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A proposal for a new arteriovenous malformation grading scale for neuroendovascular procedures and literature review.

The Spetzler-Martin (S-M) (1) grading scale has been traditionally used to estimate the risk of surgical intervention in brain arteriovenous malformation (AVM) patients. It is simple, easily applicable and has been validated (1-2) showing its relationship to outcome for surgically treated patients. It has also helped in evaluation of results for other treatment techniques, yet its applicability has recently been questioned (3). Some studies have shown a relationship between outcome and AVM grade for combined treatments (4-7). Others have shown a trend of endovascular complications and grade, suggesting underlying association between the factors included in the classification and outcome (7-9). Others have shown no asso ciatio n whatso ever (3). A scale with improved applicability to endovascular procedures including anatomical, radiological and hemodynamic factors encountered during intervention needs to be developed. We propose a preliminary classification using factors already deemed as significant determinants of risk and outcome for endovascular AVM patients. The classification scheme proposed is similar to the S-M grading system since it is very practical in clinical use. This classification will be used in a follow-up retrospective study aimed at validation and modification (if required) of the included parameters.


A literature search was performed in several medical databases including Medline, the latter showing a total of 750 results using the keywords 'arteriovenous malformation', 'embolization' and 'outcome'. Emphasis was given to those articles dealing with brain AVMs and factors related to endovascular or combined treatment complications and outcome determination. Articles were reviewed and factors like age, sex, clinical presentation, S-M grade, AVM related aneurysms, presence of arteriovenous (AV) fistula, AVM size, number of pedicles, number of embolization procedures, eloquence of adjacent areas, deep venous drainage, en-passage vessels, deep perforator feeders, and liquid embolic agents like n-BCA and Onyx[TM] were analyzed in terms of relationship to outcome and complication risk. Those factors tested for statistical significance were tabulated. Special attention was given to those factors dealing with radiological anatomy and hemodynamics, since these would be ideal ones for inclusion in a classification scheme for neuroendovascular procedures.


From the search of 750 articles, emphasis was given to those dealing with cerebral AVM embolizations and factors determining outcome and complications. Scarcely over 10 articles were found. We mention those showing trends or statistically significant results for anatomical and hemodynamical AVM descriptors.

Table 1 shows a recompilation of the factors associated with complications and unfavorable outcomes for AVM embolization procedures. In the study by Ledezma et al. (7) a series of 168 patients who underwent combined treatment procedures were analyzed in terms of embolization related complications. Twenty seven complications, combining technical and clinical, were reported. Univariate and multivariate analyses revealed close association between outcome and periprocedural hemorrhage and S-M grades III-V. Statistical results are also shown in Table 1. All other factors including demographics, clinical presentation and several morphological variables like large size, eloquent location, embolization stages and number of vascular pedicles embolized failed to show association with outcome possibly related to the small number of complications. Kim et al. (8) performed a retrospective study of 153 patients evaluated for predictors of complications after embolization. The only factor found with significant correlation to outcome was the number of branches embolized, with more than three related to worse outcome (P=0.017). Only a trend was noted when S-M grade was correlated to outcome (P>0.103). In a prospective study of 233 patients in 545 endovascular procedures Hartmann et al. (3) found a borderline correlation with patient age and number of embolizations and a significant one in the absence ofpretreatment neurological deficit. None of the morphological AVM characteristics predicted complications. Gobin et al. (5) found and association between the S-M grade and complication rates in a series of 125 AVMs, most likely due to the association with underlying factors in the classification. Haw et al. (10) using a combined retrospective/prospective database of 306 patients who underwent 513 embolization procedures found close association between complication rate and nidus location near eloquent area, a pure fistula or fistulous component and venous penetration of the glue cast. The statistical results for these parameters along with their references are shown in Table 1.


Reports about morbidity and mortality among AVM embolization procedures have been wide (7), morbidity 1.451.9% and mortality 0-6%. Certainly this depends on the goal of the endovascular intervention either as curative, adjuvant or palliative, since there is a relationship between aggressiveness of treatment and subsequent risks of intervention (11).

The major complication of AVM embolization is acute hemorrhage. This may be related to post embolization venous occlusion or stagnation (12) or to hemodynamic changes with reperfusion of chronically underperfused areas and subsequent normal perfusion pressure breakthrough (13). The study by Ledezma et al. (7) shows a correlation between high AVM S-M grade and complications, yet this may be due to a more direct association to any of the included factors in the classification and not necessarily to the grade; in addition no correlation is noted per grade, only to the group of patients with grade III-V AVMs. Worse outcome associated to periprocedural hemorrhage has a logical correlation, and may also be related to the presence of fistulous components or venous occlusion. Kim et al. (8) showed no significant correlation of S-M grade with outcome, only a trend. Yet, this may be due to the low number of complications evaluated, and also variables included in the grading system were not independently analyzed. They also showed a relationship to the number of pedicles embolized. The latter is related to size, and is a parameter more directly associated with endovascular procedures (three or fewer branches embolized had fewer complications). In a study by Hartmann et al. (3) no significant association was noted between S-M grade and complications, even when analyzing each component of the classification. Gobin et al. (5) reported an association between outcome and S-M grade postembolization and preradiosurgical. The results are not evaluated for statistical significance, yet a trend is noted toward higher grade and worse outcome. This is most likely due to implied factors in the classification like eloquence of adjacent areas, larger diameter and increasing number of pedicles with its additive risk per feeder embolization or higher probability of en-passage vessels. Also the presence of deep venous drainage suggests deep arterial feeders which are riskier to embolize. Other authors have suggested that tortuosity of vessels and the presence of associated aneurysms may also increase risks of intervention (3, 9), yet no analysis was found.

There is a definitive correlation between venous drainage impairment and hemorrhagic complications (10, 12, 14-15). Deep venous drainage has been associated with worse outcome when AVMs are surgically approached (1-2). Yet, for endovascular procedures deep venous drainage is not necessarily associated with an increased risk of complications. The hemodynamic behavior of an AVM with every embolization is more important. With each embolization an increased load of pressure is displaced to other AVM weaker areas or to chronically underperfused brain areas that may be prone to normal perfusion pressure breakthrough, causing edema and possibly hemorrhage. This has been demonstrated clinically (10, 15) and theoretically (14). Haw et al. (10) showed a significant correlation between complication rates and nidus location near eloquent areas, a pure AV fistula or fistulous component, and venous penetration of the glue cast. The last two factors may be related, since a fistulous component in an AVM may make it more likely for embolization material to occlude the venous side prematurely increasing the risk for hemorrhage. Also use of other embolic materials like fiber or detachable coils as well as more concentrated liquid embolic agents would be required, the specific combination depending on the experience and preference of the endovascular neurosurgeon.

Taking into account all the factors included in Table 1, we developed a preliminary classification scheme similar to the S-M grading system, since it is simple and practical in clinical use. Factors deemed as significant determinants of outcome and complications during endovascular embolization of an AVM were accounted for and combined in Table 2, along with a point system similar to the S-M grading scale. This classification scheme will be used in a follow-up validation study with possible modification (if required) of the included parameters.


A classification system similar to the S-M grading scale for use in risk assessment and outcome stratification in brain AVM patients treated by endovascular techniques seems adequate and clinically feasible. A preliminary classification scheme seems feasible since there is evidence in the literature dealing with factors that have shown significant correlation with risk and outcome. Retrospective validation study on its applicability and predictive value is underway at our institution.


(1.) Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg 2008;108:186-193.

(2.) Hamilton MG, Spetzler RF. The prospective application of a grading system for arteriovenous malformations. Neurosurgery 1994;34:2-6.

(3.) Hartmann A, Pile-Spellman J, Stapf C, et al. Risk of endovascular treatment of brain arteriovenous malformations. Stroke 2002;33:1816-1820.

(4.) Deruty R, Pelissou-Guyotat I, Mottolese C, et al. Prognostic value of the Spetzler's grading system in a series of cerebral AVMs treated by a combined management. Acta Neurochir (Wien) 1994;131:169-175.

(5.) Gobin YP, Laurent A, Merienne L, et al. Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 1996;85:19-28.

(6.) Hartmann A, Mast H, Mohr JP, et al. Determinants of staged endovascular and surgical treatment outcome of brain arteriovenous malformations. Stroke 2005;36:2431-2435.

(7.) Ledezma CJ, Hoh BL, Carter BS, et al. Complications of cerebral arteriovenous malformation embolization: multivariate analysis of predictive factors. Neurosurgery 2006;58:602-11.

(8.) Kim LJ, Albuquerque FC, Spetzler RF, McDougall CG. Postembolization neurological deficits in cerebral arteriovenous malformations: stratification by arteriovenous malformation grade. Neurosurgery 2006;59:53-59.

(9.) Taylor CL, Dutton K, Rappard G, et al. Complications of preoperative embolization of cerebral arteriovenous malformations. J Neurosurg 2004;100:810-812.

(10.) Haw CS, terBrugge K, Willinsky R, Tomlinson G. Complications of embolization of arteriovenous malformations of the brain. J Neurosurg 2006;104:226-232.

(11.) Valavanis A, Yasargil MG. The endovascular treatment of brain arteriovenous malformations. Adv Tech Stand Neurosurg 1998;24:131-214.

(12.) Picard L, Da Costa E, Anxionnat R, et al. Acute spontaneous hemorrhage after embolization of brain arteriovenous malformation with N-butyl cyanoacrylate. J Neuroradiol 2001;28:147-165.

(13.) Spetzler RF, Wilson CB, Weinstein P, et al. Normal perfusion pressure breakthrough theory. Clin Neurosurg 1978;25:651-672.

(14.) Hademenos GJ, Massoud TF. Risk of intracranial arteriovenous malformation rupture due to venous drainage impairment. A theoretical analysis. Stroke 1996;27:1072-1083.

(15.) Hollerhage HG. Venous drainage system and risk of hemorrhage from AVM's. J Neurosurg 1992;77:652-654.

Caleb E. Feliciano, MD; Ramon de Leon-Berra, MD; Manuel S. Hernandez-Gaitan, MD; Rafael Rodriguez-Mercado, MD, FACS

Department of Surgery, Section of Neurological Surgery Neuroendovascular Surgery Program

The authors have no conflicts of interest to disclose. No funding was used for this study.

Address correspondence to: Caleb Feliciano, MD, University of Puerto Rico, Medical Sciences Campus, PO Box 365067, San Juan, Puerto Rico 00936-5067. Tel: (787) 754-0101 xt. 4195 * Fax: (787) 294-3627 * Email:
Table 1. Factors associated with complications and unfavorable
outcomes for AVM embolization procedures.

Factor                       Reference         Statistical Weight

S-M (a) grade IIII-V         Ledezma et al.    OR 10.6 (b), P<0.05 (c)
Periprocedural hemorrage     Ledezma et al.    OR 17 (b), P<0.0001 (c)
Deep venous drainage         Ledezma et al.    P<0.05 (c)
Number of branches           Kim et at.        P=0.017 (c)
S-M (a) grade                Gobin et al.      N/A (d)
Increasing age               Hartmann et al.   OR 1.04 (b), P=0.021
                                               & OR 5.59 (c)
Number of embolizations      Hartmann et al.   OR 1.41 (b)
Absence of neurological      Hartmann et al.   OR 4.55 (b)
Presentation with            Hartmann et al.   P=0.017 & OR 9.59 (c)
Small AVM (a) size           Hartmann et al.   P=0.005 & OR 5.30 (c)
Presence of deep feeders     Hartmann et al.   P=0.021 & OR 6.60 (c)
Location in eloquent area    Haw et al.        P=0.039 & OR 2.48 (b)
Presence of AVa fistula      Haw et al.        P=0.0056 & OR 2.29 (b)
Venous penetration of glue   Haw et al.        P=0.0012 & OR 2.65 (b)

(a.) S-M=Spetzler-Martin, AVM=arteriovenous malformation,

(b.) multivariate analysis

(c.) univariate analysis

(d.) no test for significance

Table 2. Classification scheme for risk assessment during embolization
procedures for brain AVMs.

AVMa feature                                                 Points

Number of feeding vessels     <3                               1
                              3-5                              2
                              [greater than or equal to] 6     3
Eloquence of adjacent areas   Non-eloquent                     0
                              Eloquent                         1
Presence of AVa fistula(e)    No AVFa                          0
                              AVFa                             1

(a.) AVM=arteriovenous malformation, AV=arteriovenous,
AVF=arteriovenous fistula or fistulous component
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Title Annotation:SPECIAL ARTICLE
Author:Feliciano, Caleb E.; de Leon-Berra, Ramon; Hernandez-Gaitan, Manuel S.; Rodriguez-Mercado, Rafael
Publication:Puerto Rico Health Sciences Journal
Article Type:Perspectiva general de la enferm
Date:Jun 1, 2010
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