*3. Characterization of the diagnosis scores and scales

3.1. Spetzler-Martin Grading System (1986) [95]

The Spetzler-Martin (SM) grading system [95] is a simple and practical scale used worldwide world wide to evaluate surgical risk. It is also very reproducible being useful for comparing different surgical series.

Although it was originally described to assess the risk associated with microsurgical AVM resection, and not for endovascular and radiosurgical risks, it helps in making decisions about all the therapeutic management as will be explained in the treatment.

This grading system is based on three parameters (Table 1) : AVM size, presence of deep venous drainage, and the eloquence of the location. The classification may vary from grade 1 to 5, and the higher the grade, the higher the risk of surgical treatment. A negative point is that there is a great heterogeneity of AVM with the same grade, mainly in the grade III, as discussed later.

3.2. Spetzler-Ponce Classification (2010) [96]

This classification is just a modification of the one described above, gathering AVMs of similar prognosis in three classes :
 Class A : corresponds to grades 1 and 2 of Spetzler-Martin (SM) grading ;
 Class B : corresponds to grades 3 of SM grading ;
 Class C : corresponds to grades 4 and 5 of SM grading.

3.3. Lawton sub-classification of grade III AVM of Spetzler-Martin [45]

Analyzing the grade III AVM, we may observe that inside this group there is a great heterogeneity of AVM anatomy, therapeutic possibilities and risks. The grade III, may be presented in four subtypes : S1V1E1, S2V1E0, S2V0E1, S3V0E0. (S : size, V : venous, E : Eloquent)

Lawton et al. [45] in 2003 described a consecutive series of 174 brain AVMs resected from 174 patients during a period of 4.8 years. The grade III was present in 76 AVMs (45.2%) with an overall risk for new deficit or death of 8%. He proposed a subdivision of the SM III :
 S1V1E1 (III -) : 35 (46.1%) small AVMs. New deficit or death : 2.9%
 S2V1E0 (III) : 14 (18.4%) medium/deep AVMs. New deficit or death : 7.1%
 S2V0E1 (III +) : 27 (35.5%) medium/eloquent AVMs. New deficit or death : 14.8%
 S3V0E0 (III*) : no case. Lawton et al. [45] believe that this subtype is extremely rare or may be a theoretical lesion ; because a nidus exceeding 6 cm in diameter or having a deep draining vein or involve eloquent brain tissue (changing its classification to SM IV).

There was no statistical significant difference between these groups probably because of the relative small number of patients.

3.4. Lawton Supplementary Grading Scale [47]

Lawton et al. [47] proposed a supplement to the SM grading system, and just like it, the supplementary grading system is a tool to assess the risk of AVM resection (Table 2).
Unlike the Spetzler-Martin score, the supplementary score can change with other treatments or with time. Example : after radiosurgery, an AVM can lose its diffuseness, it can rupture during the latency period, and a pediatric patient can transition to an adult patient.

Lawton et al. [47] found that using only the supplementary grading scale it had high predictive accuracy on its own (area under the ROC curve, 0.73 vs. 0.65 for the Spetzler-Martin grading system), and stratified surgical risk more evenly. Therefore, the supplementary grade can be considered separately, or it can be combined with the Spetzler-Martin grade. Patients with supplementary grades ≤3 or combined grades ≤6 stratify into low- or moderate-risk groups that predict acceptably low surgical morbidity.

3.5. Pollock-Flickinger radiosurgery-based grading system for arteriovenous malformations (2002) [84]

Pollock and Flickinger (PF) [84] in 2002 proposed a new grading system for predicting the outcome of patients with AVM submitted to radiosurgery. Because the Spetzler–Martin grade was created to predict microsurgery outcome and did not correlate with excellent patient outcomes (complete AVM obliteration without any new neurological deficit) (p = 0.13) in radiosurgery. [84]

The SM grading system is probably unreliable for radiosurgery and embolization because the complications of these types of treatment differ from those of surgery, and because deeper lesions are not as difficult to access with radiosurgery and embolization, as with microsurgery.

The PF grading system was based on the multivariate analysis of data obtained from 220 patients treated between 1987 and 1991 (Group 1) and tested on a separate set of 136 patients with AVMs treated between 1990 and 1996 (Group 2) at a different center. After this, they proposed the following equation to predict patient outcomes after AVM radiosurgery based on factors relevant to AVM radiosurgery rather than microsurgery :
AVM score = (0.1)(AVM volume in cm3) + (0.02)(patient age in years) + (0.3)(location of lesion)
 AVM volume : π/6 x width x length x height
 Location of lesion : frontal or temporal = 0 ; parietal, occipital, intraventricular, corpus callosum, cerebellar = 1 ; or basal ganglia, thalamic, or brainstem = 2.
The score interpretation was :
 Score of 1 or less : > 95% patients had an excellent outcome ;
 Score of 1.25 : > 80% patients had an excellent outcome ;
 Score of 1.5 : > 70% patients had an excellent outcome ;
 Score of 1.75 : > 60% patients had an excellent outcome ;
 Score of 2 : > 50% patients had an excellent outcome ;
 Score greater than 2 : < 40% patients had an excellent outcome.

Excellent patient outcome was defined as complete AVM obliteration without any new neurological deficit. One hundred twenty-one (55%) of 220 Group 1 patients had excellent outcomes. In addition, seventy-nine (58%) of 136 Group 2 patients had excellent outcomes.

The authors concluded that the system allows a more accurate prediction of outcomes from radiosurgery to guide choices between surgical and radiosurgical management for individual patients with AVMs.

Although, there are some important limitations highlighted by the authors :
 This system was created to predict patient outcomes after a single radiosurgery procedure.
 Complications after AVM radiosurgery may occur many years after angiographically verified obliteration. [41, 111] Hence, the final results of AVM radiosurgery may change with a longer follow up.
 The grading system was developed and tested at centers at which only the gamma knife is used to perform radiosurgery

3.6. Pollock-Flickinger modified radiosurgery-based grading system for arteriovenous malformations (2008) [85]

In 2008, Pollock-Flickinger proposed a simplification of their original grading system, using location as a two-tiered variable. They analyzed 220 patients who underwent AVM radiosurgery between 1987 and 1992 and 247 patients who underwent AVM radiosurgery between 1990 and 2001 at another center.

They proposed the following equation :
 AVM score = (0.1)(AVM volume in cm3) + (0.02)(patient age in years) + (0.5)(location of lesion)
 Location of lesion : frontal, temporal, parietal, occipital, intraventricular, corpus callosum, cerebellar = 0 (other location) ; basal ganglia, thalamus, brainstem = 1 (deep location).
The score interpretation was :
 Score ≤ 1 : 89% patients had an excellent outcome and 0% had a decline in Modified Rankin Scale ;
 Score of 1.01-1.50 : 70% patients had an excellent outcome and 13% had a decline in Modified Rankin Scale ;
 Score of 1.5-1.99 : 64% patients had an excellent outcome and 20% had a decline in Modified Rankin Scale ;
 Score ≥ 2 : 46% patients had an excellent outcome and 36% had a decline in Modified Rankin Scale ;

Excellent patient outcome was defined as complete AVM obliteration without any new neurological deficit.

They found no difference between the original and modified scale with regard to AVM obliteration without new neurological deficits (p = 0.53) or decline in Modified Rankin Scale (p = 0.56).

As the first PF grade, this new grade was developed at centers performing gamma knife radiosurgery, but it has also been demonstrated to work equally well with linear accelerator radiosurgery.[4, 49, 85, 114]