Stereotactic radiosurgery for arteriovenous malformations, Part 3: outcome predictors and risks after repeat radiosurgery

Clinical article

Restricted access

Object

The object of this study was to evaluate the outcomes and risks of repeat stereotactic radiosurgery (SRS) for incompletely obliterated cerebral arteriovenous malformations (AVMs).

Methods

Between 1987 and 2006, Gamma Knife surgery was performed in 996 patients with AVMs. During this period, repeat SRS was performed in 105 patients who had incompletely obliterated AVMs at a median of 40.9 months after initial SRS (range 27.5–139 months). The median AVM target volume was 6.4 cm3 (range 0.2–26.3 cm3) at initial SRS but was reduced to 2.3 cm3 (range 0.1–18.2 cm3) at the time of the second procedure. The median margin dose at both initial SRS and repeat SRS was 18 Gy.

Results

The actuarial rate of total obliteration by angiography or MR imaging after repeat SRS was 35%, 68%, 77%, and 80% at 3, 4, 5, and 10 years, respectively. The median time to complete angiographic or MR imaging obliteration after repeat SRS was 39 months. Factors associated with a higher rate of AVM obliteration were smaller residual AVM target volume (p = 0.038) and a volume reduction of 50% or more after the initial procedure (p = 0.014). Seven patients (7%) had a hemorrhage in the interval between initial SRS and repeat SRS. Seventeen patients (16%) had hemorrhage after repeat SRS and 6 patients died. The cumulative actuarial rates of new AVM hemorrhage after repeat SRS were 1.9%, 8.1%, 10.1%, 10.1%, and 22.4% at 1, 2, 3, 5, and 10 years, respectively, which translate to annual hemorrhage rates of 4.05% and 1.79% of patients developing new post–repeat-SRS hemorrhages per year for Years 0–2 and 2–10 following repeat SRS. Factors associated with a higher risk of hemorrhage after repeat SRS were a greater number of prior hemorrhages (p = 0.008), larger AVM target volume at initial SRS (p = 0.010), larger target volume at repeat SRS (p = 0.002), initial AVM volume reduction less than 50% (p = 0.019), and a higher Pollock-Flickinger score (p = 0.010). Symptomatic adverse radiation effects developed in 5 patients (4.8%) after initial SRS and in 10 patients (9.5%) after repeat SRS. Prior embolization (p = 0.022) and a higher Spetzler-Martin grade (p = 0.004) were significantly associated with higher rates of adverse radiation effects after repeat SRS. Delayed cyst formation occurred in 5 patients (4.8%) at a median of 108 months after repeat SRS (range 47–184 months).

Conclusions

Repeat SRS for incompletely obliterated AVMs increases the eventual obliteration rate. Hemorrhage after obliteration did not occur in this series. The best results for patients with incompletely obliterated AVMs were seen in patients with a smaller residual nidus volume and no prior hemorrhages.

Abbreviations used in this paper: ARE = adverse radiation effect; AVM = arteriovenous malformation; HR = hazard ratio; SRS = stereotactic radiosurgery.

Article Information

Address correspondence to: L. Dade Lunsford, M.D., Department of Neurological Surgery, University of Pittsburgh, Suite B-400, UPMC Presbyterian, 200 Lothrop Street, Pittsburgh, Pennsylvania 15213. email: lunsfordld@upmc.edu.

Please include this information when citing this paper: published online November 11, 2011; DOI: 10.3171/2011.9.JNS101741.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Upper: Kaplan-Meier curves for total obliteration as documented by MR imaging or angiography after repeat SRS for AVMs with corrected time (solid line). Uncorrected Kaplan-Meier curves for total obliteration by MR imaging or angiography after repeat radiosurgery for AVMs with uncorrected time (broken line). Lower: Kaplan-Meier curves for total obliteration by angiography alone after repeat radiosurgery for AVMs with corrected time (solid line). Uncorrected Kaplan-Meier curves for total obliteration by angiography alone after repeat radiosurgery for pediatric AVMs with uncorrected time (broken line).

  • View in gallery

    Kaplan-Meier curve for bleeding rate after repeat SRS for residual AVMs.

  • View in gallery

    Upper: Kaplan-Meier curves for total obliteration on angiography or MR imaging after repeat SRS for residual AVMs with a volume reduction rate of 50% or more versus less than 50%. A volume reduction rate of 50% or more after initial SRS was significantly associated with higher total obliteration rate on angiography or MR imaging (p = 0.014). Lower: Kaplan-Meier curves for bleeding rate after repeat SRS for residual AVMs with a volume reduction rate of 50% or more versus less than 50%. A volume reduction rate of 50% or more after initial SRS was significantly associated with lower bleeding rate (p = 0.019).

  • View in gallery

    A: Anterior and lateral carotid artery angiograms obtained in a 48-year-old man documenting the right frontal AVM with a volume of 10 cm3 at the time of SRS. The margin dose was 17 Gy. B: Anterior and lateral carotid artery angiograms obtained 43 months after initial SRS showing a residual nidus with a volume of 2.9 cm3 in the SRS field. This residual nidus was treated by the second SRS with a margin dose of 18 Gy. C: Anterior and lateral carotid artery angiograms obtained 3 years after the second SRS showing the absence of nidus.

References

1

Auger RGWiebers DO: Management of unruptured intracranial arteriovenous malformations: a decision analysis. Neurosurgery 30:5615691992

2

Brown RD JrWiebers DOForbes GO'Fallon WMPiepgras DGMarsh WR: The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68:3523571988

3

da Costa LWallace MCTer Brugge KGO'Kelly CWillinsky RATymianski M: The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke 40:1001052009

4

Firlik ADLevy EIKondziolka DYonas H: Staged volume radiosurgery followed by microsurgical resection: a novel treatment for giant cerebral arteriovenous malformations: technical case report. Neurosurgery 43:122312281998

5

Fleetwood IGSteinberg GK: Arteriovenous malformations. Lancet 359:8638732002

6

Flickinger JCKondziolka DLunsford LDKassam APhuong LKLiscak R: Development of a model to predict permanent symptomatic postradiosurgery injury for arteriovenous malformation patients. Int J Radiat Oncol Biol Phys 46:114311482000

7

Flickinger JCKondziolka DLunsford LDPollock BEYamamoto MGorman DA: A multi-institutional analysis of complication outcomes after arteriovenous malformation radiosurgery. Int J Radiat Oncol Biol Phys 44:67741999

8

Flickinger JCKondziolka DMaitz AHLunsford LD: An analysis of the dose-response for arteriovenous malformation radiosurgery and other factors affecting obliteration. Radiother Oncol 63:3473542002

9

Fournier DTerBrugge KGWillinsky RLasjaunias PMontanera W: Endovascular treatment of intracerebral arteriovenous malformations: experience in 49 cases. J Neurosurg 75:2282331991

10

Gobin YPLaurent AMerienne LSchlienger MAymard AHoudart E: Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 85:19281996

11

Graf CJPerret GETorner JC: Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58:3313371983

12

Jayaraman MVMarcellus MLHamilton SDo HMCampbell DChang SD: Neurologic complications of arteriovenous malformation embolization using liquid embolic agents. AJNR Am J Neuroradiol 29:2422462008

13

Kader AGoodrich JTSonstein WJStein BMCarmel PWMichelsen WJ: Recurrent cerebral arteriovenous malformations after negative postoperative angiograms. J Neurosurg 85:14181996

14

Karlsson BKihlström LLindquist CSteiner L: Gamma knife surgery for previously irradiated arteriovenous malformations. Neurosurgery 42:161998

15

Karlsson BLindquist CJohansson ASteiner L: Annual risk for the first hemorrhage from untreated cerebral arteriovenous malformations. Minim Invasive Neurosurg 40:40461997

16

Kihlström LGuo WYKarlsson BLindquist CLindqvist M: Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery. J Neurosurg 86:5895931997

17

Lunsford LDKondziolka DFlickinger JCBissonette DJJungreis CAMaitz AH: Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 75:5125241991

18

Maesawa SFlickinger JCKondziolka DLunsford LD: Repeated radiosurgery for incompletely obliterated arteriovenous malformations. J Neurosurg 92:9619702000

19

Maruyama KKawahara NShin MTago MKishimoto JKurita H: The risk of hemorrhage after radiosurgery for cerebral arteriovenous malformations. N Engl J Med 352:1461532005

20

Maruyama KShin MTago MKishimoto JMorita AKawahara N: Radiosurgery to reduce the risk of first hemorrhage from brain arteriovenous malformations. Neurosurgery 60:4534592007

21

Ogilvy CSStieg PEAwad IBrown RD JrKondziolka DRosenwasser R: AHA Scientific Statement: Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Stroke 32:145814712001

22

Ogilvy CSStieg PEAwad IBrown RD JrKondziolka DRosenwasser R: Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Circulation 103:264426572001

23

Ondra SLTroupp HGeorge EDSchwab K: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:3873911990

24

Paulsen RDSteinberg GKNorbash AMMarcellus MLMarks MP: Embolization of basal ganglia and thalamic arteriovenous malformations. Neurosurgery 44:9919971999

25

Pollock BEBrown RD Jr: Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations. Neurosurgery 49:2592652001

26

Pollock BEFlickinger JC: A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79852002

27

Pollock BEFlickinger JCLunsford LDBissonette DJKondziolka D: Hemorrhage risk after stereotactic radiosurgery of cerebral arteriovenous malformations. Neurosurgery 38:6526611996

28

Pollock BEFlickinger JCLunsford LDMaitz AKondziolka D: Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 42:123912471998

29

Pollock BEKondziolka DFlickinger JCPatel AKBissonette DJLunsford LD: Magnetic resonance imaging: an accurate method to evaluate arteriovenous malformations after stereotactic radiosurgery. J Neurosurg 85:104410491996

30

Pollock BEKondziolka DLunsford LDBissonette DFlickinger JC: Repeat stereotactic radiosurgery of arteriovenous malformations: factors associated with incomplete obliteration. Neurosurgery 38:3183241996

31

Sanchez-Mejia ROMcDermott MWTan JKim HYoung WLLawton MT: Radiosurgery facilitates resection of brain arteriovenous malformations and reduces surgical morbidity. Neurosurgery 64:2312402009

32

Schlienger MNataf FLefkopoulos DMammar HMissir OMeder JF: Repeat linear accelerator radiosurgery for cerebral arteriovenous malformations. Int J Radiat Oncol Biol Phys 56:5295362003

33

Sinclair JKelly MESteinberg GK: Surgical management of posterior fossa arteriovenous malformations. Neurosurgery 58:4 Suppl 2ONS-189ONS-2012006

34

Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

35

Weber WKis BSiekmann RKuehne D: Endovascular treatment of intracranial arteriovenous malformations with onyx: technical aspects. AJNR Am J Neuroradiol 28:3713772007

36

Wegner REOysul KPollock BESirin SKondziolka DNiranjan A: A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79:114711502011

37

Williamson RKondziolka DKanaan HLunsford LDFlickinger JC: Adverse radiation effects after radiosurgery may benefit from oral vitamin E and pentoxifylline therapy: a pilot study. Stereotact Funct Neurosurg 86:3593662008

38

Yamamoto MJimbo MHara MSaito IMori K: Gamma knife radiosurgery for arteriovenous malformations: long-term follow-up results focusing on complications occurring more than 5 years after irradiation. Neurosurgery 38:9069141996

39

Yen CPJain SHaq IUJagannathan JSchlesinger DSheehan J: Repeat Gamma Knife surgery for incompletely obliterated cerebral arteriovenous malformations. Neurosurgery 67:55642010

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 14 14 14
Full Text Views 106 106 28
PDF Downloads 121 121 55
EPUB Downloads 0 0 0

PubMed

Google Scholar