Abstract
Background
Cerebral arteriovenous malformations or angiomas are congenital vascular anomalies defined by abnormal arteriovenous shunt.
Materials and methods
We conducted a retrospective study between January 1992 and December 2010 at the Timone Hospital radiosurgery unit, 1557 patients were treated by radiosurgery for arteriovenous malformation of which 53 for thalamic localization (3,4%).
Results
The mean age was 35.8-/+16.6 years (4–75). 14 patients underwent pre-radiosurgical embolization (26.4%), discovery mode for 47 patients (88.7%) was haemorrhage. The average treatment volume was 1.43 cm3. The average RBAS score was 1.36. The average prescription to the 50% isodose envelope delivered was 22.9 +/-2.9 Gy (12-30), the median margin dose was 24 Gy. Our global obliteration rate after one or two procedures 66.7% for an average follow-up period of 56.7 months. We noted 3.9% of mortality, 5.9% of bleeding after procedure and 3.9% of radio-induced neurological deficit.
Conclusion
Radiosurgery became indispensable in the treatment of thalamic AVM even when there is a persistent risk of haemorrhage until total recovery.
Keywords: arteriovenous malformations, thalamus, radiosurgery
Introduction
Arteriovenous malformations or cerebral angiomas are congenital vascular anomalies defined by the presence of abnormal arteriovenous (“shunt”) communication. [1, 2, 3, 4,5]. They are diagnosed in both sexes around the 3rd and 4th decades of life, with a variable incidence of 1/100,000 [1, 2,5]. Thalamus and basal ganglia malformations represent around 6 to 13% of AVM [5, 6, 7,8]. Some location such the brainstem and the basal ganglia due to risk it present for the patient represent a real surgical challenge [4, 9, 10, 11]. These difficulties related to their microsurgical excision lead some authors to consider them as inoperable [12]. Deep localizations have more aggressive natural history with an annual haemorrhagic risk of 10 to 34% versus 2 to 4% for other locations [5-13]. The main revelation mode was haemorrhage in 75- 91% depending to the series versus 50-67% for the other locations and a mortality of approximately 62% [5, 14, 15] justifying the need of a curative treatment.
Radiosurgery is a therapeutic modality with good tolerance, however with an obliteration rate lower than in other locations [6,7,8,15,16]. Embolization is often considered as a complementary treatment to radiosurgery wich allow complete obliteration in only 15% of the cases [8, 21, 22]. In the literature, studies of thalamic AVM are rare with insignificant cohorts [6, 10, 12,20, 21,22 23]. The total obliteration rate in one or more radiosurgical procedures varies from 50-76% and requires a delay of 2 to 5 years with a haemorrhage persisting risk during this period. [6, 7,8-12, 16,23]. Besides the challenge the management of these malformations implies, it is interesting to be able to predict the outcome of the treatment to inform the patients. The Spetzler Martin grading is suitable for microsurgery and for radiosurgery it is more appropriate to use the predictive RBAS score (Radiosurgery based AVM) developed by Pollock [24,25].
The purpose of this retrospective study is to analyse the obliteration rate in patients treated for thalamus AVM in La Timone radiosurgery department and relate it to this predictive score. We chose this group because the thalamic location is weighted 1 in the RBAS score equation (radiosurgery based AVM score) while the other locations are weighted 0.
Methods
Patients
Between January 1992 and December 2010, 1557 patients were treated by radiosurgery for a cerebral AVM, of which 53 (3.4%) was located on the thalamus. The sex ratio was 1,4 (31 men for 22 women) with an average age of 35.8- / +16.6 years (4-75). In this cohort of 53 patients, 14 patients underwent preoperative surgical embolization (26.4%) and 5 patients (9.4%) had a partial resection surgery. The revelation mode was haemorrhage for 47 patients (88.7%), neurological disorders for 4 patients such as paraesthesia and headaches (7.5%) and serendipitous for 2 patients (3.8%). Among the patients who had experienced a haemorrhage, 43 patients presented a neurological deficit most often such as a hemiparesis related to the localization or the size of the hematoma.
The Spetzler-Martin grading was II for 6 patients (11.3%), III for 22 patients (41.5%), 15 patients (28.3%) were grade IV and 10 patients (18.9%) were grade V.
The modified Pollock-Flickinger[25] score was used to evaluate the malformation grading and was calculated with the following equation: Score = (0.1) (volume in cm3) + (0.02) (age in years) + (0.5) (location: thalamus = 1).
Indications for Gamma Knife radiosurgery treatment have been validated by a multidisciplinary team including neurosurgeons, radiotherapists and interventional neuroradiologists.
Treatment
The procedure requires, first of all, the installation of a stereotaxic (Leksell) under local anaesthesia and analgesic protocol. Imaging in stereotaxic conditions included: millimetric T1-weighted MRI with gadolinium and coronal T2-weighted sequences; cerebral CT-Scan with contrast and cerebral arteriography (Figure 1). The children were under general anaesthesia throughout the procedure. For computerized treatments (53), stereotaxic imaging has been localized in the Gamma Plan software and any previous imagery recorded in the same time. On those 53 files, 47 were planned with computer software to calculate the average volume of treatment which was 1.43 +/- 1.96 cm3 (0.09-14.20). The RBAS score average was 1.36 +/- 0.34 (0.64-2.35).
Figure 1.
Brain imaging of a 66-year-old patient at the time of treatment : a) Axial CT angiography showing an aspect in favour of a right thalamic AVM fed by one of the branches of the posterior cerebral artery ; b) TOF MRA with coronal reconstitution at the arterial phase showing a right thalamic AVM ; c) Stereotactic cerebral angiography of the right vertebral artery: a right thalamic AVM fed by the posterior choroidal artery with deep venous drainage; d) Cerebral angiography of the right vertebral artery with 3D reconstruction illustrating a right thalamic AVM fed by the posterior choroidal artery with deep venous drainage.
The aim of the contouring was to target the foot of the drainage vein and the nidus. The mean isodose 50% delivered was 22.9 +/- 2.9 Gy (12-30), the median dose was 24 Gy. The mean isocenter number was 3 (1-12). Cf (Table 1).
Table 1.
Radiosurgical treatment parameters.
| Parameters | Median value | Mean value (limits ) |
| Treatment volume, cm3 | 2.07 | 1.43 (0.09-14.2) |
| Maximum diameter, cm | 3.6 | 2.8 (0.68-7.86) |
| Average dose, Gy | 24GY | 22.9 (12-30) |
| Maximum dose, Gy | 48GY | 45.95 (30-62.5) |
| Number of isocenters | 7 | 03 (1-12) |
The treatment was performed on a Gamma Knife B model, then 4 C then Perfexion (Elekta). For all the patients, hospitalization duration was 48 hours. The follow-up protocol set up to realize MRI at 6 months, 1 year and 2 years, followed by arteriography at 3 years. In case of the nidus or drainage vein persistence a new radiosurgical procedure was proposed to the patient. The healing criteria were arteriography with inexistent nidus and drainage vein.
Statistical Analysis
The totality of the factors which may have an impact on the obliteration of AVM, the bleeding after the procedure as well as the onset of complications were analysed with SPSS 10 a statistical software by Windows (the stata logiciel/SE 13.0 was our statistical specific test).the test was a hazard analysis regression. The parameters with p <0.05 were statistically significant (Table 2).
Table 2.
multivariate analysis for obliteration.
| Parameters | Value | ||||
| Odds Ratio | Std. Err. | Z | P>|z| | [95% Conf. Interval] | |
| RBAS <2 | 0.1080545 | 0.1070202 | −2.25 | 0.025 | [0.0155092 0.752899] |
| DOSE | 1.039589 | 0.1039771 | 0.39 | 0.698 | [0.8545287 1.264727] |
| AVM rupture | 1.380885 | 0.70468 | 0.75 | 0.452 | [0.0327894 2142.135] |
The parameters with p <0.05 were statistically significant
Results
Among the 53 patients, 2 patients had their follow-up performed abroad so we were unable to retrieve the data. On the remaining 51 patients, 2 patients (3.9%) died by 2 years following the treatment, due to AVM bleeding for one and pneumonia for the other one. For the remaining 49 patients, the mean follow-up period was 56.7 months +/- 43.3 (8.1-251.7).
Obliteration
The post-treatment obliteration was evaluated by arteriography (absence of nidus and drainage vein) and by default MRI in case of denial of the patient. Out of 51 patients (deceased include) followed-up, 25 had complete obliteration (49%) confirmed by arteriography (88%) and 3 by MRI (12%) with a mean delay of 42.7 +/- 42.5 months (8.1-251.7) after the first procedure (Figure 2). For the remaining patients with incomplete obliteration confirmed by arteriography or MRI another radiosurgery procedure was proposed. Among the 26 non-occluded patients, 9 had complete obliteration, 8 remain partially occluded after 3 years of follow-up and 9 haven’t yet sufficient follow-up to conclude. A third procedure was proposed to the 9 patients not obliterated but they denied the treatment.
Figure 2.
Cerebral angiography of the right vertebral artery during treatment and 3 years later: a) Stereotactic cerebral angiography of the right vertebral artery during treatment (right thalamic AVM fed by the posterior choroidal artery with deep venous drainage) ; b) cerebral angiography of the right vertebral artery 3 months after treatment: normal.
Among the 14 followed patients who underwent embolization, 6 patients (42.8%) obliterated their AVM after treatment.
After statistical analysis, the factor related to a complete obliteration was only the RBAS score < 2 (p: 0025).
The delivered dose and the AVM rupture were not statistically significant as found in all the studies.
Retreatment
The average delay between the first and the second procedure was 37.45 months. The mean volume of treatment was: 1.21 cm3 (0.7-3.97cm), the average dose of prescription to isodose 50% was 20.54Gy (12-25) and the median dose was 16Gy. After one or two procedures in our center, 34 out of the 51 patients followed up (including deceased) had their AVM occluded as a complete occlusion rate of 66.7%.
Between 3-5 years of follow up 31 patients had complete obliteration (60.8%). At 10 years 3 more patients had occluded their AVM (66.7%). After 10 years, no further complete occlusion was noted.
Obliterated AVM mean RBAS score was 1.23 +/- 0.3 (0.64-1.90) against 1.42 +/- 0.34 (0.70-2.35) for non-obliterated AVM.
Post therapeutic hemorrhage
One MAV rebleeding occurred 9 months after the first treatment resulting to the patient death what made a mortality rate of 1.79 related to rebleeding. Two other patients had haemorrhage with new neurological deficit at 6 months and 15 months after the first Gamma Knife procedure, thereby the post SRS haemorrhage rate after one year was at: 3.9% and 1.9% in the second year following the procedure. Nidus size was the main factor related to post treatment haemorrhage (p = 0.041). (Figure 3).
Figure 3.
Obliteration and post SRS haemorrhage curves.
Complications
Two patients (3.9%) had symptomatic radio induced effects, these patients had on MRI a ring enhancement on T1-weighted sequence associated with a perilesional hyper signal on T2-weighted sequence. For one these patients those effects occurred 8 months after the first radiosurgery procedure on a right thalamic AVM, and 12 months after the 2nd radiosurgery procedure for a left thalamic AVM grade V in the other case. Patients had benefited of corticotherapy for several months with disappearance of paresthesia for the first and persistence of paresthesia for the second with appearance of a right unilateral tremor unresponsive to corticotherapy.
Discussion
In our series the mean age at diagnosis was 35 years comparable to Ding [14] and Kano series [20,21] with a mean age of 31 years. Natural history of basal ganglia AVM is more aggressive, their haemorrhagic risk and morbimortality are much higher than in other locations [5,6, 14]. In Kano series [20,21] haemorrhage rate is 76% and 85%, Kiran [6] reports 81% of bleeding at diagnosis. In our study 88.7% of patients bled one to many times before treatment this rate is well above the 64% of Potts [28, 27].
The treatment of cerebral malformations in functional and deep locations, particularly in thalamus, is difficult and remains as a challenge [10, 27, 28]. Radiosurgery is less risky than microsurgery in these locations [8,12, 23] but requires a latent period of several years. A combined strategy of surgery followed by radiosurgery in case of residue can also be considered [28]. Potts [26] propose in first intention surgery by a trans-sylvian approach for young patients with ruptured basal ganglia AVM, nidus sizes higher than 3cm and carrying a neurological deficit to reduce initially the lesion volume and secondarily perform a radiosurgery wich will allow an obliteration rate of 78% against 71% and 23% for each technique. Gross [29] indicate that surgery still remain as a treatment of choice for thalamus and basal ganglia AVM allowing a complete nidus resection in 91% of patients with 2.4% mortality.
In all published series for deep located AVM, the rate of complete obliteration with embolization only does not exceed 15% [17,19] with a morbidity than can reach 40%. In the management strategy of these AVM, embolization can help sometimes to reduce the volume of the nidus, slow down the flow; it is then necessary to complete the treatment with radiosurgery in order to increase the chances of obliteration [6, 7, 22, 23]. The inconvenient can be difficulties to visualise the nidus hided by embolization product (Onyx), resulting in under-covering some area of the AVM and reducing the obliteration rate.Oermann [32] in his case-control study, reported that prior embolization reduce the risk of radiosurgery-induced complications (haemorrhage latency period and radio-induced effects) by decreasing of the angiostructural complexity.It is preferable in case of small-volume AVM to propose radiosurgery in first intention even if embolization is partially possible [16, 22, 30, 31].
The post-radiosurgery obliteration percentage for brainstem, basal ganglia and thalamus AVM after a procedure varies from 23 to 70% according to literature data. At 3 years following Potts [27] noted 23% of complete obliteration in 42 patients treated only by radiosurgery, this percentage rise to 45% at 5 years and 63% after a 2nd procedure. Kurita [16] reported in his series of 27 patients, a total obliteration rate of 44% while Massager and al. [18] had a rate of 52% at 3 years. Kano [21] in his series of 67 brainstem AVM reports a rate of 41%, 70% and 76% at 3, 5 and 10 years respectively after the first treatment based to MRI data. Pollock [23] reported total obliteration rate of 43 % for basal ganglia (10 cases), thalamus (30 cases) and brainstem (16 cases) AVM after 45 months of follow-up. This percentage for complete obliteration confirmed by MRI or associated arteriography after one or more procedures was 47% and 66% at 3 and 4 years, respectively.
These variations of obliteration rate seem to be at their maximum after 5 years, in fact the obliteration rate in AVM series of thalamus and basal ganglia was 57%, 70%, 72% and 72% at 3, 5, 7 and 10 years respectively on MRI criteria. Kano [9] and Koga [22] report an obliteration rate of 81% at 5 years. In our series, the overall rate of obliteration was 66.7% for followed patients, this rate is comparable to most studies in the literature. This rate could be improved by a lower rate of embolization : 26.4% in our work against 3% and 18% in both Kano series [20,21]), yet embolization is a factor wich can reduce the occlusion rate after radiosurgery [17]. The other treatment parameters as well as the characteristics of the malformation were almost similar.
Low RBAS score lower than 1.5 is recognized by all authors as being the main factor which can influence complete occlusion of the nidus in all possible locations [14, 20, 22, 25].In Our study the RBAS < 2 gives a good rate obliteration 66.7%.
Ding and al. in his series about Grade III supra and infra tentorial AVM [14] had found 69% of complete occlusion in one procedure with a low RBAS≤1.5.
The prescribed dose for optimal efficiency is theoretically 24 Gy, however in functional area and depending on the AVM volume, the prescription is modulated downward to reduce the risk of radiation-induced effect. That explain the lower limits of prescription in our series also found in the series of Kano which had an average dose of 20 Gy (14-25.6) and 17 Gy (15-20) in the series of Potts [24]. For Kano [20,21] a dose superior or equal to 17Gy would be sufficient to occlude a profound AVM.
The haemorrhagic risk after radiosurgical treatment is variable according to the series 1.3-9.5%. In our series, the percentage of haemorrhage was 5.8% at the last follow-up (3.9 % at the first year and 1.9% at second year). It should be noted, however, that the risk is mainly present during the first 2 years, as long as the AVM is not occluded. The onset delay of bleeding is variable most authors report early onset before the occlusion of the malformation. Kano and al. [20,21] report that the risk of bleeding still exist as long as the malformation is not obliterated even if the risk is higher the two years following the treatment. Potts and al. [28] found 3.9% of rebleeding after radiosurgery in his series and a mortality rate of 4%. Against 1.9% of haemorrhagic risk with a mortality of 4.5% [21].
Radiosurgical treatment despite proven tolerance by most authors is sometimes a source of complications as radiation-induced effects. Flickinger [33] reports that patients with deep located AVM (thalamus, posterior fossa) were more likely to develop radiation-induced effects than in other locations with a susceptibility coefficient of 8.33 for the posterior fossa while 2.35 for the frontal region. Massager [16] reports that this risk of developing transient or permanent radiation-induced phenomena was of 5%. The risk of permanent secondary injuries related to treatment of basal ganglia and brainstem AVM ranges from 4 to 11.9% depending on the series [10, 17, 20,21-23,34]. These effects are correlated with a high dose according to Flickinger [33], in his opinion a treatment dose superior to 12Gy is source of complications whereas for Pollock [24,25] the effective dose would be around 18Gy, beyond 20Gy the risk of radiation-induced effects is increased. Our data are consistent with those of literature as we find a radio-induced effects risk of 3.9%. In our study the risk of radiation-induced effects was mainly related to the high treatment volume p = 0.0301, the mean treatment volume of the two patients with radiation-induced effects was 7.9 cm3 at the second treatment. Cysts at the level of the irradiated areas are often found after radiosurgical treatment and are most often asymptomatic Pollock [24,25].
Conclusion
Radiosurgery has become indispensable in the treatment of thalamic and basal ganglia malformations because of the difficulties and risks of microsurgical treatment, even if there is a persistent risk of bleeding until the cure, (5.9% of haemorrhage after procedure). The complete obliteration rate is 66.7% confirmed by arteriography to 88%. Despite its apparent harmless, radiosurgery sometimes has radiation-induced effects (3.9%) with deficits that may be transient or permanent. The mortality rate is 1.9% after the procedure most often related to rebleeding.
Abbreviations
AVM: Arteriovenous malformation
RBAS: radiosurgery based AVM score
MRI: magnetic resonance imaging
SRS: stereotactic radiosurgery
Acknowledgments
Authors’ disclosure of potential conflicts of interest
The authors have nothing to disclose.
Author contributions
Conception and design: Mohameth Faye, Manal Sghiouar
Data collection: Mohameth Faye, Moussa Diallo, El Hadji Cheikh Ndiaye Sy
Data and analysis of interpretation: Mohameth Faye, Pierre Yves Borius
Manuscript writing: Mohameth Faye, Manal Sghiouar
Final approval of manuscript: Pierre Yves Borius, Jean-Marie Régis
References
- 1. ApSimon HT, Reef H, Phadke RV, Popovic EA. A population-based study of brain arteriovenous malformation: long-term treatment outcomes. Stroke 2002;33:794–800. [DOI] [PubMed] [Google Scholar]
- 2. Doppman JL. The nidus concept of spinal cord arteriovenous malformations. A surgical recommendation based upon angiographic observations. J Br Radiol. 1971;44:758–63. [DOI] [PubMed] [Google Scholar]
- 3. Ondra SL, Troupp H, George ED, Schawab K. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 1990;73:387–91. [DOI] [PubMed] [Google Scholar]
- 4. Perret G, Nishioka H. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg. 1966;25(4):467–490. [DOI] [PubMed] [Google Scholar]
- 5. Stapf C, Mohr JP, Pile-Spellman J, Solomon RA, Sacco RL, Connolly ES. Epidemiology and natural history of arteriovenous malformations. Neurosurg Focus. 2001;11(5):1-5. [DOI] [PubMed] [Google Scholar]
- 6. Kiran NA, Kale SS, Kasliwal MK, Vaishya S, Gupta A, Singh Sharma M, Shankar Sharma B, Kumar Mahapatra A. Gamma Knife radiosurgery for arteriovenous malformations of basal ganglia, thalamus and brainstem — A retrospective study comparing the results with that for AVMs at other intracranial locations. Acta Neurochir (Wien). 2009;151:1575–1582. [DOI] [PubMed] [Google Scholar]
- 7. Cohen-Inbar O, Ding D, Chen CJ, Sheehan JP. Stereotactic radiosurgery for deep intracranial arteriovenous malformations, Part 1: Brainstem arteriovenous malformations. J Clin Neurosci. 2016;24:30-36. [DOI] [PubMed] [Google Scholar]
- 8. Cohen-Inbar O, Ding D, Chen CJ, Sheehan JP. Stereotactic radiosurgery for deep intracranial arteriovenous malformations, Part 2: Basal ganglia end thalamus arteriovenous malformations. J Clin Neurosci. 2016;24:37-42. [DOI] [PubMed] [Google Scholar]
- 9. Nozaki K, Hashimoto N, Kikuta K, Takagi Y, Kikuchi H: Surgical applications to arteriovenous malformations involving the brainstem. Neurosurgery.2006;58(4 Suppl 2):ONS-270–ONS-279. [DOI] [PubMed] [Google Scholar]
- 10. Solomon RA, Stein BM: Management of arteriovenous malformations of the brain stem. J Neurosurg, 1986;64:857–864. [DOI] [PubMed] [Google Scholar]
- 11. Yaşargil MG. (ed). Infratentorial (central) AVMs. In: Microneurosurgery, Vol IIIB, pp 358–361. Stuttgart: Thieme, 1987. [Google Scholar]
- 12. Lawton MT, Hamilton MG, Spetzler RF: Multimodality treatment of deep arteriovenous malformations: thalamus, basal ganglia, and brain stem. Neurosurgery 37:29–36, 1995, 15. [DOI] [PubMed] [Google Scholar]
- 13. Fleetwood IG, Marcellus ML, Levy RP, Marks MP, Steinberg GK. Deep arteriovenous malformations of the basal ganglia and thalamus: natural history. J Neurosurg. 2003;98(4):747–750. [DOI] [PubMed] [Google Scholar]
- 14. Ding D, Yen CP, Starke RM, Xu Z, Sun X, Sheehan JP. Radiosurgery for Spetzler-Martin Grade III arteriovenous malformations. Neurosurg 2014;120:959–969. [DOI] [PubMed] [Google Scholar]
- 15. Sasaki T, Kurita H, Saito I, Kawamoto S, Nemoto S, Terahara A, Kirino T, Takakura K. Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101cases. J Neurosurg. 1998;88(2):285–292. [DOI] [PubMed] [Google Scholar]
- 16. Kurita H, Kawamoto S, Sasaki T, Shin M, Tago M, Terahara A, Ueki K, Kirino T. Results of radiosurgery for brain stem arteriovenous malformations. J Neurol Neurosurg Psychiatry 2000;68:563–570. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Maruyama K, Kondziolka D, Niranjan A, Flickinger JC, Lunsford LD: Stereotactic radiosurgery for brainstem arteriovenous malformations: factors affecting outcome. J Neurosurg, 2004;100:407–413. [DOI] [PubMed] [Google Scholar]
- 18. Massager N, Régis J, Kondziolka D, Njee T, Levivier M. Gamma Knife radiosurgery for brainstem arteriovenous malformations: Preliminary results. J Neurosurg 1993;(Suppl 3):102–103. [DOI] [PubMed] [Google Scholar]
- 19. Hurst RW, Berenstein A, Kupersmith MJ, Madrid M, Flamm ES: Deep central arteriovenous malformations of the brain: the role of endovascular treatment. J Neurosurg. 1995;82:190–195. [DOI] [PubMed] [Google Scholar]
- 20. Kano H, Kondziolka D, Flickinger JC, Yang HC, Flannery TJ, Niranjan A, Novotny J, Jr, Lunsford LD. Stereotactic radiosurgery for arteriovenous malformations, Part 4: Management of basal ganglia and thalamus arteriovenous malformations. Clinical article. J Neurosurg 2012;116:71- 75. [DOI] [PubMed] [Google Scholar]
- 21. Kano H, Kondziolka D, Flickinger JC, Yang HC, Flannery TJ, Niranjan A, Novotny MJ, Jr, Lunsford LD. Stereotactic radiosurgery for arteriovenous malformations, Part 5 : Management of brainstem arteriovenousmal formations J Neurosurg 2012;116:44–53. World Neurosurg. 2014;82(0):386–394. doi: 10.1016/j.wneu.2014.03.0 [DOI] [PubMed] [Google Scholar]
- 22. Koga T, Shin M, Maruyama K, Terahara A, Saito N. Long term outcomes of stereotactic radiosurgery for arteriovenous malformations in the thalamus. Neurosurgery 2010;67:398–403. [DOI] [PubMed] [Google Scholar]
- 23. Pollock BE, Gorman DA, Brown PD. Radiosurgery for arteriovenous malformations of the basal ganglia, thalamus, and brainstem. J Neurosurg. 2004;100(2):210–214. [DOI] [PubMed] [Google Scholar]
- 24. Pollock BE, Brown RD., Jr Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations. Neurosurgery. 2001;49:259–265. [DOI] [PubMed] [Google Scholar]
- 25. Pollock BE, Flickinger JC. Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery. 2008;63(2):239–243. [PubMed: 18797353] [DOI] [PubMed] [Google Scholar]
- 26. Potts MB, Chang EF, Young WL, Lawton MT. UCSF Brain AVM Study Project. Trans sylvian transinsular approaches to the insula and basal ganglia: Operative techniques and results with vascular lesions. Neurosurgery. 2012;70(4):824–834. discussion 834 [PubMed: 21937930] [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Potts MB, Young WL, Lawton MT, for the UCSF Brain AVM Study Project. Deep arteriovenous malformations in the basal ganglia, thalamus, and insula: Microsurgical management, techniques, and results. World Neurosurgery. 2014;82(0):386-394. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Potts MB, Jahangiri A, Jen M, Sneed PK, McDermott MW, Gupta N, Hetts SW, Young WL, Lawton MT. Deep arteriovenous malformations in the basal ganglia, thalamus, and insula: Multimodality management, patient selection and results. World Neurosurg. 2014;82(0):386–394. doi:10.1016/j.wneu.2014.03.033 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Gross BA, Duckworth EAM, Getch CC, Bendok BR, Batjer HH. Challenging traditional beliefs: Microsurgery for arteriovenous malformations of the basal ganglia and thalamus. Neurosurgery. 2008;63(3):393–410. discussion 410–1. [DOI] [PubMed] [Google Scholar]
- 30. Nagy G, Major O, Rowe JG, Radatz MWR, Hodgson TJ, Coley SC, Kemeny AA. Stereotactic radiosurgery for arteriovenous malformations located in deep critical regions. Neurosurgery. 2012;70(6):1458-1471. [DOI] [PubMed] [Google Scholar]
- 31. Nicolato A, Foroni R, Crocco A, Zampieri PG, Alessandrini F, Bricolo A, Gerosa MA. Gamma Knife radiosurgery in the management of arteriovenous malformations of the basal ganglia region of the brain. Minim Invasive Neurosurg. 2002;45(4):211–223. [DOI] [PubMed] [Google Scholar]
- 32. Oermann EK, Ding D, Yen CP, Starke RM, Bederson JB, Kondziolka D, Sheehan JP. Effect of prior embolization on cerebral AVM radiosurgery outcomes: A case-control study. Neurosurgery. 2015;77(3):406-417. [DOI] [PubMed] [Google Scholar]
- 33. Flickinger JC, Kondziolka D, Maitz AH, Lunsford LD. An analysis of the dose-response for arteriovenous malformation radiosurgery and other factors affecting obliteration. Radiother Oncol. 2002;63(3):347–354. [DOI] [PubMed] [Google Scholar]
- 34. Andrade-Souza YM, Zadeh G, Scora D, Tsao MN, Schwartz ML. Radiosurgery for basal ganglia, internal capsule, and thalamus arteriovenous malformation: Clinical outcome. Neurosurgery. 2005;56(1):56–63. [DOI] [PubMed] [Google Scholar]