Semin intervent Radiol 2022; 39(03): 261-270
DOI: 10.1055/s-0042-1751260
Review Article

Pulmonary Arteriovenous Malformations: What the Interventional Radiologist Should Know

Claire S. Kaufman
1   Dotter Department of Interventional Radiology, Pacific Northwest HHT Center of Excellence, Oregon Health & Sciences University, Portland, Oregon
,
Jamie McDonald
2   Department of Pathology, University of Utah, Salt Lake City, Utah
,
Heather Balch
3   HHT Center of Excellence, Department of Internal Medicine, University of Utah, Salt Lake City, Utah
,
Kevin Whitehead
4   HHT Center of Excellence, Division of Cardiovascular Medicine, University of Utah, Salt Lake City, Utah
› Institutsangaben

Abstract

Pulmonary arteriovenous malformations (PAVMs) are abnormal connections between the pulmonary artery and pulmonary vein bypassing the normal capillary bed causing a right-to-left shunt. The majority (80–90%) of PAVMs are associated with hereditary hemorrhagic telangiectasia (HHT). PAVMs may be asymptomatic or present with symptoms of hypoxia, shortness of breath, migraines, sequelae of paradoxical embolization, or rupture. Transcatheter embolization has become the standard of care. This article will review the clinical presentation, workup, genetics, imaging findings, embolization, complications, and follow-up for patients with PAVMs.



Publikationsverlauf

Artikel online veröffentlicht:
31. August 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Shovlin CL. Pulmonary arteriovenous malformations. Am J Respir Crit Care Med 2014; 190 (11) 1217-1228
  • 2 Nakayama M, Nawa T, Chonan T. et al. Prevalence of pulmonary arteriovenous malformations as estimated by low-dose thoracic CT screening. Intern Med 2012; 51 (13) 1677-1681
  • 3 Saboo SS, Chamarthy M, Bhalla S. et al. Pulmonary arteriovenous malformations: diagnosis. Cardiovasc Diagn Ther 2018; 8 (03) 325-337
  • 4 McDonald J, Bayrak-Toydemir P, Pyeritz RE. Hereditary hemorrhagic telangiectasia: an overview of diagnosis, management, and pathogenesis. Genet Med 2011; 13 (07) 607-616
  • 5 Cottin V, Plauchu H, Bayle JY, Barthelet M, Revel D, Cordier JF. Pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. Am J Respir Crit Care Med 2004; 169 (09) 994-1000
  • 6 Faughnan ME, Mager JJ, Hetts SW. et al. Second international guidelines for the diagnosis and management of hereditary hemorrhagic telangiectasia. Ann Intern Med 2020; 173 (12) 989-1001
  • 7 Faughnan ME, Palda VA, Garcia-Tsao G. et al; HHT Foundation International - Guidelines Working Group. International guidelines for the diagnosis and management of hereditary haemorrhagic telangiectasia. J Med Genet 2011; 48 (02) 73-87
  • 8 Hsu CC, Kwan GN, Evans-Barns H, van Driel ML. Embolisation for pulmonary arteriovenous malformation. Cochrane Database Syst Rev 2018; 1: CD008017
  • 9 Shovlin CL, Guttmacher AE, Buscarini E. et al. Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome). Am J Med Genet 2000; 91 (01) 66-67
  • 10 McDonald J, Pyeritz RE. Hereditary hemorrhagic telangiectasia. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Mirzaa G. et al, eds. GeneReviews((R)). Seattle, WA: 1993
  • 11 McDonald J, Wooderchak-Donahue W, VanSant Webb C, Whitehead K, Stevenson DA, Bayrak-Toydemir P. Hereditary hemorrhagic telangiectasia: genetics and molecular diagnostics in a new era. Front Genet 2015; 6: 1 DOI: 10.3389/fgene.2015.00001.
  • 12 Kritharis A, Al-Samkari H, Kuter DJ. Hereditary hemorrhagic telangiectasia: diagnosis and management from the hematologist's perspective. Haematologica 2018; 103 (09) 1433-1443
  • 13 Gallione CJ, Repetto GM, Legius E. et al. A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4). Lancet 2004; 363 (9412): 852-859
  • 14 Gallione C, Aylsworth AS, Beis J. et al. Overlapping spectra of SMAD4 mutations in juvenile polyposis (JP) and JP-HHT syndrome. Am J Med Genet A 2010; 152A (02) 333-339
  • 15 van Gent MW, Post MC, Snijder RJ, Westermann CJ, Plokker HW, Mager JJ. Real prevalence of pulmonary right-to-left shunt according to genotype in patients with hereditary hemorrhagic telangiectasia: a transthoracic contrast echocardiography study. Chest 2010; 138 (04) 833-839
  • 16 Kjeldsen AD, Møller TR, Brusgaard K, Vase P, Andersen PE. Clinical symptoms according to genotype amongst patients with hereditary haemorrhagic telangiectasia. J Intern Med 2005; 258 (04) 349-355
  • 17 Topiwala KK, Patel SD, Nouh AM, Alberts MJ. Novel GDF2 gene mutation associated with pulmonary arteriovenous malformation. J Stroke Cerebrovasc Dis 2020; 29 (12) 105301
  • 18 Hodgson J, Ruiz-Llorente L, McDonald J. et al. Homozygous GDF2 nonsense mutations result in a loss of circulating BMP9 and BMP10 and are associated with either PAH or an “HHT-like” syndrome in children. Mol Genet Genomic Med 2021; 9 (12) e1685
  • 19 El Hajjam M, Mekki A, Palmyre A. et al. RASA1 phenotype overlaps with hereditary haemorrhagic telangiectasia: two case reports. J Med Genet 2021; 58 (09) 645-647
  • 20 Rigelsky CM, Jennings C, Lehtonen R, Minai OA, Eng C, Aldred MA. BMPR2 mutation in a patient with pulmonary arterial hypertension and suspected hereditary hemorrhagic telangiectasia. Am J Med Genet A 2008; 146A (19) 2551-2556
  • 21 Soon E, Southwood M, Sheares K, Pepke-Zaba J, Morrell NW. Better off blue: BMPR-2 mutation, arteriovenous malformation, and pulmonary arterial hypertension. Am J Respir Crit Care Med 2014; 189 (11) 1435-1436
  • 22 Duncan BW, Desai S. Pulmonary arteriovenous malformations after cavopulmonary anastomosis. Ann Thorac Surg 2003; 76 (05) 1759-1766
  • 23 Majumdar S, McWilliams JP. Approach to pulmonary arteriovenous malformations: a comprehensive update. J Clin Med 2020; 9 (06) E1927
  • 24 Ratjen A, Au J, Carpenter S, John P, Ratjen F. Growth of pulmonary arteriovenous malformations in pediatric patients with hereditary hemorrhagic telangiectasia. J Pediatr 2019; 208: 279-281
  • 25 Trerotola SO, Pyeritz RE. PAVM embolization: an update. AJR Am J Roentgenol 2010; 195 (04) 837-845
  • 26 Santhirapala V, Williams LC, Tighe HC, Jackson JE, Shovlin CL. Arterial oxygen content is precisely maintained by graded erythrocytotic responses in settings of high/normal serum iron levels, and predicts exercise capacity: an observational study of hypoxaemic patients with pulmonary arteriovenous malformations. PLoS One 2014; 9 (03) e90777
  • 27 Clark K, Pyeritz RE, Trerotola SO. Angina pectoris or myocardial infarctions, pulmonary arteriovenous malformations, hereditary hemorrhagic telangiectasia, and paradoxical emboli. Am J Cardiol 2013; 112 (05) 731-734
  • 28 Ma X, Jie B, Yu D, Li LL, Jiang S. Massive haemorrhagic complications of ruptured pulmonary arteriovenous malformations: outcomes from a 12 years' retrospective study. BMC Pulm Med 2021; 21 (01) 230
  • 29 de Gussem EM, Lausman AY, Beder AJ. et al. Outcomes of pregnancy in women with hereditary hemorrhagic telangiectasia. Obstet Gynecol 2014; 123 (03) 514-520
  • 30 Shovlin CL, Sodhi V, McCarthy A, Lasjaunias P, Jackson JE, Sheppard MN. Estimates of maternal risks of pregnancy for women with hereditary haemorrhagic telangiectasia (Osler-Weber-Rendu syndrome): suggested approach for obstetric services. BJOG 2008; 115 (09) 1108-1115
  • 31 Remy-Jardin M, Dumont P, Brillet PY, Dupuis P, Duhamel A, Remy J. Pulmonary arteriovenous malformations treated with embolotherapy: helical CT evaluation of long-term effectiveness after 2-21-year follow-up. Radiology 2006; 239 (02) 576-585
  • 32 White Jr RI, Pollak JS, Wirth JA. Pulmonary arteriovenous malformations: diagnosis and transcatheter embolotherapy. J Vasc Interv Radiol 1996; 7 (06) 787-804
  • 33 Pierucci P, Murphy J, Henderson KJ, Chyun DA, White Jr RI. New definition and natural history of patients with diffuse pulmonary arteriovenous malformations: twenty-seven-year experience. Chest 2008; 133 (03) 653-661
  • 34 Meek ME, Meek JC, Beheshti MV. Management of pulmonary arteriovenous malformations. Semin Intervent Radiol 2011; 28 (01) 24-31
  • 35 Kjeldsen AD, Oxhøj H, Andersen PE, Elle B, Jacobsen JP, Vase P. Pulmonary arteriovenous malformations: screening procedures and pulmonary angiography in patients with hereditary hemorrhagic telangiectasia. Chest 1999; 116 (02) 432-439
  • 36 Müller-Hülsbeck S, Marques L, Maleux G. et al. CIRSE standards of practice on diagnosis and treatment of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 2020; 43 (03) 353-361
  • 37 Barzilai B, Waggoner AD, Spessert C, Picus D, Goodenberger D. Two-dimensional contrast echocardiography in the detection and follow-up of congenital pulmonary arteriovenous malformations. Am J Cardiol 1991; 68 (15) 1507-1510
  • 38 Zukotynski K, Chan RP, Chow CM, Cohen JH, Faughnan ME. Contrast echocardiography grading predicts pulmonary arteriovenous malformations on CT. Chest 2007; 132 (01) 18-23
  • 39 Parra JA, Cuesta JM, Zarrabeitia R. et al. Screening pulmonary arteriovenous malformations in a large cohort of Spanish patients with hemorrhagic hereditary telangiectasia. Int J Cardiol 2016; 218: 240-245
  • 40 Chick JFB, Reddy SN, Pyeritz RE, Trerotola SO. A survey of pulmonary arteriovenous malformation screening, management, and follow-up in hereditary hemorrhagic telangiectasia centers of excellence. Cardiovasc Intervent Radiol 2017; 40 (07) 1003-1009
  • 41 Lacombe P, Lacout A, Marcy PY. et al. Diagnosis and treatment of pulmonary arteriovenous malformations in hereditary hemorrhagic telangiectasia: an overview. Diagn Interv Imaging 2013; 94 (09) 835-848
  • 42 Shin SM, Kim HK, Crotty EJ, Hammill AM, Wusik K, Kim DH. CT angiography findings of pulmonary arteriovenous malformations in children and young adults with hereditary hemorrhagic telangiectasia. AJR Am J Roentgenol 2020; 214 (06) 1369-1376
  • 43 Hamamoto K, Matsuura K, Chiba E, Okochi T, Tanno K, Tanaka O. Feasibility of non-contrast-enhanced MR angiography using the time-SLIP technique for the assessment of pulmonary arteriovenous malformation. Magn Reson Med Sci 2016; 15 (03) 253-265
  • 44 Van den Heuvel DAF, Post MC, Koot W. et al. Comparison of contrast enhanced magnetic resonance angiography to computed tomography in detecting pulmonary arteriovenous malformations. J Clin Med 2020; 9 (11) E3662
  • 45 Schneider G, Uder M, Koehler M. et al. MR angiography for detection of pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. AJR Am J Roentgenol 2008; 190 (04) 892-901
  • 46 Kawai T, Shimohira M, Kan H. et al. Feasibility of time-resolved MR angiography for detecting recanalization of pulmonary arteriovenous malformations treated with embolization with platinum coils. J Vasc Interv Radiol 2014; 25 (09) 1339-1347
  • 47 Hosman AE, de Gussem EM, Balemans WAF. et al. Screening children for pulmonary arteriovenous malformations: evaluation of 18 years of experience. Pediatr Pulmonol 2017; 52 (09) 1206-1211
  • 48 Porstmann W. Therapeutic Embolization of Arteriovenous Pulmonary Fistula by Catheter Technique. Berlin, Germany: Springer; 1977
  • 49 White Jr RI, Lynch-Nyhan A, Terry P. et al. Pulmonary arteriovenous malformations: techniques and long-term outcome of embolotherapy. Radiology 1988; 169 (03) 663-669
  • 50 Todo K, Moriwaki H, Higashi M, Kimura K, Naritomi H. A small pulmonary arteriovenous malformation as a cause of recurrent brain embolism. AJNR Am J Neuroradiol 2004; 25 (03) 428-430
  • 51 Mager JJ, Overtoom TT, Blauw H, Lammers JW, Westermann CJ. Embolotherapy of pulmonary arteriovenous malformations: long-term results in 112 patients. J Vasc Interv Radiol 2004; 15 (05) 451-456
  • 52 Pollak JS, Saluja S, Thabet A, Henderson KJ, Denbow N, White Jr RI. Clinical and anatomic outcomes after embolotherapy of pulmonary arteriovenous malformations. J Vasc Interv Radiol 2006; 17 (01) 35-44 , quiz 45
  • 53 Shovlin CL, Jackson JE, Bamford KB. et al. Primary determinants of ischaemic stroke/brain abscess risks are independent of severity of pulmonary arteriovenous malformations in hereditary haemorrhagic telangiectasia. Thorax 2008; 63 (03) 259-266
  • 54 Trerotola SO, Pyeritz RE, Bernhardt BA. Outpatient single-session pulmonary arteriovenous malformation embolization. J Vasc Interv Radiol 2009; 20 (10) 1287-1291
  • 55 Faughnan ME, Lui YW, Wirth JA. et al. Diffuse pulmonary arteriovenous malformations: characteristics and prognosis. Chest 2000; 117 (01) 31-38
  • 56 Gershon AS, Faughnan ME, Chon KS. et al. Transcatheter embolotherapy of maternal pulmonary arteriovenous malformations during pregnancy. Chest 2001; 119 (02) 470-477
  • 57 Saluja S, Sitko I, Lee DW, Pollak J, White Jr RI. Embolotherapy of pulmonary arteriovenous malformations with detachable balloons: long-term durability and efficacy. J Vasc Interv Radiol 1999; 10 (07) 883-889
  • 58 Milic A, Chan RP, Cohen JH, Faughnan ME. Reperfusion of pulmonary arteriovenous malformations after embolotherapy. J Vasc Interv Radiol 2005; 16 (12) 1675-1683
  • 59 Roberts DG, Sparks HD, Cusumano LR, Mathevosian S, Duckwiler GR, McWilliams JP. Comparison of feeding-artery-only versus nidus-plus-feeding-artery embolization of pulmonary arteriovenous malformations. J Vasc Interv Radiol 2021; 32 (07) 993-1001
  • 60 Contegiacomo A, Del Ciello A, Rella R. et al. Pulmonary arteriovenous malformations: what the interventional radiologist needs to know. Radiol Med (Torino) 2019; 124 (10) 973-988
  • 61 Vaidya S, Tozer KR, Chen J. An overview of embolic agents. Semin Intervent Radiol 2008; 25 (03) 204-215
  • 62 Trerotola SO, Pyeritz RE. Does use of coils in addition to Amplatzer vascular plugs prevent recanalization?. AJR Am J Roentgenol 2010; 195 (03) 766-771
  • 63 Tapping CR, Ettles DF, Robinson GJ. Long-term follow-up of treatment of pulmonary arteriovenous malformations with AMPLATZER Vascular Plug and AMPLATZER Vascular Plug II devices. J Vasc Interv Radiol 2011; 22 (12) 1740-1746
  • 64 Letourneau-Guillon L, Faughnan ME, Soulez G. et al. Embolization of pulmonary arteriovenous malformations with Amplatzer vascular plugs: safety and midterm effectiveness. J Vasc Interv Radiol 2010; 21 (05) 649-656
  • 65 Kucukay F, Özdemir M, Şenol E, Okten S, Ereren M, Karan A. Large pulmonary arteriovenous malformations: long-term results of embolization with Amplatzer vascular plugs. J Vasc Interv Radiol 2014; 25 (09) 1327-1332
  • 66 Abdel Aal AK, Ibrahim RM, Moustafa AS, Hamed MF, Saddekni S. Persistence of pulmonary arteriovenous malformations after successful embolotherapy with Amplatzer vascular plug: long-term results. Diagn Interv Radiol 2016; 22 (04) 358-364
  • 67 Conrad MB, Ishaque BM, Surman AM. et al. Intraprocedural safety and technical success of the MVP Micro Vascular Plug for embolization of pulmonary arteriovenous malformations. J Vasc Interv Radiol 2015; 26 (11) 1735-1739
  • 68 Mahdjoub E, Tavolaro S, Parrot A, Cornelis F, Khalil A, Carette MF. Pulmonary arteriovenous malformations: safety and efficacy of microvascular plugs. AJR Am J Roentgenol 2018; 211 (05) 1135-1143
  • 69 Boatta E, Jahn C, Canuet M. et al. Pulmonary arteriovenous malformations embolized using a micro vascular plug system: technical note on a preliminary experience. Cardiovasc Intervent Radiol 2017; 40 (02) 296-301
  • 70 Ratnani R, Sutphin PD, Koshti V. et al. Retrospective comparison of pulmonary arteriovenous malformation embolization with the polytetrafluoroethylene-covered nitinol microvascular plug, AMPLATZER plug, and coils in patients with hereditary hemorrhagic telangiectasia. J Vasc Interv Radiol 2019; 30 (07) 1089-1097
  • 71 Stein PD, Mahur VS, Herman MV, Levine HD. Complete heart block induced during cardiac catheterization of patients with pre-existent bundle-branch block. The hazard of bilateral bundle-branch block. Circulation 1966; 34 (05) 783-791
  • 72 Gupta P, Mordin C, Curtis J, Hughes JM, Shovlin CL, Jackson JE. Pulmonary arteriovenous malformations: effect of embolization on right-to-left shunt, hypoxemia, and exercise tolerance in 66 patients. AJR Am J Roentgenol 2002; 179 (02) 347-355
  • 73 Curnes NR, Desjardins B, Pyeritz R, Chittams J, Sienko D, Trerotola SO. Lack of growth of small (≤2 mm feeding artery) untreated pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. J Vasc Interv Radiol 2019; 30 (08) 1259-1264
  • 74 Lee WL, Graham AF, Pugash RA. et al. Contrast echocardiography remains positive after treatment of pulmonary arteriovenous malformations. Chest 2003; 123 (02) 351-358
  • 75 DePietro DM, Curnes NR, Chittams J, Ferrari VA, Pyeritz RE, Trerotola SO. Postembolotherapy pulmonary arteriovenous malformation follow-up: a role for graded transthoracic contrast echocardiography prior to high-resolution chest CT scan. Chest 2020; 157 (05) 1278-1286
  • 76 Woodward CS, Pyeritz RE, Chittams JL, Trerotola SO. Treated pulmonary arteriovenous malformations: patterns of persistence and associated retreatment success. Radiology 2013; 269 (03) 919-926