Object.Radiosurgery has been widely adopted for the treatment of cerebral arteriovenous malformations (AVMs) in which the practical endpoint is angiographic evidence of obliteration, presumed to be consistent with elimination of the risk of hemorrhage. To test this unverified assumption, the authors followed 236 radiosurgery-treated AVMs between 1 and 133 months (median 77 months) after angiographic evidence of obliteration.
Methods.Four patients experienced hemorrhage between 16 and 51 months after angiographic confirmation of AVM obliteration, and two underwent resection. The histological findings in these patients showed occlusion of the AVM by thickening of the intimal layer with dense hyalinization as well as a small amount of residual AVM vessels and a tiny vasculature. The risks of hemorrhage from these presumaby obliterated AVMs were 0.3% for the annual bleeding risk and 2.2% for the cumulative risk over 10 years. Continuous enhancement of the nidus on computerized tomography (CT) or magnetic resonance (MR) imaging was the only significant factor positively associated with hemorrhage in the statistical analysis (p = 0.0212).
Conclusions.Because the study was based on limited follow-up data, its significance for defining predictive features of hemorrhage after angiographic evidence of obliteration is still indeterminable. Nevertheless, disappearance of the AVM on angiography after radiosurgery does not always indicate total elimination of the disease, especially when CT or MR imaging continues to demonstrate an enhancing lesion. The authors therefore recommend continual follow up even after evidence of AVM obliteration on angiography.
Address reprint requests to:Masahiro Shin, M.D., Ph.D., Department of Neurosurgery, University of Tokyo Hospital, 7–3–1 Hongo, Bunkyo-ku, Tokyo, 113–8655, Japan. email:shinmasa@ka2.so-net.ne.jp.
Del CurlingOJr,,KellyDLJr,,ElsterAD,&CravenTE:An analysis of the natural history of cavernous angiomas.J Neurosurg75:702–708,1991Del Curling O Jr, Kelly DL Jr, Elster AD, Craven TE: An analysis of the natural history of cavernous angiomas.J Neurosurg 75:702–708, 1991
Del Curling
O
Jr
,
Kelly
DL
Jr
,
Elster
AD
,
Craven
TE
:
An analysis of the natural history of cavernous angiomas.J Neurosurg
75
:
702
–
708
,
1991
Del Curling O Jr, Kelly DL Jr, Elster AD, Craven TE: An analysis of the natural history of cavernous angiomas.
J Neurosurg 75:702–708, 1991
10.3171/jns.1991.75.5.0702)| false
HartmannA,,StapfC,,HofmeisterC,,MohrJP,,SciaccaRR,&SteinBM,et al:Determinants of neurological outcome after surgery for brain arteriovenous malformation.Stroke31:2361–2364,2000Hartmann A, Stapf C, Hofmeister C, Mohr JP, Sciacca RR, Stein BM, et al: Determinants of neurological outcome after surgery for brain arteriovenous malformation.Stroke 31:2361–2364, 2000
Hartmann
A
,
Stapf
C
,
Hofmeister
C
,
Mohr
JP
,
Sciacca
RR
,
Stein
BM
,
et al
:
Determinants of neurological outcome after surgery for brain arteriovenous malformation.Stroke
31
:
2361
–
2364
,
2000
Hartmann A, Stapf C, Hofmeister C, Mohr JP, Sciacca RR, Stein BM, et al: Determinants of neurological outcome after surgery for brain arteriovenous malformation.
Stroke 31:2361–2364, 2000
10.1161/01.STR.31.10.2361)| false
KadotaO,,SakakiS,,KumonY,,OhtaS,&KohnoK:Large cystic cavernous angioma of the cerebellum—case report.Neurol Med Chir34:768–772,1994Kadota O, Sakaki S, Kumon Y, Ohta S, Kohno K: Large cystic cavernous angioma of the cerebellum—case report.Neurol Med Chir 34:768–772, 1994
Kadota
O
,
Sakaki
S
,
Kumon
Y
,
Ohta
S
,
Kohno
K
:
Large cystic cavernous angioma of the cerebellum—case report.Neurol Med Chir
34
:
768
–
772
,
1994
Kadota O, Sakaki S, Kumon Y, Ohta S, Kohno K: Large cystic cavernous angioma of the cerebellum—case report.
Neurol Med Chir 34:768–772, 1994
10.2176/nmc.34.768)| false
KihlströmL,,GuoWY,,KarlssonB,,LindqvistC,&LindquistM:Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery.J Neurosurg86:589–593,1997Kihlström L, Guo WY, Karlsson B, Lindqvist C, Lindquist M: Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery.J Neurosurg 86:589–593, 1997
Kihlström
L
,
Guo
WY
,
Karlsson
B
,
Lindqvist
C
,
Lindquist
M
:
Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery.J Neurosurg
86
:
589
–
593
,
1997
Kihlström L, Guo WY, Karlsson B, Lindqvist C, Lindquist M: Magnetic resonance imaging of obliterated arteriovenous malformations up to 23 years after radiosurgery.
J Neurosurg 86:589–593, 1997
10.3171/jns.1997.86.4.0589)| false
KondziolkaD,,LunsfordLD,&KestleJR:The natural history of cerebral cavernous malformations.J Neurosurg83:820–824,1995Kondziolka D, Lunsford LD, Kestle JR: The natural history of cerebral cavernous malformations.J Neurosurg 83:820–824, 1995
KuritaH,,KawamotoS,,SasakiT,,ShinM,,TagoM,&TaraharaA,et al:Results of radiosurgery for brain stem arteriovenous malformations.J Neurol Neurosurg Psychiatry68:563–570,2000Kurita H, Kawamoto S, Sasaki T, Shin M, Tago M, Tarahara A, et al: Results of radiosurgery for brain stem arteriovenous malformations.J Neurol Neurosurg Psychiatry 68:563–570, 2000
Kurita
H
,
Kawamoto
S
,
Sasaki
T
,
Shin
M
,
Tago
M
,
Tarahara
A
,
et al
:
Results of radiosurgery for brain stem arteriovenous malformations.J Neurol Neurosurg Psychiatry
68
:
563
–
570
,
2000
Kurita H, Kawamoto S, Sasaki T, Shin M, Tago M, Tarahara A, et al: Results of radiosurgery for brain stem arteriovenous malformations.
J Neurol Neurosurg Psychiatry 68:563–570, 2000
10.1136/jnnp.68.5.563)| false
Levy
EI
,
Niranjan
A
,
Thompson
TP
,
Scarrow
AM
,
Kondziolka
D
,
Flickinger
JC
,
et al
:
Radiosurgery for childhood intracranial arteriovenous malformations.开云体育app官方网站下载入口
47
:
834
–
842
,
2000
Levy EI, Niranjan A, Thompson TP, Scarrow AM, Kondziolka D, Flickinger JC, et al: Radiosurgery for childhood intracranial arteriovenous malformations.
Neurosurgery 47:834–842, 2000
10.1097/00006123-200010000-00008)| false
LindqvistM,,KarlssonB,,GuoWY,,KihlströmL,,LippitzB,&YamamotoM:Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery.开云体育app官方网站下载入口46:803–810,2000Lindqvist M, Karlsson B, Guo WY, Kihlström L, Lippitz B, Yamamoto M: Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery.Neurosurgery 46:803–810, 2000
Lindqvist
M
,
Karlsson
B
,
Guo
WY
,
Kihlström
L
,
Lippitz
B
,
Yamamoto
M
:
Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery.开云体育app官方网站下载入口
46
:
803
–
810
,
2000
Lindqvist M, Karlsson B, Guo WY, Kihlström L, Lippitz B, Yamamoto M: Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery.
Neurosurgery 46:803–810, 2000)| false
LunsfordLD,,KondziolkaD,,FlickingerJC,,BissonetteDJ,,JungreisCA,&MaitzAH,et al:立体定向放射治疗动静脉malformations of the brain.J Neurosurg75:512–524,1991Lunsford LD, Kondziolka D, Flickinger JC, Bissonette DJ, Jungreis CA, Maitz AH, et al: Stereotactic radiosurgery for arteriovenous malformations of the brain.J Neurosurg 75:512–524, 1991
MastH,,YoungWL,,KoenneckeHC,,SciaccaRR,,OsipovA,&Pile-SpellmenJ,et al:Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation.Lancet350:1065–1068,1997Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellmen J, et al: Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation.Lancet 350:1065–1068, 1997
Mast
H
,
Young
WL
,
Koennecke
HC
,
Sciacca
RR
,
Osipov
A
,
Pile-Spellmen
J
,
et al
:
Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation.Lancet
350
:
1065
–
1068
,
1997
Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellmen J, et al: Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation.
Lancet 350:1065–1068, 1997
10.1016/S0140-6736(97)05390-7)| false
OgilvyCS,,StiegPE,,AwadI,,BrownRDJr,,KondziolkaD,&RosenwasserR,et al: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.Stroke32:1458–1471,2001Ogilvy CS, Stieg PE, Awad I, Brown RD Jr, Kondziolka D, Rosenwasser R, et al: 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 32:1458–1471, 2001
Ogilvy
CS
,
Stieg
PE
,
Awad
I
,
Brown
RD
Jr
,
Kondziolka
D
,
Rosenwasser
R
,
et al
:
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
:
1458
–
1471
,
2001
Ogilvy CS, Stieg PE, Awad I, Brown RD Jr, Kondziolka D, Rosenwasser R, et al: 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 32:1458–1471, 2001
10.1161/01.STR.32.6.1458)| false
OndraSK,,TrouppH,,GeorgeED,&SchwabK:The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment.J Neurosurg73:387–391,1990Ondra SK, Troupp H, George ED, Schwab K: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment.J Neurosurg 73:387–391, 1990
Ondra
SK
,
Troupp
H
,
George
ED
,
Schwab
K
:
The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment.J Neurosurg
73
:
387
–
391
,
1990
Ondra SK, Troupp H, George ED, Schwab K: The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment.
J Neurosurg 73:387–391, 1990
10.3171/jns.1990.73.3.0387)| false
PikJHT,&MorganMK:Microsurgery for small arteriovenous malformations of the brain: results in 110 consecutive patients.开云体育app官方网站下载入口47:571–577,2000Pik JHT, Morgan MK: Microsurgery for small arteriovenous malformations of the brain: results in 110 consecutive patients.Neurosurgery 47:571–577, 2000
Pik
JHT
,
Morgan
MK
:
Microsurgery for small arteriovenous malformations of the brain: results in 110 consecutive patients.开云体育app官方网站下载入口
47
:
571
–
577
,
2000
Pik JHT, Morgan MK: Microsurgery for small arteriovenous malformations of the brain: results in 110 consecutive patients.
Neurosurgery 47:571–577, 2000)| false
PollockBE,&BrownRDJr:Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations.开云体育app官方网站下载入口49:259–265,2001Pollock BE, Brown RD Jr: Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations.Neurosurgery 49:259–265, 2001
Pollock
BE
,
Brown
RD
Jr
:
Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations.开云体育app官方网站下载入口
49
:
259
–
265
,
2001
Pollock BE, Brown RD Jr: Management of cysts arising after radiosurgery to treat intracranial arteriovenous malformations.
Neurosurgery 49:259–265, 2001)| false
RivaD,,PantaleoniC,,DevotiM,,LindquistC,,SteinerL,&GiorgiC:Radiosurgery for cerebral AVMs in children and adolescents: the neurobehavioral outcome.J Neurosurg86:207–210,1997莉娃D, Pantaleoni C, Devoti M,林奎斯特C,斯坦er L, Giorgi C: Radiosurgery for cerebral AVMs in children and adolescents: the neurobehavioral outcome.J Neurosurg 86:207–210, 1997
Riva
D
,
Pantaleoni
C
,
Devoti
M
,
Lindquist
C
,
Steiner
L
,
Giorgi
C
:
Radiosurgery for cerebral AVMs in children and adolescents: the neurobehavioral outcome.J Neurosurg
86
:
207
–
210
,
1997
莉娃D, Pantaleoni C, Devoti M,林奎斯特C,斯坦er L, Giorgi C: Radiosurgery for cerebral AVMs in children and adolescents: the neurobehavioral outcome.
J Neurosurg 86:207–210, 1997
10.3171/jns.1997.86.2.0207)| false
SasakiT,,KuritaH,,SaitoI,,KawamotoS,,NemotoS,&TeraharaA,et al:Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases.J Neurosurg88:285–292,1998Sasaki T, Kurita H, Saito I, Kawamoto S, Nemoto S, Terahara A, et al: Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases.J Neurosurg 88:285–292, 1998
Sasaki
T
,
Kurita
H
,
Saito
I
,
Kawamoto
S
,
Nemoto
S
,
Terahara
A
,
et al
:
Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases.J Neurosurg
88
:
285
–
292
,
1998
Sasaki T, Kurita H, Saito I, Kawamoto S, Nemoto S, Terahara A, et al: Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases.
J Neurosurg 88:285–292, 1998
10.3171/jns.1998.88.2.0285)| false
ShinM,,MaruyamaK,,KuritaH,,KawamotoS,,TagoM,&TeraharaA,et al:Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience.J Neurosurg101:18–24,2004Shin M, Maruyama K, Kurita H, Kawamoto S, Tago M, Terahara A, et al: Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience.J Neurosurg 101:18–24, 2004
Shin
M
,
Maruyama
K
,
Kurita
H
,
Kawamoto
S
,
Tago
M
,
Terahara
A
,
et al
:
Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience.J Neurosurg
101
:
18
–
24
,
2004
Shin M, Maruyama K, Kurita H, Kawamoto S, Tago M, Terahara A, et al: Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience.
J Neurosurg 101:18–24, 2004
10.3171/jns.2004.101.1.0018)| false
SiddiquiAA,&JoomaR:Neoplastic growth of cerebral cavernous malformation presenting with impending cerebral herniation: a case report and review of the literature on de novo growth of cavernomas.Surg Neurol56:42–45,2001Siddiqui AA, Jooma R: Neoplastic growth of cerebral cavernous malformation presenting with impending cerebral herniation: a case report and review of the literature on de novo growth of cavernomas.Surg Neurol 56:42–45, 2001
Siddiqui
AA
,
Jooma
R
:
Neoplastic growth of cerebral cavernous malformation presenting with impending cerebral herniation: a case report and review of the literature on de novo growth of cavernomas.Surg Neurol
56
:
42
–
45
,
2001
Siddiqui AA, Jooma R: Neoplastic growth of cerebral cavernous malformation presenting with impending cerebral herniation: a case report and review of the literature on de novo growth of cavernomas.
Surg Neurol 56:42–45, 2001
10.1016/S0090-3019(01)00505-5)| false
SpetzlerRF,&MartinNA:A proposed grading system for arteriovenous malformations.J Neurosurg65:476–483,1986Spetzler RF, Martin NA: A proposed grading system for arteriovenous malformations.J Neurosurg 65:476–483, 1986
Spetzler
RF
,
Martin
NA
:
A proposed grading system for arteriovenous malformations.J Neurosurg
65
:
476
–
483
,
1986
Spetzler RF, Martin NA: A proposed grading system for arteriovenous malformations.
J Neurosurg 65:476–483, 1986
10.3171/jns.1986.65.4.0476)| false
TomlinsonFH,,HouserOW,,ScheithauerBW,,SundtTMJr,,OkazakiH,&ParisiJE:Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination.开云体育app官方网站下载入口34:792–799,1994Tomlinson FH, Houser OW, Scheithauer BW, Sundt TM Jr, Okazaki H, Parisi JE: Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination.Neurosurgery 34:792–799, 1994
Tomlinson
FH
,
Houser
OW
,
Scheithauer
BW
,
Sundt
TM
Jr
,
Okazaki
H
,
Parisi
JE
:
Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination.开云体育app官方网站下载入口
34
:
792
–
799
,
1994
Tomlinson FH, Houser OW, Scheithauer BW, Sundt TM Jr, Okazaki H, Parisi JE: Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination.
Neurosurgery 34:792–799, 1994)| false
YamamotoM,,IdeM,,JimboM,,TakakuraK,,LindquistC,&SteinerL:Neuroimaging studies of postobliteration nidus changes in cerebral arteriovenous malformations treated by gamma knife radiosurgery.Surg Neurol45:110–122,1996Yamamoto M, Ide M, Jimbo M, Takakura K, Lindquist C, Steiner L: Neuroimaging studies of postobliteration nidus changes in cerebral arteriovenous malformations treated by gamma knife radiosurgery.Surg Neurol 45:110–122, 1996
Yamamoto
M
,
Ide
M
,
Jimbo
M
,
Takakura
K
,
Lindquist
C
,
Steiner
L
:
Neuroimaging studies of postobliteration nidus changes in cerebral arteriovenous malformations treated by gamma knife radiosurgery.Surg Neurol
45
:
110
–
122
,
1996
Yamamoto M, Ide M, Jimbo M, Takakura K, Lindquist C, Steiner L: Neuroimaging studies of postobliteration nidus changes in cerebral arteriovenous malformations treated by gamma knife radiosurgery.
Surg Neurol 45:110–122, 1996
10.1016/S0090-3019(96)80003-6)| false
YamamotoM,,JimboM,,KobayashiM,,ToyodaC,,IdeM,&TanakaN,et al:Long-term results of radiosurgery for arteriovenous malformation: neurodiagnostic imaging and histological studies of angiographically confirmed nidus obliteration.Surg Neurol37:219–230,1992山本M,吉伯M,小林M,丰田章男C, Ide M,Tanaka N, et al: Long-term results of radiosurgery for arteriovenous malformation: neurodiagnostic imaging and histological studies of angiographically confirmed nidus obliteration.Surg Neurol 37:219–230, 1992
Yamamoto
M
,
Jimbo
M
,
Kobayashi
M
,
Toyoda
C
,
Ide
M
,
Tanaka
N
,
et al
:
Long-term results of radiosurgery for arteriovenous malformation: neurodiagnostic imaging and histological studies of angiographically confirmed nidus obliteration.Surg Neurol
37
:
219
–
230
,
1992
山本M,吉伯M,小林M,丰田章男C, Ide M,Tanaka N, et al: Long-term results of radiosurgery for arteriovenous malformation: neurodiagnostic imaging and histological studies of angiographically confirmed nidus obliteration.
Surg Neurol 37:219–230, 1992
10.1016/0090-3019(92)90235-F)| false
