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Microsurgical Treatment of Deep and Eloquent AVMs

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Cerebrovascular Surgery

Part of the book series: Advances and Technical Standards in Neurosurgery ((NEUROSURGERY,volume 44))

Abstract

Over the past 30 years, the treatment of deep and eloquent arteriovenous malformations (AVMs) has moved away from microneurosurgical resection and towards medical management and the so-called minimally invasive techniques, such as endovascular embolization and radiosurgery. The Spetzler–Martin grading system (and subsequent modifications) has done much to aid in risk stratification for surgical intervention; however, the system does not predict the risk of hemorrhage nor risk from other interventions. In more recent years, the ARUBA trial has suggested that unruptured AVMs should be medically managed. In our experience, although these eloquent regions of the brain should be discussed with patients in assessing the risks and benefits of intervention, we believe each AVM should be assessed based on the characteristics of the patient and the angio-architecture of the AVM, in particular venous hypertension, which may guide us to treat even high-grade AVMs when we believe we can (and need to) to benefit the patient. Advances in imaging and intraoperative adjuncts have helped us in decision making, preoperative planning, and ensuring good outcomes for our patients. Here, we present several cases to illustrate our primary points that treating low-grade AVMs can be more difficult than treating high-grade ones, mismanagement of deep and eloquent AVMs at the behest of dogma can harm patients, and the treatment of any AVM should be tailored to the individual patient and that patient’s lesion.

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Abbreviations

3D:

Three dimensional

ACA:

Anterior cerebral artery

AED:

Antiepileptic drug

AP:

Anteroposterior

ARUBA:

A randomized controlled trial of unruptured brain AVMs

AVM:

Arteriovenous malformation

CT:

Computed tomography

CTA:

Computed tomography angiography

DSA:

Digital subtraction angiography

fMRI:

Functional magnetic resonance imaging

ICA:

Internal carotid artery

ICG:

Indocyanine green

MCA:

Middle cerebral artery

MRI:

Magnetic resonance imaging

mRS:

Modified Rankin Scale

PCA:

Posterior cerebral artery

SM:

Spetzler–Martin

References

  1. Yasargil MG. Microneurosurgery, volume IIIA: AVM of the brain, history, embryology, pathological considerations, hemodynamics, diagnostic studies, microsurgical anatomy. New York: Georg Thieme Verlag; 1987. https://medone.thieme.com.

    Google Scholar 

  2. Yasargil MG. Microneurosurgery, volume IIIB: AVM of the brain, clinical considerations, general and special operative techniques, surgical results, nonoperated cases, cavernous and venous angiomas, neuroanesthesia. New York: Georg Thieme Verlag; 1988.

    Google Scholar 

  3. Valavanis A, Yaşargil MG. The endovascular treatment of brain arteriovenous malformations. In: Cohadon F, Dolenc VV, Antunes JL, Nornes H, Pickard JD, Reulen H-J, et al., editors. Advances and technical standards in neurosurgery, vol. 24. Vienna: Springer Vienna; 1998. p. 131–214. https://doi.org/10.1007/978-3-7091-6504-1_4.

    Chapter  Google Scholar 

  4. Chen C-J, Ding D, Derdeyn CP, Lanzino G, Friedlander RM, Southerland AM, et al. Brain arteriovenous malformations: a review of natural history, pathobiology, and interventions. Neurology. 2020;95:917–27. http://www.ncbi.nlm.nih.gov/pubmed/33004601.

    Article  PubMed  Google Scholar 

  5. Locksley HB. Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the cooperative study. J Neurosurg. 1966;25:219–39. http://www.ncbi.nlm.nih.gov/pubmed/5911370.

    Article  CAS  PubMed  Google Scholar 

  6. Volovici V, Schouten JW, Vajkoczy P, Dammers R, Meling TR. Unruptured arteriovenous malformations. Stroke. 2021;52:1143–6. http://www.ncbi.nlm.nih.gov/pubmed/33494639.

    Article  PubMed  Google Scholar 

  7. Garzelli L, Shotar E, Blauwblomme T, Sourour N, Alias Q, Stricker S, et al. Risk factors for early brain AVM rupture: cohort study of pediatric and adult patients. Am J Neuroradiol. 2020;41:2358–63. http://www.ncbi.nlm.nih.gov/pubmed/33122204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ding D, Chen C-J, Starke RM, Kano H, Lee JYK, Mathieu D, et al. Risk of brain arteriovenous malformation hemorrhage before and after stereotactic radiosurgery. Stroke. 2019;50:1384–91. http://www.ncbi.nlm.nih.gov/pubmed/31043153.

    Article  PubMed  Google Scholar 

  9. Alqadi M, Brunozzi D, Linninger A, Amin-Hanjani S, Charbel FT, Alaraj A. Cerebral arteriovenous malformation venous stenosis is associated with hemodynamic changes at the draining vein-venous sinus junction. Med Hypotheses. 2019;123:86–8. http://www.ncbi.nlm.nih.gov/pubmed/30696602.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Lin TM, Yang HC, Lee CC, Wu HM, Hu YS, Luo CB, et al. Stasis index from hemodynamic analysis using quantitative DSA correlates with hemorrhage of supratentorial arteriovenous malformation: a cross-sectional study. J Neurosurg. 2019;132:1–9. http://www.ncbi.nlm.nih.gov/pubmed/31026828.

    Google Scholar 

  11. Brunozzi D, Hussein AE, Shakur SF, Linninger A, Hsu C-Y, Charbel FT, et al. Contrast time-density time on digital subtraction angiography correlates with cerebral arteriovenous malformation flow measured by quantitative magnetic resonance angiography, angioarchitecture, and hemorrhage. Neurosurgery. 2018;83:210–6. http://www.ncbi.nlm.nih.gov/pubmed/29106647.

    Article  PubMed  Google Scholar 

  12. Shakur SF, Valyi-Nagy T, Amin-Hanjani S, Ya’Qoub L, Aletich VA, Charbel FT, et al. Effects of nidus microarchitecture on cerebral arteriovenous malformation hemodynamics. J Clin Neurosci. 2016;26:70–4. http://www.sciencedirect.com/science/article/pii/S0967586815005354.

    Article  PubMed  Google Scholar 

  13. Abecassis IJ, Xu DS, Batjer HH, Bendok BR. Natural history of brain arteriovenous malformations: a systematic review. Neurosurg Focus. 2014;37:E7. http://www.ncbi.nlm.nih.gov/pubmed/25175445.

    Article  PubMed  Google Scholar 

  14. Gross BA, Du R. Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg. 2013;118:437–43. http://www.ncbi.nlm.nih.gov/pubmed/23198804.

    Article  PubMed  Google Scholar 

  15. Lv X, Wu Z, Jiang C, Yang X, Li Y, Sun Y, et al. Angioarchitectural characteristics of brain arteriovenous malformations with and without hemorrhage. World Neurosurg. 2011;76:95–9. https://linkinghub.elsevier.com/retrieve/pii/S1878875011001173.

    Article  PubMed  Google Scholar 

  16. Stapf C, Mast H, Sciacca RR, Choi JH, Khaw AV, Connolly ES, et al. Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology. 2006;66:1350–5. www.neurology.org.

    Article  CAS  PubMed  Google Scholar 

  17. Stefani MA, Porter PJ, TerBrugge KG, Montanera W, Willinsky RA, Wallace MC. Large and deep brain arteriovenous malformations are associated with risk of future hemorrhage. Stroke. 2002;33:1220–4. http://www.ncbi.nlm.nih.gov/pubmed/11988594.

    Article  PubMed  Google Scholar 

  18. Ogilvy CS, Stieg PE, Awad I, Brown RD, Kondziolka D, Rosenwasser R, et al. Recommendations for the management of intracranial arteriovenous malformations. Circulation. 2001;103:2644–57. http://www.ncbi.nlm.nih.gov/pubmed/11382737.

    Article  CAS  PubMed  Google Scholar 

  19. Mohr JP, Overbey JR, Von Kummer R, Stefani MA, Libman R, Stapf C, et al. Functional impairments for outcomes in a randomized trial of unruptured brain AVMs. Neurology. 2017;89(14):1499–506. http://www.neurology.org/lookup/doi/10.1212/WNL.0000000000004532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mohr JP, Overbey JR, Hartmann A, von Kummer R, Al-Shahi Salman R, Kim H, et al. Medical management with interventional therapy versus medical management alone for unruptured brain arteriovenous malformations (ARUBA): final follow-up of a multicentre, non-blinded, randomised controlled trial. Lancet Neurol. 2020;19:573–81. www.thelancet.com/neurology.

    Article  PubMed  Google Scholar 

  21. Magro E, Gentric J-C, Darsaut TE, Ziegler D, Bojanowski MW, Raymond J. Responses to ARUBA: a systematic review and critical analysis for the design of future arteriovenous malformation trials. J Neurosurg. 2017;126:486–94. http://www.ncbi.nlm.nih.gov/pubmed/27128584.

    Article  PubMed  Google Scholar 

  22. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, et al. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet. 2014;383:614–21. http://www.ncbi.nlm.nih.gov/pubmed/24268105.

    Article  CAS  PubMed  Google Scholar 

  23. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–83. http://www.ncbi.nlm.nih.gov/pubmed/3760956.

    Article  CAS  PubMed  Google Scholar 

  24. Tayebi Meybodi A, Lawton MT. Modern radiosurgical and endovascular classification schemes for brain arteriovenous malformations. Neurosurg Rev. 2020;43:49–58. http://www.ncbi.nlm.nih.gov/pubmed/29728873.

    Article  PubMed  Google Scholar 

  25. Luessenhop AJ. AVM grading in assessing surgical risk. J Neurosurg. 1987;66:637–8. http://www.ncbi.nlm.nih.gov/pubmed/3559733.

    CAS  PubMed  Google Scholar 

  26. Stefani MA, Sgarabotto Ribeiro D, Mohr JP. Grades of brain arteriovenous malformations and risk of hemorrhage and death. Ann Clin Transl Neurol. 2019;6:508–14. http://www.ncbi.nlm.nih.gov/pubmed/30911574.

    Article  PubMed  PubMed Central  Google Scholar 

  27. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7. http://www.ncbi.nlm.nih.gov/pubmed/3363593.

    Article  PubMed  Google Scholar 

  28. Hamilton MG, Spetzler RF. The prospective application of a grading system for arteriovenous malformations. Neurosurgery. 1994;34:2–7. https://academic.oup.com/neurosurgery/article/34/1/2/2857379.

    CAS  PubMed  Google Scholar 

  29. Joint Writing Group of the Technology Assessment Committee American Society of Interventional and Therapeutic Neuroradiology; Joint Section on Cerebrovascular Neurosurgery a Section of the American Association of Neurological Surgeons and Congress of Neur, Atkinson RP, Awad IA, Batjer HH, Dowd CF, Furlan A, et al. Reporting terminology for brain arteriovenous malformation clinical and radiographic features for use in clinical trials. Stroke. 2001;32:1430–42. http://ahajournals.org.

  30. Lawton MT, Hamilton MG, Spetzler RF. Multimodality treatment of deep arteriovenous malformations: thalamus, basal ganglia, and brain stem. Neurosurgery. 1995;37:29–36. http://www.ncbi.nlm.nih.gov/pubmed/8587687.

    Article  CAS  PubMed  Google Scholar 

  31. Tew JM, Lewis AI, Reichert KW. Management strategies and surgical techniques for deep-seated supratentorial arteriovenous malformations. Neurosurgery. 1995;36:1065–72. https://academic.oup.com/neurosurgery/article/36/6/1065/2757617.

    Article  PubMed  Google Scholar 

  32. de Oliveira E, Tedeschi H, Siqueira MG, Ono M, Rhoton AL. Arteriovenous malformations of the basal ganglia region: rationale for surgical management. Acta Neurochir (Wien). 1997;139:487–506. http://link.springer.com/10.1007/BF02750990.

    Article  Google Scholar 

  33. Gross BA, Duckworth EAM, Getch CC, Bendok BR, Batjer HH. Challenging traditional beliefs: microsurgery for arteriovenous malformations of the basal ganglia and thalamus. Neurosurgery. 2008;63:393–410; discussion 410–1. http://www.ncbi.nlm.nih.gov/pubmed/18812951.

    Article  PubMed  Google Scholar 

  34. Potts MB, Young WL, Lawton MT. Deep arteriovenous malformations in the basal ganglia, thalamus, and insula. Neurosurgery. 2013;73:417–29. http://www.ncbi.nlm.nih.gov/pubmed/23728451.

    Article  PubMed  Google Scholar 

  35. Potts MB, Jahangiri A, Jen M, Sneed PK, McDermott MW, Gupta N, et al. Deep arteriovenous malformations in the basal ganglia, thalamus, and insula: multimodality management, patient selection, and results. World Neurosurg. 2014;82:386–94. http://www.ncbi.nlm.nih.gov/pubmed/24657255.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Laakso A, Dashti R, Juvela S, Isarakul P, Niemelä M, Hernesniemi J. Risk of hemorrhage in patients with untreated Spetzler-Martin grade IV and V arteriovenous malformations. Neurosurgery. 2011;68:372–8. http://www.ncbi.nlm.nih.gov/pubmed/21135742.

    Article  PubMed  Google Scholar 

  37. Kato Y, Dong V, Chaddad F, Takizawa K, Izumo T, Fukuda H, et al. Expert consensus on the management of brain arteriovenous malformations. Asian J Neurosurg. 2019;14:1074. http://www.ncbi.nlm.nih.gov/pubmed/31903343.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Zuurbier SM, Salman RAS. Interventions for treating brain arteriovenous malformations in adults. Cochrane Database Syst Rev. 2019:CD003436. http://www.ncbi.nlm.nih.gov/pubmed/31503327.

  39. de Tribolet N. Radiosurgery of deep arteriovenous malformations. J Neurosurg. 2004;100:205–7. http://www.ncbi.nlm.nih.gov/pubmed/15086224.

    Article  PubMed  Google Scholar 

  40. Rutledge WC, Abla AA, Nelson J, Halbach VV, Kim H, Lawton MT. Treatment and outcomes of ARUBA-eligible patients with unruptured brain arteriovenous malformations at a single institution. Neurosurg Focus. 2014;37:E8. http://www.ncbi.nlm.nih.gov/pubmed/25175446.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Potts MB, Lau D, Abla AA, Kim H, Young WL, Lawton MT. Current surgical results with low-grade brain arteriovenous malformations. J Neurosurg. 2015;122:912–20. http://www.ncbi.nlm.nih.gov/pubmed/25658789.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Han PP, Ponce FA, Spetzler RF. Intention-to-treat analysis of Spetzler—Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg. 2003;98:3–7. http://www.ncbi.nlm.nih.gov/pubmed/12546345.

    Article  PubMed  Google Scholar 

  43. Morgan MK, Davidson AS, Assaad NNA, Stoodley MA. Critical review of brain AVM surgery, surgical results and natural history in 2017. Acta Neurochir (Wien). 2017;159:1457–78. http://www.ncbi.nlm.nih.gov/pubmed/28555270.

    Article  Google Scholar 

  44. Cenzato M, Boccardi E, Beghi E, Vajkoczy P, Szikora I, Motti E, et al. European consensus conference on unruptured brain AVMs treatment (supported by EANS, ESMINT, EGKS, and SINCH). Acta Neurochir (Wien). 2017;159:1059–64. http://www.ncbi.nlm.nih.gov/pubmed/28389875.

    Article  Google Scholar 

  45. Pollock BE, Gorman DA, Brown PD. Radiosurgery for arteriovenous malformations of the basal ganglia, thalamus, and brainstem. J Neurosurg. 2004;100:210–4. http://www.ncbi.nlm.nih.gov/pubmed/15086226.

    Article  PubMed  Google Scholar 

  46. Valavanis A, Pangalu A, Tanaka M. Endovascular treatment of cerebral arteriovenous malformations with emphasis on the curative role of embolisation. Interv Neuroradiol. 2005;11:37–43. http://www.ncbi.nlm.nih.gov/pubmed/20584458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kano H, Kondziolka D, Flickinger JC, Yang H, Flannery TJ, Niranjan A, et al. Stereotactic radiosurgery for arteriovenous malformations, part 4: management of basal ganglia and thalamus arteriovenous malformations. J Neurosurg. 2012;116:33–43. http://www.ncbi.nlm.nih.gov/pubmed/22077451.

    Article  PubMed  Google Scholar 

  48. Catapano JS, Frisoli FA, Nguyen CL, Wilkinson DA, Majmundar N, Cole TS, et al. Spetzler-Martin grade III arteriovenous malformations: a multicenter propensity-adjusted analysis of the effects of preoperative embolization. Neurosurgery. 2021;88(5):996–1002. http://www.ncbi.nlm.nih.gov/pubmed/33427287.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Donzelli GF, Nelson J, McCoy D, McCulloch CE, Hetts SW, Amans MR, et al. The effect of preoperative embolization and flow dynamics on resection of brain arteriovenous malformations. J Neurosurg. 2020;132:1836–44. http://www.ncbi.nlm.nih.gov/pubmed/31100732.

    Article  Google Scholar 

  50. Morgan MK, Davidson AS, Koustais S, Simons M, Ritson EA. The failure of preoperative ethylene-vinyl alcohol copolymer embolization to improve outcomes in arteriovenous malformation management: case series. J Neurosurg. 2013;118:969–77. http://www.ncbi.nlm.nih.gov/pubmed/23350776.

    Article  CAS  PubMed  Google Scholar 

  51. Henkes H, Gotwald TF, Brew S, Kaemmerer F, Miloslavski E, Kuehne D. Pressure measurements in arterial feeders of brain arteriovenous malformations before and after endovascular embolization. Neuroradiology. 2004;46:673–7. http://www.ncbi.nlm.nih.gov/pubmed/15205863.

    Article  CAS  PubMed  Google Scholar 

  52. Haw CS, TerBrugge K, Willinsky R, Tomlinson G. Complications of embolization of arteriovenous malformations of the brain. J Neurosurg. 2006;104:226–32. http://www.ncbi.nlm.nih.gov/pubmed/16509496.

    Article  PubMed  Google Scholar 

  53. Kim LJ, Albuquerque FC, Spetzler RF, McDougall CG. Postembolization neurological deficits in cerebral arteriovenous malformations: stratification by arteriovenous malformation grade. Neurosurgery. 2006;59:53–9; discussion 53–9. www.neurosurgery-online.com.

    PubMed  Google Scholar 

  54. Rutledge C, Nelson J, Lu A, Nisson P, Jonzzon S, Winkler EA, et al. Cost determinants in management of brain arteriovenous malformations. Acta Neurochir (Wien). 2020;162:169–73. http://www.ncbi.nlm.nih.gov/pubmed/31760534.

    Article  Google Scholar 

  55. Crowley RW, Ducruet AF, McDougall CG, Albuquerque FC. Endovascular advances for brain arteriovenous malformations. Neurosurgery. 2014;74:S74–82. http://www.ncbi.nlm.nih.gov/pubmed/24402496.

    Article  PubMed  Google Scholar 

  56. Baharvahdat H, Blanc R, Fahed R, Pooyan A, Mowla A, Escalard S, et al. Endovascular treatment as the main approach for Spetzler–Martin grade III brain arteriovenous malformations. J Neurointerv Surg. 2021;13(3):241–6. http://www.ncbi.nlm.nih.gov/pubmed/32989031.

    Article  PubMed  Google Scholar 

  57. Conger A, Kulwin C, Lawton M, Cohen-Gadol A. Endovascular and microsurgical treatment of cerebral arteriovenous malformations: current recommendations. Surg Neurol Int. 2015;6:39. http://www.ncbi.nlm.nih.gov/pubmed/25883831.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Crowley RW, Ducruet AF, Kalani MYS, Kim LJ, Albuquerque FC, McDougall CG. Neurological morbidity and mortality associated with the endovascular treatment of cerebral arteriovenous malformations before and during the Onyx era. J Neurosurg. 2015;122:1492–7. http://www.ncbi.nlm.nih.gov/pubmed/25816081.

    Article  PubMed  Google Scholar 

  59. Morgan MK, Heller GZ. The role of embolization before surgery for Spetzler-Ponce class B and C brain AVMs: a prospective cohort series. J Neurosurg Sci. 2018;62:429–36. http://www.ncbi.nlm.nih.gov/pubmed/29480692.

    Article  PubMed  Google Scholar 

  60. Hashimoto N. Microsurgery for cerebral arteriovenous malformations: a dissection technique and its theoretical implications. Neurosurgery. 2001;48:1278–81. https://academic.oup.com/neurosurgery/article/48/6/1278/3773532.

    CAS  PubMed  Google Scholar 

  61. Kim H, Abla AA, Nelson J, McCulloch CE, Bervini D, Morgan MK, et al. Validation of the supplemented Spetzler-Martin grading system for brain arteriovenous malformations in a multicenter cohort of 1009 surgical patients. Neurosurgery. 2015;76:25–33. http://www.ncbi.nlm.nih.gov/pubmed/25251197.

    Article  PubMed  Google Scholar 

  62. Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery. 2010;66:702–13. http://www.ncbi.nlm.nih.gov/pubmed/20190666.

    Article  PubMed  Google Scholar 

  63. Spetzler RF, Ponce FA. A 3-tier classification of cerebral arteriovenous malformations. J Neurosurg. 2011;114:842–9. http://www.ncbi.nlm.nih.gov/pubmed/20932095.

    Article  PubMed  Google Scholar 

  64. Hafez A, Koroknay-Pál P, Oulasvirta E, Elseoud AA, Lawton MT, Niemelä M, et al. The application of the Novel Grading Scale (Lawton-Young Grading System) to predict the outcome of brain arteriovenous malformation. Neurosurgery. 2019;84:529–36. http://www.ncbi.nlm.nih.gov/pubmed/29733392.

    Article  PubMed  Google Scholar 

  65. Lasjaunias PL, Landrieu P, Rodesch G, Alvarez H, Ozanne A, Holmin S, et al. Cerebral proliferative angiopathy. Stroke. 2008;39:878–85. http://www.ncbi.nlm.nih.gov/pubmed/18239181.

    Article  PubMed  Google Scholar 

  66. Du R, Keyoung HM, Dowd CF, Young WL, Lawton MT. The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery. 2007;60:638–46; discussion 646–8. http://www.ncbi.nlm.nih.gov/pubmed/17415200.

    Article  PubMed  Google Scholar 

  67. Chin LS, Raffel C, Gonzalez-Gomez I, Giannotta SL, McComb JG. Diffuse arteriovenous malformations: a clinical, radiological, and pathological description. Neurosurgery. 1992;31:863–8; discussion 868–9. http://www.ncbi.nlm.nih.gov/pubmed/1436409.

    CAS  PubMed  Google Scholar 

  68. Fierstra J, Spieth S, Tran L, Conklin J, Tymianski M, ter Brugge KG, et al. Severely impaired cerebrovascular reserve in patients with cerebral proliferative angiopathy. J Neurosurg Pediatr. 2011;8:310–5. http://www.ncbi.nlm.nih.gov/pubmed/21882924.

    Article  PubMed  Google Scholar 

  69. Spears J, TerBrugge KG, Moosavian M, Montanera W, Willinsky RA, Wallace MC, et al. A discriminative prediction model of neurological outcome for patients undergoing surgery of brain arteriovenous malformations. Stroke. 2006;37:1457–64. http://www.ncbi.nlm.nih.gov/pubmed/16690897.

    Article  PubMed  Google Scholar 

  70. Abla AA, Nelson J, Kim H, Hess CP, Tihan T, Lawton MT. Silent arteriovenous malformation hemorrhage and the recognition of “unruptured” arteriovenous malformation patients who benefit from surgical intervention. Neurosurgery. 2015;76:592–600. http://www.ncbi.nlm.nih.gov/pubmed/25714514.

    Article  PubMed  Google Scholar 

  71. Chen X, Cooke DL, Saloner D, Nelson J, Su H, Lawton MT, et al. Higher flow is present in unruptured arteriovenous malformations with silent intralesional microhemorrhages. Stroke. 2017;48:2881–4. http://www.ncbi.nlm.nih.gov/pubmed/28855391.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Cunha e Sa MJ, Stein BM, Solomon RA, McCormick PC. The treatment of associated intracranial aneurysms and arteriovenous malformations. J Neurosurg. 1992;77:853–9. http://www.ncbi.nlm.nih.gov/pubmed/1432126.

  73. da Costa L, Wallace MC, ter Brugge KG, O’Kelly C, Willinsky RA, Tymianski M. The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke. 2009;40:100–5. http://www.ncbi.nlm.nih.gov/pubmed/19008469.

    Article  PubMed  Google Scholar 

  74. Burkhardt J-K, Chen X, Winkler EA, Cooke DL, Kim H, Lawton MT. Delayed venous drainage in ruptured arteriovenous malformations based on quantitative color-coded digital subtraction angiography. World Neurosurg. 2017;104:619–27. http://www.ncbi.nlm.nih.gov/pubmed/28457930.

    Article  PubMed  Google Scholar 

  75. Grüter BE, Sun W, Fierstra J, Regli L, Germans MR. Systematic review of brain arteriovenous malformation grading systems evaluating microsurgical treatment recommendation. Neurosurg Rev. 2021. http://link.springer.com/10.1007/s10143-020-01464-3.

  76. Sundt TM. Neurovascular microsurgery. World J Surg. 1979;3:53–65. http://www.ncbi.nlm.nih.gov/pubmed/483834.

    Article  PubMed  Google Scholar 

  77. Stein BM, Wolpert SM. Arteriovenous malformations of the brain. I: current concepts and treatment. Arch Neurol. 1980;37:1–5. https://jamanetwork.com/.

    Article  CAS  PubMed  Google Scholar 

  78. Stein BM, Wolpert SM. Arteriovenous malformations of the brain. II: current concepts and treatment. Arch Neurol. 1980;37:69–75. https://jamanetwork.com/.

    Article  CAS  PubMed  Google Scholar 

  79. Drake CG. Cerebral arteriovenous malformations: considerations for and experience with surgical treatment in 166 cases. Neurosurgery. 1979;26:145–208. https://academic.oup.com/neurosurgery/article/26/CN_suppl_1/145/4099519.

    Article  CAS  Google Scholar 

  80. Rhoton AL. The cerebrum. Neurosurgery. 2007;61:37–118. http://www.ncbi.nlm.nih.gov/pubmed/18813175.

    Article  PubMed  Google Scholar 

  81. Foster CH, Morone PJ, Tomlinson SB, Cohen-Gadol AA. Application of indocyanine green during arteriovenous malformation surgery: evidence, techniques, and practical pearls. Front Surg. 2019;6:70. http://www.ncbi.nlm.nih.gov/pubmed/31921884.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Kato N, Prinz V, Dengler J, Vajkoczy P. Blood flow assessment of arteriovenous malformations using intraoperative indocyanine green videoangiography. Stroke Res Treat. 2019;2019:1–8. http://www.ncbi.nlm.nih.gov/pubmed/31007890.

    Article  Google Scholar 

  83. Della Puppa A, Scienza R. Multimodal flow-assisted resection of brain AVMs. Acta Neurochir Suppl. 2016;123:141–5. http://www.ncbi.nlm.nih.gov/pubmed/27637641.

    Article  PubMed  Google Scholar 

  84. Walkden JS, Zador Z, Herwadkar A, Kamaly-Asl ID. Use of intraoperative Doppler ultrasound with neuronavigation to guide arteriovenous malformation resection: a pediatric case series. J Neurosurg Pediatr. 2015;15:291–300. http://www.ncbi.nlm.nih.gov/pubmed/25525933.

    Article  PubMed  Google Scholar 

  85. Kato Y, Yamada Y, Sadato A, Nouri M, Cherian I, Tanaka T, et al. Intraoperative anatomical and hemodynamic analysis of intracerebral arteriovenous malformations by semi-quantitative color-coded indocyanine green videoangiography. Asian J Neurosurg. 2017;12:638. http://www.ncbi.nlm.nih.gov/pubmed/29114275.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Amin-Hanjani S, Meglio G, Gatto R, Bauer A, Charbel FT. The utility of intraoperative blood flow measurement during aneurysm surgery using an ultrasonic perivascular flow probe. Oper Neurosurg. 2006;58:ONS-305–12. http://www.ncbi.nlm.nih.gov/pubmed/16582654.

    Article  Google Scholar 

  87. Morgan MK, Drummond KJ, Grinnell V, Sorby W. Surgery for cerebral arteriovenous malformation: risks related to lenticulostriate arterial supply. J Neurosurg. 1997;86:801–5. http://www.ncbi.nlm.nih.gov/pubmed/9126895.

    Article  CAS  PubMed  Google Scholar 

  88. Luostarinen T, Takala RSK, Niemi TT, Katila AJ, Niemelä M, Hernesniemi J, et al. Adenosine-induced cardiac arrest during intraoperative cerebral aneurysm rupture. World Neurosurg. 2010;73:79–83. https://doi.org/10.1016/j.surneu.2009.06.018.

    Article  PubMed  Google Scholar 

  89. Cannesson M, Desebbe O, Rosamel P, Delannoy B, Robin J, Bastien O, et al. Pleth variability index to monitor the respiratory variations in the pulse oximeter plethysmographic waveform amplitude and predict fluid responsiveness in the operating theatre. Br J Anaesth. 2008;101:200–6. https://doi.org/10.1093/bja/aen133.

    Article  CAS  PubMed  Google Scholar 

  90. Marc Samama C, Thiry D, Elalamy I, Diaby M, Guillosson J-J, Kieffer E, et al. Perioperative activation of hemostasis in vascular surgery patients. Anesthesiology. 2001;94:74–8. http://www.ncbi.nlm.nih.gov/pubmed/11135724.

    Article  Google Scholar 

  91. Snyder CW, Weinberg JA, McGwin G, Melton SM, George RL, Reiff DA, et al. The relationship of blood product ratio to mortality: survival benefit or survival bias? J Trauma Inj Infect Crit Care. 2009;66:358–64. http://www.ncbi.nlm.nih.gov/pubmed/19204508.

    Article  Google Scholar 

  92. Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D. Normal perfusion pressure breakthrough theory. Neurosurgery. 1978;25:651–72. https://academic.oup.com/neurosurgery/article/25/CN_suppl_1/651/4099752.

    Article  CAS  Google Scholar 

  93. Young WL, Kader A, Prohovnik I, Ornstein E, Fleischer LH, Ostapkovich N, et al. Pressure autoregulation is intact after arteriovenous malformation resection. Neurosurgery. 1993;32:491–7. http://www.ncbi.nlm.nih.gov/pubmed/8474637.

    Article  CAS  PubMed  Google Scholar 

  94. Al-Rodhan NRF, Sundt TM, Piepgras DG, Nichols DA, Rßfenacht D, Stevens LN. Occlusive hyperemia: a theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations. J Neurosurg. 1993;78:167–75. http://www.ncbi.nlm.nih.gov/pubmed/8421198.

    Article  CAS  PubMed  Google Scholar 

  95. Spetzler RF, Hargraves RW, McCormick PW, Zabramski JM, Flom RA, Zimmerman RS. Relationship of perfusion pressure and size to risk of hemorrhage from arteriovenous malformations. J Neurosurg. 1992;76:918–23. http://www.ncbi.nlm.nih.gov/pubmed/1588424.

    Article  CAS  PubMed  Google Scholar 

  96. Soldozy S, Akyeampong DK, Barquin DL, Norat P, Yağmurlu K, Sokolowski JD, et al. Systematic review of functional mapping and cortical reorganization in the setting of arteriovenous malformations, redefining anatomical eloquence. Front Surg. 2020;7:514247. http://www.ncbi.nlm.nih.gov/pubmed/33195382.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Ilyas A, Chen C-J, Ding D, Buell TJ, Raper DMS, Lee C-C, et al. Radiation-induced changes after stereotactic radiosurgery for brain arteriovenous malformations: a systematic review and meta-analysis. Neurosurgery. 2018;83:365–76. http://www.ncbi.nlm.nih.gov/pubmed/29040700.

    Article  PubMed  Google Scholar 

  98. Morgan MK, Zurin AAR, Harrington T, Little N. Changing role for preoperative embolisation in the management of arteriovenous malformations of the brain. J Clin Neurosci. 2000;7:527–30. http://www.ncbi.nlm.nih.gov/pubmed/11029234.

    Article  CAS  PubMed  Google Scholar 

  99. Bi WL, Brown PA, Abolfotoh M, Al-Mefty O, Mukundan S, Dunn IF. Utility of dynamic computed tomography angiography in the preoperative evaluation of skull base tumors. J Neurosurg. 2015;123:1–8. http://www.ncbi.nlm.nih.gov/pubmed/25839925.

    Article  PubMed  Google Scholar 

  100. Salomon EJ, Barfett J, Willems PWA, Geibprasert S, Bacigaluppi S, Krings T. Dynamic CT angiography and CT perfusion employing a 320-detector row CT: protocol and current clinical applications. Klin Neuroradiol. 2009;19:187–96. http://www.ncbi.nlm.nih.gov/pubmed/19705072.

    Article  PubMed  Google Scholar 

  101. Conger A, Kulwin C, Lawton M, Cohen-Gadol A. Diagnosis and evaluation of intracranial arteriovenous malformations. Surg Neurol Int. 2015;6:76. http://www.ncbi.nlm.nih.gov/pubmed/25984390.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Nornes H, Grip A, Wikeby P. Intraoperative evaluation of cerebral hemodynamics using directional Doppler technique. J Neurosurg. 1979;50:145–51. http://www.ncbi.nlm.nih.gov/pubmed/430124.

    Article  CAS  PubMed  Google Scholar 

  103. Rubin JM, Hatfield MK, Chandler WF, Black KL, DiPietro MA. Intracerebral arteriovenous malformations: intraoperative color Doppler flow imaging. Radiology. 1989;170:219–22. http://www.ncbi.nlm.nih.gov/pubmed/2642343.

    Article  CAS  PubMed  Google Scholar 

  104. Serra C, Türe H, Yaltırık CK, Harput MV, Türe U. Microneurosurgical removal of thalamic lesions: surgical results and considerations from a large, single-surgeon consecutive series. J Neurosurg. 2020:1–11. https://thejns.org/view/journals/j-neurosurg/aop/article-10.3171-2020.6.JNS20524/article-10.3171-2020.6.JNS20524.xml.

  105. Keleş A, Harput MV, Türe U. Microneurosurgical removal of a globus pallidus tumor with cottonoid-guided intraoperative ultrasonography: 2-dimensional operative video. Oper Neurosurg. 2020;19:E154. http://www.ncbi.nlm.nih.gov/pubmed/31768549.

    Article  Google Scholar 

  106. Amin-Hanjani S, Charbel FT. Is extracranial-intracranial bypass surgery effective in certain patients? Neurosurg Clin N Am. 2008;19:477–87. https://doi.org/10.1016/j.nec.2008.07.009.

    Article  PubMed  Google Scholar 

  107. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52:132–9; discussion 139. www.neurosurgery-online.com.

    PubMed  Google Scholar 

  108. Raabe A, Beck J, Seifert V. Technique and image quality of intraoperative indocyanine green angiography during aneurysm surgery using surgical microscope integrated near-infrared video technology. Zentralbl Neurochir. 2005;66:1–6. http://www.ncbi.nlm.nih.gov/pubmed/15744621.

    Article  CAS  PubMed  Google Scholar 

  109. Nishiyama Y, Kinouchi H, Senbokuya N, Kato T, Kanemaru K, Yoshioka H, et al. Endoscopic indocyanine green video angiography in aneurysm surgery: an innovative method for intraoperative assessment of blood flow in vasculature hidden from microscopic view. J Neurosurg. 2012;117:302–8. http://www.ncbi.nlm.nih.gov/pubmed/22680246.

    Article  PubMed  Google Scholar 

  110. Cai Z, Zhu L, Wang M, Roe AW, Xi W, Qian J. NIR-II fluorescence microscopic imaging of cortical vasculature in non-human primates. Theranostics. 2020;10:4265–76. http://www.ncbi.nlm.nih.gov/pubmed/32226552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Kamada K, Guger C, Takeuchi F. Multispectrum indocyanine green videography for visualizing brain vascular pathology. World Neurosurg. 2019;132:e545–53. https://doi.org/10.1016/j.wneu.2019.08.078.

    Article  PubMed  Google Scholar 

  112. Oermann EK, Ding D, Yen C-P, Starke RM, Bederson JB, Kondziolka D, et al. Effect of prior embolization on cerebral arteriovenous malformation radiosurgery outcomes. Neurosurgery. 2015;77:406–17. http://www.ncbi.nlm.nih.gov/pubmed/25875580.

    Article  PubMed  Google Scholar 

  113. Türe U, Kaya AH. Principles for managing cavernous malformations in eloquent locations. In: Rigamonti D, editor. Cavernous malformations of the nervous system. Cambridge: Cambridge University Press; 2011. p. 161–72. https://www.cambridge.org/core/product/identifier/9781139003636%23c76427-3076/type/book_part.

    Chapter  Google Scholar 

  114. Fried I. The myth of eloquent cortex, or what is non-eloquent cortex? J Neurosurg. 1993;78:1009–10. http://www.ncbi.nlm.nih.gov/pubmed/8487065.

    CAS  PubMed  Google Scholar 

  115. Drake CG. Surgical treatment of ruptured aneurysms of the basilar artery. J Neurosurg. 1965;23:457–73. http://www.ncbi.nlm.nih.gov/pubmed/5858437.

    Article  CAS  PubMed  Google Scholar 

  116. Shi Y, Chen X. A proposed scheme for grading intracranial arteriovenous malformations. J Neurosurg. 1986;65:484–9. http://www.ncbi.nlm.nih.gov/pubmed/3760957.

    Article  CAS  PubMed  Google Scholar 

  117. Lazar RM. Neuropsychological function and brain arteriovenous malformations: redefining eloquence as a risk for treatment. Neurosurg Focus. 2001;11:1–4. http://www.ncbi.nlm.nih.gov/pubmed/16466236.

    Article  Google Scholar 

  118. Link TW, Winston G, Schwarz JT, Lin N, Patsalides A, Gobin P, et al. Treatment of unruptured brain arteriovenous malformations: a single-center experience of 86 patients and a critique of the a randomized trial of unruptured brain arteriovenous malformations (ARUBA) trial. World Neurosurg. 2018;120:e1156–62. http://www.ncbi.nlm.nih.gov/pubmed/30218805.

    Article  PubMed  Google Scholar 

  119. Cenzato M, Tartara F, D’Aliberti G, Bortolotti C, Cardinale F, Ligarotti G, et al. Unruptured versus ruptured AVMs: outcome analysis from a multicentric consecutive series of 545 surgically treated cases. World Neurosurg. 2018;110:e374–82. http://www.ncbi.nlm.nih.gov/pubmed/29155066.

    Article  PubMed  Google Scholar 

  120. Ding D, Starke RM, Kano H, Mathieu D, Huang P, Kondziolka D, et al. Radiosurgery for cerebral arteriovenous malformations in a randomized trial of unruptured brain arteriovenous malformations (ARUBA)-eligible patients. Stroke. 2016;47:342–9. http://www.ncbi.nlm.nih.gov/pubmed/26658441.

    Article  PubMed  Google Scholar 

  121. Schramm J, Schaller K, Esche J, Boström A. Microsurgery for cerebral arteriovenous malformations: subgroup outcomes in a consecutive series of 288 cases. J Neurosurg. 2017;126:1056–63. https://thejns.org/view/journals/j-neurosurg/126/4/article-p1056.xml.

    Article  PubMed  Google Scholar 

  122. Pollock BE, Storlie CB, Link MJ, Stafford SL, Garces YI, Foote RL. Comparative analysis of arteriovenous malformation grading scales in predicting outcomes after stereotactic radiosurgery. J Neurosurg. 2017;126:852–8. http://www.ncbi.nlm.nih.gov/pubmed/27058199.

    Article  PubMed  Google Scholar 

  123. Gupta R, Adeeb N, Moore JM, Motiei-Langroudi R, Griessenauer CJ, Patel AS, et al. Validity assessment of grading scales predicting complications from embolization of cerebral arteriovenous malformations. Clin Neurol Neurosurg. 2016;151:102–7. http://www.ncbi.nlm.nih.gov/pubmed/27821297.

    Article  PubMed  Google Scholar 

  124. Türe U, Yaşargil MG, Al-Mefty O, Yaşargil DCH. Arteries of the insula. J Neurosurg. 2000;92:676–87. http://www.ncbi.nlm.nih.gov/pubmed/10761659.

    Article  PubMed  Google Scholar 

  125. Türe U, Yaşargil DCH, Al-Mefty O, Yaşargil MG. Topographic anatomy of the insular region. J Neurosurg. 1999;90:720–33. http://www.ncbi.nlm.nih.gov/pubmed/10193618.

    Article  PubMed  Google Scholar 

  126. Huber P, Yasargil MG, Krayenbühl H. Cerebral angiography. 2nd ed. New York: Georg Thieme Verlag; 1982.

    Google Scholar 

  127. Türe U, Harput MV, Kaya AH, Baimedi P, Firat Z, Türe H, et al. The paramedian supracerebellar-transtentorial approach to the entire length of the mediobasal temporal region: an anatomical and clinical study. J Neurosurg. 2012;116:773–91. http://www.ncbi.nlm.nih.gov/pubmed/22264179.

    Article  PubMed  Google Scholar 

  128. Mai JK, Paxinos G, Voss T. Atlas of the human brain. 3rd ed. New York: Elsevier; 2008.

    Google Scholar 

  129. Harput MV, Gonzalez-Lopez P, Türe U. Three-dimensional reconstruction of the topographical cerebral surface anatomy for presurgical planning with free OsiriX software. Oper Neurosurg. 2014;10:426–35. http://www.ncbi.nlm.nih.gov/pubmed/24662508.

    Article  Google Scholar 

  130. Türe U, Yaşargil MG, Krisht AF. The arteries of the corpus callosum: a microsurgical anatomic study. Neurosurgery. 1996;39:1075–84. http://www.ncbi.nlm.nih.gov/pubmed/8938760.

    Article  PubMed  Google Scholar 

  131. Kano H, Kondziolka D, Flickinger JC, Yang H, Flannery TJ, Awan NR, et al. Stereotactic radiosurgery for arteriovenous malformations, part 3: outcome predictors and risks after repeat radiosurgery. J Neurosurg. 2012;116:21–32. http://www.ncbi.nlm.nih.gov/pubmed/22077445.

    Article  PubMed  Google Scholar 

  132. Serra C, Türe U, Krayenbühl N, Şengül G, Yaşargil DCH, Yaşargil MG. Topographic classification of the thalamus surfaces related to microneurosurgery: a white matter fiber microdissection study. World Neurosurg. 2017;97:438–52. http://www.ncbi.nlm.nih.gov/pubmed/27725299.

    Article  PubMed  Google Scholar 

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Cezayirli, P.C., Türe, H., Türe, U. (2022). Microsurgical Treatment of Deep and Eloquent AVMs. In: Kato, Y., Ansari, A. (eds) Cerebrovascular Surgery. Advances and Technical Standards in Neurosurgery, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-030-87649-4_2

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