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Staged Surgical Resection of Brain Arteriovenous Malformations
Original Article
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Staged Surgical Resection of Brain Arteriovenous Malformations
S. Sussman1, Santosh E. Gummidipundi2, Arjun V. Pendharkar1, Ephraim W. Church1, Allen L. Ho1, Summer S. Han1,2, Gary K. Steinberg1
BACKGROUND: Staged treatment of brain arteriovenous malformations (AVMs) is sometimes necessary to minimize risks associated with sudden changes in cerebral hemodynamics. With the increasing availability and optimization of endovascular techniques, multiple surgical resections are rarely necessary, although, due to specific anatomic circumstances, some AVMs still require staged surgery. Here, we describe the largest reported series of staged surgical resections of brain AVMs.
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METHODS: This is a retrospective review of surgically resected AVMs at a single institution from 1998e2018. Patients who underwent ‡2 resections within 1 year were reviewed. Only those in whom initial resection was terminated with intention for further resection were included in analysis.
functional outcome (defined as modified Rankin Scale score £2) was achieved in 14 patients (70%). CONCLUSIONS: Staged surgical resection of large and complex AVMs can be performed with good outcomes in carefully selected patients.
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INTRODUCTION
RESULTS: Twenty patients underwent deliberately staged resection from 1998e2018. Average age at treatment was 36.2 years (SD 16.5 years). Eleven patients (55%) were female, and 12 (60%) had left-sided AVMs. Median SpetzlerMartin grade was 4 (interquartile range [IQR]: 3e4). Average AVM nidus diameter was 5.0 cm (SD 1.7 cm). Seven patients (35%) presented with AVM rupture, and 12 (60%) presented with focal neurologic deficits without hemorrhage. Seventeen patients (85%) underwent preoperative embolization, median number of embolizations was 3 (IQR: 2e4). Three patients (15%) underwent preoperative radiosurgery. Median number of days between surgeries was 28 (IQR: 8e41 days). Perioperative course was complicated by hemorrhage in 3 patients (15%); 1 required decompressive hemicraniectomy prior to the second stage of surgery. Good
erebral arteriovenous malformations (AVMs) present a unique clinical challenge, and treatment of these lesions is associated with significant risk of perioperative neurologic morbidity.1,2 In addition to the technical risks associated with AVM resection, significant changes in cerebral hemodynamics following treatment can lead to hemorrhagic complications, even following a technically successful resection. The risk of this so-called reperfusion hemorrhage is particularly relevant in the case of large, high-flow AVMs, due to the transition from chronic under-perfusion of peri-lesional tissue to sudden normalization of perfusion pressure after AVM resection.3 Staged treatment of AVMs may mitigate the risk of reperfusion hemorrhage by allowing for the gradual normalization of perfusion pressure to the peri-lesional brain tissue as the AVM nidus is obliterated in a stepwise fashion. Historically, staged surgical resection has been performed, often with suboptimal clinical outcomes.4 Over the past several decades, however, advances in endovascular techniques have allowed for the strategic and stepwise reduction of flow through an AVM nidus prior to definitive surgical resection.5-8 Such a multimodality treatment strategy has obviated the need for staged surgical resection in most cases.
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From the 1Department of Neurosurgery and Stanford Stroke Center, Stanford School of Medicine, Stanford, California, USA; and 2Division of Med/Quantitative Sciences Unit, Department of Medicine, Stanford School of Medicine, Palo Alto, California, USA
Key words Arteriovenous malformation - Microsurgery - Staged resection -
To whom correspondence should be addressed: Gary K. Steinberg, M.D., Ph.D. [E-mail: [email protected]]
Abbreviations and Acronyms AVM: Arteriovenous malformation IQR: Interquartile range mRS: Modified Rankin Scale SD: Standard deviation SM: Spetzler-Martin
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Citation: World Neurosurg. (2020). https://doi.org/10.1016/j.wneu.2020.11.036 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2020 Elsevier Inc. All rights reserved.
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Still, in rare instances, as in the treatment of very large and high-flow AVMs, or when the vascular anatomy of a malformation precludes aggressive preoperative embolization, staged surgery may still be necessary in order to achieve safe and curative resection. Here, we report the largest series of deliberately staged microsurgical resection of AVMs. METHODS This was an institutional review boardeapproved retrospective review of a single surgeon’s prospectively maintained database of surgically resected cerebral AVMs. Informed consent was waived, per the institutional review board protocol. The database was queried to identify all patients who underwent 2 or more surgical resections within a 1-year period of time, between 1998 and 2018. For each patient identified, preoperative and operative notes were reviewed to identify those patients in whom the initial resection was deliberately terminated with the intention of returning for further surgical resection at a later date. Demographic, clinical, and radiographic data were reviewed in detail for each patient who underwent intentionally staged AVM resection. This included review of perioperative inpatient records, as well as all documentation during the period of time between the stages of surgical resection. Any additional treatments performed on the index lesion, either preoperatively or postoperatively, were also recorded. Clinical outcome was assessed using the modified Rankin Scale (mRS) score, which was recorded at the time of discharge after the first stage of surgery, at the time of discharge after the second stage of surgery, and at the last available followup. The primary clinical outcome measures were hemorrhage during the interoperative period and change in mRS from baseline to last available follow-up. Statistical analyses were performed using R version 3.5.3 (https://www.R-project.org; R Foundation for Statistical Computing, Vienna, Austria). Descriptive statistics for variables of interest include the frequency and proportion for categorical variables, mean and standard deviation (SD) for continuous variables, and when applicable, median and interquartile range (IQR). Linear regression models were used to model effect of factors on continuous outcomes. Logistic regression models were used to model effect of factors on binary outcomes.
Table 1. Patient Cohort Characteristics Characteristic Demographics Age at diagnosis, years
34.0 (17.7)
Age at treatment, years
36.2 (16.5)
Sex, female
11 (55%)
AVM characteristics Spetzler-Martin grade
0 (0%)
2
3 (15%)
3
6 (30%)
4
9 (45%)
5
2 (10%)
Size, cm
5.0 (1.7)
Drainage, deep
6 (30%)
Eloquence, yes
11 (55%)
Side, left
12 (60%)
Location, hemispheric only
17 (85%)
Location, basal ganglia/thalamus
1 (5%)
Location, cerebellum
2 (10%)
Clinical presentation Baseline mRS score
1 (1e1)
Preoperative seizure
5 (25%)
Ruptured presentation
5 (25%)
Rupture prior to treatment
7 (35%)
Preoperative therapies Preoperative embolization
17 (85%)
Number of preoperative embolizations
3 (2e4)
Preoperative radiosurgery
3 (15%)
Operative details
Number of days between surgeries
The data regarding patient demographics, AVM characteristics, clinical presentation, treatment details, and clinical follow-up are presented in Table 1. Between 1998 and 2018, 907 patients with intracranial AVMs were treated at Stanford Medicine (Stanford Health Care and Stanford Children’s Health, Stanford, CA). Twenty patients (2.2%) underwent deliberately staged surgical resection of cerebral AVMs during this period. The average age at treatment was 36.2 years (SD 16.5). Eleven patients (55%) were female. The AVM was on the left side in 12 patients (60%). The median Spetzler-Martin (SM) grade was 4 (IQR: 3e4). The average maximal diameter of the AVM nidus was 5.0 cm (SD 1.7). Seven patients (35%) presented with AVM rupture, and 12 patients (60%) presented with only focal neurologic deficits without radiographic evidence of hemorrhage. Two of the patients who
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4 (3e4)
1
Staging anticipated
RESULTS
Value
Hemorrhage between surgeries
8 (40%) 28 (8e41) 3 (15%)
Clinical follow-up mRS score at discharge after first stage
1 (1e2)
mRS score at discharge after second stage
2 (1e3.75)
mRS score at last follow-up
1.5 (1e3)
Change in mRS score from baseline to last follow-up
0 (0e1)
Values are presented as mean (SD), n (%), or median (IQR). mRS, modified Rankin Scale.
bled before treatment initially presented with focal neurologic deficits only. Among the patients who bled prior to treatment, the average number of clinically significant hemorrhagic events was
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Table 2. Univariate Regression Analyses for Change in mRS Score From Baseline to Last Available Follow-up Q6
Beta Coefficient
P Value
Age at diagnosis
0.02
0.11
Age at treatment
0.02
0.15
Sex, female
0.21
0.68
Demographics
Table 3. Univariate Regression Analyses for Hemorrhage Between Stages of Surgical Resection Beta Coefficient
P Value
Age at diagnosis
1.04
0.34
Age at treatment
1.04
0.42
Sex, female
0.56
0.66
Demographics
AVM characteristics
AVM characteristics
SM grade 1/2 (reference)
1
SM grade 3 SM grade 4/5 Size
SM grade 1/2 (reference)
0.17
0.81
SM grade 3
e0.80
0.22
SM grade 4/5
1 <0.0001
0.99
0.05
0.06
0.02
0.88
Size
0.84
0.69
Drainage, deep
e0.60
0.36
Drainage, deep
<0.0001
0.99
Eloquence, yes
1.33
0.001
Eloquence, yes
<0.0001
0.99
Side, left Location, hemispheric only
0.42
0.39
Side, left
3.67
0.33
e0.28
0.57
Location, hemispheric only
<0.0001
0.99
Location, basal ganglia/thalamus
<0.0001
0.99
0.97
0.21
Location, cerebellum
<0.0001
0.99
Location, basal ganglia/thalamus Location, cerebellum Clinical presentation
Clinical presentation
Baseline mRS score
e0.34
0.34
Baseline mRS score
0.50
0.56
Preoperative seizure
0.77
0.15
Preoperative seizure
9.33
0.11
Ruptured presentation
0.13
0.81
<0.0001
0.99
0.27
0.36
1.19
0.65
<0.0001
0.99
Preoperative therapies
Ruptured presentation Preoperative therapies
Preoperative embolization Number of preoperative embolizations Preoperative radiosurgery
0.35
0.59
Preoperative embolization
0.10
0.47
Number of preoperative embolizations
e0.80
0.17
Preoperative radiosurgery
Operative details
Operative details
Staging anticipated Number of days between surgeries
0.31
0.55
Staging anticipated
0.64
0.74
e0.01
0.16
Number of days between surgeries
0.94
0.24
1.7 (SD 0.9). One patient (5%) presented with an incidentally diagnosed AVM detected on magnetic resonance imaging performed as part of a research study. Seventeen patients (85%) underwent embolization prior to staged resection, with a median of 3 (IQR: 2e4) embolizations performed. In all three patients who did not undergo preoperative embolization prior to resection, embolization was deemed to be prohibitively dangerous in the context of short feeding artery branch pedicles arising from proximally located large cerebral vessels. Three patients (15%) underwent preoperative radiosurgery. Staged surgical resection was planned prior to undertaking the first resection in 8 patients (40%) based on the size and degree of arteriovenous shunting on preoperative angiogram, and the degree of preoperative embolization that was achieved. The most common rationale for staging the surgical resection was to allow for the normalization of cerebral hemodynamics in the setting of angiomatous vascular changes and
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refractory intraoperative bleeding from deep white matter feeders. The median number of days between surgeries was 28 (IQR: 8-41 days). Perioperative course was complicated by hemorrhage in 3 patients (15%), and 1 required decompressive hemicraniectomy prior to the second stage of surgical resection. Perioperative course was uncomplicated from a neurologic perspective in 17 patients (85%). The median mRS score at the time of initial presentation was 1 (IQR: 1e1). Among the 12 patients (60%) who were discharged after the first stage, but prior to the second stage of surgical resection, the median mRS score was 1 (1e2), and at the time of discharge following the second stage of surgery, median mRS score was 2 (1e3.75). At last available follow-up, at a median of 19.5 months (IQR: 10.5e67.5 months) after AVM resection, median mRS score was 1.5 (IQR: 1 3). The median change in mRS score from baseline to last available follow-up was 0 (IQR: 0e1). Fourteen patients (70%) had a good functional outcome (defined as mRS 2) at last available follow up.
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Figure 1. Angiographic images throughout the treatment course for one representative patient. Panel 1: Baseline imaging at the time of initial diagnosis, including anteroposterior (AP) and lateral angiographic runs of the left internal carotid (1A, 1B) and right vertebral (1C, 1D) arteries, as well as a fused left internal carotid artery and right vertebral artery 3-dimensional angiographic run (1E). These images demonstrate a large Spetzler-Martin grade 4 AVM supplied primarily by left lateral lenticulostriate arteries, anterior thalamoperforators, and posterior lateral and medial choroidal arteries, and deep venous drainage into the galenic system. Panel 2: Repeat imaging 7 years post-diagnosis, and status post four rounds of endovascular embolization and one course of CyberKnife radiosurgery. These AP and lateral angiographic runs of the left internal carotid (2A, 2B) and left vertebral (2C, 2D) arteries demonstrate modest interval decrease in the size of the AVM. A 3-dimensional reconstruction of the left internal carotid artery injection (2E) was also obtained after 1
The only patient who had a poor functional outcome (defined as mRS 4) at last available follow up suffered from AVM hemorrhage between stages of surgical resection. Of the 5 patients who had a mRS score of 3 at last available follow-up, 3 of these patients presented with mRS score of 3. Among the subset of patients in whom staged resection was anticipated prior to the first surgery (n ¼ 8; 40% of the full cohort),
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additional round of endovascular embolization. Panel 3: Repeat AP and lateral angiographic runs of the left internal carotid (3A, 3B) and right vertebral (3C, 3D) arteries, as well as a repeat 3-dimensional reconstruction of the left internal carotid artery injection (3E) after the first stage of planned staged surgical resection, in which approximately 30% of the AVM nidus was circumferentially dissected, demonstrates further interval modest decrease in the arterial supply to the AVM nidus, with significant residual filling of the AVM from left lateral lenticulostriate arteries, left middle cerebral artery branches, thalamoperforators, and posterior lateral and medial lenticulostriate arteries. Panel 4: Repeat AP and lateral angiographic runs of the left internal carotid (4A, 4B) and right vertebral (4C, 4D) arteries demonstrate complete angiographic cure, including no evidence of residual high-flow arteriovenous shunting or early venous opacification.
the median SM grade was 4 (IQR: 3e4), with a median nidus diameter of 5 cm (IQR: 4e6.6 cm), eloquent location in 4 of 8 (50%), and deep venous drainage in 6 of 8 (75%). Preoperative embolization was performed in 7 of 8 (88%), including a median of 4 treatments (IQR: 2.5e4), and preoperative radiosurgery was performed in 2 of 8 (25%). Median baseline mRS score in this subset of patients was 1 (IQR: 1e1.5), and median mRS score at last
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available follow-up was 2 (IQR: 1e3), for a median change of 0 (IQR: 0e1.5) between baseline and last available follow up. For comparison, among the subset of patients in whom staged resection was not anticipated prior to the first surgery (n ¼ 12; 60% of the full cohort), the median SM grade was also 4 (IQR: 3e4), with a median nidus diameter of 5 cm (IQR: 3.6e5 cm), eloquent location in 7 of 12 (58%), and deep venous drainage in 9 of 12 (75%). Preoperative embolization was performed in 10 of 12 (83%), including a median of 3 treatments (IQR: 2.75e4), and preoperative radiosurgery was performed in 3 of 12 (25%). Median baseline mRS score in this subset of patients was 1 (IQR: 1e1), and median mRS score at last available follow-up was 1 (IQR: 1e2), for a median change of 0 (IQR: 0e0.75) between baseline and last available follow-up. There were no significant differences between these patient subsets. Univariate regression analyses were performed in order to identify covariates predictive of a change in mRS from baseline to last available follow-up, or of hemorrhage between the 2 stages of surgery. Eloquent location of the lesion was the only variable found to be associated with a change in mRS score from baseline to last available follow up (beta coefficient 1.333, P ¼ 0.001; Table 2). There were no variables found to be predictive of hemorrhage between the 2 stages of surgical resection, although there was a nonsignificant trend towards higher rates of interoperative hemorrhage in patients with higher-grade (SM grade 4 and 5) AVMs (Table 3).
surgery, embolization, and radiosurgery.14 A similar approach was adopted for the patients in this series, with 85% of patients having undergone preoperative embolization and/or radiosurgery, and only 15% of patients treated with microsurgical resection alone. A representative case is demonstrated in Figure 1. It is important to note that staged microsurgical resection of AVMs is not the preferred surgical strategy. The decision to halt the initial surgery in favor of returning at a later date for completion of surgical resection is typically made intraoperatively, when persistent, refractory bleeding from the deep white matter feeders is encountered, or new peri-AVM brain parenchyma that was previously noted to have complete hemostasis begins bleeding. Anecdotally, this is often preceded by return of large pulsations to the peri-lesional tissue, and likely represents an inflection point in the surgical resection when the arterial supply to the AVM is disrupted to the point that normal perfusion returns to the surrounding brain. For particularly large and high-flow lesions, and in those for which thorough preoperative embolization is not possible, the need for staged surgery may be anticipated preoperatively, as in 40% of the cases in this series. However, in the majority of cases, the decision to stage the microsurgical resection must be made intraoperatively, based on subtle intraoperative findings and the intuition of the operating surgeon. CONCLUSIONS
DISCUSSION Much of the existing literature regarding staged surgical resection of cerebral AVMs dates back to the late 1980s and 1990s,4,9-12 and, as described above, the early experience with staged surgical resection was largely unfavorable. In the interim since the publication of these early experiences, preoperative embolization of cerebral AVMs has become common practice, and thus staged resection is rarely necessary in modern neurosurgical practice. Nonetheless, a small subset of AVMs still requires staged surgery in order to achieve safe and curative resection. In this paper, we describe the largest series of staged surgical AVM resections reported to date. This series consists almost entirely of patients with large, highgrade symptomatic AVMs. In the existing literature, the rate of new neurologic morbidity following surgical resection of similarly high-grade lesions is approximately 15% to 50%.1,2,13 It is remarkable, therefore, that good functional outcome, defined as mRS score 2, was achieved in 70% of the patients in this series. Further, of the patients who had mRS score 3 at the last available follow up, half of these patients presented initially with mRS score ¼ 3. Our group has previously reported excellent outcomes in patients with giant intracranial AVMs using a multi-modality approach consisting of a combination of
REFERENCES 1. Davidson AS, Morgan MK. How safe is arteriovenous malformation surgery? A prospective, observational study of surgery as first-line treatment for brain arteriovenous malformations. Neurosurgery. 2010;66:498-504.
Staged surgical resection is sometimes necessary to achieve curative resection of large, high-flow AVMs. High-grade AVMs and those located in eloquent tissue may be associated with new functional deficits and increased risk of perioperative hemorrhage, respectively. However, in carefully selected patients, staged AVM resection can be safely accomplished for the majority of cases. CRediT AUTHORSHIP CONTRIBUTION STATEMENT Eric S. Sussman: Conceptualization, Methodology, Writing original draft, Writing - review & editing. Santosh E. Gummidipundi: Formal analysis, Writing - review & editing. Arjun V. Pendharkar: Writing - review & editing. Ephraim W. Church: Methodology, Writing - review & editing. Allen L. Ho: Writing review & editing. Summer S. Han: Methodology, Formal analysis, Writing - review & editing. Gary K. Steinberg: Conceptualization, Resources, Writing - review & editing, Supervision, Funding acquisition. ACKNOWLEDGMENTS The authors would like to thank Christine Plant for editorial Q 5 support.
2. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476-483.
4. Morgan MK, Sundt TM. The case against staged operative resection of cerebral arteriovenous malformations. Neurosurgery. 1989;25:429-435.
3. Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D. Normal perfusion pressure breakthrough theory. Clin Neurosurg. 1978;25: 651-672.
5. Spetzler RF, Zabramski JM. Grading and staged resection of cerebral arteriovenous malformations. Clin Neurosurg. 1990;36:318-337.
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6. Loh Y, Duckwiler GR, Onyx Trial Investigators. A prospective, multicenter, randomized trial of the Onyx liquid embolic system and N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations. Clinical article. J Neurosurg. 2010;113:733-741. 7. N-BCA Trail Investigators. N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations: results of a prospective, randomized, multi-center trial. AJNR Am J Neuroradiol. 2002;23: 748-755. 8. Frizzel RT, Fisher WS. Cure, morbidity, and mortality associated with embolization of brain arteriovenous malformations: a review of 1246 patients in 32 series over a 35-year period. Neurosurgery. 1995;37:1031-1039. 9. Andrews BT, Wilson CB. Staged treatment of arteriovenous malformations of the brain. Neurosurgery. 1987;21:314-323.
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10. Kader A, Young WL, Massaro AR, et al. Transcranial Doppler changes during staged surgical resection of cerebral arteriovenous malformations: a report of three cases. Surg Neurol. 1993;39: 392-398.
14. Chang SD, Marcellus ML, Marks MP, Levy RP, Do HM, Steinberg GK. Multimodality treatment of giant intracranial arteriovenous malformations. Neurosurgery. 2007;61:432-442.
11. Nishizawa S, Ryu H, Yokoyama T, Kitamura S, Uemura K. Intentionally staged operation for large and high-flow cerebral arteriovenous malformation. J Clin Neurosci. 1998;5:78-83.
Conflict of interest statement: This work was supported in part by funding from Bernard and Ronni Lacroute and the William Randolph Hearst Foundation.
12. Hongo K, Kobayashi S, Takemae T, Nakagawa H, Mabuchi S. Staged surgery for a large cerebral arteriovenous malformation to prevent the overload phenomenon. J Clin Neurosci. 1998;5:84-86.
Citation: World Neurosurg. (2020). https://doi.org/10.1016/j.wneu.2020.11.036
13. Kim H, Abla AA, Nelson J, et al. Validation of the supplemented Spetzler-Martin grading system for brain arteriovenous malformations in a multicenter cohort of 1009 surgical patients. Neurosurgery. 2015; 76:25-31.
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Received 26 September 2020; accepted 7 November 2020
Journal homepage: www.journals.elsevier.com/worldneurosurgery 1878-8750/$ - see front matter ª 2020 Elsevier Inc. All rights reserved.
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Staged Surgical Resection of Brain Arteriovenous Malformations
S. Sussman1, Santosh E. Gummidipundi2, Arjun V. Pendharkar1, Ephraim W. Church1, Allen L. Ho1, Summer S. Han1,2, Gary K. Steinberg1
BACKGROUND: Staged treatment of brain arteriovenous malformations (AVMs) is sometimes necessary to minimize risks associated with sudden changes in cerebral hemodynamics. With the increasing availability and optimization of endovascular techniques, multiple surgical resections are rarely necessary, although, due to specific anatomic circumstances, some AVMs still require staged surgery. Here, we describe the largest reported series of staged surgical resections of brain AVMs.
-
METHODS: This is a retrospective review of surgically resected AVMs at a single institution from 1998e2018. Patients who underwent ‡2 resections within 1 year were reviewed. Only those in whom initial resection was terminated with intention for further resection were included in analysis.
functional outcome (defined as modified Rankin Scale score £2) was achieved in 14 patients (70%). CONCLUSIONS: Staged surgical resection of large and complex AVMs can be performed with good outcomes in carefully selected patients.
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INTRODUCTION
RESULTS: Twenty patients underwent deliberately staged resection from 1998e2018. Average age at treatment was 36.2 years (SD 16.5 years). Eleven patients (55%) were female, and 12 (60%) had left-sided AVMs. Median SpetzlerMartin grade was 4 (interquartile range [IQR]: 3e4). Average AVM nidus diameter was 5.0 cm (SD 1.7 cm). Seven patients (35%) presented with AVM rupture, and 12 (60%) presented with focal neurologic deficits without hemorrhage. Seventeen patients (85%) underwent preoperative embolization, median number of embolizations was 3 (IQR: 2e4). Three patients (15%) underwent preoperative radiosurgery. Median number of days between surgeries was 28 (IQR: 8e41 days). Perioperative course was complicated by hemorrhage in 3 patients (15%); 1 required decompressive hemicraniectomy prior to the second stage of surgery. Good
erebral arteriovenous malformations (AVMs) present a unique clinical challenge, and treatment of these lesions is associated with significant risk of perioperative neurologic morbidity.1,2 In addition to the technical risks associated with AVM resection, significant changes in cerebral hemodynamics following treatment can lead to hemorrhagic complications, even following a technically successful resection. The risk of this so-called reperfusion hemorrhage is particularly relevant in the case of large, high-flow AVMs, due to the transition from chronic under-perfusion of peri-lesional tissue to sudden normalization of perfusion pressure after AVM resection.3 Staged treatment of AVMs may mitigate the risk of reperfusion hemorrhage by allowing for the gradual normalization of perfusion pressure to the peri-lesional brain tissue as the AVM nidus is obliterated in a stepwise fashion. Historically, staged surgical resection has been performed, often with suboptimal clinical outcomes.4 Over the past several decades, however, advances in endovascular techniques have allowed for the strategic and stepwise reduction of flow through an AVM nidus prior to definitive surgical resection.5-8 Such a multimodality treatment strategy has obviated the need for staged surgical resection in most cases.
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C
From the 1Department of Neurosurgery and Stanford Stroke Center, Stanford School of Medicine, Stanford, California, USA; and 2Division of Med/Quantitative Sciences Unit, Department of Medicine, Stanford School of Medicine, Palo Alto, California, USA
Key words Arteriovenous malformation - Microsurgery - Staged resection -
To whom correspondence should be addressed: Gary K. Steinberg, M.D., Ph.D. [E-mail: [email protected]]
Abbreviations and Acronyms AVM: Arteriovenous malformation IQR: Interquartile range mRS: Modified Rankin Scale SD: Standard deviation SM: Spetzler-Martin
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Citation: World Neurosurg. (2020). https://doi.org/10.1016/j.wneu.2020.11.036 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2020 Elsevier Inc. All rights reserved.
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Still, in rare instances, as in the treatment of very large and high-flow AVMs, or when the vascular anatomy of a malformation precludes aggressive preoperative embolization, staged surgery may still be necessary in order to achieve safe and curative resection. Here, we report the largest series of deliberately staged microsurgical resection of AVMs. METHODS This was an institutional review boardeapproved retrospective review of a single surgeon’s prospectively maintained database of surgically resected cerebral AVMs. Informed consent was waived, per the institutional review board protocol. The database was queried to identify all patients who underwent 2 or more surgical resections within a 1-year period of time, between 1998 and 2018. For each patient identified, preoperative and operative notes were reviewed to identify those patients in whom the initial resection was deliberately terminated with the intention of returning for further surgical resection at a later date. Demographic, clinical, and radiographic data were reviewed in detail for each patient who underwent intentionally staged AVM resection. This included review of perioperative inpatient records, as well as all documentation during the period of time between the stages of surgical resection. Any additional treatments performed on the index lesion, either preoperatively or postoperatively, were also recorded. Clinical outcome was assessed using the modified Rankin Scale (mRS) score, which was recorded at the time of discharge after the first stage of surgery, at the time of discharge after the second stage of surgery, and at the last available followup. The primary clinical outcome measures were hemorrhage during the interoperative period and change in mRS from baseline to last available follow-up. Statistical analyses were performed using R version 3.5.3 (https://www.R-project.org; R Foundation for Statistical Computing, Vienna, Austria). Descriptive statistics for variables of interest include the frequency and proportion for categorical variables, mean and standard deviation (SD) for continuous variables, and when applicable, median and interquartile range (IQR). Linear regression models were used to model effect of factors on continuous outcomes. Logistic regression models were used to model effect of factors on binary outcomes.
Table 1. Patient Cohort Characteristics Characteristic Demographics Age at diagnosis, years
34.0 (17.7)
Age at treatment, years
36.2 (16.5)
Sex, female
11 (55%)
AVM characteristics Spetzler-Martin grade
0 (0%)
2
3 (15%)
3
6 (30%)
4
9 (45%)
5
2 (10%)
Size, cm
5.0 (1.7)
Drainage, deep
6 (30%)
Eloquence, yes
11 (55%)
Side, left
12 (60%)
Location, hemispheric only
17 (85%)
Location, basal ganglia/thalamus
1 (5%)
Location, cerebellum
2 (10%)
Clinical presentation Baseline mRS score
1 (1e1)
Preoperative seizure
5 (25%)
Ruptured presentation
5 (25%)
Rupture prior to treatment
7 (35%)
Preoperative therapies Preoperative embolization
17 (85%)
Number of preoperative embolizations
3 (2e4)
Preoperative radiosurgery
3 (15%)
Operative details
Number of days between surgeries
The data regarding patient demographics, AVM characteristics, clinical presentation, treatment details, and clinical follow-up are presented in Table 1. Between 1998 and 2018, 907 patients with intracranial AVMs were treated at Stanford Medicine (Stanford Health Care and Stanford Children’s Health, Stanford, CA). Twenty patients (2.2%) underwent deliberately staged surgical resection of cerebral AVMs during this period. The average age at treatment was 36.2 years (SD 16.5). Eleven patients (55%) were female. The AVM was on the left side in 12 patients (60%). The median Spetzler-Martin (SM) grade was 4 (IQR: 3e4). The average maximal diameter of the AVM nidus was 5.0 cm (SD 1.7). Seven patients (35%) presented with AVM rupture, and 12 patients (60%) presented with only focal neurologic deficits without radiographic evidence of hemorrhage. Two of the patients who
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4 (3e4)
1
Staging anticipated
RESULTS
Value
Hemorrhage between surgeries
8 (40%) 28 (8e41) 3 (15%)
Clinical follow-up mRS score at discharge after first stage
1 (1e2)
mRS score at discharge after second stage
2 (1e3.75)
mRS score at last follow-up
1.5 (1e3)
Change in mRS score from baseline to last follow-up
0 (0e1)
Values are presented as mean (SD), n (%), or median (IQR). mRS, modified Rankin Scale.
bled before treatment initially presented with focal neurologic deficits only. Among the patients who bled prior to treatment, the average number of clinically significant hemorrhagic events was
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Table 2. Univariate Regression Analyses for Change in mRS Score From Baseline to Last Available Follow-up Q6
Beta Coefficient
P Value
Age at diagnosis
0.02
0.11
Age at treatment
0.02
0.15
Sex, female
0.21
0.68
Demographics
Table 3. Univariate Regression Analyses for Hemorrhage Between Stages of Surgical Resection Beta Coefficient
P Value
Age at diagnosis
1.04
0.34
Age at treatment
1.04
0.42
Sex, female
0.56
0.66
Demographics
AVM characteristics
AVM characteristics
SM grade 1/2 (reference)
1
SM grade 3 SM grade 4/5 Size
SM grade 1/2 (reference)
0.17
0.81
SM grade 3
e0.80
0.22
SM grade 4/5
1 <0.0001
0.99
0.05
0.06
0.02
0.88
Size
0.84
0.69
Drainage, deep
e0.60
0.36
Drainage, deep
<0.0001
0.99
Eloquence, yes
1.33
0.001
Eloquence, yes
<0.0001
0.99
Side, left Location, hemispheric only
0.42
0.39
Side, left
3.67
0.33
e0.28
0.57
Location, hemispheric only
<0.0001
0.99
Location, basal ganglia/thalamus
<0.0001
0.99
0.97
0.21
Location, cerebellum
<0.0001
0.99
Location, basal ganglia/thalamus Location, cerebellum Clinical presentation
Clinical presentation
Baseline mRS score
e0.34
0.34
Baseline mRS score
0.50
0.56
Preoperative seizure
0.77
0.15
Preoperative seizure
9.33
0.11
Ruptured presentation
0.13
0.81
<0.0001
0.99
0.27
0.36
1.19
0.65
<0.0001
0.99
Preoperative therapies
Ruptured presentation Preoperative therapies
Preoperative embolization Number of preoperative embolizations Preoperative radiosurgery
0.35
0.59
Preoperative embolization
0.10
0.47
Number of preoperative embolizations
e0.80
0.17
Preoperative radiosurgery
Operative details
Operative details
Staging anticipated Number of days between surgeries
0.31
0.55
Staging anticipated
0.64
0.74
e0.01
0.16
Number of days between surgeries
0.94
0.24
1.7 (SD 0.9). One patient (5%) presented with an incidentally diagnosed AVM detected on magnetic resonance imaging performed as part of a research study. Seventeen patients (85%) underwent embolization prior to staged resection, with a median of 3 (IQR: 2e4) embolizations performed. In all three patients who did not undergo preoperative embolization prior to resection, embolization was deemed to be prohibitively dangerous in the context of short feeding artery branch pedicles arising from proximally located large cerebral vessels. Three patients (15%) underwent preoperative radiosurgery. Staged surgical resection was planned prior to undertaking the first resection in 8 patients (40%) based on the size and degree of arteriovenous shunting on preoperative angiogram, and the degree of preoperative embolization that was achieved. The most common rationale for staging the surgical resection was to allow for the normalization of cerebral hemodynamics in the setting of angiomatous vascular changes and
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refractory intraoperative bleeding from deep white matter feeders. The median number of days between surgeries was 28 (IQR: 8-41 days). Perioperative course was complicated by hemorrhage in 3 patients (15%), and 1 required decompressive hemicraniectomy prior to the second stage of surgical resection. Perioperative course was uncomplicated from a neurologic perspective in 17 patients (85%). The median mRS score at the time of initial presentation was 1 (IQR: 1e1). Among the 12 patients (60%) who were discharged after the first stage, but prior to the second stage of surgical resection, the median mRS score was 1 (1e2), and at the time of discharge following the second stage of surgery, median mRS score was 2 (1e3.75). At last available follow-up, at a median of 19.5 months (IQR: 10.5e67.5 months) after AVM resection, median mRS score was 1.5 (IQR: 1 3). The median change in mRS score from baseline to last available follow-up was 0 (IQR: 0e1). Fourteen patients (70%) had a good functional outcome (defined as mRS 2) at last available follow up.
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Figure 1. Angiographic images throughout the treatment course for one representative patient. Panel 1: Baseline imaging at the time of initial diagnosis, including anteroposterior (AP) and lateral angiographic runs of the left internal carotid (1A, 1B) and right vertebral (1C, 1D) arteries, as well as a fused left internal carotid artery and right vertebral artery 3-dimensional angiographic run (1E). These images demonstrate a large Spetzler-Martin grade 4 AVM supplied primarily by left lateral lenticulostriate arteries, anterior thalamoperforators, and posterior lateral and medial choroidal arteries, and deep venous drainage into the galenic system. Panel 2: Repeat imaging 7 years post-diagnosis, and status post four rounds of endovascular embolization and one course of CyberKnife radiosurgery. These AP and lateral angiographic runs of the left internal carotid (2A, 2B) and left vertebral (2C, 2D) arteries demonstrate modest interval decrease in the size of the AVM. A 3-dimensional reconstruction of the left internal carotid artery injection (2E) was also obtained after 1
The only patient who had a poor functional outcome (defined as mRS 4) at last available follow up suffered from AVM hemorrhage between stages of surgical resection. Of the 5 patients who had a mRS score of 3 at last available follow-up, 3 of these patients presented with mRS score of 3. Among the subset of patients in whom staged resection was anticipated prior to the first surgery (n ¼ 8; 40% of the full cohort),
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additional round of endovascular embolization. Panel 3: Repeat AP and lateral angiographic runs of the left internal carotid (3A, 3B) and right vertebral (3C, 3D) arteries, as well as a repeat 3-dimensional reconstruction of the left internal carotid artery injection (3E) after the first stage of planned staged surgical resection, in which approximately 30% of the AVM nidus was circumferentially dissected, demonstrates further interval modest decrease in the arterial supply to the AVM nidus, with significant residual filling of the AVM from left lateral lenticulostriate arteries, left middle cerebral artery branches, thalamoperforators, and posterior lateral and medial lenticulostriate arteries. Panel 4: Repeat AP and lateral angiographic runs of the left internal carotid (4A, 4B) and right vertebral (4C, 4D) arteries demonstrate complete angiographic cure, including no evidence of residual high-flow arteriovenous shunting or early venous opacification.
the median SM grade was 4 (IQR: 3e4), with a median nidus diameter of 5 cm (IQR: 4e6.6 cm), eloquent location in 4 of 8 (50%), and deep venous drainage in 6 of 8 (75%). Preoperative embolization was performed in 7 of 8 (88%), including a median of 4 treatments (IQR: 2.5e4), and preoperative radiosurgery was performed in 2 of 8 (25%). Median baseline mRS score in this subset of patients was 1 (IQR: 1e1.5), and median mRS score at last
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available follow-up was 2 (IQR: 1e3), for a median change of 0 (IQR: 0e1.5) between baseline and last available follow up. For comparison, among the subset of patients in whom staged resection was not anticipated prior to the first surgery (n ¼ 12; 60% of the full cohort), the median SM grade was also 4 (IQR: 3e4), with a median nidus diameter of 5 cm (IQR: 3.6e5 cm), eloquent location in 7 of 12 (58%), and deep venous drainage in 9 of 12 (75%). Preoperative embolization was performed in 10 of 12 (83%), including a median of 3 treatments (IQR: 2.75e4), and preoperative radiosurgery was performed in 3 of 12 (25%). Median baseline mRS score in this subset of patients was 1 (IQR: 1e1), and median mRS score at last available follow-up was 1 (IQR: 1e2), for a median change of 0 (IQR: 0e0.75) between baseline and last available follow-up. There were no significant differences between these patient subsets. Univariate regression analyses were performed in order to identify covariates predictive of a change in mRS from baseline to last available follow-up, or of hemorrhage between the 2 stages of surgery. Eloquent location of the lesion was the only variable found to be associated with a change in mRS score from baseline to last available follow up (beta coefficient 1.333, P ¼ 0.001; Table 2). There were no variables found to be predictive of hemorrhage between the 2 stages of surgical resection, although there was a nonsignificant trend towards higher rates of interoperative hemorrhage in patients with higher-grade (SM grade 4 and 5) AVMs (Table 3).
surgery, embolization, and radiosurgery.14 A similar approach was adopted for the patients in this series, with 85% of patients having undergone preoperative embolization and/or radiosurgery, and only 15% of patients treated with microsurgical resection alone. A representative case is demonstrated in Figure 1. It is important to note that staged microsurgical resection of AVMs is not the preferred surgical strategy. The decision to halt the initial surgery in favor of returning at a later date for completion of surgical resection is typically made intraoperatively, when persistent, refractory bleeding from the deep white matter feeders is encountered, or new peri-AVM brain parenchyma that was previously noted to have complete hemostasis begins bleeding. Anecdotally, this is often preceded by return of large pulsations to the peri-lesional tissue, and likely represents an inflection point in the surgical resection when the arterial supply to the AVM is disrupted to the point that normal perfusion returns to the surrounding brain. For particularly large and high-flow lesions, and in those for which thorough preoperative embolization is not possible, the need for staged surgery may be anticipated preoperatively, as in 40% of the cases in this series. However, in the majority of cases, the decision to stage the microsurgical resection must be made intraoperatively, based on subtle intraoperative findings and the intuition of the operating surgeon. CONCLUSIONS
DISCUSSION Much of the existing literature regarding staged surgical resection of cerebral AVMs dates back to the late 1980s and 1990s,4,9-12 and, as described above, the early experience with staged surgical resection was largely unfavorable. In the interim since the publication of these early experiences, preoperative embolization of cerebral AVMs has become common practice, and thus staged resection is rarely necessary in modern neurosurgical practice. Nonetheless, a small subset of AVMs still requires staged surgery in order to achieve safe and curative resection. In this paper, we describe the largest series of staged surgical AVM resections reported to date. This series consists almost entirely of patients with large, highgrade symptomatic AVMs. In the existing literature, the rate of new neurologic morbidity following surgical resection of similarly high-grade lesions is approximately 15% to 50%.1,2,13 It is remarkable, therefore, that good functional outcome, defined as mRS score 2, was achieved in 70% of the patients in this series. Further, of the patients who had mRS score 3 at the last available follow up, half of these patients presented initially with mRS score ¼ 3. Our group has previously reported excellent outcomes in patients with giant intracranial AVMs using a multi-modality approach consisting of a combination of
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Staged surgical resection is sometimes necessary to achieve curative resection of large, high-flow AVMs. High-grade AVMs and those located in eloquent tissue may be associated with new functional deficits and increased risk of perioperative hemorrhage, respectively. However, in carefully selected patients, staged AVM resection can be safely accomplished for the majority of cases. CRediT AUTHORSHIP CONTRIBUTION STATEMENT Eric S. Sussman: Conceptualization, Methodology, Writing original draft, Writing - review & editing. Santosh E. Gummidipundi: Formal analysis, Writing - review & editing. Arjun V. Pendharkar: Writing - review & editing. Ephraim W. Church: Methodology, Writing - review & editing. Allen L. Ho: Writing review & editing. Summer S. Han: Methodology, Formal analysis, Writing - review & editing. Gary K. Steinberg: Conceptualization, Resources, Writing - review & editing, Supervision, Funding acquisition. ACKNOWLEDGMENTS The authors would like to thank Christine Plant for editorial Q 5 support.
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Conflict of interest statement: This work was supported in part by funding from Bernard and Ronni Lacroute and the William Randolph Hearst Foundation.
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Citation: World Neurosurg. (2020). https://doi.org/10.1016/j.wneu.2020.11.036
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Received 26 September 2020; accepted 7 November 2020
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