Magnetic resonance imaging in the diagnosis of brain arteriovenous malformations and in the evaluation of the results of stereotactic radiosurgery (review)
https://doi.org/10.17650/1683-3295-2021-23-1-135-145
Abstract
Arteriovenous malformations (AVM) are quite rare, but they are dangerous pathology due to the risk of rupture and intracranial hemorrhage, which leads to disability. This review enlights the epidemiology of AVM and their symptoms, current methods of diagnostics and treatment as well as prognosis and treatment outcomes. Nowadays microsurgical removal, endovascular embolization, stereotactic radiosurgery and combination of these methods are used in clinical practice for AVMs treatment. Stereotactic radiosurgery is a highly effective non-invasive technique resulting in high degree of AVM obliteration with low risk of complications. The results of magnetic resonance imaging usage in assessing the degree of obliteration and the development of post-radiation complications are presented in this article. The optimization of magnetic resonance imaging algorithm is necessary for determination of statistically significant factors affecting the obliteration process.
About the Authors
A. S. Tokarev
Moscow Healthcare Department; N.V. Sklifosovsky Research Institute for Emergency Medicine, Moscow Healthcare Department
Russian Federation
Russian Federation
43 Oruzheyny Ln., Moscow 127006, Russia
3 Bolshaya Sukharevskaya Sq., Moscow 129090, Russia
S. A. Chuvilin
Russian Federation
M. V. Neznanova
N.V. Sklifosovsky Research Institute for Emergency Medicine, Moscow Healthcare Department
Russian Federation
Russian Federation
Maria Viktorovna Neznanova
3 Bolshaya Sukharevskaya Sq., Moscow 129090, Russia
References
1. Abecassis I.J., Xu D.S., Batjer Н.Н., Bendok B.R. Natural history of brain arteriovenous malformations: a systematic review. Neurosurg Focus 2014;37(3):Е7. DOI: 10.3171/2014.6.FOCUS14250.
2. Maryashev S.A. Stereotactic irradiation of arteriovenous malformations of the brain. Dis. … doct. of med. sciences. Moscow, 2016. Available at: https://search.rsl.ru/ru/record/0100510304.(In Russ.).
3. Hunter W. Further observations upon a particular species of aneurisme. Med Obs Inq 1764;2:390–414.
4. Olivecrona H., Riives J. Arteriovenous aneurysms of the brain, their diagnosis and treatment. Arch Neurol Psychiatry 1948;59(5):567–602. DOI: 10.1001/archneurpsyc.1948.02300400003001.
5. Svistov D.V., Kandyba D.V., Savello A.V. Arteriovenous malformations of the brain: clinic, diagnosis, complex treatment. In: Collection of textbooks on topical issues of neurosurgery. Ed. by V.E. Parfenov, D.V. Svistov. Saint Petersburg: Foliant, 2002. P. 199–260. (In Russ.).
6. McCormick W.F. Pathology of vascular malformations of the brain. In: Intracranial arteriovenous malformations. Ed. by C.B. Wilson, B.M. Stein. Baltimore: Williams & Wilkins, 1984.
7. Brown R.D. Jr, Wiebers D.O., Tomer J.C. et al. Frequency of intracranial hemorrhage as a presenting symptom and subtype analysis: a population-based study of intracranial vascular malformation in Olmsted County, Minnesota. J Neurosurg 1996;85(1):29–32. DOI: 10.3171/jns.1996.85.1.0029.
8. Yasargil M.G. Microneurosurgery. 3A. AVM of the brain: history, embryology, pathological considerations, hemodynamics, diagnostic studies, microsurgical anatomy. Stuttgart: Georg Thieme, 1987.
9. Hitchon P., Schneider P.B. Arteriovenous malformations of the brain. Neirobase: the information resource for clinical neurology. Arbor Publishing Corp., 2005.
10. Bokhari M.R., Bokhari S.R.A. Arteriovenous malformation of the brain. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2021 Jan. 2020 Jun 30. Available at: https://www.ncbi.nlm.nih.gov/books/NBK430744.
11. Hartmann A., Mast H., Mohr J.P. et al. Morbidity of intracranial hemorrhage in patients with cerebral arteriovenous malformation. Stroke 1998;29(5):931–4. DOI: 10.1161/01.str.29.5.931.
12. Kim H., Sidney S., McCulloch C.E. et al. Racial/ethnic differences in longitudinal risk of intracranial hemorrhage in brain arteriovenous malformation patients. Stroke 2007;38(9):2430–7. DOI: 10.1161/STROKEAHA.107.485573.
13. Abla A.A., Nelson J., Rutledge W.C. et al. The natural history of AVM hemorrhage in the posterior fossa: comparison of hematoma volumes and neurological outcomes in patients with ruptured infraand supratentorial AVMs. Neurosurg Focus 2014;37(3):E6. DOI: 10.3171/2014.7.FOCUS14211.
14. Ondra S.L., Troupp H., George E.D. et al. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 1990;73(3):387–91. DOI: 10.3171/jns.1990.73.3.0387.
15. Hernesniemi J.A., Dashti R., Juvela S. et al. Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery 2008;63(5):823–31. DOI: 10.1227/01.NEU.0000330401.82582.5E.
16. Stapf C., Mohr J.P., Pile-Spellman J. et al. Epidemiology and natural history of arteriovenous malformations. Neurosurg Focus 2001;11(5):e1. DOI: 10.3171/foc.2001.11.5.2.
17. Inoue H.K., Ohye C. Hemorrhage risks and obliteration rates of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg 2002;97(Suppl 5):474–6. DOI: 10.3171/jns.2002.97.supplement.
18. Berkutov E.S., Lazarev V.A., Shahnovich V.A. et al. Effect of arteriovenous malformations of the brain on the general and cerebral hemodynamicsshunting with cerebral arteriovenous. Voprosy nejrohirurgii im. N.N. Burdenko = Problems of neurosurgery by N.N. Burdenko 2007;2:21–6.(In Russ.).
19. Flores B.C., Klinger D.R., Rickert K.L. et al. Management of intracranial aneurysms associated with arteriovenous malformations. Neurosurg Focus 2014;37(3): E11. DOI: 10.3171/2014.6.FOCUS14165.
20. Macko D.E. Malformations of the vessels of the brain and spinal cord. Pathological anatomy of surgical diseases of the nervous system. Saint Petersburg: RNHI im. prof. A.L. Polenova, 1991. С. 104–121. (In Russ.).
21. Lawton M.T., Rutledge W.C., Kim H. et al. Brain arteriovenous malformations. Nat Rev Dis Primers 2015;1:15047. Available at: https://www.nature.com/articles/nrdp201547. DOI: 10.1038/nrdp.2015.47.
22. Eddleman C.S., Jeong H.J., Hurley M.C. et al. 4D radial acquisition contrastenhanced MR angiography and intracranial arteriovenous malformations: quickly approaching digital subtraction angiography. Stroke 2009;40(8):2749–53. DOI: 10.1161/STROKEAHA.108.546663.
23. Berger M.O., Anxionnat R., Kerrien E. et al. A methodology for validating a 3D imaging modality for brain AVM delineation: application to 3DRA. Comput Med Imaging Graph 2008;32(7):544–53. DOI: 10.1016/j.compmedimag.2008.06.003.
24. Hadizadeh D.R., von Falkenhausen M., Gieseke J. et al. Cerebral arteriovenous malformation: Spetzler-Martin classification at subsecond-temporalresolution fourdimensional MR angiography compared with that at DSA. Radiology 2008;246:205–13. DOI: 10.1148/radiol.2453061684.
25. Kim D.J., Krings T. Whole-brain perfusion CT patterns of brain arteriovenous malformations: a pilot study in 18 patients. AJNR Am J Neuroradiol 2011;32(11):2061–6. DOI: 10.3174/ajnr.A2659.
26. Palkowitsch P.K., Bostelmann S., Lengsfeld P. Safety and tolerability of iopromide intravascular use: a pooled analysis of three non-interventional studies in 132,012 patients. Acta Radiol 2014;55(6):707–14. DOI: 10.1177/0284185113504753.
27. Sehgal V., Delproposto Z., Haacke E.M. et al. Clinical applications of neuroimaging with susceptibility-weighted imaging. J Magn Reson Imaging 2005;22(4):439–50. DOI: 10.1002/jmri.20404.
28. Haacke E.M., Mittal S., Wu Z. et al. Susceptibility-weighted imaging: technical aspects and clinical applications, part 1. AJNR Am J Neuroradiol 2009;30(1):19–30. DOI: 10.3174/ajnr.A1400.
29. Geibprasert S., Pongpech S., Jiarakongmun P. et al. Radiologic assessment of brain arteriovenous malformations: what clinicians need to know. Radiographics 2010;30(2):483–501. DOI: 10.1148/rg.302095728.
30. Wolf R.L., Detre J.A. Clinical neuroimaging using arterial spinlabeled perfusion magnetic resonance imaging. Neurotherapeut 2007;4(3):346–59. DOI: 10.1016/j.nurt.2007.04.005.
31. Hunt C.H., Hartman R.P., Hesley G.K. Frequency and severity of adverse effects of iodinated and gadolinium contrast materials: retrospective review of 456,930 doses. Am J Roentgenol 2009;193(4):1124–7. DOI: 10.2214/AJR.09.2520.
32. Stereotactic radiosurgery for patients with intracranial arteriovenous malformations (AVM). Harrisburg(PA): International RadioSurgery Association(IRSA), 2009. 22 p.
33. Filatov Yu.M. Arterio-venous aneurysms of the cerebral hemispheres. Clinic, diagnosis and surgical treatment. Dis. … doct. of med. sciences: 14.00.28. Moscow, 1972. Available at: https://search.rsl.ru/ru/record/01007063184 (In Russ.).
34. Hernesniemi J., Romani R., Lehecka M. et al. Present state of microneurosurgery of cerebral arteriovenous malformations. Acta Neurochir Suppl 2010;107:71–6. DOI: 10.1007/978-3-211-99373-6_11.
35. Starke R.M., Komotar R.J., Otten M.L. et al. Adjuvant embolization with N-butyl cyanoacrylate in the treatment of cerebral arteriovenous malformations: outcomes, complications, and predictors of neurologic deficits. Stroke 2009;40(8):2783–90. DOI: 10.1161/STROKEAHA.108.539775.
36. Theofanis T., Chalouhi N., Dalyai R. et al. Microsurgery for cerebral arteriovenous malformations: postoperative outcomes and predictors of complications in 264 cases. Neurosurg Focus 2014:37(3):E10. DOI: 10.3171/2014.7.FOCUS14160.
37. Parfenov V.E., Svistov D.V., Eliava Sh.Sh. et al. Clinical recommendations for the diagnosis and treatment of arteriovenous malformations of the central nervous system. Moscow, 2014. (In Russ.).
38. Martinez J.L., Macdonald R.L. Surgical strategies for acutely ruptured arteriovenous malformations. Front Neurol Neurosci 2015;37:166–81. DOI: 10.1159/000437121.
39. Yakovlev S.B. Arteriovenous fistulas of the head and neck. Clinic, angioarchitectonics, endovascular treatment. Dis. … doct. of med. sciences: 14.00.28. Moscow, 2009. Available at: https://www.dissercat.com/content/arteriovenoznye-fistulygolovy-i-shei-klinika-angioarkhitektonikaendovaskulyarnoe-lechenie (In Russ.).
40. Steiger H.-J., Schmid-Elaesser R., Maucevic A. et al. Neurosurgery of arteriovenous malformations and fistulas: a multimodal approach. Berlin: Springer-Verlag, 2002.
41. Gobin Y.P., Laurent A., Merienne L. et al. Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 1996;85(1):19–28. DOI: 10.3171/jns.1996.85.1.0019.
42. Leksell L. The stereotaxic method and radiosurgery of the brain. Acta Chir Scand 1951;102(4):316–9.
43. Steiner L., Leksell L., Forster D.M. et al. Stereotactic radiosurgery in intracranial arterio-venous malformations. Acta Neurochir (Wien) 1974;21:195–209. DOI: 10.1007/978-3-7091-8355-7_26.
44. Jokura H., Kawagishi J., Sugai K. et al. Gamma knife radiosurgery for arteriovenous malformations: the Furukawa experience. Prog Neurol Surg 2009;22: 20–30. DOI: 10.1159/000163379.
45. Liscak R., Vladyka V., Simonova G. et al. Arteriovenous malformations after Leksell gamma knife radiosurgery: rate of obliteration and complications. Neurosurgery 2007;60(6):1005–14. DOI: 10.1227/01.NEU.0000255474.60505.4A.
46. Szeifert G.T., Levivier M., Lorenzoni J. et al. Morphological observations in brain arteriovenous malformations after gamma knife radiosurgery. Prog Neurol Surg 2013;27:119–29. DOI: 10.1159/000341772.
47. Pollock B.E., Flickinger J.C., Lunsford L.D. et al. Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 1998:42(6): 1239–44. DOI: 10.1097/00006123-199806000-00020.
48. Zammar S.G., El Tecle N.E., Ahmadieh T.Y. et al. A biological approach to treating brain arteriovenous malformations. Neurosurgery 2014:74(4):15–7. DOI: 10.1227/01.neu.0000445336.
49. 60.
50. Zipfel G.J., Bradshaw P., Bova F.J. et al. Do the morphological characteristics of arteriovenous malformations affect the results of radiosurgery? J Neurosurg 2004;101(3):393–401. DOI: 10.3171/jns.2004.101.3.0393.
51. Sirin S., Kondziolka D., Niranjan A. et al. Prospective staged volume radiosurgery for large arteriovenous malformations: indications and outcomes in otherwise untreatable patients. Neurosurgery 2006;58(1):17–27. DOI: 10.1227/01.neu.0000190653.42970.6b.
52. Yang S.Y., Kim D.G., Chung H.T. et al. Radiosurgery for large cerebral arteriovenous malformations. Acta Neurochir(Wien) 2009;151(2):113–24. DOI: 10.1007/s00701-008-0173-5.
53. Matsuo T., Kamada К., Izumo Т. et al. Linear accelerator-based radiosurgery alone for arteriovenous malformation: more than 12 years of observation. Int J Radiat Oncol Biol Phys 2014;89(3):576–83. DOI: 10.1016/j.ijrobp.2014.03.017.
54. Kano H., Kondziolka D., Flickinger J.C. et al. Stereotactic radiosurgery for arteriovenous malformations. Part 6: multistaged volumetric management of large arteriovenous malformations. J Neurosurg 2012;116(1):54–65. DOI: 10.3171/2011.9.JNS11177.
55. Lindvall P., Grayson D., Bergström P. et al. Hypofractionated stereotactic radiotherapy in medium-sized to large arteriovenous malformations. J Clin Neurosci 2015;22(6):955–8. DOI: 10.1016/j.jocn.2014.12.015.
56. Mathis J.A., Barr J.D., Horton J.A. et al. The efficacy of particulate embolization combined with stereotactic radiosurgery for treatment of large arteriovenous malformations of the brain. AJNR Am J Neuroradiol 1995;16(2):299–306.
57. AlKhalili K., Chalouhi N., Tjoumakaris S. et al. Staged-volume radiosurgery for large arteriovenous malformations: a review. Neurosurg Focus 2014;37:E3. DOI: 10.3171/2014.6.FOCUS14217.
58. Moosa S., Chen C.J., Ding D. et al. Volume-staged versus dose-staged radiosurgery outcomes for large intracranial arteriovenous malformations. Neurosurg Focus 2014;37(3):E18. DOI: 10.3171/2014.5.FOCUS14205.
59. Friedman W.A., Bova F.J. Radiosurgery for arteriovenous malformations. Neurol Res 2011;33(8):803–19. DOI: 10.1179/1743132811Y.0000000043.
60. Pollock B.E., Gorman D.A., Coffey R.J. Patient outcomes after arteriovenous malformation radiosurgical management: Results based on a 5- to 14-year follow-up study. Neurosurgery 2003;52(6):1291–7. DOI: 10.1227/01.neu.0000064800.26214.fe.
61. Sasaki T., Kurita H., Saito I. et al. Arteriovenous malformations in the basal ganglia and thalamus: Management and results in 101 cases. J Neurosurg 1998;88(2):285–92. DOI: 10.3171/jns.1998.88.2.0285.
62. Kim J.M., Miller J.A., Kotecha R. et al. The risk of radiation necrosis following stereotactic radiosurgery with concurrent systemic therapies. J Neurooncol 2017;133(2):357–68. DOI: 10.1007/s11060-017-2442-8.
63. Spetzler R.F., Martin N.A. A proposed grading system for arteriovenous malformations. J Neurosurg 1986;65(4):476–83. DOI: 10.3171/jns.1986.65.4.0476.
64. Yamamoto M., Hara M., Ide M. et al. Radiation-related adverse effects observed on neuro-imaging several years after radiosurgery for cerebral arteriovenous malformations. Surg Neurol 1998;49(4):385–98. DOI: 10.1016/s0090-3019(97)00531-4.
65. Kondziolka D., Lunsford L.D., Flickinger J.C. Gamma knife stereotactic radiosurgery for cerebral vascular malformations. In: Stereotactic Radiosurgery. Ed. by E. Alexander Jr., J.S. Loeffler, L.D. Lunsford. New York: McGraw-Hill, 1993. P. 136–146.
66. Rothbart D., Awad I.A., Lee J. et al. Expression of angiogenic factors and structural proteins in central nervous system vascular malformations. Neurosurgery 1996;38(5):915–25. DOI: 10.1097/00006123-199605000-00011.
67. Strugar J., Rothbart D., Harrington W. et al. Vascular permeability factor in brain metastases: Correlation with vasogenic brain edema and tumour angiogenesis. J Neurosurg 1994;81(4):560–6. DOI: 10.3171/jns.1994.81.4.0560.
68. Heffez D.S., Osterdock R.J., Alderete L. et al. The effect of incomplete patient follow-up on the reported results of AVM radiosurgery. Surg Neurol 1998;49(4):373–81. DOI: 10.1016/s0090-3019(97)00441-2.
69. Lunsford L.D., Kondziolka D., Flickinger J.C. et al. Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 1991;75(4):512–24. DOI: 10.3171/jns.1991.75.4.0512.
70. Dawkins A.A., Evans A.L., Wattam J. et al. Complications of cerebral angiography: a prospective analysis of 2,924 consecutive procedures. Neuroradiology 2007;49(9):753–9. DOI: 10.1007/s00234-007-0252-y.
71. Abdelaziz O., Shereen A., Inoue T. et al. Correlation of appearance of MRI perinidal T2 hyperintensity signal and eventual nidus obliteration following photon radiosurgery of brain AVMs: combined results of LINAC and Gamma Knife centers. J Neurol Surg A Cent Eur Neurosurg 2019 May;80(3):187–97. DOI: 10.1055/s-0039-1678710.
72. Lee C.C., Reardon M.A., Ball B.Z. et al. The predictive value of magnetic resonance imaging in evaluating intracranial arteriovenous malformation obliteration after stereotactic radiosurgery. J Neurosurg 2015;123(1):136–44. DOI: 10.3171/2014.10.JNS141565.
73. Mukherji S.K., Quisling R.G., Kubilis P.S. et al. Intracranial arteriovenous malformations: quantitative analysis of magnitude contrast MR angiography versus gradient-echo MR imaging versus conventional angiography. Radiology 1995;196(1):187–93. DOI: 10.1148/radiology.196.1.7784565.
74. Stock K.W., Wetzel S., Kirsch E. et al. Anatomic evaluation of the circle of Willis: MR angiography versus intraarterial digital subtraction angiography. AJNR Am J Neuroradiol 1996;17:1495–9.
75. Tsuruda J., Saloner D., Norman D. Artifacts associated with MR neuroangiography. AJNR Am J Neuroradiol 1992;13(5):1411–22.
76. Ward E.V., Galizia M.S., Usman A. et al. Comparison of quiescent inflow singleshot and native space for nonenhanced peripheral MR angiography. J Magn Reson Imaging 2013:38:1531–8. DOI: 10.1002/jmri.24124.
77. Buis D.R., Bot J.C., Barkhof F. et al. The predictive value of 3D time-of-flight MR angiography in assessment of brain arteriovenous malformation obliteration after radiosurgery. AJNR Am J Neuroradiol 2012;33(2):232–8. DOI: 10.3174/ajnr.A2744.
Review
For citations:
Tokarev A.S., Chuvilin S.A., Neznanova M.V. Magnetic resonance imaging in the diagnosis of brain arteriovenous malformations and in the evaluation of the results of stereotactic radiosurgery (review). Russian journal of neurosurgery. 2021;23(1):135‑145. (In Russ.) https://doi.org/10.17650/1683-3295-2021-23-1-135-145
Views:
670
Email this article 