Angiogenesis

, Volume 18, Issue 4, pp 511–524 | Cite as

Executive summary of the 11th HHT international scientific conference

  • Helen Arthur
  • Urban Geisthoff
  • James R. Gossage
  • Christopher C. W. Hughes
  • Pascal Lacombe
  • Mary E. Meek
  • Paul Oh
  • Beth L. Roman
  • Scott O. Trerotola
  • Sebastiaan Velthuis
  • Whitney Wooderchak-Donahue
Executive Summary

Abstract

Hereditary hemorrhagic telangiectasia (HHT) is a hereditary condition that results in vascular malformations throughout the body, which have a proclivity to rupture and bleed. HHT has a worldwide incidence of about 1:5000 and approximately 80 % of cases are due to mutations in ENG, ALK1 (aka activin receptor-like kinase 1 or ACVRL1) and SMAD4. Over 200 international clinicians and scientists met at Captiva Island, Florida from June 11–June 14, 2015 to present and discuss the latest research on HHT. 156 abstracts were accepted to the meeting and 60 were selected for oral presentations. The first two sections of this article present summaries of the basic science and clinical talks. Here we have summarized talks covering key themes, focusing on areas of agreement, disagreement, and unanswered questions. The final four sections summarize discussions in the Workshops, which were theme-based topical discussions led by two moderators. We hope this overview will educate as well as inspire those within the field and from outside, who have an interest in the science and treatment of HHT.

Keywords

HHT Hereditary hemorrhagic telangiectasia Endoglin ALK1 Arteriovenous malformation Epistaxis 

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References

  1. 1.
    Shovlin CL, Hughes JM, Tuddenham EG, Temperley I, Perembelon YF, Scott J, Seidman CE, Seidman JG (1994) A gene for hereditary haemorrhagic telangiectasia maps to chromosome 9q3. Nat Genet 6:205–209CrossRefPubMedGoogle Scholar
  2. 2.
    Johnson DW, Berg JN, Baldwin MA, Gallione CJ, Marondel I, Yoon SJ, Stenzel TT, Speer M et al (1996) Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet 13:189–195CrossRefPubMedGoogle Scholar
  3. 3.
    Gallione CJ, Repetto GM, Legius E, Rustgi AK, Schelley SL, Tejpar S, Mitchell G, Drouin E et al (2004) A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4). Lancet 363:852–859CrossRefPubMedGoogle Scholar
  4. 4.
    McDonald J, Damjanovich K, Millson A, Wooderchak W, Chibuk JM, Stevenson DA, Gedge F, Bayrak-Toydemir P (2011) Molecular diagnosis in hereditary hemorrhagic telangiectasia: findings in a series tested simultaneously by sequencing and deletion/duplication analysis. Clin Genet 79:335–344CrossRefPubMedGoogle Scholar
  5. 5.
    McDonald J, Wooderchak-Donahue W, VanSant Webb C, Whitehead K, Stevenson DA, Bayrak-Toydemir P (2015) Hereditary hemorrhagic telangiectasia: genetics and molecular diagnostics in a new era. Front Genet 6(1):1–8. doi:10.3389/fgene.2015.00001
  6. 6.
    Bushby K, Finkel R, Wong B, Barohn R, Campbell C, Comi GP, Connolly AM, Day JW et al (2014) Ataluren treatment of patients with nonsense mutation dystrophinopathy. Muscle Nerve 50(4):477–487CrossRefPubMedGoogle Scholar
  7. 7.
    Kerem E, Konstan MW, De Boeck K, Accurso FJ, Sermet-Gaudelus I, Wilschanski M, Elborn JS et al (2014) Ataluren for the treatment of nonsense-mutation cystic fibrosis: a randomised, double-blind, placebo-controlled phase 3 trial. Lancet Respir Med 2(7):539–547CrossRefPubMedGoogle Scholar
  8. 8.
    Wooderchak-Donahue W, McDonald J, O’Fallon B, Upton PD, Li W, Roman BL, Young S, Plant P et al (2013) BMP9 mutations cause a vascular anomaly syndrome with phenotypic overlap with hereditary hemorrhagic telangiectasia. Am J Hum Genet 93:1–8CrossRefGoogle Scholar
  9. 9.
    Rigelsky CM, Jennings C, Lehtonen R, Minai OA, Eng C, Aldred MA (2008) BMPR2 mutation in a patient with pulmonary arterial hypertension and suspected hereditary hemorrhagic telangiectasia. Am J Med Genet A 146A(19):2551–2556CrossRefPubMedGoogle Scholar
  10. 10.
    Larrivée B, Prahst C, Gordon E, del Toro R, Mathivet T, Duarte A, Simons M, Eichmann A (2012) ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev Cell 22(3):489–500PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    Cartin-Ceba R, Swanson KL, Krowka MJ (2013) Pulmonary arteriovenous malformations. Chest 144:1033–1044CrossRefPubMedGoogle Scholar
  12. 12.
    Kjeldsen AD, Oxhoj H, Andersen PE, Green A, Vase P (2000) Prevalence of pulmonary arteriovenous malformations (PAVM) and occurrence of neurological symptoms in patients with hereditary haemorrhagic telangiectasia (HHT). J Intern Med 248:255–262CrossRefPubMedGoogle Scholar
  13. 13.
    Moussouttas M, Fayad P, Rosenblatt M, Hashimoto M, Pollak J, Henderson K, Ma TY, White RI (2000) Pulmonary arteriovenous malformations: cerebral ischemia and neurologic manifestations. Neurology 55:959–964CrossRefPubMedGoogle Scholar
  14. 14.
    Shovlin CL, Jackson JE, Bamford KB, Jenkins IH, Benjamin AR, Ramadan H, Kulinskaya E (2008) Primary determinants of ischaemic stroke/brain abscess risks are independent of severity of pulmonary arteriovenous malformations in hereditary haemorrhagic telangiectasia. Thorax 63:259–266CrossRefPubMedGoogle Scholar
  15. 15.
    Velthuis S, Buscarini E, van Gent MW, Gazzaniga P, Manfredi G, Danesino C, Schonewille WJ, Westermann CJ et al (2013) Grade of pulmonary right-to-left shunt on contrast echocardiography and cerebral complications: a striking association. Chest 144:542–548CrossRefPubMedGoogle Scholar
  16. 16.
    Faughnan ME, Palda VA, Garcia-Tsao G, Geisthoff UW, McDonald J, Proctor DD, Spears J, Brown DH et al (2011) International guidelines for the diagnosis and management of hereditary haemorrhagic telangiectasia. J Med Genet 48:73–87CrossRefPubMedGoogle Scholar
  17. 17.
    Velthuis S, Buscarini E, Gossage JR, Snijder RJ, Mager JJ, Post MC (2015) Clinical implications of pulmonary shunting on saline contrast echocardiography. J Am Soc Echocardiogr 28:255–263CrossRefPubMedGoogle Scholar
  18. 18.
    Elliott JE, Nigam SM, Laurie SS, Beasley KM, Goodman RD, Hawn JA, Gladstone IM, Chesnutt MS, Lovering AT (2013) Prevalence of left heart contrast in healthy, young, asymptomatic humans at rest breathing room air. Respir Physiol Neurobiol 188:71–78CrossRefPubMedGoogle Scholar
  19. 19.
    Lovering AT, Stickland MK, Amann M, Murphy JC, O’Brien MJ, Hokanson JS, Eldridge MW (2008) Hyperoxia prevents exercise-induced intrapulmonary arteriovenous shunt in healthy humans. J Physiol 586(18):4559–4565PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Li W, Niu B, Henderson K, Northrup V, Pollak JS, Trow T, Fahey J, White RI Jr (2011) Reproducibility of oxygen saturation monitoring during six-minute walk test and exercise stress test in patients with pulmonary arteriovenous malformations associated with hereditary hemorrhagic telangiectasia. Pediatr Cardiol 32:590–594CrossRefPubMedGoogle Scholar
  21. 21.
    Faughnan ME, Thabet A, Mei-Zahav M, Colombo M, Maclusky I, Hyland RH, Pugash RA, Chait P, Henderson KJ, White RI (2004) Pulmonary arteriovenous malformations in children: outcomes of transcatheter embolotherapy. J Pediatr 145:826–831CrossRefPubMedGoogle Scholar
  22. 22.
    Galiè N, Hoeper MM, Humbert M, Torbicki A, Vachiery JL, Barbera JA, Beghetti M, Corris P et al (2009) Guidelines for the diagnosis and treatment of pulmonary hypertension: the Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS), endorsed by the International Society of Heart and Lung Transplantation (ISHLT). Eur Heart J 30:2493–2537CrossRefPubMedGoogle Scholar
  23. 23.
    Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, Charlton R, Parums DV et al (2000) Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 217:42–53CrossRefPubMedGoogle Scholar
  24. 24.
    Bourdeau A, Dumont DJ, Letarte M (1999) A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 104:1343–1351PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    Mahmoud M, Allinson KR, Zhai Z, Oakenfull R, Ghandi P, Adams RH, Fruttiger M, Arthur HM (2010) Pathogenesis of arteriovenous malformations in the absence of endoglin. Circ Res 106:1425–1433CrossRefPubMedGoogle Scholar
  26. 26.
    Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K et al (2000) Activin receptor-like kinase 1 modulates transforming growth factor-b1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 97:2626–2631PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Park SO, Lee YJ, Seki T, Hong KH, Fliess N, Jiang Z, Park A, Wu X et al (2008) ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2. Blood 111:633–642PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Park SO, Wankhede M, Lee YJ, Choi EJ, Fliess N, Choe SW, Oh SH, Walter G et al (2009) Real-time imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia. J Clin Invest 119:3487–3496PubMedCentralPubMedGoogle Scholar
  29. 29.
    Roman BL, Pham VN, Lawson ND, Kulik M, Childs S, Lekven AC, Garrity DM, Moon RT et al (2002) Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129:3009–3019PubMedGoogle Scholar
  30. 30.
    Srinivasan S, Hanes MA, Dickens T, Porteous ME, Oh SP, Hale LP, Marchuk DA (2003) A mouse model for hereditary hemorrhagic telangiectasia (HHT) type 2. Hum Mol Genet 12:473–482CrossRefPubMedGoogle Scholar
  31. 31.
    Urness LD, Sorensen LK, Li DY (2000) Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat Genet 26:328–331CrossRefPubMedGoogle Scholar
  32. 32.
    Bourdeau A, Cymerman U, Paquet ME, Meschino W, McKinnon WC, Guttmacher AE, Becker L, Letarte M (2000) Endoglin expression is reduced in normal vessels but still detectable in arteriovenous malformations of patients with hereditary hemorrhagic telangiectasia type 1. Am J Pathol 156:911–923PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Hawinkels LJ, Kuiper P, Wiercinska E, Verspaget HW, Liu Z, Pardali E, Sier CF, ten Dijke P (2010) Matrix metalloproteinase-14 (MT1–MMP)-mediated endoglin shedding inhibits tumor angiogenesis. Cancer Res 70:4141–4150CrossRefPubMedGoogle Scholar
  34. 34.
    Valbuena-Diez AC, Blanco FJ, Oujo B, Langa C, Gonzalez-Nunez M, Llano E, Pendas AM, Diaz M et al (2012) Oxysterol-induced soluble endoglin release and its involvement in hypertension. Circulation 126:2612–2624CrossRefPubMedGoogle Scholar
  35. 35.
    Mallet C, Lamribet K, Giraud S, Dupuis-Girod S, Feige JJ, Bailly S, Tillet E (2014) Functional analysis of endoglin mutations from hereditary hemorrhagic telangiectasia type 1 patients reveals different mechanisms for endoglin loss of function. Hum Mol Genet 24(4):1142–1154CrossRefPubMedGoogle Scholar
  36. 36.
    Corti P, Young S, Chen CY, Patrick MJ, Rochon ER, Pekkan K, Roman BL (2011) Interaction between alk1 and blood flow in the development of arteriovenous malformations. Development 138:1573–1582PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Choi EJ, Walker EJ, Shen F, Oh SP, Arthur HM, Young WL, Su H (2012) Minimal homozygous endothelial deletion of Eng with VEGF stimulation is sufficient to cause cerebrovascular dysplasia in the adult mouse. Cerebrovasc Dis 33:540–547PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Garrido-Martin EM, Nguyen HL, Cunningham TA, Choe SW, Jiang Z, Arthur HM, Lee YJ, Oh SP (2014) Common and distinctive pathogenetic features of arteriovenous malformations in hereditary hemorrhagic telangiectasia 1 and hereditary hemorrhagic telangiectasia 2 animal models—brief report. Arterioscler Thromb Vasc Biol 34:2232–2236CrossRefPubMedGoogle Scholar
  39. 39.
    Han C, Choe SW, Kim YH, Acharya AP, Keselowsky BG, Sorg BS, Lee YJ, Oh SP (2014) VEGF neutralization can prevent and normalize arteriovenous malformations in an animal model for hereditary hemorrhagic telangiectasia 2. Angiogenesis 17:823–830PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Hao Q, Zhu Y, Su H, Shen F, Yang GY, Kim H, Young WL (2010) VEGF induces more severe cerebrovascular dysplasia in endoglin than in alk1 mice. Transl Stroke Res 1:197–201PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Walker EJ, Su H, Shen F, Choi EJ, Oh SP, Chen G, Lawton MT, Kim H et al (2011) Arteriovenous malformation in the adult mouse brain resembling the human disease. Ann Neurol 69:954–962PubMedCentralCrossRefPubMedGoogle Scholar
  42. 42.
    Bayrak-Toydemir P, McDonald J, Markewitz B, Lewin S, Miller F, Chou LS, Gedge F, Tang W et al (2006) Genotype–phenotype correlation in hereditary hemorrhagic telangiectasia: mutations and manifestations. Am J Med Genet A 140(5):463–470CrossRefPubMedGoogle Scholar
  43. 43.
    Berg J, Porteous M, Reinhardt D, Gallione C, Holloway S, Umasunthar T, Lux A, McKinnon W et al (2003) Hereditary haemorrhagic telangiectasia: a questionnaire based study to delineate the different phenotypes caused by endoglin and ALK1 mutations. J Med Genet 40(8):585–590PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Kjeldsen AD, Møller TR, Brusgaard K, Vase P, Andersen PE (2005) Clinical symptoms according to genotype amongst patients with hereditary haemorrhagic telangiectasia. J Intern Med 258(4):349–355CrossRefPubMedGoogle Scholar
  45. 45.
    Letteboer TG, Mager HJ, Snijder RJ, Lindhout D, Ploos van Amstel HK, Zanen P, Westermann KJ (2008) Genotype–phenotype relationship for localization and age distribution of telangiectases in hereditary hemorrhagic telangiectasia. Am J Med Genet A 146A(21):2733–2739CrossRefPubMedGoogle Scholar
  46. 46.
    Letteboer TG, Mager JJ, Snijder RJ, Koeleman BP, Lindhout D, Ploos van Amstel JK, Westermann CJ (2006) Genotype–phenotype relationship in hereditary haemorrhagic telangiectasia. J Med Genet 43(4):371–377PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Shovlin CL (2010) Hereditary haemorrhagic telangiectasia: pathophysiology, diagnosis and treatment. Blood Rev 24(6):203–219CrossRefPubMedGoogle Scholar
  48. 48.
    Wever-Pinzon O, Selzman CH, Drakos SG, Saidi A, Stoddard GJ, Gilbert EM, Labedi M, Reid BB et al (2013) Pulsatility and the risk of nonsurgical bleeding in patients supported with the continuous-flow left ventricular assist device HeartMate II. Circ Heart Fail 6(3):517–526CrossRefPubMedGoogle Scholar
  49. 49.
    Tual-Chalot S, Mahmoud M, Allinson KR, Redgrave RE, Zhai Z, Oh SP, Fruttiger M, Arthur HM (2014) Endothelial depletion of Acvrl1 in mice leads to arteriovenous malformations associated with reduced endoglin expression. PLoS ONE 9(6):e98646PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Yoshimatsu Y, Lee YG, Akatsu Y, Taguchi L, Suzuki HI, Cunha SI, Maruyama K, Suzuki Y (2013) Bone morphogenetic protein-9 inhibits lymphatic vessel formation via activin receptor-like kinase 1 during development and cancer progression. Proc Natl Acad Sci USA 110(47):18940–18945PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    Gaillard S, Dupuis-Girod S, Boutitie F, Riviere S, Moriniere S, Hatron PY, Manfredi G, Kaminsky P et al (2014) Tranexamic acid for epistaxis in hereditary hemorrhagic telangiectasia patients: a European cross-over controlled trial in a rare disease. J Thromb Haemost 12:1494–1502CrossRefPubMedGoogle Scholar
  52. 52.
    Geisthoff UW, Seyfert UT, Kubler M, Bieg B, Plinkert PK, Konig J (2014) Treatment of epistaxis in hereditary hemorrhagic telangiectasia with tranexamic acid—a double-blind placebo-controlled cross-over phase IIIB study. Thromb Res 134:565–571CrossRefPubMedGoogle Scholar
  53. 53.
    Cirulli A, Liso A, D’Ovidio F, Mestice A, Pasculli G, Gallitelli M, Rizzi R, Specchia G, Sabba C (2003) Vascular endothelial growth factor serum levels are elevated in patients with hereditary hemorrhagic telangiectasia. Acta Haematol 110:29–32CrossRefPubMedGoogle Scholar
  54. 54.
    Dupuis-Girod S, Ginon I, Saurin JC, Marion D, Guillot E, Decullier E, Roux A, Carette MF et al (2012) Bevacizumab in patients with hereditary hemorrhagic telangiectasia and severe hepatic vascular malformations and high cardiac output. JAMA 307:948–955CrossRefPubMedGoogle Scholar
  55. 55.
    Thompson AB, Ross DA, Berard P, Figueroa-Bodine J, Livada N, Richer SL (2014) Very low dose bevacizumab for the treatment of epistaxis in patients with hereditary hemorrhagic telangiectasia. Allergy Rhinol 5:e91–e95. doi:10.2500/ar.2014.5.0091 CrossRefGoogle Scholar
  56. 56.
    Riss D, Burian M, Wolf A, Kranebitter V, Kaider A, Arnoldner C (2015) Intranasal submucosal bevacizumab for epistaxis in hereditary hemorrhagic telangiectasia: a double-blind, randomized, placebo-controlled trial. Head Neck 37(6):783–787CrossRefPubMedGoogle Scholar
  57. 57.
    Dupuis-Girod S, Ambrun A, Decullier E, Samson G, Roux A, Fargeton AE, Rioufol C, Schwiertz V et al (2014) ELLIPSE Study: a Phase 1 study evaluating the tolerance of bevacizumab nasal spray in the treatment of epistaxis in hereditary hemorrhagic telangiectasia. MAbs 6:794–799CrossRefPubMedGoogle Scholar
  58. 58.
    Lebrin F, Srun S, Raymond K, Martin S, van den Brink S, Freitas C, Breant C, Mathivet T et al (2010) Thalidomide stimulates vessel maturation and reduces epistaxis in individuals with hereditary hemorrhagic telangiectasia. Nat Med 16:420–428CrossRefPubMedGoogle Scholar
  59. 59.
    Jameson JJ, Cave DR (2004) Hormonal and antihormonal therapy for epistaxis in hereditary hemorrhagic telangiectasia. Laryngoscope 114:705–709CrossRefPubMedGoogle Scholar
  60. 60.
    Van Cutsem E, Rutgeerts P, Vantrappen G (1990) Treatment of bleeding gastrointestinal vascular malformations with oestrogen-progesterone. Lancet 335:953–955CrossRefPubMedGoogle Scholar
  61. 61.
    Vase P (1981) Estrogen treatment of hereditary hemorrhagic telangiectasia. A double-blind controlled clinical trial. Acta Med Scand 209:393–396CrossRefPubMedGoogle Scholar
  62. 62.
    Bergler W, Sadick H, Gotte K, Riedel F, Hormann K (2002) Topical estrogens combined with argon plasma coagulation in the management of epistaxis in hereditary hemorrhagic telangiectasia. Ann Otol Rhinol Laryngol 111:222–228CrossRefPubMedGoogle Scholar
  63. 63.
    Yaniv E, Preis M, Hadar T, Shvero J, Haddad M (2009) Antiestrogen therapy for hereditary hemorrhagic telangiectasia: a double-blind placebo-controlled clinical trial. Laryngoscope 119:284–288CrossRefPubMedGoogle Scholar
  64. 64.
    AlbinanaV Bernabeu-Herrero ME, Zarrabeitia R, Bernabeu C, Botella LM (2010) Estrogen therapy for hereditary haemorrhagic telangiectasia (HHT): effects of raloxifene, on endoglin and ALK1 expression in endothelial cells. Thromb Haemost 103:525–534CrossRefGoogle Scholar
  65. 65.
    Bjelakovic B, Bojanovic M, Lukic S, Saranac L, Vukomanovic V, Prijic S, Zivkovic N, Randjelovic D (2013) The therapeutic efficacy of propranolol in children with recurrent primary epistaxis. Drug Des Devel Ther 7:127–129PubMedCentralCrossRefPubMedGoogle Scholar
  66. 66.
    de Gussem EM, Snijder RJ, Disch FJ, Zanen P, Westermann CJ, Mager JJ (2009) The effect of N-acetylcysteine on epistaxis and quality of life in patients with HHT: a pilot study. Rhinology 47:85–88PubMedGoogle Scholar
  67. 67.
    Reh DD, Hur K, Merlo CA (2013) Efficacy of a topical sesame/rose geranium oil compound in patients with hereditary hemorrhagic telangiectasia associated epistaxis. Laryngoscope 123:820–822CrossRefPubMedGoogle Scholar
  68. 68.
    Faughnan ME, Lui YW, Wirth JA, Pugash RA, Redelmeier DA, Hyland RH, White RI (2000) Diffuse pulmonary arteriovenous malformations: characteristics and prognosis. Chest 117:31–38CrossRefPubMedGoogle Scholar
  69. 69.
    Lacombe P, Lacout A, Marcy PY, Binsse S, Sellier J, Bensalah M, Chinet T, Bourgault-Villada I et al (2013) Diagnosis and treatment of pulmonary arteriovenous malformations in hereditary hemorrhagic telangiectasia: an overview. Diagn Interv Imaging 94:835–848CrossRefPubMedGoogle Scholar
  70. 70.
    Lacombe P, Lagrange C, El Hajjam M, Chinet T, Pelage JP (2005) Reperfusion of complex pulmonary arteriovenous malformations after embolization: report of three cases. Cardiovasc Intervent Radiol 28:30–35CrossRefPubMedGoogle Scholar
  71. 71.
    Milic A, Chan RP, Cohen JH, Faughnan ME (2005) Reperfusion of pulmonary arteriovenous malformations after embolotherapy. J Vasc Interv Radiol 16:1675–1683CrossRefPubMedGoogle Scholar
  72. 72.
    Pollak JS, Saluja S, Thabet A, Henderson KJ, Denbow N, White RI (2006) Clinical and anatomic outcomes after embolotherapy of pulmonary arteriovenous malformations. J Vasc Interv Radiol 17:35–45CrossRefPubMedGoogle Scholar
  73. 73.
    Brillet PY, Dumont P, Bouaziz N, Duhamel A, Laurent F, Remy J, Remy-Jardin M (2007) Pulmonary arteriovenous malformation treated with embolotherapy: systemic collateral supply at multidetector CT angiography after 2–20-year follow-up. Radiology 242:267–276CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Helen Arthur
    • 1
  • Urban Geisthoff
    • 2
  • James R. Gossage
    • 3
  • Christopher C. W. Hughes
    • 4
  • Pascal Lacombe
    • 5
  • Mary E. Meek
    • 6
  • Paul Oh
    • 7
  • Beth L. Roman
    • 8
  • Scott O. Trerotola
    • 9
  • Sebastiaan Velthuis
    • 10
  • Whitney Wooderchak-Donahue
    • 11
  1. 1.Institute of Genetic Medicine, Centre for LifeNewcastle UniversityNewcastle upon TyneUK
  2. 2.Department of OtorhinolaryngologyEssen University HospitalEssenGermany
  3. 3.Department of MedicineGeorgia Regents UniversityAugustaUSA
  4. 4.Department of Molecular Biology and BiochemistryUniversity of California IrvineIrvineUSA
  5. 5.Department of Diagnostic and Interventional RadiologyHôpital Ambroise Paré, Université de Versailles, Assistance Publique-Hôpitaux de ParisBoulogne-BillancourtFrance
  6. 6.Department of Interventional RadiologyUniversity of Arkansas for Medical SciencesLittle RockUSA
  7. 7.Department of Physiology and Functional GenomicsUniversity of Florida College of MedicineGainesvilleUSA
  8. 8.Department of Human Genetics and Vascular Medicine InstituteUniversity of PittsburghPittsburghUSA
  9. 9.Department of Radiology, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  10. 10.Department of CardiologySt. Antonius HospitalNieuwegeinThe Netherlands
  11. 11.ARUP Institute for Clinical and Experimental Pathology, Department of PathologyUniversity of UtahSalt Lake CityUSA

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