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Location of embolization affects patency after coil embolization for pulmonary arteriovenous malformations: importance of time-resolved magnetic resonance angiography for diagnosis of patency

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  • Published:
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Abstract

Objectives

This study aimed to assess the diagnostic accuracy of computed tomography (CT) and time-resolved magnetic resonance angiography (TR-MRA) for patency after coil embolization of pulmonary arteriovenous malformations (PAVMs) and identify factors affecting patency.

Methods

Data from the records of 205 patients with 378 untreated PAVMs were retrospectively analyzed. Differences in proportional reduction of the sac or draining vein on CT between occluded and patent PAVMs were examined, and receiver operating characteristic analysis was performed to assess the accuracy of CT using digital subtraction angiography (DSA) as the definitive diagnostic modality. The accuracy of TR-MRA was also assessed in comparison to DSA. Potential factors affecting patency, including sex, age, number of PAVMs, location of PAVMs, type of PAVM, and location of embolization, were evaluated.

Results

The sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy of CT were 82%, 81%, 77%, 85%, and 82%, respectively, when the reduction rate threshold was set to 55%, which led to the highest diagnostic accuracy. The sensitivity, specificity, PPV, NPV, and accuracy of TR-MRA were 89%, 95%, 89%, 95%, and 93%, respectively. On both univariable and multivariable analyses, embolization of the distal position to the last normal branch of the pulmonary artery was a factor that significantly affected the prevention of patency.

Conclusions

TR-MRA appears to be an appropriate method for follow-up examinations due to its high accuracy for the diagnosis of patency after coil embolization of PAVMs. The location of embolization is a factor affecting patency.

Key Points

• Diagnosis of patency after coil embolization for pulmonary arteriovenous malformations (PAVMs) is important because a patent PAVM can lead to neurologic complications.

• The diagnostic accuracies of CT with a cutoff value of 55% and TR-MRA were 82% and 93%, respectively.

• The positioning of the coils relative to the sac and the last normal branch of the artery was significant for preventing PAVM patency.

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Abbreviations

AVP:

AMPLATZER Vascular Plug

CT:

Computed tomography

DSA:

Digital subtraction angiography

HHT:

Hereditary hemorrhagic telangiectasia

MVP:

MVP Micro Vascular Plug

NPV:

Negative predictive value

PAVM:

Pulmonary arteriovenous malformation

PPV:

Positive predictive value

ROC:

Receiver operating characteristic

TR-MRA:

Time-resolved magnetic resonance angiography

References

  1. White RI Jr, Pollak JS, Wirth JA (1996) Pulmonary arteriovenous malformations: diagnosis and transcatheter embolotherapy. J Vasc Interv Radiol 7:787–804

    Article  PubMed  Google Scholar 

  2. Gossage JR, Kanj G (1998) Pulmonary arteriovenous malformations: a state of the art review. Am J Respir Crit Care Med 158:643–661

    Article  CAS  PubMed  Google Scholar 

  3. Etievant J, Si-Mohamed S, Vinurel N et al (2018) Pulmonary arteriovenous malformations in hereditary haemorrhagic telangiectasia: correlations between computed tomography findings and cerebral complications. Eur Radiol 28:1338–1344

    Article  PubMed  Google Scholar 

  4. Woodward CS, Pyeritz RE, Chittams JL, Trerotola SO (2013) Treated pulmonary arteriovenous malformations: patterns of persistence and associated retreatment success. Radiology 269:919–926

    Article  PubMed  Google Scholar 

  5. Lee DW, White RI Jr, Egglin TK et al (1997) Embolotherapy of large pulmonary arteriovenous malformations: long-term results. Ann Thorac Surg 64:930–940

    Article  CAS  PubMed  Google Scholar 

  6. Prasad V, Chan RP, Faughnan ME (2004) Embolotherapy of pulmonary arteriovenous malformations: efficacy of platinum versus stainless steel coils. J Vasc Interv Radiol 15:153–160

    Article  PubMed  Google Scholar 

  7. Remy-Jardin M, Dumont P, Brillet PY, Dupuis P, Duhamel A, Remy J (2006) Pulmonary arteriovenous malformations treated with embolotherapy: helical CT evaluation of long-term effectiveness after 2-21-year follow-up. Radiology 239:576–585

    Article  PubMed  Google Scholar 

  8. Milic A, Chan RP, Cohen JH, Faughnan ME (2005) Reperfusion of pulmonary arteriovenous malformations after embolotherapy. J Vasc Interv Radiol 16:1675–1683

    Article  PubMed  Google Scholar 

  9. Hayashi S, Baba Y, Senokuchi T, Nakajo M (2012) Efficacy of venous sac embolization for pulmonary arteriovenous malformations: comparison with feeding artery embolization. J Vasc Interv Radiol 23:1566–1577

    Article  PubMed  Google Scholar 

  10. Letourneau-Guillon L, Faughnan ME, Soulez G et al (2010) Embolization of pulmonary arteriovenous malformations with amplatzer vascular plugs: safety and midterm effectiveness. J Vasc Interv Radiol 21:649–656

    Article  PubMed  Google Scholar 

  11. Kajiwara K, Urashima M, Yamagami T et al (2014) Venous sac embolization of pulmonary arteriovenous malformation: safety and effectiveness at mid-term follow-up. Acta Radiol 55:1093–1098

    Article  PubMed  Google Scholar 

  12. Gamondès D, Si-Mohamed S, Cottin V et al (2016) Vein diameter on unenhanced multidetector CT predicts reperfusion of pulmonary arteriovenous malformation after embolotherapy. Eur Radiol 26:2723–2739

    Article  PubMed  Google Scholar 

  13. Goyen M, Ruehm SG, Jagenburg A, Barkhausen J, Kröger K, Debatin JF (2001) Pulmonary arteriovenous malformation: characterization with time-resolved ultrafast 3D MR angiography. J Magn Reson Imaging 13:458–460

    Article  CAS  PubMed  Google Scholar 

  14. Fink C, Eichhorn J, Bock M (2002) Pulmonary arteriovenous malformation and aortopulmonary collateral imaged by time resolved contrast enhanced magnetic resonance angiography. Heart 88:292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Boussel L, Cernicanu A, Geerts L et al (2010) 4D time-resolved magnetic resonance angiography for noninvasive assessment of pulmonary arteriovenous malformations patency. J Magn Reson Imaging 32:1110–1116

    Article  PubMed  Google Scholar 

  16. Kawai T, Shimohira M, Kan H et al (2014) Feasibility of time-resolved MR angiography for detecting recanalization of pulmonary arteriovenous malformations treated with embolization with platinum coils. J Vasc Interv Radiol 25:1339–1347

    Article  PubMed  Google Scholar 

  17. Shimohira M, Kawai T, Hashizume T et al (2015) Reperfusion rates of pulmonary arteriovenous malformations after coil embolization: evaluation with time-resolved MR angiography or pulmonary angiography. J Vasc Interv Radiol 26:856–864.e1

    Article  PubMed  Google Scholar 

  18. Shovlin CL, Guttmacher AE, Buscarini E et al (2000) Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome). Am J Med Genet 91:66–67

    Article  CAS  PubMed  Google Scholar 

  19. Kawai T, Shimohira M, Ohta K et al (2016) The role of time-resolved MRA for post-treatment assessment of pulmonary arteriovenous malformations: a pictorial essay. Cardiovasc Intervent Radiol 39:965–672

    Article  PubMed  Google Scholar 

  20. Zhang J, Ding S, Zhao H et al (2020) Evaluation of chronic carotid artery occlusion by non-contrast 3D-MERGE MR vessel wall imaging: comparison with 3D-TOF-MRA, contrast-enhanced MRA, and DSA. Eur Radiol 30(11):5805–5814

  21. Zhang X, Cao YZ, Mu XH et al (2020) Highly accelerated compressed sensing time-of-flight magnetic resonance angiography may be reliable for diagnosing head and neck arterial steno-occlusive disease: a comparative study with digital subtraction angiography. Eur Radiol 30:3059–3065

    Article  CAS  PubMed  Google Scholar 

  22. Schneider G, Uder M, Koehler M et al (2008) MR angiography for detection of pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. AJR Am J Roentgenol 190:892–901

    Article  PubMed  Google Scholar 

  23. Meaney JF, Weg JG, Chenevert TL, Stafford-Johnson D, Hamilton BH, Prince MR (1994) Diagnosis of pulmonary embolism with magnetic resonance angiography. N Engl J Med 336:1422–1427

    Article  Google Scholar 

  24. Togao O, Obara M, Helle M et al (2020) Vessel-selective 4D-MR angiography using super-selective pseudo-continuous arterial spin labeling may be a useful tool for assessing brain AVM hemodynamics. Eur Radiol 30(12):6452–6463

  25. Anzalone N, Righi C, Simionato F et al (2000) Three-dimensional time-of-flight MR angiography in the evaluation of intracranial aneurysms treated with Guglielmi detachable coils. AJNR Am J Neuroradiol 21:746–752

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Hennemeyer CT, Wicklow K, Feinberg DA, Derdeyn CP (2001) In vitro evaluation of platinum Guglielmi detachable coils at 3 T with a porcine model: safety issues and artifacts. Radiology 219:732–737

    Article  CAS  PubMed  Google Scholar 

  27. D’Orazio F, Splendiani A, Gallucci M (2014) 320-Row detector dynamic 4D-CTA for the assessment of brain and spinal cord vascular shunting malformations. A technical note. Neuroradiol J 27:710–717

    Article  PubMed  PubMed Central  Google Scholar 

  28. Hadizadeh DR, Marx C, Gieseke J, Schild HH, Willinek WA (2014) High temporal and high spatial resolution MR angiography (4D-MRA). Rofo 186:847–859

    Article  CAS  PubMed  Google Scholar 

  29. Tamada D, Kromrey ML, Ichikawa S, Onishi H, Motosugi U (2020) Motion artifact reduction using a convolutional neural network for dynamic contrast enhanced MR imaging of the liver. Magn Reson Med Sci 19:64–76

    Article  CAS  PubMed  Google Scholar 

  30. Hamamoto K, Matsuura K, Chiba E, Okochi T, Tanno K, Tanaka O (2016) Feasibility of non-contrast-enhanced MR angiography using the time-SLIP technique for the assessment of pulmonary arteriovenous malformation. Magn Reson Med Sci 15:253–265

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sagara K, Miyazono N, Inoue H, Ueno K, Nishida H, Nakajo M (1998) Recanalization after coil embolotherapy of pulmonary arteriovenous malformations: study of long-term outcome and mechanism for recanalization. AJR Am J Roentgenol 170:727–730

    Article  CAS  PubMed  Google Scholar 

  32. Saouti N, Westerhof N, Postmus PE, Vonk-Noordegraaf A (2010) The arterial load in pulmonary hypertension. Eur Respir Rev 19:197–203

    Article  CAS  PubMed  Google Scholar 

  33. Rosenhek R, Korschineck I, Gharehbaghi-Schnell E et al (2003) Fibrinolytic balance of the arterial wall: pulmonary artery displays increased fibrinolytic potential compared with aorta. Lab Invest 83:871–876

    Article  CAS  PubMed  Google Scholar 

  34. Dinkel HP, Triller J (2002) Pulmonary arteriovenous malformations: embolotherapy with superselective coaxial catheter placement and filling of venous sac with Guglielmi detachable coils. Radiology 223:709–714

    Article  PubMed  Google Scholar 

  35. Shimohira M, Kawai T, Hashizume T, Muto M, Kitase M, Shibamoto Y (2018) Usefulness of hydrogel-coated coils in embolization of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 41:848–855

    Article  PubMed  PubMed Central  Google Scholar 

  36. Maruno M, Kiyosue H, Tanoue S et al (2016) Renal arteriovenous shunts: clinical features, imaging appearance, and transcatheter embolization based on angioarchitecture. Radiographics 36:580–595

    Article  PubMed  Google Scholar 

  37. Kim DJ, Willinsky RA, Krings T, Agid R, Terbrugge K (2011) Intracranial dural arteriovenous shunts: transarterial glue embolization--experience in 115 consecutive patients. Radiology 258:554–561

    Article  PubMed  Google Scholar 

  38. Jacobowitz GR, Rosen RJ, Rockman CB et al (2001) Transcatheter embolization of complex pelvic vascular malformations: results and long-term follow-up. J Vasc Surg 33:51–55

    Article  CAS  PubMed  Google Scholar 

  39. Maruno M, Kiyosue H, Hongo N, Matsumoto S, Mori H (2018) Where is the origin of the last normal branch from feeding artery of pulmonary arteriovenous malformations? Cardiovasc Intervent Radiol 41:1849–1856

    Article  PubMed  PubMed Central  Google Scholar 

  40. Stein EJ, Chittams JL, Miller M, Trerotola SO (2017) Persistence in coil-embolized pulmonary arteriovenous malformations with feeding artery diameters of 3 mm or less: a retrospective single-center observational study. J Vasc Interv Radiol 28:442–449

    Article  PubMed  Google Scholar 

  41. Tapping CR, Ettles DF, Robinson GJ (2011) Long-term follow-up of treatment of pulmonary arteriovenous malformations with AMPLATZER vascular plug and AMPLATZER vascular plug II devices. J Vasc Interv Radiol 22:1740–1746

    Article  PubMed  Google Scholar 

  42. Kucukay F, Özdemir M, Şenol E, Okten S, Ereren M, Karan A (2014) Large pulmonary arteriovenous malformations: long-term results of embolization with AMPLATZER vascular plugs. J Vasc Interv Radiol 25:1327–1332

    Article  PubMed  Google Scholar 

  43. Ratnani R, Sutphin PD, Koshti V et al (2019) 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 30:1089–1097

    Article  PubMed  Google Scholar 

  44. Bailey CR, Arun A, Towsley M et al (2019) MVP™ micro vascular plug systems for the treatment of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 42:389–395

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to express our deep appreciation to Masaki Komiyama, Tatsuya Kawai and the members of HHT JAPAN.

Funding

This study has received funding by the Clinical Research Group of the Japanese Society for Transcatheter Hepatic Arterial Embolization.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masashi Shimohira.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Masashi Shimohira.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise.

Informed consent

The requirement to obtain informed consent was waived because of the retrospective design.

Ethical approval

Institutional Review Board approval was obtained in each institution.

Approval number was as follows:

Nagoya City University Graduate School of Medical60160070

Oita University1061

Osaka University Graduate School of Medicine16362

Okayama University Medical Schoolken1611-009

Saitama Medical Center, Jichi Medical UniversityS16-090

Osaka City General Hospital1708047

Kobe University Graduate School of Medicine180012

Kurume University School of Medicine16194

Aichi Medical University2016-H272

Hyogo College of Medicine2522

Study subjects or cohorts overlap

Some study subjects or cohorts have been previously reported in following articles.

Makimoto S, Hiraki T, Gobara H, et al (2014) Association between reperfusion and shrinkage percentage of the aneurysmal sac after embolization of pulmonary arteriovenous malformation: evaluation based on contrast-enhanced thin-section CT images. Jpn J Radiol 32:266–273

Osuga K, Kishimoto K, Tanaka K, et al (2014) Initial experience with use of hydrogel microcoils in embolization of pulmonary arteriovenous malformations. Springerplus 17;3:609

Hamamoto K, Matsuura K, Chiba E, et al (2016) Feasibility of non-contrast-enhanced MR angiography using the time-SLIP technique for the assessment of pulmonary arteriovenous malformation. Magn Reson Med Sci 15:253–265

Maruno M, Kiyosue H, Hongo N, et al (2018) Where is the origin of the last normal branch from feeding artery of pulmonary arteriovenous malformations? Cardiovasc Intervent Radiol 41:1849–1856

Shimohira M, Kawai T, Hashizume T, et al (2015) Reperfusion rates of pulmonary arteriovenous malformations after coil embolization: evaluation with time-resolved MR angiography or pulmonary angiography. J Vasc Interv Radiol 26:856–864.e1

Shimohira M, Kawai T, Hashizume T, Muto M, Kitase M, Shibamoto Y (2018) Usefulness of hydrogel-coated coils in embolization of pulmonary arteriovenous malformations. Cardiovasc Intervent Radiol 41:848–855

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• diagnostic or prognostic study

• multicenter study

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Shimohira, M., Kiyosue, H., Osuga, K. et al. Location of embolization affects patency after coil embolization for pulmonary arteriovenous malformations: importance of time-resolved magnetic resonance angiography for diagnosis of patency. Eur Radiol 31, 5409–5420 (2021). https://doi.org/10.1007/s00330-020-07669-w

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  • DOI: https://doi.org/10.1007/s00330-020-07669-w

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