Does eloquence subtype influence outcome following arteriovenous malformation surgery?

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OBJECTIVE

Although numerous arteriovenous malformation (AVM) grading scales consider eloquence in risk assessment, none differentiate the types of eloquence. The purpose of this study was to determine if eloquence subtype affects clinical outcome.

METHODS

This is a retrospective review of a prospectively collected clinical database of brain AVMs treated with microsurgery in the period from 1997 to 2017. The only inclusion criterion for this study was the presence of eloquence as defined by the Spetzler-Martin grading scale. Eloquence was preoperatively categorized by radiologists. Poor outcome was defined as a modified Rankin Scale (mRS) score 3–6, and worsening clinical status was defined as an increase in the mRS score at follow-up. Logistic regression analyses were performed.

RESULTS

Two hundred forty-one patients (49.4% female; average age 33.9 years) with eloquent brain AVMs were included in this review. Of the AVMs (average size 2.7 cm), 54.4% presented with hemorrhage, 46.2% had deep venous drainage, and 17.0% were diffuse. The most common eloquence type was sensorimotor (46.1%), followed by visual (27.0%) and language (22.0%). Treatments included microsurgery alone (32.8%), microsurgery plus embolization (51.9%), microsurgery plus radiosurgery (7.9%), and all three modalities (7.5%). Motor mapping was used in 9% of sensorimotor AVM cases, and awake speech mapping was used in 13.2% of AVMs with language eloquence. Complications occurred in 24 patients (10%). At the last follow-up (average 24 months), 71.4% of the patients were unchanged or improved and 16.6% had a poor outcome. There was no statistically significant difference in the baseline patient and AVM characteristics among the different subtypes of eloquence. In a multivariate analysis, in comparison to visual eloquence, both sensorimotor (OR 7.4, p = 0.004) and language (OR 6.5, p = 0.015) eloquence were associated with poor outcomes. Additionally, older age (OR 1.31, p = 0.016) and larger AVM size (OR 1.37, p = 0.034) were associated with poor outcomes.

CONCLUSIONS

Unlike visual eloquence, sensorimotor and language eloquence were associated with worse clinical outcomes after the resection of eloquent AVMs. This nuance in AVM eloquence demands consideration before deciding on microsurgical intervention, especially when numerical grading systems produce a score near the borderline between operative and nonoperative management.

ABBREVIATIONS AVM = arteriovenous malformation; fMRI = functional MRI; LED = lesion-to-eloquence distance; mRS = modified Rankin Scale; MSI = magnetic source imaging; SM = Spetzler-Martin.

Article Information

Correspondence Michael T. Lawton: Barrow Neurological Institute, Phoenix, AZ. michael.lawton@barrowbrainandspine.com.

INCLUDE WHEN CITING Published online October 5, 2018; DOI: 10.3171/2018.4.JNS18403.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

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Figures

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    Images featuring examples of eloquence subtypes: sensorimotor (A), language (B), vision (C), corpus callosum (D), thalamic (E), deep cerebellar nuclei (F), and brainstem (G).

References

  • 1

    Banks JLMarotta CA: Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke 38:109110962007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Cockroft KMChang KELehman EBHarbaugh RE: AVM Management Equipoise Survey: physician opinions regarding the management of brain arteriovenous malformations. J Neurointerv Surg 6:7487532014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Du RKeyoung HMDowd CFYoung WLLawton MT: The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery 60:6386482007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Dumont TMKan PSnyder KVHopkins LNSiddiqui AHLevy EI: A proposed grading system for endovascular treatment of cerebral arteriovenous malformations: Buffalo score. Surg Neurol Int 6:32015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Feliciano CEde León-Berra RHernández-Gaitán MSRodríguez-Mercado R: A proposal for a new arteriovenous malformation grading scale for neuroendovascular procedures and literature review. P R Health Sci J 29:1171202010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Gabarrós AYoung WLMcDermott MWLawton MT: Language and motor mapping during resection of brain arteriovenous malformations: indications, feasibility, and utility. Neurosurgery 68:7447522011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Gross BADu R: Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:4374432013

  • 8

    Höllerhage HGDewenter KMDietz H: Grading of supratentorial arteriovenous malformations on the basis of multivariate analysis of prognostic factors. Acta Neurochir (Wien) 117:1291341992

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Hung ALYang WWestbroek EMGarzon-Muvdi TCaplan JMBraileanu M: Differences in functional outcome across subtypes with Spetzler-Martin grade II arteriovenous malformations. Neurosurgery 81:4414492017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Jiao YLin FWu JLi HChen XLi Z: Brain arteriovenous malformations located in premotor cortex: surgical outcomes and risk factors for postoperative neurologic deficits. World Neurosurg 105:4324402017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Jiao YLin FWu JLi HWang LJin Z: Lesion-to-eloquent fiber distance is a crucial risk factor in presurgical evaluation of arteriovenous malformations in the temporo-occipital junction. World Neurosurg 93:3553642016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Jiao YLin FWu JLi HWang LJin Z: A supplementary grading scale combining lesion-to-eloquence distance for predicting surgical outcomes of patients with brain arteriovenous malformations. J Neurosurg 128:5305402018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Kim HAbla AANelson JMcCulloch CEBervini DMorgan MK: Validation of the supplemented Spetzler-Martin grading system for brain arteriovenous malformations in a multicenter cohort of 1009 surgical patients. Neurosurgery 76:25332015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Lawton MT: Spetzler-Martin Grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery 52:7407492003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Lawton MTDu RTran MNAchrol ASMcCulloch CEJohnston SC: Effect of presenting hemorrhage on outcome after microsurgical resection of brain arteriovenous malformations. Neurosurgery 56:4854932005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Lawton MTKim HMcCulloch CEMikhak BYoung WL: A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery 66:7027132010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Lee LSitoh YYNg INg WH: Cortical reorganization of motor functional areas in cerebral arteriovenous malformations. J Clin Neurosci 20:6496532013

  • 18

    Lin FZhao BWu JWang LJin ZCao Y: Risk factors for worsened muscle strength after the surgical treatment of arteriovenous malformations of the eloquent motor area. J Neurosurg 125:2892982016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lopes DKMoftakhar RStraus DMunich SAChaus FKaszuba MC: Arteriovenous malformation embocure score: AVMES. J Neurointerv Surg 8:6856912016

  • 20

    Pandey PMarks MPHarraher CDWestbroek EMChang SDDo HM: Multimodality management of Spetzler-Martin Grade III arteriovenous malformations. J Neurosurg 116:127912882012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Pertuiset BAncri DKinuta YHaisa TBordi LLin C: Classification of supratentorial arteriovenous malformations. A score system for evaluation of operability and surgical strategy based on an analysis of 66 cases. Acta Neurochir (Wien) 110:6161991

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Pollock BEFlickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:2392432008

  • 23

    Pollock BEFlickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79852002

  • 24

    Sanchez-Mejia ROChennupati SKGupta NFullerton HYoung WLLawton MT: Superior outcomes in children compared with adults after microsurgical resection of brain arteriovenous malformations. J Neurosurg 105 (2 Suppl):82872006

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

  • 26

    Spetzler RFPonce FA: A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg 114:8428492011

  • 27

    Stapf CMast HSciacca RRChoi JHKhaw AVConnolly ES: Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66:135013552006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Starke RMYen CPDing DSheehan JP: A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg 119:9819872013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Vates GELawton MTWilson CBMcDermott MWHalbach VVRoberts TP: Magnetic source imaging demonstrates altered cortical distribution of function in patients with arteriovenous malformations. Neurosurgery 51:6146272002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Wegner REOysul KPollock BESirin SKondziolka DNiranjan A: A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79:114711502011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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