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A 3-Tier Classification of Cerebral Arteriovenous: Malformations
A 3-Tier Classification of Cerebral Arteriovenous: Malformations
A 3-Tier Classification of Cerebral Arteriovenous: Malformations
Clinical article
Robert F. Spetzler, M.D., and Francisco A. Ponce, M.D.
Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center,
Phoenix, Arizona
Object. The authors propose a 3-tier classification for cerebral arteriovenous malformations (AVMs). The clas-
sification is based on the original 5-tier Spetzler-Martin grading system, and reflects the treatment paradigm for these
lesions. The implications of this modification in the literature are explored.
Methods. Class A combines Grades I and II AVMs, Class B are Grade III AVMs, and Class C combines Grades
IV and V AVMs. Recommended management is surgery for Class A AVMs, multimodality treatment for Class B, and
observation for Class C, with exceptions to the latter including recurrent hemorrhages and progressive neurological
deficits. To evaluate whether combining grades is warranted from the perspective of surgical outcomes, the 3-tier
system was applied to 1476 patients from 7 surgical series in which results were stratified according to Spetzler-
Martin grades.
Results. Pairwise comparisons of individual Spetzler-Martin grades in the series analyzed showed the fewest
significant differences (p < 0.05) in outcomes between Grades I and II AVMs and between Grades IV and V AVMs.
In the pooled data analysis, significant differences in outcomes were found between all grades except IV and V (p =
0.38), and the lowest relative risks were found between Grades I and II (1.066) and between Grades IV and V (1.095).
Using the pooled data, the predictive accuracies for surgical outcomes of the 5-tier and 3-tier systems were equivalent
(receiver operating characteristic curve area 0.711 and 0.713, respectively).
Conclusions. Combining Grades I and II AVMs and combining Grades IV and V AVMs is justified in part be-
cause the differences in surgical results between these respective pairs are small. The proposed 3-tier classification of
AVMs offers simplification of the Spetzler-Martin system, provides a guide to treatment, and is predictive of outcome.
The revised classification not only simplifies treatment recommendations; by placing patients into 3 as opposed to 5
groups, statistical power is markedly increased for series comparisons. (DOI: 10.3171/2010.8.JNS10663)
T Methods
he Spetzler-Martin grading system31 was designed
as a tool to assist with the complexity surround-
ing surgical decision making for cerebral AVMs.7 Proposed 3-Tier Model
Since its introduction in 1986, this grading system has The proposed system consists of 3 classes of AVM
been frequently cited in the medical literature,25,26 and and is derived by combining Spetzler-Martin Grades I
other large surgical series have validated its use.2,7,9,11 Its and II AVMs into Class A and Grades IV and V lesions
popularity reflects both its simplicity and its predictive into Class C; Grade III AVMs become Class B (Fig. 1).
capabilities with respect to postoperative deficits.21 Each class of AVM corresponds to a separate treatment
The management of AVMs at the Barrow Neurologi- paradigm (Table 1).
cal Institute follows a treatment paradigm whereby Grades
I and II lesions are managed similarly, as are Grades IV Identification of Articles
and V.30 This study reflects our management strategy by
evaluating a 3-tier AVM classification and comparing We examined whether combining the grades as de-
this modification to the standard 5-tier Spetzler-Martin scribed is justified from the perspective of surgical out-
grading system. comes reported in the literature. The database Thomson’s
ISI Web of Science (accessed April 2010) was used to
identify 672 published works that have cited the Spet-
Abbreviations used in this paper: AVM = arteriovenous malfor- zler-Martin grading system.31 The types of documents
mation; mRS = modified Rankin Scale; ROC = receiver operating included 490 articles, 85 proceedings papers, 46 reviews,
characteristic; RR = relative risk. 20 editorial materials, 20 letters, 7 reprints, 2 notes, and
Fig. 1. Diagrammatic representation of the combinations of graded variables (size, eloquence, and venous drainage) for each
class of AVM. The Spetzler-Martin system assigns a score of 1 for small AVMs (< 3 cm), 2 for medium (3–6 cm), and 3 for large
(> 6 cm). The eloquence of adjacent brain is scored as either noneloquent (0) or eloquent (1). The venous drainage is scored
as superficial only (0) or including drainage to the deep cerebral veins (1). Scores for each feature are totaled to determine the
grade. In the system described in this article, Class A includes Spetzler-Martin Grades I and II; Class B includes Grade III; and
Class C includes Grades IV and V. Modified from Spetzler and Martin. (Modified with permission from Spetzler RF, Martin NA: A
proposed grading system for arteriovenous malformations. J Neurosurg 65:476–483, 1986.)
37 (26–49)
31 (25–37)
Combined
18 (15–22)
18 (15–22)
32 (27–38)
8 (6–10)
10 (7–13)
4 (2–7)
parisons were significantly different, the exception being
between Grades IV and V AVMs (p = 0.38). The lowest
RRs were between Grades I and II (RR 1.066, 95% CI
1.027–1.107) and between Grades IV and V (RR 1.095,
Lawton et al.
100 (37–100)
14 (10–20) 30 (21–40)
14 (10–20) 30 (21–40)
34 (24–47) 35 (21–53)
24 (18–33)
20 (14–26)
17 (21–45) 31 (17–49)
95% CI 0.895–1.340; not significant).
9 (3–20)
Stratification of outcomes reported in each series
5 (7–12)
Morgan
0.7 (0–3)
to determine whether differences were significant (Table
4). In the series reported by Davidson and Morgan,2 all
32 (20–46)
65 (46–81)
33 (6–80)
8 (0–38)
Late
76 (58–88)
32 (20–46)
32 (20–46)
29 (18–43)
36 (22–52)
23 (13–37)
38 (21–29)
3 (0–17)
0 (0–6)
1 (0–7)
64 (44–80)
25 (15–39)
57 (42–70)
57 (42–70)
21 (13–31)
57 (37–76)
3 (0–15)
0 (0–17)
0 (0–9)
Hamilton & Spetzler
Late‡
3 (0–15)
0 (0–17)
2.5 (0–14)
Early
the ROC area was 0.711 for the 5-tier system and 0.713
for the 3-tier system, suggesting that the predictive ac-
curacies of both systems were clinically useful18,29,32 and
equivalent.
38 (21–59)
21 (13–33)
8 (0–38)
12 (5–26)
3 (0–16)
4 (4–15)
0 (0–7)
0 (0–7)
Late
Discussion
Heros et al.
11 (4.5–24)
71 (50–86)
50 (38–62)
39 (26–54)
4 (4–15)
6 (1–20)
Early
29 (16–47)
31 (14–56)
16 (6–35)
16 (5–36)
5 (0–24)
0 (0–13)
2 (0–13)
3-tier
IV
III
C
V
A
B
II
I
TABLE 4: Summary of results from pairwise comparisons of individual tiers within the 5-tier and 3-tier systems from 7 surgical series*
Heros et al. Hamilton & Spetzler Schaller et al. Hartmann et al. Davidson
System Spetzler & Martin Early Late Early Late Early Late Early Late & Morgan Lawton et al. Total (+)
5-tier
I, II − − − − − − − − − − + 1
II, III − − − − − + + − − + − 3
III, IV − + + + + − − + + + − 7
IV, V − + + − − − − − − − − 2
I, III − − − − − + + − − + + 4
II, IV − + − + + + + + + + − 8
III, V − + + + − − − + − + − 5
I, IV + + − + − + + + + + + 9
II, V − + + + − + + − − + − 6
I, V + + − + − + + + − + + 8
3-tier
A, B − − − − − + + − − + − 3
B, C − + + + + − − + + + − 7
A, C + + + + + + + + + + − 10
* Pairwise comparisons were done using the Fisher exact test. A “+” indicates that differences in outcomes were significant (p < 0.05), and a “−” indicates
that differences were not significant (p ≥ 0.05). The column labeled “Total (+)” indicates the number of outcome sets (of 11 total) with significant differ-
ences for each pairwise comparison.
AVMs appear to be minimal. In pairwise analysis, only 1 differences within Grade III AVMs. The modification by
of 11 outcome sets demonstrated a significant difference de Oliveira et al.3 divides the grade into 2 subgroups: IIIA
between these 2 grades. Although the pooled analysis (large) and IIIB (small, in eloquent areas) and proposes
was significant, the RR associated with surgery in these embolization plus surgery for the former and radiosur-
grades was the smallest of the 10 pairwise comparisons. gery for the latter. The modification by Lawton17 suggests
In the 3-tier classification, Grades I and II AVMs are breaking this grade down into all 4 subgroups, and de-
combined as Class A.
The recommended management of Class A AVMs
is microsurgical resection. In the initial report from our TABLE 5: Analysis of pooled data*
institution, the incidence of deficits in this cohort was
2%.31 The subsequent prospective application of the sys- System p Value RR 95% CI
tem showed a 2.5% incidence of early deficits, and no late
5-tier
deficits.7 The recent study by Davidson and Morgan2 re-
ported a 0.7% risk of adverse surgery-related outcomes I, II 0.003 1.066 1.027–1.107
for Class A AVMs, further reinforcing the role of surgery II, III 0.0003 1.100 1.045–1.158
as first-line therapy. III, IV 0.0002 1.187 1.076–1.309
While the benefit of including endovascular embo- IV, V 0.38† 1.095 0.895–1.340
lization preoperatively in the management of Class A
I, III <0.0001 1.173 1.117–1.232
AVMs is under evaluation, procedural risk of this mo-
dality should be considered. A recent series of 47 AVMs II, IV <0.0001 1.305 1.189–1.433
treated preoperatively with Onyx included 25 patients III, V 0.0006 1.300 1.079–1.566
with Class A AVMs, of which 4 (16%) showed a decline I, IV <0.0001 1.392 1.270–1.525
in their mRS score after embolization.35 The potential II, V <0.0001 1.430 1.190–1.718
role of embolization as a curative single modality has also
I, V <0.0001 1.524 1.270–1.830
been suggested, although the risk profile appears to be
higher than with surgery.16,36 Although we do not believe 3-tier
that radiosurgery is indicated for this class of AVM, a re- A, B <0.0001 1.125 1.073–1.180
cent study reported an increased rate of hemorrhage af- B, C <0.0001 1.208 1.103–1.322
ter radiosurgery in low-grade compared with high-grade A, C <0.0001 1.358 1.251–1.475
AVMs.15
* Data consist of p values (according to the Fisher exact test) and RR,
Class B: Grade III AVMs with 95% CIs for pairwise comparisons (also according to the Fisher
A number of authors have suggested that the Spet- exact test) of each tier for both the 5-tier and 3-tier systems.
zler-Martin grading system be modified to emphasize the † Not significant.
Morgan,2 who caution that their surgical results for elo- Rankin scale score was coded as ‘new neurological deficit.’ New
quent Grades III, IV, and V AVMs are not generalizable neurological deficits were classified as ‘disabling’ when Rankin
because 14% of the patients evaluated who had similar scores were 3, 4, or 5 (for patients with preoperative Rankin scores
of 2 or worse, any score increase was classified as disabling.)”
lesions had been refused surgery due to its perceived dif-
ficulty. Considering the fact that we recommend complete Davidson and Morgan. 2 “Outcomes assessment was per-
treatment of Class C AVMs for only 5% of our patients,8 formed using the modified Rankin Scale (mRS) score, which was
selection bias may be partially responsible for the rela- allocated preoperatively at 6 weeks and 12 months of follow-up. A
tively few significant differences in surgical outcomes poor outcome was considered to be any patient with a 12-month
mRS score greater than 1. To differentiate between the neurologic
seen between grades in the 2 studies from our institu- effects of AVM presentation (hemorrhage, focal neurologic defi-
tion.7,31 The decision-making process profoundly affects cit) and the effects of treatment, adverse outcomes were attributed
the results of a surgical series and can account for the to one of the following factors at the 6-week clinical assessment:
differences in rates of morbidity and mortality among natural history, surgery, embolization, or focused irradiation. For
different studies.8 As treatment patterns trend toward a the purposes of this article, an adverse outcome due to surgery also
more conservative approach for Class C AVMs, subse- included patients who had an adverse outcome due to planned pre-
quent improvements in surgical outcomes may render dif- operative embolization… To account for the gradual improvement
in neurologic deficits, only those patients whose surgery-related
ferences more difficult to detect, making the combining deficits persisted at the 12-month assessment were declared to
of categories desirable. have had an adverse outcome due to surgery.”
Lawton et al.18 “Outcomes were analyzed in terms of change
Conclusions between preoperative and final postoperative mRS scores (mRS
We propose that the original 5-tier Spetzler-Martin final − mRS preoperative)… Improvement was defined as a change
in mRS score of less than or equal to 0 (improved or unchanged),
grading system be condensed to a 3-tier classification that and deterioration was defined as a change in mRS score of greater
reflects a treatment paradigm for these lesions. This sys- than 0 (worse or dead).”
tem serves as a guide for treatment and is not intended
to replace individual analysis of AVMs. The modifica- Disclosure
tion is easily applied to earlier studies that have used the
Spetzler-Martin grading system because the criteria are The authors report no conflict of interest concerning the mate-
the same. It retains the predictive accuracy of outcomes, rials or methods used in this study or the findings specified in this
as shown in both cohorts from our institution as well as paper.
in other large AVM series. In eliminating what are argu- Author contributions to the study and manuscript preparation
include the following. Acquisition of data: Ponce. Analysis and
ably 2 redundant tiers from the 5-tier system, the 3-tier interpretation of data: Ponce. Drafting the article: Ponce. Critically
system offers the advantage of simplification.30 The re- revising the article: Ponce. Reviewed final version of the manuscript
vised classification not only simplifies treatment recom- and approved it for submission: both authors. Administrative/techni-
mendations, but by placing patients into 3 as opposed to 5 cal/material support: Ponce. Study supervision: Spetzler.
groups, statistical power is markedly increased for series
comparisons. Acknowledgment
Appendix Kristina Kupanoff, Ph.D., provided assistance with statistical
analysis.
Description of Outcomes in Each Study
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