Perspectives Commentary on: Deep Arteriovenous Malformations in the Basal Ganglia, Thalamus, and Insula: Multimodality Management, Patient Selection, and Results by Potts et al. World Neurosurg 2014 http://dx.doi.org/10.1016/j.wneu.2014.03.033
H. Hunt Batjer, M.D. Professor and Chair Department of Neurological Surgery The University of Texas Southwestern
Management of Deep Arteriovenous Malformations Jonathan A. White and H. Hunt Batjer
T
his issue of WORLD NEUROSURGERY contains a welldocumented, observational study of a cohort of 97 patients with arteriovenous malformations (AVMs) of the thalamus, basal ganglia, or insula who were treated with multimodality therapy, including surgical resection, stereotactic radiosurgery, embolization, and observation. Patients in the cohort crossed over treatment arms when appropriate, and the authors use their outcome data to present their treatment algorithm for these difficult cases. Deep AVMS pose an especially difficult challenge. There is significant evidence that these lesions have a higher rupture rate then AVMs of the supratentorial cortical surface. Fleetwood et al. (2) published the Stanford experience in 2003. Patients who became symptomatic from a basal ganglia or thalamic AVM who were referred to their center were reviewed. Because many of these patients had been followed for a significant time period before referral, the authors were able to calculate the AVM rupture risk. With >500 patient-years of follow-up, 25 patients were found to have bled 49 times for a rupture risk of 9.8% per patient year. This risk is significantly higher than the 4% per year risk of rupture published by Ondra et al. (7) based on their thorough review of patients with AVMs at all locations in the stable Helsinki population in 1990 and the more recent estimate of 2.2% per year published by the international a randomised trial of unruptured brain arteriovenous malformations (ARUBA) investigators (6). The 9.8% risk is likely an overestimate. Patients referred to a regional center probably represent a higher risk group than patients followed generally, but nevertheless it seems likely that deep lesions do carry a higher rupture risk. Although it is probable that deep AVMs carry a higher hemorrhage risk, it is clear that these AVMs carry a higher treatment risk. Important risk factors for poor surgical outcome include eloquent
Key words Arteriovenous malformations - Basal ganglia - Radiosurgery - Surgery - Thalamus - Therapeutic embolization -
Abbreviations and Acronyms AVM: Arteriovenous malformation
WORLD NEUROSURGERY - [-]: ---, MONTH 2014
location, deep venous drainage, and arterial supply from perforating vessels (1, 10). AVMs of the basal ganglia and thalamus usually have all of these features. Insular AVMs are relatively rare, have fewer of these features, and are intermediate in surgical risk between noneloquent cortical AVMs and basal ganglia and thalamic lesions. Lesions in these deep locations are rarely >6 cm. Treatment risk is increased not only for open surgical resection but also for radiosurgery. In a retrospective review of 56 patients undergoing radiosurgery for basal ganglia, thalamic, or brainstem AVM conducted at a respected, high-volume center, only 43% of patients had AVM obliteration after a single treatment; this percentage increased to 57% after multiple treatments (9). In the study, excellent outcome was defined as total obliteration with no new neurologic deficit. This result was achieved in 48% of patients. The authors’ conclusions discuss the difficulty in treating deeply located AVMs, including the need to reduce total dose and the need to make hard choices about how much to include as nidus. Is there a way to predict accurately the risk of treating these deep AVMs? The most widely used classification system for AVMs of all locations is the Spetzler-Martin grading system. Familiar to almost everyone, this system gives points for size, eloquent location, and deep venous drainage. The assigned grade correlates well with surgical outcome (3). The problem here, as pointed out in the article by Potts et al., is that the Spetzler-Martin grading system distinguishes only between the sizes of deep AVMs because they all are in eloquent cortex and have deep venous drainage. Kim et al. (5) proposed a supplemental grading system designed to hold on to the deep-rooted Spetzler-Martin grading system while adding additional factors to enhance prediction of surgical outcome. Variables included in this supplemental system are age, hemorrhagic presentation, and diffuseness of the nidus.
Department of Neurological Surgery, The University of Texas Southwestern, Dallas, Texas, USA To whom correspondence should be addressed: H. Hunt Batjer, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.06.033
www.WORLDNEUROSURGERY.org
1
PERSPECTIVES
For deep AVMs, diffuseness is probably the major additional contributor here, particularly if one wants to limit the discussion to the characteristics of the AVM, rather than clinical variables. When assessing the surgical resectability of these deep lesions, the detailed anatomic variables are another consideration. Compactness of the nidus is an important factor, but not all eloquent brain is created equally. The insula is more forgiving than the basal ganglia. Even the thalamus itself has areas relatively more forgiving and relatively more dangerous, at least in terms of obviously detectable new neurologic deficit. More recently, grading systems have been developed to predict the efficacy and safety of radiosurgery for AVMs. As an early example, Karlsson et al. (4) focused mainly on obliteration rates of which size and dose were key variables. Later Pollock and Flickinger (8) turned toward predicting clinical outcome. Toward that end, they reviewed 220 patients with AVMs at all locations and in a multivariate analysis identified size, patient age, and AVM location as being significant predictors of radiosurgery outcome. Not surprisingly in this study, deep, eloquent location added significantly to the risk of negative outcome. More recently, Starke et al. (11) reviewed 1012 patients whose AVMs were treated with Gamma Knife to create the Virginia Radiosurgery AVM Scale. In this system, points were given for volume, eloquence, and history of previous hemorrhage. Increasing score correlated with an increased rate of poor outcome. Although none of these scales is designed specifically for deep AVMs, they each support the observation that deep AVMs treated radiosurgically have a higher complication rate and a lower obliteration rate. If these deep AVMs carry a more treacherous natural history but also carry a significantly higher risk of new neurologic deficit with attempted microsurgical or radiosurgical cure and when treated tend to have high residual AVM rates with higher rebleed risk after treatment compared with AVMs at other locations, what is the best way to approach these lesions? In their article, Potts et al. present a cogent discussion of this issue. In their article, they describe the management of 97 patients with AVMs located in the basal ganglia, thalamus, or insula. Presentation was with hemorrhage in 64% of patients, and seizure or focal deficit
REFERENCES 1. Du R, Keyoung HM, Dowd CF, Young WL, Lawton MT: The effects of diffuseness and deep perforating arterial supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery 60:638-648, 2007. 2. Fleetwood IG, Marcellus ML, Levy RP, Marks MP, Steinberg GK: Arteriovenous malformations of the basal ganglia and thalamus: natural history. J Neurosurg 98:747-750, 2003. 3. Hamilton MG, Spetzler RF: The prospective application of a grading system for arteriovenous malformations. Neurosurgery 34:2-7, 1994. 4. Karlsson B, Lindquest C, Steiner L: Prediction of obliteration after Gamma Knife surgery for cerebral arteriovenous malformations. Neurosurgery 40:425-431, 1997. 5. Kim H, Pourmohamad T, Westbroek EM, McCulloch CE, Lawton MT, Young WL: Evaluating
2
www.SCIENCEDIRECT.com
accounted for most of the remaining patients. Only 5% of these AVMs were incidental. The 2 main outcome variables reviewed were AVM obliteration rates and functional outcomes. Patients who had surgical treatment tended to be younger and to have AVMs located in the insula. They also tended to present with hemorrhage and to be in worse shape neurologically. AVMs were managed with surgical resection (42%), stereotactic radiosurgery (45%), or observation (13%). Presurgical embolization was used in 51% of patients. Surgical approach was transsylvian in 68% of cases, transcortical in 17%, and transcallosal in 17%. Complete obliteration after initial treatment was achieved in 71% of patients undergoing surgery and 23% of patients receiving radiosurgery. None of the observed AVMs disappeared. Approximately 20% of patients in the surgical group and 30% in the radiosurgery group underwent additional treatment with radiosurgery. In the radiosurgery group, complete obliteration was achieved, after multiple treatments, in 45% of patients. Overall, 82% of patients were improved or unchanged neurologically after treatment. In their discussion, Potts et al. give some sage advice about the management of these deep lesions. Small, compact AVMs in younger patients who present with hemorrhage, particularly lesions located in the insula, tend to favor surgery. Patients who are older, with more diffuse AVMs, particularly lesions located in the thalamus or basal ganglia, tend to favor radiosurgery or observation. There still remains considerable opportunity to improve treatments for these deep AVMs. Improvements in functional brain mapping and tractography and refinements in intraoperative navigation may help design safer corridors for the microsurgical treatment of deep AVMs. Continued advances in targeting software and the exploration of the benefits of staged stereotactic radiation may improve the obliteration rate and decrease the complication rates of stereotactic radiosurgery. In the meantime, careful selection of patients, outstanding training for surgeons, and critical reporting of results, as done by Potts et al., should help to decrease morbidity and improve efficacy.
performance of the Spetzler-Martin supplemented model in selecting patients with brain arteriovenous malformation for surgery. Stroke 43:2497-2499, 2012.
9. Pollock BE, Gorman DA, Brown PD: Radiosurgery for arteriovenous malformations of the basal ganglia, thalamus and brainstem. J Neurosurg 100:210-214, 2004.
6. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, Al-Shahi Salman R, Vicaut E, Young WL, Houdart E, Cordonnier C, Stefani MA, Hartmann A, von Kummer R, Biondi A, Berkefeld J, Klijn CJM, Harkness K, Libman R, Barreau X, Moskowitz AJinternational ARUBA investigators: Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383:614-621, 2014.
10. Spetzler RF, Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:476-483, 1986.
7. Ondra SL, Troupp H, George ED: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:387-391, 1990.
11. Starke RM, Yen C, Ding D, Sheehan J: A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg 119:981-987, 2013.
Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.06.033 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
8. Pollock BE, Flickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79-85, 2002.
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.06.033
H. Hunt Batjer, M.D. Professor and Chair Department of Neurological Surgery The University of Texas Southwestern
Management of Deep Arteriovenous Malformations Jonathan A. White and H. Hunt Batjer
T
his issue of WORLD NEUROSURGERY contains a welldocumented, observational study of a cohort of 97 patients with arteriovenous malformations (AVMs) of the thalamus, basal ganglia, or insula who were treated with multimodality therapy, including surgical resection, stereotactic radiosurgery, embolization, and observation. Patients in the cohort crossed over treatment arms when appropriate, and the authors use their outcome data to present their treatment algorithm for these difficult cases. Deep AVMS pose an especially difficult challenge. There is significant evidence that these lesions have a higher rupture rate then AVMs of the supratentorial cortical surface. Fleetwood et al. (2) published the Stanford experience in 2003. Patients who became symptomatic from a basal ganglia or thalamic AVM who were referred to their center were reviewed. Because many of these patients had been followed for a significant time period before referral, the authors were able to calculate the AVM rupture risk. With >500 patient-years of follow-up, 25 patients were found to have bled 49 times for a rupture risk of 9.8% per patient year. This risk is significantly higher than the 4% per year risk of rupture published by Ondra et al. (7) based on their thorough review of patients with AVMs at all locations in the stable Helsinki population in 1990 and the more recent estimate of 2.2% per year published by the international a randomised trial of unruptured brain arteriovenous malformations (ARUBA) investigators (6). The 9.8% risk is likely an overestimate. Patients referred to a regional center probably represent a higher risk group than patients followed generally, but nevertheless it seems likely that deep lesions do carry a higher rupture risk. Although it is probable that deep AVMs carry a higher hemorrhage risk, it is clear that these AVMs carry a higher treatment risk. Important risk factors for poor surgical outcome include eloquent
Key words Arteriovenous malformations - Basal ganglia - Radiosurgery - Surgery - Thalamus - Therapeutic embolization -
Abbreviations and Acronyms AVM: Arteriovenous malformation
WORLD NEUROSURGERY - [-]: ---, MONTH 2014
location, deep venous drainage, and arterial supply from perforating vessels (1, 10). AVMs of the basal ganglia and thalamus usually have all of these features. Insular AVMs are relatively rare, have fewer of these features, and are intermediate in surgical risk between noneloquent cortical AVMs and basal ganglia and thalamic lesions. Lesions in these deep locations are rarely >6 cm. Treatment risk is increased not only for open surgical resection but also for radiosurgery. In a retrospective review of 56 patients undergoing radiosurgery for basal ganglia, thalamic, or brainstem AVM conducted at a respected, high-volume center, only 43% of patients had AVM obliteration after a single treatment; this percentage increased to 57% after multiple treatments (9). In the study, excellent outcome was defined as total obliteration with no new neurologic deficit. This result was achieved in 48% of patients. The authors’ conclusions discuss the difficulty in treating deeply located AVMs, including the need to reduce total dose and the need to make hard choices about how much to include as nidus. Is there a way to predict accurately the risk of treating these deep AVMs? The most widely used classification system for AVMs of all locations is the Spetzler-Martin grading system. Familiar to almost everyone, this system gives points for size, eloquent location, and deep venous drainage. The assigned grade correlates well with surgical outcome (3). The problem here, as pointed out in the article by Potts et al., is that the Spetzler-Martin grading system distinguishes only between the sizes of deep AVMs because they all are in eloquent cortex and have deep venous drainage. Kim et al. (5) proposed a supplemental grading system designed to hold on to the deep-rooted Spetzler-Martin grading system while adding additional factors to enhance prediction of surgical outcome. Variables included in this supplemental system are age, hemorrhagic presentation, and diffuseness of the nidus.
Department of Neurological Surgery, The University of Texas Southwestern, Dallas, Texas, USA To whom correspondence should be addressed: H. Hunt Batjer, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.06.033
www.WORLDNEUROSURGERY.org
1
PERSPECTIVES
For deep AVMs, diffuseness is probably the major additional contributor here, particularly if one wants to limit the discussion to the characteristics of the AVM, rather than clinical variables. When assessing the surgical resectability of these deep lesions, the detailed anatomic variables are another consideration. Compactness of the nidus is an important factor, but not all eloquent brain is created equally. The insula is more forgiving than the basal ganglia. Even the thalamus itself has areas relatively more forgiving and relatively more dangerous, at least in terms of obviously detectable new neurologic deficit. More recently, grading systems have been developed to predict the efficacy and safety of radiosurgery for AVMs. As an early example, Karlsson et al. (4) focused mainly on obliteration rates of which size and dose were key variables. Later Pollock and Flickinger (8) turned toward predicting clinical outcome. Toward that end, they reviewed 220 patients with AVMs at all locations and in a multivariate analysis identified size, patient age, and AVM location as being significant predictors of radiosurgery outcome. Not surprisingly in this study, deep, eloquent location added significantly to the risk of negative outcome. More recently, Starke et al. (11) reviewed 1012 patients whose AVMs were treated with Gamma Knife to create the Virginia Radiosurgery AVM Scale. In this system, points were given for volume, eloquence, and history of previous hemorrhage. Increasing score correlated with an increased rate of poor outcome. Although none of these scales is designed specifically for deep AVMs, they each support the observation that deep AVMs treated radiosurgically have a higher complication rate and a lower obliteration rate. If these deep AVMs carry a more treacherous natural history but also carry a significantly higher risk of new neurologic deficit with attempted microsurgical or radiosurgical cure and when treated tend to have high residual AVM rates with higher rebleed risk after treatment compared with AVMs at other locations, what is the best way to approach these lesions? In their article, Potts et al. present a cogent discussion of this issue. In their article, they describe the management of 97 patients with AVMs located in the basal ganglia, thalamus, or insula. Presentation was with hemorrhage in 64% of patients, and seizure or focal deficit
REFERENCES 1. Du R, Keyoung HM, Dowd CF, Young WL, Lawton MT: The effects of diffuseness and deep perforating arterial supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery 60:638-648, 2007. 2. Fleetwood IG, Marcellus ML, Levy RP, Marks MP, Steinberg GK: Arteriovenous malformations of the basal ganglia and thalamus: natural history. J Neurosurg 98:747-750, 2003. 3. Hamilton MG, Spetzler RF: The prospective application of a grading system for arteriovenous malformations. Neurosurgery 34:2-7, 1994. 4. Karlsson B, Lindquest C, Steiner L: Prediction of obliteration after Gamma Knife surgery for cerebral arteriovenous malformations. Neurosurgery 40:425-431, 1997. 5. Kim H, Pourmohamad T, Westbroek EM, McCulloch CE, Lawton MT, Young WL: Evaluating
2
www.SCIENCEDIRECT.com
accounted for most of the remaining patients. Only 5% of these AVMs were incidental. The 2 main outcome variables reviewed were AVM obliteration rates and functional outcomes. Patients who had surgical treatment tended to be younger and to have AVMs located in the insula. They also tended to present with hemorrhage and to be in worse shape neurologically. AVMs were managed with surgical resection (42%), stereotactic radiosurgery (45%), or observation (13%). Presurgical embolization was used in 51% of patients. Surgical approach was transsylvian in 68% of cases, transcortical in 17%, and transcallosal in 17%. Complete obliteration after initial treatment was achieved in 71% of patients undergoing surgery and 23% of patients receiving radiosurgery. None of the observed AVMs disappeared. Approximately 20% of patients in the surgical group and 30% in the radiosurgery group underwent additional treatment with radiosurgery. In the radiosurgery group, complete obliteration was achieved, after multiple treatments, in 45% of patients. Overall, 82% of patients were improved or unchanged neurologically after treatment. In their discussion, Potts et al. give some sage advice about the management of these deep lesions. Small, compact AVMs in younger patients who present with hemorrhage, particularly lesions located in the insula, tend to favor surgery. Patients who are older, with more diffuse AVMs, particularly lesions located in the thalamus or basal ganglia, tend to favor radiosurgery or observation. There still remains considerable opportunity to improve treatments for these deep AVMs. Improvements in functional brain mapping and tractography and refinements in intraoperative navigation may help design safer corridors for the microsurgical treatment of deep AVMs. Continued advances in targeting software and the exploration of the benefits of staged stereotactic radiation may improve the obliteration rate and decrease the complication rates of stereotactic radiosurgery. In the meantime, careful selection of patients, outstanding training for surgeons, and critical reporting of results, as done by Potts et al., should help to decrease morbidity and improve efficacy.
performance of the Spetzler-Martin supplemented model in selecting patients with brain arteriovenous malformation for surgery. Stroke 43:2497-2499, 2012.
9. Pollock BE, Gorman DA, Brown PD: Radiosurgery for arteriovenous malformations of the basal ganglia, thalamus and brainstem. J Neurosurg 100:210-214, 2004.
6. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, Al-Shahi Salman R, Vicaut E, Young WL, Houdart E, Cordonnier C, Stefani MA, Hartmann A, von Kummer R, Biondi A, Berkefeld J, Klijn CJM, Harkness K, Libman R, Barreau X, Moskowitz AJinternational ARUBA investigators: Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383:614-621, 2014.
10. Spetzler RF, Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:476-483, 1986.
7. Ondra SL, Troupp H, George ED: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:387-391, 1990.
11. Starke RM, Yen C, Ding D, Sheehan J: A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg 119:981-987, 2013.
Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.06.033 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
8. Pollock BE, Flickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79-85, 2002.
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.06.033
