Letters to the Editor / Clinical Neurology and Neurosurgery 131 (2015) 86–91
aphasia in which there are deficits of written as well as spoken language. Interestingly, aphemia was first described by Broca [2] predating his description of the eponymous aphasia. Aphemia has been described in lesion to the left frontal operculum or left precentral gyrus. While aphemia certainly can be persistent [3], curiously, as in our case, that of Fox et al. [1] and another [4] aphemia can show significant recovery within days, while complete recovery of severe aphasia is seen in less than 10% of cases and then only after some weeks at the least [5]. This difference in recovery from the two deficits may warrant further study. Competing interests None. References [1] Fox RJ, Kasner SE, Chatterjee A, Chalela JA. Aphemia: an isolated disorder of articulation. Clin Neurol Neurosurg 2001;103:123–6. [2] Broca P. Remarques sur le siège de la faculté du langage articulé; suivies d’une observation d’aphémie (perte de la parole). Bull Soc Anat Paris 1861;36: 330–57. [3] Ojha PK, Nandavar S, Pearson DM, Demchuk AM. Aphemia as a presenting syndrome in acute stroke. Neurol India 2011;59:432–4. [4] Ottomeyer C, Reuter B, Jäger T, Rossmanith C, Hennerici MG, Szabo K. Aphemia: an isolated disorder of speech associated with an ischemic lesion of the left precentral gyrus. J Neurol 2009;256:1166–8. [5] Pedersen PM, Jorgensen HS, Nakayam H, Raaschou HO, Olsen TS. Aphasia in acute stroke: incidence, determinants, and recovery. Ann Neurol 1995;38:659–66.
Alexander J. Feng Kwame O. Asante Department of Physical Medicine and Rehabilitation, Temple University School of Medicine, Philadelphia, USA Camilo Guiterrez Department of Neurology, Temple University School of Medicine, Philadelphia, USA Eric L. Altschuler ∗ Department of Physical Medicine and Rehabilitation, Temple University School of Medicine, Philadelphia, USA ∗ Corresponding author at: Department of Physical Medicine and Rehabilitation, 3401 N. Broad Street, Philadelphia 19140, USA. Tel.: +1 215 707 7021; fax: +1 215 707 9168. E-mail address: [email protected] (E.L. Altschuler)
12 August 2014 Available online 22 January 2015 http://dx.doi.org/10.1016/j.clineuro.2014.12.025
87
emergency medical system or in the neurological intensive care unit. Antiepileptic treatment appropriate for the electrical and clinical pattern in the patient should be initiated at scene on an emergency basis. In addition to these symptomatic measures, the treatment strategy should include rigorous aetiological investigations for a cause to the status epilepticus, followed by etiological treatment. However, the existence of functional impairments in half the survivors of convulsive status epilepticus requiring ICU management [2] indicates a need for neuroprotective interventions. Therapeutic hypothermia has been reported to exert not only anticonvulsant but also neuroprotective effects [3] in studies of rats with self-sustaining status epilepticus. Hyperthermia between 39.5 ◦ C and 42 ◦ C promoted the occurrence of seizures and exacerbated local and hippocampal neuronal damage, whereas cooling to 32.5 ◦ C significantly decreased the occurrence of such damage. Hypothermia between 28 ◦ C and 31 ◦ C decreased the incidence of epileptic activity and associated neuronal lesions. After pre-treatment with mild hypothermia (32–34 ◦ C), the rats were protected from the onset of status epilepticus (increased latency to onset of seizures and time to onset of status epilepticus) and also had fewer apoptotic neurons in the hippocampus. Another study has shed light on the pathophysiological mechanisms involved in the neuroprotective effect of hypothermia. Moderate hypothermia (32–34 ◦ C) was associated with regulation of the expression of the GluR1 and GluR2 subunits of the AMPA glutamate receptors, an effect that decreased the number of necrotic or apoptotic hippocampal neurons. Furthermore, cerebral oedema induced by ongoing seizures was decreased by the use of therapeutic hypothermia immediately after status epilepticus induced by kainic acid. All these effects were potentiated by the concomitant administration of anticonvulsant benzodiazepine therapy. However, hypothermia was not effective to prevent epilepsy after status epilepticus. In humans, therapeutic hypothermia has been used as an adjuvant treatment in refractory epilepsy and during neurosurgery. Successful treatment with hypothermia has also been reported in paediatric patients with severely refractory status epilepticus. Finally, therapeutic hypothermia may also target some causes of status epilepticus such as ischaemic or haemorrhagic stroke, subarachnoid haemorrhage, and even traumatic brain injury [4]. Conversely, the use of therapeutic hypothermia in severe bacterial meningitis has been demonstrated to increase the risk of death [5]. In conclusion, whether therapeutic hypothermia is beneficial in humans with status epilepticus remains to be demonstrated. Pathophysiological considerations and experimental data suggest a role for therapeutic hypothermia. A French multicentre randomised study for which patient recruitment is ongoing can be expected to clarify this point (HYBERNATUS, NCT01359332). Until the results are available, all patients with status epilepticus may benefit from non-specific measures aimed at preventing secondary brain damage, including at least targeted temperature management. The use of therapeutic hypothermia must still be restricted to severely refractory status epilepticus, in the absence of contraindications. Financial support
Dual anticonvulsant and neuroprotective effects of therapeutic hypothermia after status epilepticus Sir, We read with a great interest the recent and innovative article by Bennett et al. [1]. Their report is original and at times thoughtprovoking, notably regarding the use of therapeutic hypothermia for super refractory status epilepticus. Patients with status epilepticus require the symptomatic measures usually taken in the emergency department, prehospital
We declare no financial support. Conflict of interest We declare no conflict of interest. References [1] Bennett AE, Hoesch RE, DeWitt LD, Afra P, Ansari SA. Therapeutic hypothermia for status epilepticus: a report, historical perspective, and review. Clin Neurol Neurosurg 2014;126:103–9.
88
Letters to the Editor / Clinical Neurology and Neurosurgery 131 (2015) 86–91
[2] Legriel S, Azoulay E, Resche-Rigon M, Lemiale V, Mourvillier B, Kouatchet A, et al. Functional outcome after convulsive status epilepticus. Crit Care Med 2010;38:2295–303. [3] Schmitt FC, Buchheim K, Meierkord H, Holtkamp M. Anticonvulsant properties of hypothermia in experimental status epilepticus. Neurobiol Dis 2006;23:689–96. [4] Polderman KH. Induced hypothermia and fever control for prevention and treatment of neurological injuries. Lancet 2008;371:1955–69. [5] Mourvillier B, Tubach F, van de Beek D, Garot D, Pichon N, Georges H, et al. Induced hypothermia in severe bacterial meningitis: a randomized clinical trial. JAMA 2013;310:2174–83.
Stéphane Legriel ∗ Intensive Care Unit, Hôpital de Versailles – Site André Mignot, 177 rue de Versailles, 78150 Le Chesnay Cedex, France Matthieu Resche-Rigon a,b,c SBIM, Biostatistics and Clinical Epidemiology Research Unit, Hôpital Saint-Louis, APHP, 1 Avenue Claude Vellefaux, Paris, France b Denis Diderot University – Paris 7, Paris, France c ECSTRA Team, UMR 1153 Inserm, Paris, France a
Alain Cariou a,b,c Medical Intensive Care Unit, Cochin University Hospital, Hopitaux Universitaires, Paris Centre, AP-HP, Paris, France b Paris Descartes University, Sorbonne Paris Cité – Medical School, Paris, France c INSERM U970, Paris Cardiovascular Research Center, Paris, France a
These findings lend credence to the controversial notion that SRS is an acceptable treatment option for patients harboring symptomatic brainstem CMs. In the following discussion, our aim is to critically examine the role of SRS in the management of CMs. We believe that the controversy regarding the use of SRS for CMs is rooted in two important points of contention. First, the baseline AHR of a CM varies considerably depending on the method of calculation. If one assumes that CMs are congenital lesions, the AHR should be calculated from the time of the patient’s birth. On the other hand, if one assumes that CMs are acquired lesions, the AHR should be calculated from the time of initial diagnosis. Proponents of SRS for CMs use the former assumption to derive very high baseline AHRs, thereby rationalizing the use of SRS. In addition to the methodological differences in calculating the baseline AHR, the effect of SRS may be further confounded by the phenomenon of temporal clustering [2]. Second, the radiobiological effect of SRS on CMs is unpredictable and cannot be reliably assessed by currently available neuroimaging modalities. This is in contrast to SRS for cerebral arteriovenous malformations, for which progressive occlusion can be readily monitored with magnetic resonance imaging or angiography and the predictors of obliteration and complications are relatively consistent across different series [3–16]. Therefore, until the pathobiology of intracranial vascular malformations is better understood, the role of SRS in the management of CMs will continue to be shrouded in controversy [17–21]. For eloquently located CMs with multiple symptomatic hemorrhages, SRS may be more appropriately considered as an alternative to observation, rather than to surgical resection.
∗ Corresponding
author at: Service de Réanimation medico-chirurgicale, Hôpital de Versailles – Site André Mignot, 177 rue de Versailles, 78150 Le Chesnay Cedex, France. Tel.: +33 139 638 839; fax: +33 139 638 688. E-mail address: [email protected] (S. Legriel) 19 September 2014 Available online 22 January 2015
http://dx.doi.org/10.1016/j.clineuro.2015.01.013
Controversies in the management of brainstem cavernous malformations: Role of stereotactic radiosurgery Keywords: Brainstem Cavernous malformation Intracranial hemorrhage Radiosurgery Stroke
Dear Editor, I have read, with interest, a recently published article in Clinical Neurology and Neurosurgery by Kim et al. [1] titled ‘Gamma knife radiosurgery of the symptomatic brain stem cavernous angioma with low marginal dose’. This retrospective cohort study analyzes the outcomes of 39 patients with brainstem cavernous malformations (CM) who underwent treatment with Gamma Knife stereotactic radiosurgery (SRS). The annual hemorrhage rate (AHR) was 33.6% between initial diagnosis and treatment. The median margin dose was 13 Gy, and the mean follow-up duration was 4.1 years. The AHR following SRS was 8.1% for the first 2 years, and then 2.4% thereafter. The rates of symptomatic SRS-induced complications and clinical deterioration were 5% and 10%, respectively.
References [1] Kim BS, Yeon JY, Kim JS, Hong SC, Lee JI. Gamma knife radiosurgery of the symptomatic brain stem cavernous angioma with low marginal dose. Clin Neurol Neurosurg 2014;126C:110–4. [2] Barker 2nd FG, Amin-Hanjani S, Butler WE, Lyons S, Ojemann RG, Chapman PH, et al. Temporal clustering of hemorrhages from untreated cavernous malformations of the central nervous system. Neurosurgery 2001;49(1):15–24 [discussion 24–5]. [3] Ding D, Starke RM, Yen CP, Sheehan JP. Radiosurgery for cerebellar arteriovenous malformations: does infratentorial location affect outcome? World Neurosurg 2014;82(1–2):e209–17. [4] Ding D, Yen CP, Starke RM, Xu Z, Sheehan JP. Radiosurgery for ruptured intracranial arteriovenous malformations. J Neurosurg 2014;121(2):470–81. [5] Ding D, Yen CP, Starke RM, Xu Z, Sun X, Sheehan JP. Radiosurgery for Spetzler-Martin Grade III arteriovenous malformations. J Neurosurg 2014;120(4):959–69. [6] Ding D, Yen CP, Starke RM, Xu Z, Sun X, Sheehan JP. Outcomes following singlesession radiosurgery for high-grade intracranial arteriovenous malformations. Br J Neurosurg 2014;28(5):666–74. [7] Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for patients with unruptured intracranial arteriovenous malformations. J Neurosurg 2013;118(5):958–66. [8] Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for primary motor and sensory cortex arteriovenous malformations: outcomes and the effect of eloquent location. Neurosurgery 2013;73(5):816–24. [9] Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for low-grade intracranial arteriovenous malformations. J Neurosurg 2014;121(2):457–67. [10] Chen CJ, Chivukula S, Ding D, Starke RM, Lee CC, Yen CP, et al. Seizure outcomes following radiosurgery for cerebral arteriovenous malformations. Neurosurg Focus 2014;37(3):E17. [11] Yen CP, Ding D, Cheng CH, Starke RM, Shaffrey M, Sheehan J. Gamma Knife surgery for incidental cerebral arteriovenous malformations. J Neurosurg 2014:1–7. [12] Starke RM, Yen CP, Ding D, Sheehan JP. A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg 2013;119(4):981–7. [13] Pollock BE, Flickinger JC, Lunsford LD, Maitz A, Kondziolka D. Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 1998;42(6):1239–44 [discussion 1244–7]. [14] Moosa S, Chen CJ, Ding D, Lee CC, Chivukula S, Starke RM, et al. Volume-staged versus dose-staged radiosurgery outcomes for large intracranial arteriovenous malformations. Neurosurg Focus 2014;37(3):E18. [15] Maruyama K, Kawahara N, Shin M, Tago M, Kishimoto J, Kurita H, et al. The risk of hemorrhage after radiosurgery for cerebral arteriovenous malformations. N Engl J Med 2005;352(2):146–53.
©2015 Elsevier
aphasia in which there are deficits of written as well as spoken language. Interestingly, aphemia was first described by Broca [2] predating his description of the eponymous aphasia. Aphemia has been described in lesion to the left frontal operculum or left precentral gyrus. While aphemia certainly can be persistent [3], curiously, as in our case, that of Fox et al. [1] and another [4] aphemia can show significant recovery within days, while complete recovery of severe aphasia is seen in less than 10% of cases and then only after some weeks at the least [5]. This difference in recovery from the two deficits may warrant further study. Competing interests None. References [1] Fox RJ, Kasner SE, Chatterjee A, Chalela JA. Aphemia: an isolated disorder of articulation. Clin Neurol Neurosurg 2001;103:123–6. [2] Broca P. Remarques sur le siège de la faculté du langage articulé; suivies d’une observation d’aphémie (perte de la parole). Bull Soc Anat Paris 1861;36: 330–57. [3] Ojha PK, Nandavar S, Pearson DM, Demchuk AM. Aphemia as a presenting syndrome in acute stroke. Neurol India 2011;59:432–4. [4] Ottomeyer C, Reuter B, Jäger T, Rossmanith C, Hennerici MG, Szabo K. Aphemia: an isolated disorder of speech associated with an ischemic lesion of the left precentral gyrus. J Neurol 2009;256:1166–8. [5] Pedersen PM, Jorgensen HS, Nakayam H, Raaschou HO, Olsen TS. Aphasia in acute stroke: incidence, determinants, and recovery. Ann Neurol 1995;38:659–66.
Alexander J. Feng Kwame O. Asante Department of Physical Medicine and Rehabilitation, Temple University School of Medicine, Philadelphia, USA Camilo Guiterrez Department of Neurology, Temple University School of Medicine, Philadelphia, USA Eric L. Altschuler ∗ Department of Physical Medicine and Rehabilitation, Temple University School of Medicine, Philadelphia, USA ∗ Corresponding author at: Department of Physical Medicine and Rehabilitation, 3401 N. Broad Street, Philadelphia 19140, USA. Tel.: +1 215 707 7021; fax: +1 215 707 9168. E-mail address: [email protected] (E.L. Altschuler)
12 August 2014 Available online 22 January 2015 http://dx.doi.org/10.1016/j.clineuro.2014.12.025
87
emergency medical system or in the neurological intensive care unit. Antiepileptic treatment appropriate for the electrical and clinical pattern in the patient should be initiated at scene on an emergency basis. In addition to these symptomatic measures, the treatment strategy should include rigorous aetiological investigations for a cause to the status epilepticus, followed by etiological treatment. However, the existence of functional impairments in half the survivors of convulsive status epilepticus requiring ICU management [2] indicates a need for neuroprotective interventions. Therapeutic hypothermia has been reported to exert not only anticonvulsant but also neuroprotective effects [3] in studies of rats with self-sustaining status epilepticus. Hyperthermia between 39.5 ◦ C and 42 ◦ C promoted the occurrence of seizures and exacerbated local and hippocampal neuronal damage, whereas cooling to 32.5 ◦ C significantly decreased the occurrence of such damage. Hypothermia between 28 ◦ C and 31 ◦ C decreased the incidence of epileptic activity and associated neuronal lesions. After pre-treatment with mild hypothermia (32–34 ◦ C), the rats were protected from the onset of status epilepticus (increased latency to onset of seizures and time to onset of status epilepticus) and also had fewer apoptotic neurons in the hippocampus. Another study has shed light on the pathophysiological mechanisms involved in the neuroprotective effect of hypothermia. Moderate hypothermia (32–34 ◦ C) was associated with regulation of the expression of the GluR1 and GluR2 subunits of the AMPA glutamate receptors, an effect that decreased the number of necrotic or apoptotic hippocampal neurons. Furthermore, cerebral oedema induced by ongoing seizures was decreased by the use of therapeutic hypothermia immediately after status epilepticus induced by kainic acid. All these effects were potentiated by the concomitant administration of anticonvulsant benzodiazepine therapy. However, hypothermia was not effective to prevent epilepsy after status epilepticus. In humans, therapeutic hypothermia has been used as an adjuvant treatment in refractory epilepsy and during neurosurgery. Successful treatment with hypothermia has also been reported in paediatric patients with severely refractory status epilepticus. Finally, therapeutic hypothermia may also target some causes of status epilepticus such as ischaemic or haemorrhagic stroke, subarachnoid haemorrhage, and even traumatic brain injury [4]. Conversely, the use of therapeutic hypothermia in severe bacterial meningitis has been demonstrated to increase the risk of death [5]. In conclusion, whether therapeutic hypothermia is beneficial in humans with status epilepticus remains to be demonstrated. Pathophysiological considerations and experimental data suggest a role for therapeutic hypothermia. A French multicentre randomised study for which patient recruitment is ongoing can be expected to clarify this point (HYBERNATUS, NCT01359332). Until the results are available, all patients with status epilepticus may benefit from non-specific measures aimed at preventing secondary brain damage, including at least targeted temperature management. The use of therapeutic hypothermia must still be restricted to severely refractory status epilepticus, in the absence of contraindications. Financial support
Dual anticonvulsant and neuroprotective effects of therapeutic hypothermia after status epilepticus Sir, We read with a great interest the recent and innovative article by Bennett et al. [1]. Their report is original and at times thoughtprovoking, notably regarding the use of therapeutic hypothermia for super refractory status epilepticus. Patients with status epilepticus require the symptomatic measures usually taken in the emergency department, prehospital
We declare no financial support. Conflict of interest We declare no conflict of interest. References [1] Bennett AE, Hoesch RE, DeWitt LD, Afra P, Ansari SA. Therapeutic hypothermia for status epilepticus: a report, historical perspective, and review. Clin Neurol Neurosurg 2014;126:103–9.
88
Letters to the Editor / Clinical Neurology and Neurosurgery 131 (2015) 86–91
[2] Legriel S, Azoulay E, Resche-Rigon M, Lemiale V, Mourvillier B, Kouatchet A, et al. Functional outcome after convulsive status epilepticus. Crit Care Med 2010;38:2295–303. [3] Schmitt FC, Buchheim K, Meierkord H, Holtkamp M. Anticonvulsant properties of hypothermia in experimental status epilepticus. Neurobiol Dis 2006;23:689–96. [4] Polderman KH. Induced hypothermia and fever control for prevention and treatment of neurological injuries. Lancet 2008;371:1955–69. [5] Mourvillier B, Tubach F, van de Beek D, Garot D, Pichon N, Georges H, et al. Induced hypothermia in severe bacterial meningitis: a randomized clinical trial. JAMA 2013;310:2174–83.
Stéphane Legriel ∗ Intensive Care Unit, Hôpital de Versailles – Site André Mignot, 177 rue de Versailles, 78150 Le Chesnay Cedex, France Matthieu Resche-Rigon a,b,c SBIM, Biostatistics and Clinical Epidemiology Research Unit, Hôpital Saint-Louis, APHP, 1 Avenue Claude Vellefaux, Paris, France b Denis Diderot University – Paris 7, Paris, France c ECSTRA Team, UMR 1153 Inserm, Paris, France a
Alain Cariou a,b,c Medical Intensive Care Unit, Cochin University Hospital, Hopitaux Universitaires, Paris Centre, AP-HP, Paris, France b Paris Descartes University, Sorbonne Paris Cité – Medical School, Paris, France c INSERM U970, Paris Cardiovascular Research Center, Paris, France a
These findings lend credence to the controversial notion that SRS is an acceptable treatment option for patients harboring symptomatic brainstem CMs. In the following discussion, our aim is to critically examine the role of SRS in the management of CMs. We believe that the controversy regarding the use of SRS for CMs is rooted in two important points of contention. First, the baseline AHR of a CM varies considerably depending on the method of calculation. If one assumes that CMs are congenital lesions, the AHR should be calculated from the time of the patient’s birth. On the other hand, if one assumes that CMs are acquired lesions, the AHR should be calculated from the time of initial diagnosis. Proponents of SRS for CMs use the former assumption to derive very high baseline AHRs, thereby rationalizing the use of SRS. In addition to the methodological differences in calculating the baseline AHR, the effect of SRS may be further confounded by the phenomenon of temporal clustering [2]. Second, the radiobiological effect of SRS on CMs is unpredictable and cannot be reliably assessed by currently available neuroimaging modalities. This is in contrast to SRS for cerebral arteriovenous malformations, for which progressive occlusion can be readily monitored with magnetic resonance imaging or angiography and the predictors of obliteration and complications are relatively consistent across different series [3–16]. Therefore, until the pathobiology of intracranial vascular malformations is better understood, the role of SRS in the management of CMs will continue to be shrouded in controversy [17–21]. For eloquently located CMs with multiple symptomatic hemorrhages, SRS may be more appropriately considered as an alternative to observation, rather than to surgical resection.
∗ Corresponding
author at: Service de Réanimation medico-chirurgicale, Hôpital de Versailles – Site André Mignot, 177 rue de Versailles, 78150 Le Chesnay Cedex, France. Tel.: +33 139 638 839; fax: +33 139 638 688. E-mail address: [email protected] (S. Legriel) 19 September 2014 Available online 22 January 2015
http://dx.doi.org/10.1016/j.clineuro.2015.01.013
Controversies in the management of brainstem cavernous malformations: Role of stereotactic radiosurgery Keywords: Brainstem Cavernous malformation Intracranial hemorrhage Radiosurgery Stroke
Dear Editor, I have read, with interest, a recently published article in Clinical Neurology and Neurosurgery by Kim et al. [1] titled ‘Gamma knife radiosurgery of the symptomatic brain stem cavernous angioma with low marginal dose’. This retrospective cohort study analyzes the outcomes of 39 patients with brainstem cavernous malformations (CM) who underwent treatment with Gamma Knife stereotactic radiosurgery (SRS). The annual hemorrhage rate (AHR) was 33.6% between initial diagnosis and treatment. The median margin dose was 13 Gy, and the mean follow-up duration was 4.1 years. The AHR following SRS was 8.1% for the first 2 years, and then 2.4% thereafter. The rates of symptomatic SRS-induced complications and clinical deterioration were 5% and 10%, respectively.
References [1] Kim BS, Yeon JY, Kim JS, Hong SC, Lee JI. Gamma knife radiosurgery of the symptomatic brain stem cavernous angioma with low marginal dose. Clin Neurol Neurosurg 2014;126C:110–4. [2] Barker 2nd FG, Amin-Hanjani S, Butler WE, Lyons S, Ojemann RG, Chapman PH, et al. Temporal clustering of hemorrhages from untreated cavernous malformations of the central nervous system. Neurosurgery 2001;49(1):15–24 [discussion 24–5]. [3] Ding D, Starke RM, Yen CP, Sheehan JP. Radiosurgery for cerebellar arteriovenous malformations: does infratentorial location affect outcome? World Neurosurg 2014;82(1–2):e209–17. [4] Ding D, Yen CP, Starke RM, Xu Z, Sheehan JP. Radiosurgery for ruptured intracranial arteriovenous malformations. J Neurosurg 2014;121(2):470–81. [5] Ding D, Yen CP, Starke RM, Xu Z, Sun X, Sheehan JP. Radiosurgery for Spetzler-Martin Grade III arteriovenous malformations. J Neurosurg 2014;120(4):959–69. [6] Ding D, Yen CP, Starke RM, Xu Z, Sun X, Sheehan JP. Outcomes following singlesession radiosurgery for high-grade intracranial arteriovenous malformations. Br J Neurosurg 2014;28(5):666–74. [7] Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for patients with unruptured intracranial arteriovenous malformations. J Neurosurg 2013;118(5):958–66. [8] Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for primary motor and sensory cortex arteriovenous malformations: outcomes and the effect of eloquent location. Neurosurgery 2013;73(5):816–24. [9] Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP. Radiosurgery for low-grade intracranial arteriovenous malformations. J Neurosurg 2014;121(2):457–67. [10] Chen CJ, Chivukula S, Ding D, Starke RM, Lee CC, Yen CP, et al. Seizure outcomes following radiosurgery for cerebral arteriovenous malformations. Neurosurg Focus 2014;37(3):E17. [11] Yen CP, Ding D, Cheng CH, Starke RM, Shaffrey M, Sheehan J. Gamma Knife surgery for incidental cerebral arteriovenous malformations. J Neurosurg 2014:1–7. [12] Starke RM, Yen CP, Ding D, Sheehan JP. A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg 2013;119(4):981–7. [13] Pollock BE, Flickinger JC, Lunsford LD, Maitz A, Kondziolka D. Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 1998;42(6):1239–44 [discussion 1244–7]. [14] Moosa S, Chen CJ, Ding D, Lee CC, Chivukula S, Starke RM, et al. Volume-staged versus dose-staged radiosurgery outcomes for large intracranial arteriovenous malformations. Neurosurg Focus 2014;37(3):E18. [15] Maruyama K, Kawahara N, Shin M, Tago M, Kishimoto J, Kurita H, et al. The risk of hemorrhage after radiosurgery for cerebral arteriovenous malformations. N Engl J Med 2005;352(2):146–53.
©2015 Elsevier
