with hereditary hemorrhagic telangiectasia and correlation with their genotypes","volume":"16","author":"Canzonieri","year":"2014","journal-title":"Genet. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0016-5085(63)80110-9","article-title":"Hereditary hemorrhagic telangiectasia and gastrointestinal hemorrhage","volume":"44","author":"Smith","year":"1963","journal-title":"Gastroenterology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1016\/S0016-5085(86)80001-4","article-title":"Gastrointestinal lesions in hereditary hemorrhagic telangiectasia","volume":"91","author":"Vase","year":"1986","journal-title":"Gastroenterology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1111\/j.1572-0241.2000.01792.x","article-title":"Gastrointestinal bleeding in patients with hereditary hemorrhagic telangiectasia","volume":"95","author":"Kjeldsen","year":"2000","journal-title":"Am. J. Gastroenterol."},{"key":"ref_17","first-page":"115","article-title":"Enteroscopic evaluation of the gastrointestinal tract in symptomatic patients with hereditary hemorrhagic telangiectasia","volume":"39","author":"Proctor","year":"2005","journal-title":"J. Clin. Gastroenterol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.1055\/s-2004-826045","article-title":"Evidence of small-bowel involvement in hereditary hemorrhagic telangiectasia: A capsule-endoscopic study","volume":"36","author":"Ingrosso","year":"2004","journal-title":"Endoscopy"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1097\/01.meg.0000252633.88419.04","article-title":"Assessment of intestinal vascular malformations in patients with hereditary hemorrhagic teleangiectasia and anemia","volume":"19","author":"Letteboer","year":"2007","journal-title":"Eur. J. Gastroenterol. Hepatol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1055\/s-2007-966349","article-title":"Evaluation of patients with hereditary hemorrhagic telangiectasia with video capsule endoscopy: A single-center prospective study","volume":"39","author":"Chamberlain","year":"2007","journal-title":"Endoscopy"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/j.1572-0241.2003.07185.x","article-title":"Diagnosis and management of gastrointestinal bleeding in patients with hereditary hemorrhagic telangiectasia","volume":"98","author":"Longacre","year":"2003","journal-title":"Am. J. Gastroenterol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1016\/0140-6736(90)91010-8","article-title":"Treatment of bleeding gastrointestinal vascular malformations with oestrogen-progesterone","volume":"335","author":"Rutgeerts","year":"1990","journal-title":"Lancet"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"573","DOI":"10.7326\/0003-4819-147-8-200710160-00010","article-title":"STROBE Initiative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: Guidelines for reporting observational studies","volume":"147","author":"Altman","year":"2007","journal-title":"Ann. Intern. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1002\/lary.20818","article-title":"An epistaxis severity score for hereditary hemorrhagia telangiectasia","volume":"120","author":"Hoag","year":"2010","journal-title":"Laryngoscope"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.medcli.2018.09.015","article-title":"Hemorrhagic hereditary telangiectasia in adult patients","volume":"152","author":"Ribas","year":"2019","journal-title":"Med. Clin."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1016\/0002-9149(91)90287-U","article-title":"Two-dimensional contrast echocardiography in the detection and follow-up of congenital pulmonary arteriovenous malformations","volume":"68","author":"Barzilai","year":"1991","journal-title":"Am. J. Cardiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"10643","DOI":"10.3748\/wjg.v22.i48.10643","article-title":"Prevalence of upper gastrointestinal bleeding risk factors among the general population and osteoarthritis patients","volume":"22","author":"Kim","year":"2016","journal-title":"World J. Gastroenterol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1136\/jmg.40.8.585","article-title":"Hereditary haemorrhagic telangiectasia: A questionnaire based study to delineate the different phenotypes caused by endoglin and ALK1 mutations","volume":"40","author":"Berg","year":"2003","journal-title":"J. Med. Genet."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1111\/j.1538-7836.2007.02531.x","article-title":"Hereditary hemorrhagic telangiectasia: Clinical features in ENG and ALK1 mutation carriers","volume":"5","author":"Pasculli","year":"2007","journal-title":"J. Thromb. Haemost."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1136\/jmg.2005.035451","article-title":"Genotype-phenotype relationship in hereditary haemorrhagic telangiectasia","volume":"43","author":"Letteboer","year":"2006","journal-title":"J. Med. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2623","DOI":"10.1007\/s10620-017-4719-3","article-title":"Gastrointestinal manifestations of hereditary hemorrhagic telangiectasia (HHT): A systematic review of the literature","volume":"62","author":"Jackson","year":"2017","journal-title":"Dig. Dis. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1186\/s13023-016-0427-x","article-title":"Life expextancy of parents with hereditary haemorrhagic telangiectasia","volume":"11","author":"Edwards","year":"2016","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1390","DOI":"10.1016\/j.jacep.2017.04.022","article-title":"Systemic octreotide therapy in prevention of gastrointestinal bleeds related to arteriovenous malformations and obscure etiology in atrial fibrillation","volume":"3","author":"Vuddanda","year":"2017","journal-title":"Jacc. Clin. Electrophysiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1007\/s10620-010-1193-6","article-title":"Somatostatin analogues in the treatment of recurrent bleeding from gastrointestinal vascular malformations: An overview and systematic review of prospective observational studies","volume":"55","author":"Brown","year":"2010","journal-title":"Dig. Dis. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e00088","DOI":"10.14309\/crj.0000000000000088","article-title":"Successful treatment of hereditary hemorrhagic telangiectasia with octreotide","volume":"6","author":"Houghton","year":"2019","journal-title":"Acg. Case Rep. J."},{"key":"ref_36","first-page":"1","article-title":"Octreotide for gastrointestinal bleeding in hereditary hemorrhagic telangiectasia: A prospective case series","volume":"28","author":"Kroon","year":"2019","journal-title":"Am. J. Hematol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.mayocp.2017.11.013","article-title":"Intravenous Bevacizumab for refractory hereditary hemorrhagic telangiectasia related epistaxis and gastrointestinal bleeding","volume":"93","author":"Lyer","year":"2018","journal-title":"Mayo Clin. Proc."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"792","DOI":"10.4240\/wjgs.v8.i12.792","article-title":"Bevacizumab and gastrointestinal bleeding in hereditary hemorrhagic telangiectasia","volume":"8","author":"Ou","year":"2016","journal-title":"World J. Gastrointest. Surg."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1186\/s13023-018-0982-4","article-title":"Safety of thalidomide and bevacizumab in patients with hereditary hemorrhagic telangiectasia","volume":"14","author":"Buscarini","year":"2019","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_40","first-page":"1114","article-title":"Successful treatment of thalidomide for recurrent bleeding due to gastric angiodysplasia in hereditary hemorrhagic telangiectasia","volume":"17","author":"Wang","year":"2013","journal-title":"Eur. Rev. Med. Pharm. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Alam, M.A., Sami, S., and Babu, S. (2011). Successful treatment of bleeding gastro-intestinal angiodysplasia in hereditary haemorrhagic telangiectasia with thalidomide. Case Rep., 2011.","DOI":"10.1136\/bcr.08.2011.4585"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1124\/mol.110.067447","article-title":"Immunosuppressor FK506 increases endoglin and activin receptor-like kinase 1 expression and modulates transforming growth factor-\u03b21 signaling in endothelial","volume":"79","author":"Botella","year":"2011","journal-title":"Mol. Pharmacol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Iriarte, A., Figueras, A., Cerd\u00e0, P., Mora, J.M., Jucgl\u00e0, A., Pen\u00edn, R., Vi\u00f1als, F., and Riera-Mestre, A. (2019). PI3K (Phosphatidylinositol 3-Kinase) activation and endothelial cell proliferation in patients with hemorrhagic hereditary telangiectasia type 1. Cells, 8.","DOI":"10.3390\/cells8090971"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Ruiz, S., Zhao, H., Chandakkar, P., Papoin, J., Choi, H., Nomura-Kitabayashi, A., Patel, R., Gillen, M., Diao, L., and Chatterjee, P.K. (2019). Correcting Smad1\/5\/8, mTOR, and VEGFR2 treats pathology in hereditary hemorrhagic telangiectasia models. J. Clin. Invest., 127425.","DOI":"10.1172\/JCI127425"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/9\/1\/82\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:46:21Z","timestamp":1760190381000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/9\/1\/82"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,28]]},"references-count":44,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,1]]}},"alternative-id":["jcm9010082"],"URL":"https:\/\/doi.org\/10.3390\/jcm9010082","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,28]]}}}