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Ajay Niranjan, Ahmed Kashkoush, Hideyuki Kano, Edward A. Monaco III, John C. Flickinger and L. Dade Lunsford

OBJECTIVE

Seizures are the second-most common presenting symptom in patients with lobar arteriovenous malformations (AVMs). However, few studies have assessed the long-term effect of stereotactic radiosurgery (SRS) on seizure control. The authors of this study assess the outcome of SRS for these patients to identify prognostic factors associated with seizure control.

METHODS

Patients with AVM who presented with a history of seizure and underwent SRS at the authors’ institution between 1987 and 2012 were retrospectively assessed. The total cohort included 155 patients with a mean follow-up of 86 months (range 6–295 months). Primary outcomes assessed were seizure frequency, antiepileptic drug regimen, and seizure freedom for 6 months prior to last follow-up.

RESULTS

Seizure-free status was achieved in 108 patients (70%), with an additional 23 patients (15%) reporting improved seizure frequency as compared to their pre-SRS status. The median time to seizure-free status was estimated to be 12 months (95% CI 0–27 months) as evaluated via Kaplan-Meier survival analysis. The mean seizure frequency prior to SRS was 14.2 (95% CI 5.4–23.1) episodes per year. Although not all patients tried, the proportion of patients successfully weaned off all antiepileptic drugs was 18% (28/155 patients). On multivariate logistic regression, focal impaired awareness seizure type (also known as complex partial seizures) and superficial venous drainage were significantly associated with a decreased odds ratio for seizure-free status at last follow-up (OR 0.37 [95% CI 0.15–0.92] for focal impaired awareness seizures; OR 0.36 [95% CI 0.16–0.81] for superficial venous drainage). The effects of superficial venous drainage on seizure outcome were nonsignificant when excluding patients with < 2 years of follow-up. AVM obliteration did not correlate with long-term seizure freedom (p = 0.202, chi-square test).

CONCLUSIONS

This study suggests that SRS improves long-term seizure control and increases the likelihood of being medication free, independently of AVM obliteration. Patients with focal impaired awareness seizures were less likely to obtain long-term seizure relief.

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Daniel A. Tonetti, Bradley A. Gross, Brian T. Jankowitz, Hideyuki Kano, Edward A. Monaco III, Ajay Niranjan, John C. Flickinger and L. Dade Lunsford

OBJECTIVE

Aggressive dural arteriovenous fistulas (dAVFs) with cortical venous drainage (CVD) are known for their relatively high risk of recurrent neurological events or hemorrhage. However, recent natural history literature has indicated that nonaggressive dAVFs with CVD have a significantly lower prospective risk of hemorrhage. These nonaggressive dAVFs are typically diagnosed because of symptomatic headache, pulsatile tinnitus, or ocular symptoms, as in low-risk dAVFs. Therefore, the viability of stereotactic radiosurgery (SRS) as a treatment for this lesion subclass should be investigated.

METHODS

The authors evaluated their institutional experience with SRS for dAVFs with CVD for the period from 1991 to 2016, assessing angiographic outcomes and posttreatment hemorrhage rates. They subsequently pooled their results with those published in the literature and stratified the results based on the mode of clinical presentation.

RESULTS

In an institutional cohort of 42 dAVFs with CVD treated using SRS, there were no complications or hemorrhages after treatment in 19 patients with nonaggressive dAVFs, but there was 1 radiation-induced complication and 1 hemorrhage among the 23 patients with aggressive dAVFs. In pooling these cases with 155 additional cases from the literature, the authors found that the hemorrhage rate after SRS was significantly lower among the patients with nonaggressive dAVFs (0% vs 6.8%, p = 0.003). Similarly, the number of radiation-related complications was 0/124 in nonaggressive dAVF cases versus 6/73 in aggressive dAVF cases (p = 0.001). The annual rate of hemorrhage after SRS for aggressive fistulas was 3.0% over 164.5 patient-years, whereas none of the nonaggressive fistulas bled after radiosurgery over 279.4 patient-years of follow-up despite the presence of CVD.

CONCLUSIONS

Cortical venous drainage is thought to be a significant risk factor in all dAVFs. In the institutional experience described here, SRS proved to be a low-risk strategy associated with a very low risk of subsequent hemorrhage or radiation-related complications in nonaggressive dAVFs with CVD.

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Daniel A. Tonetti, Bradley A. Gross, Kyle M. Atcheson, Brian T. Jankowitz, Hideyuki Kano, Edward A. Monaco III, Ajay Niranjan, John C. Flickinger and L. Dade Lunsford

OBJECTIVE

The authors of this study found that, given the latency period required for arteriovenous malformation (AVM) obliteration after stereotactic radiosurgery (SRS), a study with limited follow-up cannot assess the benefit of SRS for unruptured AVMs.

METHODS

The authors reviewed their institutional experience with “ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations)–eligible” AVMs treated with SRS between 1987 and 2016, with the primary outcome defined as stroke (ischemic or hemorrhagic) or death (AVM related or AVM unrelated). Patients with at least 3 years of follow-up in addition to those who experienced stroke or died during the latency period were included. Secondary outcome measures included obliteration rates, patients with new seizure disorders, and those with new focal deficits without stroke.

RESULTS

Of 233 patients included in this study, 32 had a stroke or died after SRS over the mean 8.4-year follow-up (14%). Utilizing the 10% stroke or death rate at a mean 2.8-year follow-up for untreated AVMs in ARUBA, the rate in the authors’ study is significantly lower than that anticipated at the 8.4-year follow-up for an untreated cohort (14% vs 30%, p = 0.0003). Notwithstanding obliteration, in this study, annualized rates of hemorrhage and stroke or death after 3 years following SRS were 0.4% and 0.8%, respectively. The overall obliteration rate was 72%; new seizure disorders, temporary new focal deficits without stroke, and permanent new focal deficits without stroke occurred in 2% of patients each.

CONCLUSIONS

After a sensible follow-up period exceeding the latency period, there is a lower rate of stroke/death for patients with treated, unruptured AVMs with SRS than for patients with untreated AVMs.

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Marshall J. Huang, Hideyuki Kano, Seyed H. Mousavi, Ajay Niranjan, Edward A. Monaco III, Yoshio Arai, John C. Flickinger and L. Dade Lunsford

OBJECTIVE

The goal of this retrospective cohort study was to assess long-term outcomes in patients with vestibular schwannoma (VS) who underwent stereotactic radiosurgery (SRS) after initial microsurgical resection.

METHODS

From the authors' database of 1770 patients with VS, the authors retrospectively analyzed data from 173 Gamma Knife SRS procedures for VS after 1 (128 procedures) or multiple (45 procedures) microsurgical resections. The median length of the interval between the last resection and SRS was 42 months (range 2–329 months). The median length of clinical follow-up was 74 months (range 6–285 months). Progression-free survival after SRS was determined with Kaplan-Meier analysis.

RESULTS

At the time of SRS, the hearing of 161 patients (93%) was Gardner-Robertson Class V, and 81 patients (47%) had facial neuropathy (i.e., facial function with House-Brackmann [HB] grades of III–VI), 87 (50%) had trigeminal neuropathy, and 71 (41%) reported imbalance or disequilibrium disorders. The median tumor volume was 2.7 cm3 (range 0.2–21.6 cm3), and the median dose to the tumor margin was 13 Gy (range 11–20 Gy). Radiosurgery controlled growth of 163 (94%) tumors. Progression-free survival after SRS was 97% at 3 years, 95% at 5 years, and 90% at 10 years. Four patients with delayed tumor progression underwent repeat SRS at a median of 35 months (range 23–64 months) after the first SRS. Four patients (2.3%) with tumor progression underwent repeat resection at a median of 25 months (range 19–33 months). Among the patients with any facial dysfunction (indicated by HB grades of II–VI), 19% had improvement in this condition after SRS, and 5.5% with some facial function (indicated by HB grades of I–V) developed more facial weakness. Among patients with trigeminal neuropathy, 20% had improvement in this condition, and 5.8% developed or had worsened trigeminal neuropathy after SRS.

CONCLUSIONS

Stereotactic radiosurgery offered a safe and effective long-term management strategy for VS patients whose tumors remained or recurred after initial microsurgery.

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Seyed H. Mousavi, Ajay Niranjan, Berkcan Akpinar, Edward A. Monaco III, Jonathan Cohen, Jagdish Bhatnagar, Yue-Fang Chang, Hideyuki Kano, Sakibul Huq, John C. Flickinger and L. Dade Lunsford

OBJECTIVE

During the last 25 years, more than 100,000 patients worldwide with trigeminal neuralgia (TN) have undergone stereotactic radiosurgery (SRS) with a standard dose of radiation. However, the radiobiological effect of radiation is determined by the amount of energy delivered to the tissue (integral dose [ID] = mean dose × target volume) and is directly associated with the nerve volume. Although the trigeminal nerve volume varies among patients with TN, the clinical impact of this variation in delivered energy is unknown. The objective of this study was to evaluate the effect of delivered ID on the outcome of TN radiosurgery.

METHODS

The authors evaluated 155 patients with unilateral TN who had undergone SRS as their initial surgical management over a 13-year period. The authors measured the postganglionic ID within the SRS target and retrospectively stratified patients into 3 groups: low (< 1.4 mJ), medium (1.4–2.7 mJ), and high (> 2.7 mJ) ID. Clinical outcomes, which included pain status (scored using the Barrow Neurological Institute Pain Scale) and sensory dysfunction (scored using the Barrow Neurological Institute Numbness Scale), were evaluated at a median follow-up of 71 months.

RESULTS

Patients who were treated with a medium ID had superior pain relief either with or without medications (p = 0.006). In the medium ID group, the rates of complete pain relief without medications at 1, 3, and 6 years after SRS were 67%, 54%, and 33%, respectively, while the rates in the rest of the cohort were 55%, 36%, and 19%, respectively. Patients given a high ID had a higher rate of post-SRS trigeminal sensory deterioration (p < 0.0001). At 1, 3, and 6 years after SRS, the high ID group had an estimated rate for developing sensory dysfunction of 35%, 45%, and 50%, respectively, while the rates in patients receiving low and medium IDs were 3%, 4%, and 9%, respectively. The optimal clinical outcome (maximum pain relief and minimal trigeminal sensory dysfunction) was obtained in patients who had received a medium ID.

CONCLUSIONS

With current dose selection methods, nerve volume affects long-term clinical outcomes in patients with TN who have undergone SRS. This study suggests that the prescribed SRS dose should be customized for each TN patient based on the nerve volume.

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Greg Bowden, Hideyuki Kano, Ellen Caparosa, Daniel Tonetti, Ajay Niranjan, Edward A. Monaco III, John Flickinger, Yoshio Arai and L. Dade Lunsford

OBJECT

A visual field deficit resulting from the management of an arteriovenous malformation (AVM) significantly impacts a patient's quality of life. The present study was designed to investigate the clinical and radiological outcomes of stereotactic radiosurgery (SRS) performed for AVMs involving the postgeniculate visual pathway.

METHODS

In this retrospective single-institution analysis, the authors reviewed their experience with Gamma Knife surgery for postgeniculate visual pathway AVMs performed during the period between 1987 and 2009.

RESULTS

During the study interval, 171 patients underwent SRS for AVMs in this region. Forty-one patients (24%) had a visual deficit prior to SRS. The median target volume was 6.0 cm3 (range 0.4–22 cm3), and 19 Gy (range 14–25 Gy) was the median margin dose. Obliteration of the AVM was confirmed in 80 patients after a single SRS procedure at a median follow-up of 74 months (range 5–297 months). The actuarial rate of total obliteration was 67% at 4 years. Arteriovenous malformations with a volume < 5 cm3 had obliteration rates of 60% at 3 years and 79% at 4 years. The delivered margin dose proved significant given that 82% of patients receiving ≥ 22 Gy had complete obliteration. The AVM was completely obliterated in an additional 18 patients after they underwent repeat SRS. At a median of 25 months (range 11–107 months) after SRS, 9 patients developed new or worsened visual field deficits. One patient developed a complete homonymous hemianopia, and 8 patients developed quadrantanopias. The actuarial risk of sustaining a new visual deficit was 3% at 3 years, 5% at 5 years, and 8% at 10 years. Fifteen patients had hemorrhage during the latency period, resulting in death in 9 of the patients. The annual hemorrhage rate during the latency interval was 2%, and no hemorrhages occurred after confirmed obliteration.

CONCLUSIONS

Despite an overall treatment mortality of 5%, related to latency interval hemorrhage, SRS was associated with only a 5.6% risk of new visual deficit and a final obliteration rate close to 80% in patients with AVMs of the postgeniculate visual pathway.

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Zachary J. Tempel, Srinivas Chivukula, Edward A. Monaco III, Greg Bowden, Hideyuki Kano, Ajay Niranjan, Edward F. Chang, Penny K. Sneed, Anthony M. Kaufmann, Jason Sheehan, David Mathieu and L. Dade Lunsford

OBJECT

Gamma Knife radiosurgery (GKRS) is the least invasive treatment option for medically refractory, intractable trigeminal neuralgia (TN) and is especially valuable for treating elderly, infirm patients or those on anticoagulation therapy. The authors reviewed pain outcomes and complications in TN patients who required 3 radiosurgical procedures for recurrent or persistent pain.

METHODS

A retrospective review of all patients who underwent 3 GKRS procedures for TN at 4 participating centers of the North American Gamma Knife Consortium from 1995 to 2012 was performed. The Barrow Neurological Institute (BNI) pain score was used to evaluate pain outcomes.

RESULTS

Seventeen patients were identified; 7 were male and 10 were female. The mean age at the time of last GKRS was 79.6 years (range 51.2–95.6 years). The TN was Type I in 16 patients and Type II in 1 patient. No patient suffered from multiple sclerosis. Eight patients (47.1%) reported initial complete pain relief (BNI Score I) following their third GKRS and 8 others (47.1%) experienced at least partial relief (BNI Scores II–IIIb). The average time to initial response was 2.9 months following the third GKRS. Although 3 patients (17.6%) developed new facial sensory dysfunction following primary GKRS and 2 patients (11.8%) experienced new or worsening sensory disturbance following the second GKRS, no patient sustained additional sensory disturbances after the third procedure. At a mean follow-up of 22.9 months following the third GKRS, 6 patients (35.3%) reported continued Score I complete pain relief, while 7 others (41.2%) reported pain improvement (BNI Scores II–IIIb). Four patients (23.5%) suffered recurrent TN following the third procedure at a mean interval of 19.1 months.

CONCLUSIONS

A third GKRS resulted in pain reduction with a low risk of additional complications in most patients with medically refractory and recurrent, intractable TN. In patients unsuitable for other microsurgical or percutaneous strategies, especially those receiving long-term oral anticoagulation or antiplatelet agents, GKRS repeated for a third time was a satisfactory, low risk option.

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Hideyuki Kano, Douglas Kondziolka, John C. Flickinger, Kyung-Jae Park, Aditya Iyer, Huai-che Yang, Xiaomin Liu, Edward A. Monaco III, Ajay Niranjan and L. Dade Lunsford

Object

In this paper the authors' goal was to define the long-term benefits and risks of stereotactic radiosurgery (SRS) for patients with arteriovenous malformations (AVMs) who underwent prior embolization.

Methods

Between 1987 and 2006, the authors performed Gamma Knife surgery in 996 patients with brain AVMs; 120 patients underwent embolization followed by SRS. In this series, 64 patients (53%) had at least one prior hemorrhage. The median number of embolizations varied from 1 to 5. The median target volume was 6.6 cm3 (range 0.2–26.3 cm3). The median margin dose was 18 Gy (range 13.5–25 Gy).

Results

After embolization, 25 patients (21%) developed symptomatic neurological deficits. The overall rates of total obliteration documented by either angiography or MRI were 35%, 53%, 55%, and 59% at 3, 4, 5, and 10 years, respectively. Factors associated with a higher rate of AVM obliteration were smaller target volume, smaller maximum diameter, higher margin dose, timing of embolization during the most recent 10-year period (1997–2006), and lower Pollock-Flickinger score. Nine patients (8%) had a hemorrhage during the latency period, and 7 patients died of hemorrhage. The actuarial rates of AVM hemorrhage after SRS were 0.8%, 3.5%, 5.4%, 7.7%, and 7.7% at 1, 2, 3, 5, and 10 years, respectively. The overall annual hemorrhage rate was 2.7%. Factors associated with a higher risk of hemorrhage after SRS were a larger target volume and a larger number of prior hemorrhages. Permanent neurological deficits due to adverse radiation effects (AREs) developed in 3 patients (2.5%) after SRS, and 1 patient had delayed cyst formation 210 months after SRS. No patient died of AREs. A larger 12-Gy volume was associated with higher risk of symptomatic AREs. Using a case-control matched approach, the authors found that patients who underwent embolization prior to SRS had a lower rate of total obliteration (p = 0.028) than patients who had not undergone embolization.

Conclusions

In this 20-year experience, the authors found that prior embolization reduced the rate of total obliteration after SRS, and that the risks of hemorrhage during the latency period were not affected by prior embolization. For patients who underwent embolization to volumes smaller than 8 cm3, success was significantly improved. A margin dose of 18 Gy or more also improved success. In the future, the role of embolization after SRS should be explored.

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Ramesh Grandhi, Douglas Kondziolka, David Panczykowski, Edward A. Monaco III, Hideyuki Kano, Ajay Niranjan, John C. Flickinger and L. Dade Lunsford

Object

To better establish the role of stereotactic radiosurgery (SRS) in treating patients with 10 or more intracranial metastases, the authors assessed clinical outcomes and identified prognostic factors associated with survival and tumor control in patients who underwent radiosurgery using the Leksell Gamma Knife Perfexion (LGK PFX) unit.

Methods

The authors retrospectively reviewed data in all patients who had undergone LGK PFX surgery to treat 10 or more brain metastases in a single session at the University of Pittsburgh. Posttreatment imaging studies were used to assess tumor response, and patient records were reviewed for clinical follow-up data. All data were collected by a neurosurgeon who had not participated in patient care.

Results

Sixty-one patients with 10 or more brain metastases underwent SRS for the treatment of 806 tumors (mean 13.2 lesions). Seven patients (11.5%) had no previous therapy. Stereotactic radiosurgery was the sole prior treatment modality in 8 patients (13.1%), 22 (36.1%) underwent whole-brain radiation therapy (WBRT) only, and 16 (26.2%) had prior SRS and WBRT. The total treated tumor volume ranged from 0.14 to 40.21 cm3, and the median radiation dose to the tumor margin was 16 Gy. The median survival following SRS for 10 or more brain metastases was 4 months, with improved survival in patients with fewer than 14 brain metastases, a nonmelanomatous primary tumor, controlled systemic disease, a better Karnofsky Performance Scale score, and a lower recursive partitioning analysis (RPA) class. Prior cerebral treatment did not influence survival. The median survival for a patient with fewer than 14 brain metastases, a nonmelanomatous primary tumor, and controlled systemic disease was 21.0 months. Sustained local tumor control was achieved in 81% of patients. Prior WBRT predicted the development of new adverse radiation effects.

Conclusions

Stereotactic radiosurgery safely and effectively treats intracranial disease with a high rate of local control in patients with 10 or more brain metastases. In patients with fewer metastases, a nonmelanomatous primary lesion, controlled systemic disease, and a low RPA class, SRS may be most valuable. In selected patients, it can be considered as first-line treatment.

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Edward A. Monaco III, Aftab A. Khan, Ajay Niranjan, Hideyuki Kano, Ramesh Grandhi, Douglas Kondziolka, John C. Flickinger and L. Dade Lunsford

Object

The authors performed a retrospective review of prospectively collected data to evaluate the safety and efficacy of stereotactic radiosurgery (SRS) for the treatment of patients harboring symptomatic solitary cavernous malformations (CMs) of the brainstem that bleed repeatedly and are high risk for resection.

Methods

Between 1988 and 2005, 68 patients (34 males and 34 females) with solitary, symptomatic CMs of the brainstem underwent Gamma Knife surgery. The mean patient age was 41.2 years, and all patients had suffered at least 2 symptomatic hemorrhages (range 2–12 events) before radiosurgery. Prior to SRS, 15 patients (22.1%) had undergone attempted resection. The mean volume of the malformation treated was 1.19 ml, and the mean prescribed marginal radiation dose was 16 Gy.

Results

The mean follow-up period was 5.2 years (range 0.6–12.4 years). The pre-SRS annual hemorrhage rate was 32.38%, or 125 hemorrhages, excluding the first hemorrhage, over a total of 386 patient-years. Following SRS, 11 hemorrhages were observed within the first 2 years of follow-up (8.22% annual hemorrhage rate) and 3 hemorrhages were observed in the period after the first 2 years of follow-up (1.37% annual hemorrhage rate). A significant reduction (p < 0.0001) in the risk of brainstem CM hemorrhages was observed following radiosurgical treatment, as well as in latency period of 2 years after SRS (p < 0.0447). Eight patients (11.8%) experienced new neurological deficits as a result of adverse radiation effects following SRS.

Conclusions

The results of this study support a role for the use of SRS for symptomatic CMs of the brainstem, as it is relatively safe and appears to reduce rebleeding rates in this high-surgical-risk location.