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Timing of surgery for ruptured supratentorial arteriovenous malformations

  • Original Article - Vascular
  • Published:
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Abstract

Background

There are conflicting opinions regarding the optimal waiting time to perform surgery after rupture of supratentorial arteriovenous malformations (AVMs) to achieve the best possible outcome.

Objective

To analyze factors influencing outcomes for ruptured supratentorial AVMs after surgery, paying particular attention to the timing of the surgery.

Methods

We retrospectively investigated 59 patients admitted to our center between 2000 and 2014 for surgical treatment of ruptured supratentorial AVMs. We evaluated the effect of timing of surgery and other variables on the outcome at 2–4 months (early outcome), at 12 months (intermediate outcome) after surgery, and at final follow-up at the end of 2016 (late outcome).

Results

Age over 40 years (OR 18.4; 95% CI 1.9–172.1; p = 0.011), high Hunt and Hess grade (4 or 5) before surgery (OR 13.5; 95% CI 2.1–89.2; p = 0.007), hydrocephalus on admission (OR 12.9; 95% CI 1.8–94.4; p = 0.011), and over 400 cm3 bleeding during surgery (OR 11.5; 95% CI 1.5–86.6; p = 0.017) were associated with an unfavorable early outcome. Age over 40 years (OR 62.8; 95% CI 2.6–1524.9; p = 0.011), associated aneurysms (OR 34.7; 95% CI 1.4–829.9; p = 0.029), high Hunt and Hess grade before surgery (OR 29.2; 95% CI 2.6–332.6; p = 0.007), and over 400 cm3 bleeding during surgery (OR 35.3; 95% CI 1.7–748.7; p = 0.022) were associated with an unfavorable intermediate outcome. Associated aneurysms (OR 8.2; 95% CI 1.2–55.7; p = 0.031), high Hunt and Hess grade before surgery (OR 5.7; 95% CI 1.3–24.3; p = 0.019), and over 400 cm3 bleeding during surgery (OR 5.8; 95% CI 1.2–27.3; p = 0.027) were associated with an unfavorable outcome at last follow-up. Elapsed time between rupture and surgery did not affect early or final outcome.

Conclusions

Early surgery in patients with ruptured supratentorial arteriovenous malformation is feasible strategy, with late results comparable to those achieved with delayed surgery. Many other factors than timing of surgery play significant roles in long-term outcomes for surgically treated ruptured supratentorial AVMs.

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References

  1. Abla AA, Rutledge WC, Seymour ZA, Guo D, Kim H, Gupta N, Sneed PK, Barani IJ, Larson D, McDermott MW, Lawton MT (2015) A treatment paradigm for high-grade brain arteriovenous malformations: volume-staged radiosurgical downgrading followed by microsurgical resection. J Neurosurg 122:419–432

    Article  PubMed  Google Scholar 

  2. Ajiboye N, Chalouhi N, Starke RM, Zanaty M, Bell R (2014) Cerebral arteriovenous malformations: evaluation and management. Sci World J 2014:649036

    Article  Google Scholar 

  3. AlKhalili K, Chalouhi N, Tjoumakaris S, Rosenwasser R, Jabbour P (2014) Staged-volume radiosurgery for large arteriovenous malformations: a review. Neurosurg Focus 37:E20

    Article  PubMed  Google Scholar 

  4. Altay T (2012) Management of arteriovenous malformations related to Spetzler–Martin grading system. J Neurol Surg A Cent Eur Neurosurg 73:307–319

    Article  PubMed  Google Scholar 

  5. Andrews BT, Wilson CB (1987) Staged treatment of arteriovenous malformations of the brain. Neurosurgery 21:314–323

    Article  CAS  PubMed  Google Scholar 

  6. Beecher JS, Vance A, Lyon KA, Ban VS, McDougall CM, Whitworth LA, White JA, Samson DS, Batjer HH, Welch BG (2016) 359 delayed treatment of ruptured arteriovenous malformations: is it ok to wait? Neurosurgery 63(Suppl 1):206

    Article  PubMed  Google Scholar 

  7. Benifla M, Shelef I, Melamed I, Merkin V, Barrelly R, Cohen A (2010) Urgent removal of ruptured cerebral arteriovenous malformations in children. Harefuah 149:148–152 195

    PubMed  Google Scholar 

  8. Bir SC, Maiti TK, Konar S, Nanda A (2016) Overall outcomes following early interventions for intracranial arteriovenous malformations with hematomas. J Clin Neurosci 23:95–100

    Article  PubMed  Google Scholar 

  9. Braksick SA, Fugate JE (2015) Management of brain arteriovenous malformations. Curr Treat Options Neurol 17:358

    Article  PubMed  Google Scholar 

  10. Brown RD Jr, Flemming KD, Meyer FB, Cloft HJ, Pollock BE, Link ML (2005) Natural history, evaluation, and management of intracranial vascular malformations. Mayo Clin Proc 80:269–281

    Article  PubMed  Google Scholar 

  11. Choi JH, Mast H, Sciacca RR, Hartmann A, Khaw AV, Mohr JP, Sacco RL, Stapf C (2006) Clinical outcome after first and recurrent hemorrhage in patients with untreated brain arteriovenous malformation. Stroke 37:1243–1247

    Article  PubMed  Google Scholar 

  12. Conger A, Kulwin C, Lawton MT, Cohen-Gadol AA (2015) Diagnosis and evaluation of intracranial arteriovenous malformations. Surg Neurol Int 6:76

    Article  PubMed  PubMed Central  Google Scholar 

  13. Crawford PM, West CR, Chadwick DW, Shaw MD (1986) Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry 49:1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Crowley RW, Ducruet AF, McDougall CG, Albuquerque FC (2014) Endovascular advances for brain arteriovenous malformations. Neurosurgery 74(Suppl 1):S74–S82

    Article  PubMed  Google Scholar 

  15. Du R, Keyoung HM, Dowd CF, Young WL, Lawton MT (2007) The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery 60:638–646 discussion 646-638

    Article  PubMed  Google Scholar 

  16. Graf CJ, Perret GE, Torner JC (1983) Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58:331–337

    Article  CAS  PubMed  Google Scholar 

  17. Gross BA, Du R (2012) Rate of re-bleeding of arteriovenous malformations in the first year after rupture. J Clin Neurosci 19:1087–1088

    Article  PubMed  Google Scholar 

  18. Gross BA, Du R (2013) Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:437–443

    Article  PubMed  Google Scholar 

  19. Gross BA, Du R (2014) Diagnosis and treatment of vascular malformations of the brain. Curr Treat Options Neurol 16:279

    Article  PubMed  Google Scholar 

  20. Gross BA, Lai PM, Du R (2013) Hydrocephalus after arteriovenous malformation rupture. Neurosurg Focus 34:E11

    Article  PubMed  Google Scholar 

  21. Gross BA, Storey A, Orbach DB, Scott RM, Smith ER (2015) Microsurgical treatment of arteriovenous malformations in pediatric patients: the Boston Children’s Hospital experience. J Neurosurg Pediatr 15:71–77

    Article  PubMed  Google Scholar 

  22. Han PP, Ponce FA, Spetzler RF (2003) Intention-to-treat analysis of Spetzler–Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg 98:3–7

    Article  PubMed  Google Scholar 

  23. Hartmann A, Mohr JP (2015) Acute management of brain arteriovenous malformations. Curr Treat Options Neurol 17:346

    Article  PubMed  Google Scholar 

  24. Hernesniemi J, Romani R, Lehecka M, Isarakul P, Dashti R, Celik O, Navratil O, Niemela M, Laakso A (2010) Present state of microneurosurgery of cerebral arteriovenous malformations. Acta Neurochir Suppl 107:71–76

    Article  PubMed  Google Scholar 

  25. Hernesniemi JA, Dashti R, Juvela S, Vaart K, Niemela M, Laakso A (2008) Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery 63:823–829 discussion 829-831

    Article  PubMed  Google Scholar 

  26. Iwama T, Yoshimura K, Keller E, Imhof HG, Khan N, Leblebicioglu-Konu D, Tanaka M, Valavanis A, Yonekawa Y (2003) Emergency craniotomy for intraparenchymal massive hematoma after embolization of supratentorial arteriovenous malformations. Neurosurgery 53:1251–1258 discussion 1258-1260

    Article  PubMed  Google Scholar 

  27. Jafar JJ, Rezai AR (1994) Acute surgical management of intracranial arteriovenous malformations. Neurosurgery 34:8–12 discussion 12-13

    CAS  PubMed  Google Scholar 

  28. Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL, MARS Coinvestigators (2014) Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology 83:590–597

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kuhmonen J, Piippo A, Vaart K, Karatas A, Ishii K, Winkler P, Niemela M, Porras M, Hernesniemi J (2005) Early surgery for ruptured cerebral arteriovenous malformations. Acta Neurochir Suppl 94:111–114

    Article  CAS  PubMed  Google Scholar 

  30. Laakso A, Dashti R, Juvela S, Isarakul P, Niemela M, Hernesniemi J (2011) Risk of hemorrhage in patients with untreated Spetzler–Martin grade IV and V arteriovenous malformations: a long-term follow-up study in 63 patients. Neurosurgery 68:372–377 discussion 378

    Article  PubMed  Google Scholar 

  31. Laakso A, Dashti R, Juvela S, Niemela M, Hernesniemi J (2010) Natural history of arteriovenous malformations: presentation, risk of hemorrhage and mortality. Acta Neurochir Suppl 107:65–69

    Article  PubMed  Google Scholar 

  32. Laakso A, Hernesniemi J (2012) Arteriovenous malformations: epidemiology and clinical presentation. Neurosurg Clin N Am 23:1–6

    Article  PubMed  Google Scholar 

  33. Lawton MT, Du R, Tran MN, Achrol AS, McCulloch CE, Johnston SC, Quinnine NJ, Young WL (2005) Effect of presenting hemorrhage on outcome after microsurgical resection of brain arteriovenous malformations. Neurosurgery 56:485–493 discussion 485-493

    Article  PubMed  Google Scholar 

  34. Yasargil MG (1988) Microneurosurgery. In: Yaşargil MG (ed) vol IIIB, 2nd edn. George Thieme Verlag, Stuttgart, p 28

    Google Scholar 

  35. Martinez JL, Macdonald RL (2015) Surgical strategies for acutely ruptured arteriovenous malformations. Front Neurol Neurosci 37:166–181

    Article  PubMed  Google Scholar 

  36. Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellman J, Hacein-Bey L, Duong H, Stein BM, Mohr JP (1997) Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet 350:1065–1068

    Article  CAS  PubMed  Google Scholar 

  37. Ondra SL, Troupp H, George ED, Schwab K (1990) The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:387–391

    Article  CAS  PubMed  Google Scholar 

  38. Pavesi G, Rustemi O, Berlucchi S, Frigo AC, Gerunda V, Scienza R (2009) Acute surgical removal of low-grade (Spetzler–Martin I-II) bleeding arteriovenous malformations. Surg Neurol 72:662–667

    Article  PubMed  Google Scholar 

  39. Peschillo S, Caporlingua A, Colonnese C, Guidetti G (2014) Brain AVMs: an endovascular, surgical, and radiosurgical update. ScientificWorldJournal 2014:834931

    Article  PubMed  PubMed Central  Google Scholar 

  40. Pierot L, Cognard C, Spelle L (2004) Cerebral arteriovenous malformations: evaluation of the hemorrhagic risk and its morbidity. J Neuroradiol 31:369–375

    Article  CAS  PubMed  Google Scholar 

  41. Randell T (2010) Principles of neuroanesthesia in stroke surgery. Acta Neurochir Suppl 107:111–113

    Article  PubMed  Google Scholar 

  42. Ruiz-Sandoval JL, Cantu C, Barinagarrementeria F (1999) Intracerebral hemorrhage in young people: analysis of risk factors, location, causes, and prognosis. Stroke 30:537–541

    Article  CAS  PubMed  Google Scholar 

  43. Rutten-Jacobs LC, Maaijwee NA, Arntz RM, Schoonderwaldt HC, Dorresteijn LD, van Dijk EJ, de Leeuw FE (2014) Clinical characteristics and outcome of intracerebral hemorrhage in young adults. J Neurol 261:2143–2149

    Article  PubMed  Google Scholar 

  44. Signorelli F, Gory B, Pelissou-Guyotat I, Guyotat J, Riva R, Dailler F, Turjman F (2014) Ruptured brain arteriovenous malformations associated with aneurysms: safety and efficacy of selective embolization in the acute phase of hemorrhage. Neuroradiology 56:763–769

    Article  PubMed  Google Scholar 

  45. Soderman M, Andersson T, Karlsson B, Wallace MC, Edner G (2003) Management of patients with brain arteriovenous malformations. Eur J Radiol 46:195–205

    Article  PubMed  Google Scholar 

  46. Stapf C (2006) The neurology of cerebral arteriovenous malformations. Rev Neurol (Paris) 162:1189–1203

    Article  CAS  Google Scholar 

  47. van Beijnum J, van der Worp HB, Buis DR, Al-Shahi Salman R, Kappelle LJ, Rinkel GJ, van der Sprenkel JW, Vandertop WP, Algra A, Klijn CJ (2011) Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA 306:2011–2019

    Article  PubMed  Google Scholar 

  48. Wilkins RH (1985) Natural history of intracranial vascular malformations: a review. Neurosurgery 16:421–430

    Article  CAS  PubMed  Google Scholar 

  49. Yamada S, Takagi Y, Nozaki K, Kikuta K, Hashimoto N (2007) Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg 107:965–972

    Article  PubMed  Google Scholar 

  50. Yen CP, Varady P, Sheehan J, Steiner M, Steiner L (2007) Subtotal obliteration of cerebral arteriovenous malformations after gamma knife surgery. J Neurosurg 106:361–369

    Article  PubMed  Google Scholar 

  51. Young AM, Teo M, Martin SC, Phang I, Bhattacharya JJ, St George EJ (2015) The diagnosis and management of brain arteriovenous malformations in a single regional centre. World Neurosurg 84(6):1621–1628

  52. Zhao J, Yu T, Wang S, Zhao Y, Yang WY (2010) Surgical treatment of giant intracranial arteriovenous malformations. Neurosurgery 67:1359–1370 discussion 1370

    Article  PubMed  Google Scholar 

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Funding

The Finnish government provided financial support (Finnish government grant for academic health research #TYH2017235). First author (A.H.) was awarded a scholarship for his PhD program from C. Ehmrooth Fellowship (Fondation de Luxembourg). The sponsors had no role in the design or conduct of this research.

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Correspondence to Ahmad Hafez.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

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Comments

We have here a study from a renowned senior surgeon and an experienced group regarding early surgery approach to ruptured intracranial AVMs. The analysis is done on 59 patients culled from a total experience of 805 patients. It is a fractional sample of the overall group, but this is because careful steps were taken to ensure a complete dataset in analyzed patients. The data is instructive even though it is a small subset of the Helsinki AVM experience.

The raw data is impressive, no doubt because of the quality of this highly experienced team and center, and their ability to transfer patients quickly from throughout Finland. Mean time to surgery was 2 days. Complete excision at first surgery was achieved in 96% of patients. Mortality was 15%. Deep perforators, high Hunt-Hess grade before surgery (note that they have used Hunt and Hess grading for AVMs in the absence of a truly dedicated AVM hemorrhage acuity grading system), age over 40, hydrocephalus, amount of bleeding during surgery, and AVM-related aneurysms were associated with an increased likelihood of poor surgical outcomes. Importantly, neither time to surgery nor embolization before surgery were associated with significant differences in outcome.

This study impacts the practice of AVM surgery in several important ways. Unlike aneurysmal subarachnoid hemorrhage, in this series a policy of early AVM surgery is neither better nor worse than a policy of delayed surgery, except of course where life-threatening ICH and mass effect are present, and early surgery is thus mandated. The study also codifies that risk factors which AVM surgeons know intuitively to be negative predictors of outcome, like excessive bleeding, deep feeders, poor patient condition and the others outlined above, are validated by this analysis.

The only reservation about this paper is that of course this is a tiny subset of the extensive Helsinki experience. However, we can understand why they chose to do it this way, to obtain the best possible dataset, and we accept and recommend the article as a quality observation of many things, but especially that early AVM surgery is reasonable and can be associated with similar outcomes to delayed surgery if the team and facility is available and the surgeon elects this practice.

Christopher M. Loftus,

Philadelphia, PA, USA

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Hafez, A., Oulasvirta, E., Koroknay-Pál, P. et al. Timing of surgery for ruptured supratentorial arteriovenous malformations. Acta Neurochir 159, 2103–2112 (2017). https://doi.org/10.1007/s00701-017-3315-9

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  • DOI: https://doi.org/10.1007/s00701-017-3315-9

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