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HEMODYNAMIC CHANGES AROUND CEREBRAL ARTERIOVENOUS

MALFORMATION. PATHOPHYSIOLOGY AND TREATMENT

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 Clinical
Medicine

HEMODYNAMIC CHANGES AROUND CEREBRAL

This wrong hypothesis was supported by Luschka [55] who and the blood flow is not constant but pulsatile [44]. Howev-
in fact, provided the description of two types of cerebral er, the Hagen-Poiseuile equation is applicable to vessels of

ARTERIOVENOUS MALFORMATION.
malformations: teleangiectases and cavernous tumors. The diameter of at least 100µm [26]. As the diameter of feeding
milestones for modern understanding of complex nature of arteries tends to be larger, with the mean value of 800µm

PATHOPHYSIOLOGY AND TREATMENT

TOMASZ TYKOCKI¹, MAGDALENA ŻYCHOWSKA², BOGUSŁAW KOSTKIEWICZ³
1 Department of Neurosurgery, Institute
of Psychiatry and Neurology in Warsaw
2 I Faculty of Medicine, Warsaw Medical
University
3 Department of Neurosurgery, Central
Clinical Hospital of the Ministry of the
Interior, Warsaw, Poland
Corresponding author:
Tomasz Tykocki
ttomasz@mp.pl
Department of Neurosurgery
Institute of Psychiatry and Neurology
in Warsaw
Sobieskiego 9, 02-957 Warszawa
Poland
Abstract
The management of cerebral arteriovenous malformations (AVMs) is
amongst the most advanced and challenging of neurosurgical procedures.
The main purpose of AVMs treatment is the extirpation of the lesion as it is
the only way to eliminate the risk of hemorrhage. With the progress of tre-
atment modalities, the question has arisen as to which modality should be
applied in a particular patient and whether the risk associated with the propo-
sed treatment does not outweigh the risk of hemorrhage resulting from AVM
natural history. The first step to answer the question has been to analyze the
hemodynamic properties of the nidus and factors influencing the intranidal
pressure in particular. Electrical models and computer simulations as well as
animal models have contributed to better knowledge of baseline values inclu-
ding the distribution of flow, pressure and resistance within consecutive parts
of the AVM. The next step has been to assess the effect of AVM resection or
occlusion on hemodynamics in the neighborhood of the lesion and cerebral
blood flow (CBF). ‘Normal perfusion pressure breakthrough’ and ‘occlusive
hyperemia’ after microsurgical resection, hemorrhage or ischemic events are
controversial complications but should be treated as real threats to optimize
the choice of treatment modality.
The aim of this review is to present pathophysiological basics of hemody-
namic disturbances evoked by the presence of arteriovenous malformation
and discuss hemodynamic implications of interfering within its angioarchitec-
ture by means of three commonly used treatment modalities: microsurgery,
endovascular embolization and radiosurgery.
Keywords:
arteriovenous malformations, hemodynamics, radiosurgery, microsurgery,
embolization
AVMs were the papers written by Virchov [8]. They provided
not only the anatomical issues but focus rather on patho-
physiology and hemodynamics of AVMs. The first clinical
diagnosis of a cerebral AVMs was probably made by Hoff-
mann [35] (1898), but the effective medical treatment still
has been a real challenge.
The first complete excision of a cerebral AVM was per-
formed in 1889 by the famous French surgeon Jules Emile
Pean [107] and in 1932 Olivercona [7] performed first suc-
cessful removal of AVMs. He operated on a 37-year-old man
with left cerebellar AVM. Cushing [17] and Dandy [19] pub-
lished their AVMs operative experiences in 14 and 15 cases
respectively in 1928. They reported various intraoperative
troubles, especially those resulting from massive hemor-
rhage and probably too aggressive neurosurgical approach.
Besides, those pioneers procedures couldn’t be supported
by angiography or other sophisticated brain scans. Both,
the lack of knowledge on the morphology of AVMs or its
size, location and number of draining vessels caused, that
most of the operations had a  great risk of morbidity and
mortality. However, the introduction of cerebral angiography
by Portuguese neurologist Moniz [64] in 1927 together with
the improvements in the quality of angiograms has opened
up new dimensions in the study of the morphological and
hemodynamic aspects of AVMs. Two years later, Dott [21]
presented the angiographic descriptions of AVMs for the
first time. Therefore, in the 50s and 60s of last century the
mortality ranged form o  to 10 % after AVMs resections.
Since then much more attention was paid to hemodynam-
ic changes after operations, Murphy [68] was the first who
[97], the formula can be applied to AVM feeders and is the
introduction to further calculations in artificially created
models of AVM hemodynamics. The blood flow is inversely
proportional to vascular resistance (R), which in turn can be
expressed as R=8L η/ πr4 (where L is the length of the ves-
sel, η– blood viscosity, r – inner radius of the vessel). Substi-
tuting this equation into Hagen-Poisseuille formula reveals
that Q=π ∆P r4/8L η. Assuming the flow to be proportional
to the average blood flow velocity and vessel cross section
(Q=v πr4) and substituting into the previous equation, we
get v=∆ P r4/8Lη.
Due to the lack of capillary bed in AVMs, blood flows
directly to dilated low-resistance veins, which in turn leads
to decrease in AVM resistance in relation to other cerebral
vessels [5]. Flow resistance and resistive index (RI, systolic
velocity minus diastolic velocity over systolic velocity) calcu-
lated from spectral Doppler waveforms may help distinguish
between abnormal, low-resistant AVM vessels and normal
‘en passant’ brain vessels during surgical resection of AVM,
in particular in case of small lesions and residuals [18].
While pressures in feeding arteries and draining vein sys-
tem can be measured directly using an intracranial microca-
therer [22] during superselective angiography and mean val-
ues are reported to be 70mmHg in feeding arteries,18mmHg
in draining veins of low-flow AVMs. In high-flow AVMs these
values were 40mmHg in feeding arteries and 15mmHg in
draining veins of [71], The intranidal pressure has been of
particular interest and its contribution to hemorrhage, the
most frequent AVM clinical presentation, has been studied
thoroughly [67, 24, 29]. According to Doung et al. [22], high

C
erebral arteriovenous malformations (AVMs) are
abnormal direct connections between arteries
and veins of varying caliber without capillaries
as an interposing element [62]. AVMs focus at-
tention of neurologists and neurosurgeons be-
cause of their sophisticated nature and pathophysiological
effect exerted on the hemodynamics of cerebral blood flow
(CBF). The concept of vascular steal has gained numerous
advocates and is the best proof that AVMs are not separate
independent lesions but are part of brain circulation and to-
gether with other brain vessels should be treated as a whole.
Understanding sophisticated nature of AVMs is required be-
fore choosing an optimal therapeutic method – conservative
management or invasive treatment, taking simultaneously
into consideration hemodynamic consequences of AVM
excision such as cerebral edema or hemorrhage to the ad-
jacent parts of the brain. These hemodynamic disturbanc-
es seem to be grounded either in occlusive hyperemia as
a consequence of venous obstruction or impaired autoreg-
ulatory mechanism leading to the speculated phenomenon
of ‘normal perfusion pressure breakthrough’ (NPPB) [99].
Altered autoregulation in the region of AVMs may contrib-
ute to the hyperperfusion after the obliteration or excision
of large high-flow AVMs. Prediction of hemodynamic com-
plications after AVM excision and early detection of NPPB
initial signs enables proper postoperative care [28].
The aim of this paper is to present distinctive hemody-
namic features of AVMs, describe the way AVMs influence
CBF and finally, emphasize hemodynamic disturbances af-
ter AVMs treatment with microsurgery, embolization or ra-
diosurgery.
The history of AVMs treatment
The first historical information about any vascular mal-
formation comes from the Papyrus Ebers, written in Egyp-
tioan heratic writing dated on 1550 BC [107]. This histori-
cal manuscript contains descriptions of hemorrhoids, skin
tumors, varicose veins and aneurysms. Another primary
reports about vascular abnormalities could be found in Hip-
pokrates’s, Galen’s, Celsus’s, Aetius’s, Avicenna’s papers
[107]. The breakthrough of understanding of cerebral cir-
culation were made by Malpighi [56] (1661) who discovered
capillaries, what was soon widely analysed by Harvey [32]
(1628) and Willis (1664). William Hunter [37] (1757) was the
first who presented the anatomical and hemodynamic fea-
tures of arteriovenous malformation. He introduced the term
of “anastomosis” contributing with previous description of
“erectile tumor”. In the XIX century another over 20 terms
referring to cerebral malformations were used. Rokitan-
sky [83] concluded the neoplastic origin of malformations.
reported the cerebral steal phenomenon. The continuing
technological progress and the introduction of operating
microscope, bipolar coagulation, microinstruments and
neuroanesthetic technique improved postoperative clinical
results. Spetzler and Martin [90] presented the correlation
of the surgical results to size, location, relationship to elo-
quent area and venous drainage pattern. The further thera-
peutic innovations brought the development of non-surgical
procedures. It was in 1967 when Lars Leksell [48] invented
the gamma knife at Karolinska Institute in Sweden. The first
report of an embolization of a traumatic carotico-cavernous
fistula by Brooks [8] was in 1930 and endovascular emboli-
zation of cerebral AVMS was first described by Leussenhop
and Spence in 1960 [54].
Pathophysiology
Distinctive features of AVM hemodynamics are of par-
ticular interest to neurosurgeons due to their influence on
the risk of hemorrhage and association with complications
of various treatment modalities. The blood flow through so-
phisticated AVM angioarchitecture can be estimated using
Hagen-Poiseuille formula (Q=∆ P/R, in which Q is the flow,
∆P – pressure gradient, R-resistance) when we take into
consideration that blood is a  non-Newtonian fluid, i.e. the
blood viscosity depends on the shear rate and flow velocity,
vessels are not rigid pipes but viscoelastic tapered tubes
feeding artery pressure and deep venous drainage leading
to outflow restriction are independent risk factors of hemor-
rhage, whereas in the same study nidus size, location and
the presence of arterial aneurysms were found to be non-in-
dependent risk factors. Sorimachi et al. [88] demonstrated
that feeding artery pressure tends to be lower in feeders
with terminal divided branches (probably supporting sepa-
rate AVM compartments) than in case of feeders with sin-
gle branches terminating in the AVM. When the feeder has
a transient branch to the eloquent part of the brain (supply-
ing normal, relatively high-resistance brain tissue), the pres-
sure in the feeder is found to be significantly higher.
One way to confirm the speculated intranidal hemody-
namics is to create electrical models of AVMs. Such models
are based on the analogy between electric circuit and ves-
sel network. Current is the analog of blood flow, voltage (the
potential difference across two points) is compared to pres-
sure (as pressure difference between two ends of the vessel
causes blood flow), resistors in such artificially created cir-
cuits are equivalents of vessel resistance. The analogy be-
tween Ohm’s law ( I=V/R in which I is the current, V-voltage,
R-resistance) and Hagen-Poiseuille formula can be drawn.
The disadvantage of such models is the simplicity of their
architecture (often simulating only one feeding artery and
draining vein or containing no compartments, whereas real,
especially large high-flow AVMs, are usually either structur-

18 VOLUME 51, NR 1 VOLUME 51, NR 1 19

 Clinical
MANAGEMENT
Medicine
ally or functionally compartmentalized lesions supported by
3-4 feeding arteries), the models don’t provide for blood vis-
cosity, shear stress, pulsatile blood flow, vessel distensibili-
ty and autoregulation [27]. A biomathematical model based
on electrical network analysis, created by Hademonos et
al. [31], determines intranidal hemodynamics with particular
consideration of the differences between the plexiform and
fistulous part of AVM. The mean intranidal flow was found
to be 31,3ml/min with mean flow velocity of 66,4cm/s for
the plexiform part and 617,6ml/min with mean flow velocity
of 387,8cm/s for the fistulous part. The mean shear stress
was 187,7 dyne/cm2 for the plexiform part and 463,5dyne/
cm2 for the fistulous part. Guglielmi et al.[27] have created
two electrical models – of low-flow (105ml/min) and high-
flow (550ml/min) AVMs to define hemodynamic conditions,
including pressure and blood flow, within the successive
parts of the AVM i.e. the arterial, arteriolar, arteriolar-venu-
lar transition, venular and venous parts of the lesion and
assess the hemodynamic changes after endovascular em-
bolization, surgical extirpation and bypass creation. The
model revealed that in large, high-flow AVM, in relation to
lower resistance of the nidus when compared to small AVM,
the pressure regimen through the nidus is lower (especially
when pressures on the arterial side of large and small AVMs
are compared, 40 and 70mmHg respectively), the pressure
in the arteriolar part of the nidus is lower (25,5 vs 44mmHg
in small AVM), the flow through the venular part of large
AVM is higher (48ml/min) and the pressure in the venular
part is lower (18,5mmHg) than in small AVM (26ml/min and
24,5mmHg, respectively). The study confirmed large blood
flow through the fistulous part (365ml/min) in comparison
with the plexiform part (190ml/min) of the AVM nidus. Al-
though one might expect to find a correlation between low
feeding mean arterial pressure (FMAP) and high draining
vein pressure (DVP) in high-flow fistulas, recent studies do
not confirm such association. According to Young et al.
[108], higher FMAP is directly related to higher DVP. In high-
flow AVMs the transnidal pressure (the difference between
FMAP and DVP) seems to be lower, which results in de-
creased susceptibility to spontaneous vessel rupture.
The resistance of the feeding arteries in large AVM was
calculated to be lower than in small AVM (36Ω vs 240Ω)
due to larger cross section of feeding arteries of large AVM.
Due to larger cross section of draining veins of large AVM,
the resistance of the draining veins was lower than in small
AVM (13Ω vs 95Ω). An interesting finding is lower resistance
of brain vessels in case of large, high-flow AVM than in small
AVM (149 Ω vs 249 Ω). Brain vessels tend to dilate in order
to maintain sufficient blood supply to the brain tissue. When
the pressure drops beyond autoregulatory capabilities, the
brain becomes hypoperfused and neurological deficits tend
to appear. Large high-flow AVMs contribute to redistribution
of blood flow, more blood is directed to the low-resistant le-
sion, which in turn leads to decrease in perfusion pressure of
the brain-nutrifying vessels and the vascular steal phenom-
enon may occur if autoregulation range stays unchanged
[29, 86]. However, symptoms ascribed to ‘steal’ are a rare
finding in AVM patients thanks to ‘adaptive autoregulato-
ry displacement’ [108]. The steal phenomenon is claimed
to be responsible for progressive neurological deficits ob-
20 VOLUME 51, NR 1
served in approx 15% of patients with AVMs [12]. Sekhon et
al. [85] have demonstrated by creating an arteriovenous fis-
tula model in the rat that chronic non-infarctional ischaemia
with the 25-50% reduction in CBF leads to the impairment
of neuronal function. On the basis of analysis of 65 patients
with AVM, Marks et al. [57] have defined morphological fea-
tures associated with the risk of vascular steal, including
large nidus (mean volume of 105cm3 in patients with the
presentation of vascular steal, comparing with mean vol-
ume of 19,5cm3 in patients without such presentation), an-
giomatous change and peripheral venous drainage. Many
scientists, on the other hand, diminish the importance of
vascular steal. In a study carried out by Mast et al. [60] 11
out of 152 patients with AVM presented nonprogressive fo-
cal neurological deficits while only 2 patients suffered from
progressive deficits. Patients with hemorrhage prior to neu-
rological deficits were excluded from the study. The authors
compared pressure and mean flow velocities in feeding ar-
teries and found no difference between patients with versus
without deficits.
Another approach to shed light on the incompletely un-
derstood issue of AVM-related hemodynamic disturbanc-
es is to create such lesions in animals. This approach is
grounded in a theory of AVM pathogenesis, assuming that
morphological changes leading to the nidus formation occur
secondary to increased blood flow and shear stress in a con-
genital arteriovenous fistula [66]. An affirmation of this theo-
ry can be effective attempts of the formation of human-like
AVMs on the basis of surgically created arteriovenous fistula
in animals. Wakhloo et al. [105] have proposed increased
flow through the fistula and vessel remodeling to be respon-
sible for reduction of muscular tone, vessel dilatation (mean
diameter of 520µm after 6 months since fistula creation vs
320µm in control animals) and decreased resistance leading
to the formation of high-flow AVM. Similarities between ani-
mal models and human AVMs were histopathologically and
ultrastructurally verified and included ectasia of the model
vessels, focal intimal hyperplasia, increased collagen depo-
sition, disruption of the elastic lamina and the presence of
filopodia on the luminal surface of endothelium [98].
Other important factors leading to hemodynamic per-
turbations and, therefore, suspected to be associated with
the risk of rupture, are the presence of intranidal anerysms
(or venous ectasias) and venous stenosis, considered by
Krings et al. [45] to be ‘focal weak points’ in AVM angio-
architecture. Aneurysms within feeding arteries or nidus as
well as in remote vessels are frequent anomalies, estimated
to be present in 10-58% of AVM patients [82] and may rup-
ture before, during or immediately after AVM treatment [96].
Flow-related aneurysms tend to develop in sites of maximal
shear stress, which are branching points of major feeding
arteries. Therefore it is not surprising that they disappear
after restoration of normal hemodynamic conditions of CBF
[16]. Venous stenosis is supposed to be an excessive re-
sponse of the venous wall to high flow and shear stress. Its
correlation with the risk of rupture is disputable and proba-
bly depends on the selection bias of the patients. However,
many studies confirm positive correlation with the risk of
hemorrhage [63, 69, 103]. As intranidal aneurysms and ve-
nous stenosis are considered to be hazardous structures,
Hirai et al. [34] have recommend focusing the treatment
strategy on these lesions. In case of aneurysms both embo-
lization and radiosurgery can be performed. In large AVMs
with venous stenosis, embolization seems to be treatment
of choice.
Treatment
The main aim of AVM treatment is to eliminate the risk of
future hemorrhage by total occlusion or complete excision
and preserve neurological function. The aim can be achieved
after thorough clinical examination and radiological assess-
ment by adjusting the treatment modality to patient’s char-
acteristics and AVM angioarchitecture in the way that the
treatment-related morbidity and mortality didn’t outweigh
the risk of complication in the AVM natural history [73].
Microsurgery
As observed by Guglielmi [27] after excision of low-
flow AVMs the feeding artery pressure increases from 70
to 96mmHg with a simultaneous decrease of draining vein
pressure from 18 to 6mmHg. In case of high-flow AVMs, the
feeding artery pressure rise tends to be larger (from 40 to
87mmHg) with the draining vein pressure drop from 15 to
3mmHg. These changes result from removal of the lesion
of low resistance to blood flow. In accordance with Poi-
seuille-Hagen formula, as the feeding arteries are perma-
nently dilated and are unable to constrict immediately after
AVM excision, the new pressure gradient must be reduced
to maintain the same blood flow. This leads to a greater than
normal blood pulsatility and may result in hemorrhage from
a ruptured aneurysm or other site of vessel weakness [70].
After excision of high-flow AVM the autoregulatory mech-
anism has to intervene because large amounts of blood
supplying previously the low-resistant lesion are now di-
rected to dilated vessels of the adjacent brain [27]. Since
years scientists have tried to answer the question whether
the capillaries in the neighborhood of the nidus, adapted for
chronic ischaemia are capable of autoregulation like capil-
laries of the distant to the AVM sites of the brain. If not, the
risk of NPPB arises [4, 71, 91]. The phenomenon is due to
the impairment of autoregulation, in particular in the shift of
upper limit to the lower pressure value in cases of chronic
brain hypoperfusion induced by the presence of a low-re-
sistant lesion [38]. Paralyzed vessels adjacent to the AVM
are unable to response to the restoration of normal perfu-
sion pressure, which results in hyperemia and disruption of
the capillary bed. NPPB occurs mainly in patients with large,
high-flow AVMs, supplied by the branches of external carot-
id artery [91].
Hemorrhage during or after surgery is the most devas-
tating complication. The larger the AVM, the higher the risk
of hemorrhage. However, NPPB is only one explanation for
postoperative hemorrhage and/or cerebral edema after AVM
excision. A theory, introduced by al-Rodhan [1] is based on
studies that reduced blood flow through the draining veins
with a  simultaneous stagnant flow in the feeding arteries
may result in intravenous clot formation. Obstruction of
venous outflow leads to ‘occlusive hyperemia’. Distinctive
features of AVM angioarchitecture, including (1) high-flow
AVMs, (2) long and tortuous feeding arteries, (3) small num-
ber of draining veins, (4) pre-operative venous narrowing or
occlusion and (5) the presence of vascular steal, are found
to be associated with the elevated risk of ‘occlusive hyper-
emia’ [1].
The grading scale comprised of nidus size, pattern of
venous drainage and eloquence of the adjacent brain, pro-
posed by Spetzler and Martin [90] in 1986, has been gold
standard to assess the risk and predict the outcome of sur-
gical intervention in AVM patients. Other grading systems,
developed by Tamaki et al. [93], Hollerhage et al. [36], Pertu-
iset et al. [76] or Spears et al. [89] have not met with general
approval. In 2010 Lawton et al. [46] have presented a grad-
ing scale, based on patient age, sort of clinical presenta-
tion (hemorrhagic or unhemorrhagic) and AVM diffuseness,
as supplementary to Spetzler-Martin grading scale in order
to increase the sensitivity, specificity (or both) of predicting
the resection outcome. The authors based on statistically
significant variabilities found to be independent risk factors
of neurological complications after surgery (age, unhemor-
rhagic presentation, diffuse lesion). The aim of this simple
scale is both to confirm the surgery risk estimated by means
of Spetzler-Martin scale (when the outcome of the supple-
mentary scale corresponds with the Spetzler-Martin out-
come) and, which has more important clinical implications,
to help to decide in doubtful cases of borderline outcome
by Spetzler-Martin grading scale (with stress on Grade III
subtypes). As Sanchez-Mejia [84] recommends, ‘microsur-
gical resection should be done in case of radiated AVMs
that are not completely obliterated after the 3-year latency
period, but altered favorably for surgery, even in asymptom-
atic patients’.
Embolization
Endovascular embolization is an important facilitation of
surgery, aimed at reducing the AVM volume and flow and
occlusion of deep, surgically inaccessible feeding arteries
and intranidal fistulous compartments [101]. It is a  part of
multimodality treatment when combined with microsurgery
or radiosurgery, but it may be also applied as the sole treat-
ment method to achieve complete obliteration or as pallia-
tive treatment [73]. The data concerning postembolization
mortality and morbidity vary significantly. Taylor et al. [94]
highlight the fact that despite significant surgical facilitation
measured in reduction of intraoperative blood loss and op-
erative time, embolization is correlated with increased mor-
tality and morbidity. According to the retrospective study
carried out by the authors in 2004, 11% of patients died
or suffered from a permanent neurological deficit after the
embolization procedure. The data presented by Deruty et
al. [20] revealed a 25%-complication rate (including minor
deterioration, neurological deficits and death) after endo-
vascular embolization, compared to minor complications
(mainly minor deterioration) observed in 17% of surgically
treated patients and 10% of irradiated patients. Such high
postembolization complication rates may be only partial-
ly attributed to the fact that embolization is performed in
sophisticated AVM cases as severe complications after
embolization have been observed in low-grade AVMs as
well. Therefore Deruty et al. [20] dissuade from performing
embolization in low-grade AVMs and favour microsurgical
VOLUME 51, NR 1 21

resection or irradiation in such cases. However, updates on
the postembolization clinical outcome are more optimistic.
A  study conducted by Ledezma et al. [47] revealed 6,5%
complication rate and 1,2% mortality rate. Haw et al. [33]
reported 3,9% risk of death or permanent neurological defi-
cit after embolization.
The postembolization hemodynamic complications in-
clude both hemorrhage and ischemic events (50% each
[20]), which may lead to transient or permanent neurological
deficits. Ischemic events may result from occlusion of arteri-
al branch supplying normal brain tissue or arterial dissection
during endovascular access. Postembolization hemorrhage
in the early period after the embolization, reported in 3-15%
of patients and 1-2% of procedures [40] [77], is supposed to
be a result of the increase of feeding artery pressure. Sev-
eral factors, including (1) compact nidus, (2) large number
of feeding arteries, (3) the presence of steal phenomenon,
(4) preembolization venous stenosis or ectasia, (5) exten-
sive venous embolization, have been postulated to pre-
dispose to early hemorrhage [77]. Hemorrhage in the late
period occurs due to venous occlusion, being a  result of
slowed blood flow in the dilated veins and clot formation in
the draining vein system, or the speculated phenomenon of
NPPB. A separate issue is the periprocedural hemorrhage
secondary to mechanical vessel perforation, AVM rupture
or intranidal aneurysm rupture during catheterization [41].
The hemodynamic consequences of embolization de-
pend on the magnitude of flow and the part of the AVM,
which is occluded with the embolic agent. As the electrical
models created by Gugliemi [27] demonstrate, the most de-
sired effect is the occlusion of arterial feeders resulting in
the reduction of blood pressure and flow through the nidus
both in cases of low-flow and high-flow AVMs (with a 40%
reduction of pressure and 50% reduction of flow through
the nidus in small AVMs). However, if the embolic agent,
after occlusion of the feeding arteries, does not penetrate
to the shunt within the nidus, the risk of neoangiogenesis
or reopening of the collateral circulation arises, which will
make subsequent endovascular procedures nearly impos-
sible [45]. On the other hand, occlusion of the draining vein
system is an unwelcome result of embolization leading to
a dramatic decrease of flow through the nidus and increase
of pressure in the venular part of the nidus (in low-flow
AVMs even by 284%) with high risk of postembolization
hemorrhage [27]. Extreme caution is required during embo-
lization of AVMs combined with venous stenosis as when
even scant amount of embolic agent reaches the stenosed
vein, the pressure within the nidus may increase significant-
ly with severe hemodynamic consequences. Rupture may
also be a result of occlusion of the fistulous compartment
and the venular part of one of the channels of the plexiform
compartment in high-flow AVMs, as the increase of flow and
pressure within the nidus in such cases is noted to be 108%
and 244%, respectively. However, Yuki et al. [110] demon-
strated that embolization of the high-flow fistula, as a part
of multimodality approach to cerebral AVMs with large fis-
tulous compartments, was successful in 100% of patients,
and the complications, if occurred, were associated with
endovascular occlusion of other parts of the nidus. Single
photon emission computed tomography (SPECT) enables
22 VOLUME 51, NR 1
measurement of regional cerebral blood flow (rCBF) in close
proximity to the AVM and may show either postemboliza-
tion disappearance of rCBF decrease, observed before the
procedure, or increase of rCBF combined with hyperemic
complications [6].
In large, high-flow AVMs the risk of NPPB seems life-
like, especially when one-staged complete excision is per-
formed. Therefore, many authors recommend multimodality
treatment composed of staged embolization and final surgi-
cal resection. The key issue is the choice of optimal interval
between the embolization and surgery as too short intervals
between the procedures may contribute to severe hyper-
emic complications and within long intervals the occluded
vessels may recanalize or collateral circulation may devel-
op. Chioffi et al. [11] observed higher risk of intraoperative
complications including severe blood loss and periventric-
ular hemorrhage as well as postoperative hemodynam-
ic complications such as cerebral edema or intracerebral
hematoma when the AVM mean flow velocity exceeded
120cm/s before the surgery.
The issue that has been particularly under discussion
is the choice of the optimal embolic agent considering the
safety and effectiveness of the procedure. Embolic materi-
als can be divided into two groups: solid agents, including
polyvinyl alcohol particles (PVA), fibers, microcoils, micro-
balloons and liquid agents including cyanoacrylate mono-
mers e.g. I-butyl cyanoacrylate (IBCA) and N-butyl cyano-
acrylate (NBCA), and polymer solutions e.g. ethylene vinyl
alcohol [73]. The introduction of liquid agents revolutionized
endovascular procedures and NBCA has been the most
popular embolic material so far, with complete obliteration
rate of approximately 10% [24], achieved mainly in small
AVMs with a small number of feeding arteries [102], espe-
cially when the nidus is not compartmentalized or the fistu-
lous compartment is dominant [100]. It has been postulat-
ed that the use of particle materials, as they induce slower
obliteration, is associated with increased risk of hemorrhage
due to slow but continuous increase of pressure within the
nidus before complete obliteration [73]. Liquid agents allow
the use of flow-directed catheters, which in turn eliminates
the risk of mechanical perforation during the procedure and
enables precise placement of the catheter in close proximity
to the nidus, reducing the risk of ischemic events [106]. Eth-
ylene vinyl alcohol copolymer (Onyx) is a new liquid agent
enabling, at least theoretically, better penetration and simul-
taneous angiographic control [75]. However data concern-
ing its effectiveness vary significantly, the complete obliter-
ation rate ranging from 29%, reported by Tevah and Huete
[95], to 0% in a study conducted by Jahan [42].
In 2010 a  grading scale for AVM endovascular proce-
dures, similar to the surgically applicable Spetzler-Martin
grading scale, has been created by Feliciano et al. [23]
However, the scale, composed of the number of feeding
arteries, presence of fistulous compartments and eloquent
location of the lesion, was based only on the analysis of
outcome predictive factors described in literature and, as
the authors mention, needs further examination.
Embolization is performed when the nidus diameter is
in excess of 3cm or it is supplied by deep feeding arteries
with difficult surgical access [73]. In fear of too rapid redis-
tribution of blood flow and subsequent hemorrhage and/or
brain edema, staged embolization of the feeding arteries is
recommended. Complete surgical excision should be per-
formed within several days (1-2 weeks) after final emboliza-
tion [73].
Radiosurgery
The advantage of radiation in AVM treatment is its ability
to cause endothelial damage and hyaline thickening, result-
ing in thrombosis and AVM obliteration [72]. Radiosurgical
treatment is preferred in patients with unruptured, small (the
efficiency of this modality is limited to lesions not greater
than 3cm), deep AVMs, especially when the lesion is locat-
ed in eloquent part of the brain (considered in such case
to be treatment of choice) [73]. It is also a part of multimo-
dality approach to treatment of giant AVMs associated with
high surgical risk [73]. Radiosurgery prior to microsurgery
facilitates the resection by (1) reducing the size of high-flow
AVMs, (2) making the walls of the radiated arteries thicker
and subsequently easier to occlude, (3) reducing the blood
flow through the nidus and (4) inducing gliosis surround-
ing the lesion, which facilitates the dissection. As observed
by Sanchez-Mejia [84], radiosurgery reduces the operative
morbidity, graded according to the modified Rankin Scale
(mRS). As the effect is not immediate and the latency pe-
riod necessary to obtain obliteration is estimated to be
approximately 2 years, one must contemplate the risk of
hemorrhage within the latency period versus the capabili-
ty to immediate AVM excision [10]. Numerous studies have
been conducted to shed light on the risk of hemorrhage
associated with the radiation-induced altered flow patterns
within the latency period [15, 43, 53]. As the radiation in-
duces thickening of the nidus vessel walls and subsequent
fibrosis, one can expect the risk of hemorrhage within the
latency period to be decreased. The data vary due to the
sort of analysis and the annual risk of hemorrhage with-
in the latency period is reported to be 1,5-3,7% [14, 87,
92]. In Karlsson’s [43] study advanced age and low dose
of radiation were found to be associated with higher risk of
rupture. As a confirmation of Karlsson’s observations may
serve a biomathematical model of the influence of radiation
on the risk of hemorrhage, developed by Massoud et al. [59]
The authors stressed the elevated risk of rupture associated
with partial and/or low-dose radiosurgery. When incomplete
radiosurgery is performed, the resistance to outflow in oc-
cluded vessels increases and the blood is redistributed to
unoccluded parts of the nidus, which results in generation
of additional biomechanical stresses increasing the risk of
rupture. Interestingly, nidus vessels in close relation to the
feeding arteries and/or draining veins are the most suscep-
tible to rupture [59]. Several authors highlight the risk of
venous hypertension and ‘occlusive hyperemia’ as a result
of radiosurgically-induced venous occlusion prior to arterial
occlusion. The subsequent increase of intranidal pressure
may contribute to intracranial hemorrhage. According to
Pollock [78], venous hypertension was present in 2 of 28 pa-
tients with symptomatic postradiosurgical imaging chang-
es. Chapman et al. [11] described two cases of patients with
delayed neurological deficits due to postradiosurgical ve-
nous outflow obstruction. Celix et al. [9] consider inflamma-
Clinical
Medicine
tory response to irradiation as the most probable cause of
venous thrombosis leading to hemorrhage in the early peri-
od following radiosurgery. Therefore, ‘occlusive hyperemia’,
the term used primarily to explain pathophysiological basis
for brain edema or hemorrhage after AVM surgical resec-
tion, may be responsible for hemodynamic complications
after AVM radiosurgery, too. Other factors, including AVM
size, the presence of aneurysms and hemorrhage within one
year prior to radiosurgery, have been demonstrated to exert
effect on the generation of hemorrhage after AVM radiosur-
gery [80, 49]. As demonstrated by Lo [51], the distribution of
shear stress to the AVM shunt walls, which is directly related
to the risk of rupture, is dependent on the mechanism of
AVM obliteration. Two patterns of post-radiosurgical occlu-
sion have been described in literature. The first one, less
likely, referred to as ‘random occlusion’, signifies complete
obliteration of only some of the nidus vessels and subse-
quent blood redistribution. The second mechanism of ves-
sel occlusion is grounded in stepwise thickening of the ves-
sel walls and narrowing of the lumen (‘stepwise occlusion’)
with eventual vessel occlusion [52]. The pattern of occlusion
is probably much more complex in in vivo conditions than in
theoretical considerations and requires allowing for dynam-
ic phenomena within the nidus [59].
An incompletely understood phenomenon is the occur-
rence of hemorrhage after complete radiosurgical obliter-
ation confirmed in angiography. Delayed hemorrhage was
reported in 0,7-2,4% of patients [39, 58]. The speculat-
ed cause of such hemorrhage is recanalization of a  small
postradiosurgical thrombus, undetectable via neuroimag-
ing. The suspected risk factors include young age, female
sex and the presence of small AVM [61]. Reexamination of
such patients after complete radiosurgical obliteration is
recommended, as there is diminutive risk of AVM reappear-
ance [50].
According to Sanchez-Mejia [84], ‘radiosurgery is rec-
ommended for unruptured AVMs that are not favorable for
microsurgical resection‘. As Spetzler-Martin grading scale
does not correlate with patient outcome after AVM radio-
surgery, Pollock and Flickinger [79] developed ‘radiosur-
gery-based arteriovenous malformation score’ (RBAS).
The authors formulated an equation to calculate the AVM
score, associated with patient outcome after single irradi-
ation. The AVM score can be defined in the following way:
AVMscore=(0.1)(AVM volume in cm3) + (0,02)(patient age in
years) + (0.3)(location of lesion: 0 if frontal or temporal; 1 if
parietal, occipital, intraventricular, corpus callosum or cere-
bellar; 2 if basal ganglia, thalamic or brainstem). Lower AVM
score (1 or less) is correlated with better clinical outcome.
The grading scale, proposed in 2002, has been validated
several times [3, 65, 81] and seems to be an accurate pre-
dictor of excellent outcome not only after single radiosur-
gery but also after retreatment and may help predict the
clinical outcome after overall radiosurgical treatment [81].
Conclusions
AVM are among those brain pathologies that have been
for centuries of particular interest. Its complexity results
from the angioarchitecture and hemodynamic properties.
The essence of AVMs treatment relies on a multimodal ap-
VOLUME 51, NR 1 23
 Clinical
MANAGEMENT
Medicine
proach and commitment of a  comprehensive therapeutic
team. The development of radiosurgery, microsurgery and
endovascular techniques enables to select of the best ther-
apeutic method depending on the type of AVMs, as well as
in specific cases, a  combination of these methods. Large
AVMs in the past, considered to be inoperable, can now be
safely treated. In addition, apart from the significant diffi-
culties arising from the exclusion of the AVM from cerebral
circulation, equally important issue is to predict, control and
prevention of hemodynamic consequences after surgery.
Therefore, before proceeding with treatment, all matters re-
lating to hemodynamic complications in any case should be
examined. After a detailed analysis, an appropriate single or
multimodal method of treatment should be selected, con-
sidering the risk of postoperative complications. The perfect
course of treatment does not guarantee the avoidance of
serious hemodynamic and functional impairment later on.
NPPB, occlusive hyperemia, steel phenomenon are partic-
ularly dangerous and can cause severe clinical deteriora-
tion of patients. However, present clinical data confirms that
AVMs could be safely treated with greatly reduced risk of
serious complications compared with earlier results.
References
1. Al.-Rodhan NR, Sundt TM Jr, Piepgras DG et al.
(1993) Occlusive hyperemia: a theory for the hemo-
dynamic complications following resection of intra-
cerebral arteriovenous malformations. J Neurosurg
78(2):167-175
2. Al-Shahi R, Warlow C (2001) A systematic review of
the frequency and prognosis of arteriovenous malfor-
mations of the brain in adults. Brain 124:1900-1926
3. Andrade-Souza YM, Zadeh G, Ramanti M et al
(2005) Testing the radiosurgery-based arteriovenous
malformation score and the modified Spetzler-Mar-
tin grading system to predict radiosurgical outcome.
J Neurosurg 103(4):642-648
4. Barnett G, Little JR, Ebrahim ZY at a (1987) Cerebral
circulation during arteriovenous malformation oper-
ation. Neurosurgery 20:836-842
5. Barrow D, Dawson R (1994) Surgical management
of arteriovenous malformations in the region of the
ventricular trigone. Neurosurgery 35:1046-1054
6. Batjer HH, Purdy PD, Giller CA at al (1989) Evidence
of redistribution of cerebral blood flow during treat-
ment for an intracranial arteriovenous malformation.
Neurosurgery 25:599–605
7. Bergstrand H, Olivecrona H, Tonnis W (1936) GefaB-
miGbildungen und Gefafigeschwulste des Gehirns.
Thieme. Leipzig, p. 181
8. Brooks B. (1968) The treatment of traumatic arterio-
venous fistula. South Med J 1930;23:100–106
9. Celix JM, Douglas JG, Haynor D et al (2009) Throm-
bosis and hemorrhage in the acute period following
Gamma Knife surgery for arteriovenous malforma-
tion. Case report. J Neurosurg 111(1):124-131
10. Chaddad-Neto F, Joaquim AF, dos Santos MJ et al
(2008) Microsurgical approach of arteriovenous mal-
formations in the central lobule. Arq Neuro-Psiquiatr
66(4):872-875
24 VOLUME 51, NR 1
11. C
 hapman PH, Ogilvy CS, Loeffler JS (2004) The re-
lationship between occlusive hyperemia and compli-
cations associated with the radiosurgical treatment
of arteriovenous malformations: report of two cases.
Neurosurgery 55(1):228-233
12. C
 hioffi F, Pasqualin A, Beltramello A et al (1992) He-
modynamic effects of preoperative embolization in
cerebral arteriovenous malformations: evaluation
with transcranial Doppler sonography. Neurosurgery
31(5):877-884
13. C
 hoi JH, Mast H, Hartmann A, Marshall RS,
Pile-Spellman J, Mohr JP, Stapf C (2009) Clinical
and morphological determinants of focal neurolog-
ical deficits in patients with unruptured brain arterio-
venous malformation. J Neurol Sci 287(1-2):126-130
14. C
 offey RJ, Nichols DA, Shaw EG (1995) Stereotac-
tic radiosurgical treatment of cerebral arteriovenous
malformations. Gamma Unit Radiosurgry Study
Group. Mayo Clin Proc 70(3):214-222
15. C
 olombo F, Pozza F, Chierego G, Casentini L, De
Luca G, Francescon P. (1994) Linear accelerator ra-
diosurgery of cerebral arteriovenous malformations:
an update. Neurosurgery 34:14–21
16. C
 unha e Sa MJ, Stein BM, Solomon RA, McCormick
PC (1992) The treatment of associated intracranial
aneurysms and arteriovenous malformations. J Neu-
rosurg 77(6):853-859
17. C
 ushing, H., P. Bailey (1928) Tumours Arising from
the Blood Vessels of the Brain. Angiomatous malfor-
mations and Hemangioblastomas, vol. III. Thomas.
Springfield/Ill. p. 219
18. Dampsey RJ, Moftakhar R, Pozniak M (2004) In-
traoperative Doppler to measure cerebrovascu-
lar resistance as a  guide to complete resection
of arteriovenous malformations. Neurosurgery
55(1):155-161
19. D
 andy, W. E.: Venous abnormalities and angiomas
of the brain (1928). Arch. Surg. (Chic.) 17: 715-793,
20. D
 eruty R, Pelissou-Guyotat I, Amat D, Mottolese C,
Bascoulerque Y, Turiman F, Gerard JP (1996) Com-
plications after multidisciplinary treatment of cere-
bral arteriovenous malformations. Acta Neurochir
(Wien) 138(2):119-131
21. D
 ott, N. M (I933) Intracranial Aneurysms: Cerebral
Arterio-Radiography: Surgical Treatments. Edin-
burgh Med. Jour 40, p.219
22. D
 uong DH, Young WL, Vang MC, Sciacca RR, Mast
H, Koennecke HC et al (1993) Feeding artery pres-
sure and venous drainage pattern are primary deter-
minants of hemorrhage from cerebral arteriovenous
malformations. Stroke 29(6):1167-1176
23. F
 eliciano CE, de Leon-Berra R, Hernandez-Gaitan
MS, Rodriguez-Mercado R (2010) A  proposal for
a new arteriovenous malformation grading scale for
neuroendovascular procedures and literature review.
P R Health Sci J 29(2):117-120
24. F
 iorella D, Albuquerque FC, Woo HH, et al (2006) The
role of neuroendovascular therapy for the treatment
of brain arteriovenous malformations. Neurosurgery
59(5 suppl 3):163–177
25. Gao E, Young WL, Hademonos GJ, Massoud TF,
Sciacca RR, Ma Q at al (1998) Theoretical modeling
of arteriovenous rupture risk: a feasibility and valida-
tion study. Med Eng Phys 20(7):489-501
26. Green HD, Rapela CE (1964) Blood flow in passive
vascular beds. Circ Res(Suppl 1);15:11-16
27. Guglielmi G (2008) Analysis of the hemodynamic
characteristics of brain arteriovenous malformations
using electric models: baseline settings, surgical
extirpation, endovascular embolization and surgical
bypass. Neurosurgery 63:1-11
28. Hacein-Bey L, Young WL (1999) Hemodynamic per-
turbations in cerebral arteriovenous malformations
and management implications. Interv Neuroradiol
30(5):177-182
29. Hacein-Bey L, Young WL (1999) Hemodynamic per-
turbations in cerebral arteriovenous malformations
and management implications. Interv Neuroradiol
30(5)(Suppl 1):177-182
30. Hademenos GJ, Massoud TF (1996) An electrical
network model of intracranial arteriovenous malfor-
mations: analysis of variations in hemodynamic and
biophysical parameters. Neurol Res 18(6):575-589
31. Hademonos GJ, Massoud TF, Vinuela F (1996)
A  biomathematical model of intracranial arteriove-
nous malformations based on electrical network
analysis: theory and hemodynamics. Neurosurgery
38(5):1005-1014
32. Harvey, W (1953) De motu cordis. 1628. (First english
edition: G. Keynes. Nonsuch Press, London
33. Haw CS, terBrugge K, Willinsky R, Tomlinson G
(2006) Complications of embolization of arterio-
venous malformations of the brain. J Neurosurg
104(2):226-232
34. Hirai S, Mine S, Yamakami I, Ono J, Yamaura A (1998)
Angioarchitecture related to hemorrhage in cerebral
arteriovenous malformations. Neurol Med Chir (To-
kyo).;38 Suppl:165-70
35. Hoffmann J (1898) Aneurysma racemosum der
Gehirnarterien? Krankenvorstellung. Naturhis-
torisch-Medizinischer Verein, Heidelberg, 15. Juni
1898. Munch, med. Wschr. 2: 1159,
36. Hollerhage HG, Dewenter KM, Dietz H (1992) Grad-
ing of supratentorial arteriovenous malformations on
the basis of multivariate analysis of prognostic fac-
tors. Acta Neurochir (Wien) 117(3–4):129–134
37. Hunter, W  (1762) Further observations upon a  par-
ticular species of aneurysm. Med. Observ. Enquir.
(Lond.) 2: 390-414
38. Irikura K, Morii S, Miyasaka Y, Yamada M, Tokiwa K,
Yada K (1996) Impaired autoregulation in an exper-
imental model of chronic cerebral hypoperfusion in
rats. Stroke;27(8):1399-1404
39. Izawa M, Hayashi M, Chernov M, Nakaya K, Ochiai
T, Murata N, Takasu Y, Kubo O, Hori T, Takakura K
(2005) Long-term complications after gamma knife
surgery for arteriovenous malformations. J Neuro-
surg;102 Suppl:34-37
40. Jafar JJ, Davis AJ, Berenstein A, Choi IS, Kupersmith
MJ (1993) The effect of embolization with N-butyl
cyanoacrylate prior to surgical resection of cerebral
arteriovenous malformations. J Neurosurg 78:60–69
41. Jafar JJ, Rezai AR (1994) Acute surgical manage-
ment of intracranial arteriovenous malformations.
Neurosurgery 34:8–13,
42. Jahan R, Murayama Y, Gobin YP, et al (2001) Embo-
lization of arteriovenous malformations with Onyx:
clinicopathological experience in 23 patients. Neu-
rosurgery;48:984–997
43. Karlsson B, Lindquist C, Steiner L (1996) Effect of
gamma knife surgery on the risk of rupture prior to
AVM obliteration. Minim Invasive Neurosurg 39:21–27
44. Kerber CW, Hecht ST, Knox K (1997) Arteriovenous
malformation model for training and research. Am J
Neuroradiol 18(7):1129-32
45. Krings T, Hans FJ, Geibprasert S, Terbrugge K
(2010) Partial “targeted” embolisation of brain arte-
riovenous malformations. Eur Radiol. Jun 11. DOI:
10.1007/s00330-010-1834-3
46. Lawton MT, Kim H, McCulloch CE, Mikhak B, Young
WL (2010) A supplementary grading scale for select-
ing patients with brain arteriovenous malformations
for surgery. Neurosurgery 66(4):702-713
47. Ledezma CJ, Hoh BL, Carter BS, Pryor JC, Putman
CM, Ogilvy CS (2006) Complications of cerebral ar-
teriovenous embolization: multivariate analysis of
predictive factors. Neurosurgery 58(4):602-611
48. Leksell L (1968) Cerebral radiosurgery. I. Gammath-
alanotomy in two cases of intractable pain. Acta Chir
Scand 134(8):585-595.
49. Lindquist C (1996) Comment on “Hemorrhage risk
after stereotactic radiosurgery of cerebral arteriove-
nous malformations.” Neurosurgery 38:66
50. Lindqvist M, Karlsson B, Guo WY, Kihlstrom L, Lip-
pitz B, Yamamoto M (2000) Angiographic long-term
follow-up data for arteriovenous malformations pre-
viously proven to be obliterated after gamma knife
radiosurgery. Neurosurgery 46:803-810
51. Lo EH (1993) A theoretical analysis of hemodynamic
and biomechanical alteration in intracranial arterio-
venous malformations after radiosurgery. Int J Radi-
at Oncol Biol Phys 27(2):353-61
52. Lo EH, Fabrikant JI (1992) A  compartmental flow
model for intracranial AVMs. In: Lunsford LD, ed.
Stereotactic Radiosurgery Update. New York, NY:
Elsevier 157–161
53. Lo EH, Fabrikant JI, Levy RP, Phillips MH, Frankel KA,
Alpen EL (1991) An experimental compartmental flow
model for assessing the hemodynamic response of
intracranial arteriovenous malformations to stereo-
tactic radiosurgery. Neurosurgery 28:251–259
54. Luessenhop AJ, Spence WT (1960) Artificial emboli-
zation of cerebral arteries. Report of use in a case of
arteriovenous malformation. J Am Med Assoc. Mar
12;172:1153-1155
55. Luschka, H (1854) Cavernose Blutgeschwulst des
Gehirns. Virchows Arch. 6: 458-470
56. Malpighi, M (1686) De pulmonibus in opuscula ana-
tomica, Bologna, 1661.Opera omnia. Scott, London
(vol. I and II)
VOLUME 51, NR 1 25

57. Marks MP, Lane B, Steinberg G, Chang P (1991) Vas-
cular characteristics of intracerebral arteriovenous
malformations in patients with clinical steal. Am J
Neuroradiol 12(3):489-496
58. Maruyama K, Kawahara N, Shin M, Tago M, Kishimo-
to J, Kurita H, et al (2005) The risk of hemorrhage
after radiosurgery for cerebral arteriovenous malfor-
mations. N Eng J Med 352:146-153
59. Massoud TF, Hademonos GJ, De Salles AA, Kolberg
TD (2000) Experimental radiosurgery simulations
using a theoretical model of cerebral arteriovenous
malformations. Stroke 31(10):2466-2477
60. Mast H, Mohr JP, Osipov A, Pile-Spellman J, Mar-
shall RS, Lazar RM et al (1995). ‘Steal’ is an un-
established mechanism for the clinical presentation
of cerebral arteriovenous malformations. Stroke
26(7):1215-1220
61. Matsumoto H, Takeda T, Kohno K, Yamaguchi Y,
Kohno K, Takechi A et al (2006) Delayed hemorrhage
from completely obliterated arteriovenous malfor-
mation after gamma knife radiosurgery. Neurol Med
Chir (Tokyo) 46(4):189-190
62. McCormick WF. The pathology of vascular (“ar-
teriovenous”) malformations (1966) J Neuro-
surg;24:807–816
63. Miyasaka Y, Yada K, Owada T, Kitahara T, Kurata A,
Irikura K (1992) An analysis of the venous drainage
system as a  factor in hemorrhage from arteriove-
nous malformations. J Neurosurg 76(2):239-243
64. Moniz, E (1927) L’encephalographie arterielle, son
importance dans la localization des tumeurs cere-
brales. Rev. neurol. 2: 72-89,
65. Moreno-Jimenez S, Celis MA, Larraqa-Gutierrez JM,
Suarez-Campos Jde J, Garcia-Gardunno A, Her-
nandez-Bojorquez M, Gutierrez-Aceves GA (2007)
Intracranial arteriovenous malformations treated
with LINAC-based conformal radiosurgery: valida-
tion of the radiosurgery-based arteriovenous malfor-
mation score as a predictor of outcome. Neurol Res
29(7):712-6
66. Morgan M, Winder M (2001) Haemodynamics of ar-
teriovenous malformations of the brain and conse-
quences of resection. J Clin Neurosci 8(3):216-224
67. Muacevic A, Steiger HJ (1999) Computer-assisted
resection of cerebral arteriovenous malformations.
Neurosurgery 45(5):1164-1170
68. Murphy JP (1954) Cerebrovascular Disease, vol. V.
Yearbook Medical Publishers, Chicago pp. 73-105
69. Nataf F, Meder JF, Roux FX, Blustajn J, Merienne
L, Merland JJ, Schlienger M, Chodkiewicz JP (1997)
Angioarchitecture associated with haemorrhage in
cerebral arteriovenous malformations: a  prognostic
statistical model. Neuroradiology 39(1):52-8
70. Nicholas WW, O’Rourke MF (1990) McDonald’s
Blood Flow in Arteries. Theoretic, Experimental and
Clinical Principles, third edn, London Edward Ar-
nold,:254
71. Nornes H, Grip A  (1980) Hemodynamic aspects of
cerebral arteriovenous malformations. J Neurosurg
53:456-464
26 VOLUME 51, NR 1
View publication stats
72. O gilvy CS (1990) Radiation therapy for arteriovenous
malformations: a review. Neurosurgery 26:725-735
73. O gilvy CS, Stieg PE, Awad I, Brown Jr RD, Kondzi-
olka D, Rosenwasser R, Young WL, Hademonos G
(2001) Recommendations for the Management of In-
tracranial Arteriovenous Malformations: A statement
for Healthcare Professionals From a Special Writing
Group of the Stroke Council American Stroke Asso-
ciation. Stroke 32:1458-1471
74. P erata HJ, Tomsick TA, Tew JM (1994) Feeding ar-
tery pedicle aneurysms: association with parenchy-
ma hemorrhage and arteriovenous malformation In
the brain. J Neurosurg 80:631-634
75. P érez-Higueras A, Rossi Lopez R, Quinones Taria D
(2005) Endovascular treatment of cerebral AVM: our
experience with Onyx. Interventional Neuroradiology
11:141–157
76. P ertuiset B, Ancri D, Kinuta Y, et al (1991) Classifica-
tion of supratentorial arteriovenous malformations.
A score system for evaluation of operability and sur-
gical strategy based on an analysis of 66 cases. Acta
Neurochir (Wien). 110(1–2):6–16
77. P icard L, Da Costa E, Anxionnat R, Macho J, Brac-
ard S, Per A, Marchal JC (2001) Acute spontaneous
hemorrhage after embolization of brain arteriove-
nous malformation with N-butyl cyanoacrylate. J
Neuroradiol 28:147–165,
78. P ollock BE (2000) Occlusive hyperemia: a radiosur-
gical phenomenon? Neurosurgery 47(5):1178-82
79. P ollock BE, Flickinger JC (2002) A proposed radio-
surgery-based grading system for arteriovenous
malformations. J Neurosurg 96(1):79-85
80. P ollock BE, Flickinger JC, Lunsford LD, Bissonette
DJ, Kondziolka D (1996) Hemorrhage risk after ste-
reotactic radiosurgery of cerebral arteriovenous mal-
formations. Neurosurgery 38:652–661
81. R affa SJ, Chi YY, Boya FJ, Friedman WA (2009)
Validation of the radiosurgery-based arteriovenous
malformation score in a  large linear accelerator ra-
diosurgery experience. J Neurosurg 111(4):832-839
82. R edekop G, TerBrugge K, Montanera W, Willinsky R
(1998) Arterial aneurysms associated with cerebral
AVMs: classification, incidence, and risk of hemor-
rhage. J Neurosurgery 89(4):539-546
83. R okitansky, C (1846) Handbuch der allgemeinen pa-
thologischen Anatomie. Wien p. 277
84. Sanchez-Mejia RO, McDermott MW, Tan J, Kim H,
Young WL, Lawton MT (2009) Radiosurgery facil-
itates resection of brain arteriovenous malforma-
tions and reduces surgical morbidity. Neurosurgery
64(2):231-238
85. S ekhon LH, Morgan MK, Spence I, Weber NC (1994)
Chronic cerebral hypoperfusion and impaired neuro-
nal function in rats. Stroke 25(5):1022-1027
86. S heth RD, Bodensteiner JB (1995) Progressive neu-
rologic impairment from an arteriovenous malforma-
tion vascular steal. Pediatr Neurol 13(4):352-354
87. S hin M, Kawamoto S, Kurita H, Tago M, Sasaki T,
Morita A, Ueki K, Kirino T (2002). Retrospective anal-
ysis of a 10-year experience of stereotactic radiosur-
gery for arteriovenous malformations in children and
adolescents. J Neurosurg 97(4):779-784
88. Sorimachi T, Takeuchi S, Koike T, Minakawa T,
Abe H, Tanaka R (1995) Blood pressure monitor-
ing in feeding arteries of cerebral arteriovenous
malformations during embolization: a  preventive
role in hemodynamic complications. Neurosurgery
37(6):1041-1047
89. Spears J, Terbrugge KG, Moosavian M, et al (2006)
A  discriminative prediction model of neurological
outcome for patients undergoing surgery of brain ar-
teriovenous malformations. Stroke 37(6):1457–1464
90. Spetzler RF, Martin NA (1986) A proposed grading
system for arteriovenous malformations. J Neuro-
surg 65(4):476–483
91. Spetzler RF, Martin NF, Carter LP, Flom RA,
Raudzens PA, Wilkinson E (1987) Surgical manage-
ment of large AVMs by staged embolization and
operative excision. J Neurosurg 67:17-28
92. Steiner L, Lindquist C, Adler JR, Torner JC, Alves W,
Steiner M (1992) Clinical outcome of radiosurgery
for cerebral arteriovenous malformations. J Neuro-
surg 77(1):1-8
93. Tamaki N, Ehara K, Lin TK, et al. Cerebral arte-
riovenous malformations: factors influencing the
surgical difficulty and outcome. Neurosurgery
1991;29(6):856–863
94. Taylor CL, Dutton K, Rappard G, Pride GL, Replogle
R, Purdy PD, White J, Giller C, Kopitnik TA, Sam-
son DS (2004) Complications of preoperative em-
bolization of cerebral arteriovenous malformations.
J Neurosurg 100:810–812,
95. Tevah J, Huete I (2005) Endovascular treatment of
cerebral AVMs with a new material: Onyx. Interven-
tional Neuroradiology 11:165–170
96. Thompson RC, Steinberg GK, Levy RP, Marks MP
(1998) The management of patients with arterio-
venous malformations and associated intracranial
aneurysms. Neurosurgery 43(2):202-211
97. Todaka T, Hamada J, Kai Y, Morioka H, Ushio Y
(2003) Analysis of mean transit time of contrast
medium in ruptured and unruptured arteriovenous
malformations: a  digital subtraction angiographic
study. Stroke 34(10):2410-2414
98. Tu J, Karunanayaka A, Windsor A, Stoodley MA
(2010) Comparison of an animal model of arteriove-
nous malformation with human arteriovenous mal-
formation. J Clin Neurosci 17(1):96-102
99. Ujiie H, Tamano Y, Xiuling L, Hori T (2000) Hae-
morrhagic complications after total extirpation of
huge arteriovenous malformation. J Clin Neurosci.;
7 Suppl 1:73-77
100. Valavanis A, Christoforidis G (1999) Endovascular
management of cerebral arteriovenous malforma-
tions. Neurointerventionist;1:34–40
101. Viñuela F, Dion JE, Duckwiler G, Martin NA, Lylyk P,
Fox A et al (1991) Combined endovascular embo-
lization and surgery in the management of cerebral
arteriovenous malformations: Experience with 101
cases. J Neurosurg 75:856–864,
Clinical
Medicine
102. V
 iñuela F, Duckwiler G, Guglielmi G (1997) Contri-
bution of interventional neuroradiology in the thera-
peutic management of brain arteriovenous malfor-
mations. J Stroke Cerebrovasc Dis 4:268–271
103. V
 inuela F, Nombela L, Roach MR, Fox AJ, Pelz DM
(1985) Stenotic and occlusive disease of the ve-
nous drainage system of deep brain AVMs. J Neu-
rosurg 63(2):80-84
104. V
 irchow. R (1854) Uber cavernbse (erectile)
Geschwiilste und Teleangiektasien.Virchows Arch.
path. Anat. 6: 526-554
105. W
 akhloo AK, Lieber BB, Siekmann R, Eber DJ,
Gounis MJ (2005) Acute and chronic swine rete
arteriovenous malformation models: hemodynam-
ice and vascular remodeling. Am J Neuroradiol
26(7):1702-1706
106. W
 allace RC, Flom RA, Khayata MH, Dean BL,
McKenzie J, Rand JC et al (1995) The safety and
effectiveness of brain arteriovenous malforma-
tion embolization using acrylic and particles: the
experience of a  single institution. Neurosurgery
37(4):606-615
107. Y
 asargil MG (1987) Microneurosurgery IIIA. Thieme
New York, p.7
108. Y
 oung WL, Kader A, Pile-Spellman J, Ornstein E,
Stein BM (1994) Arteriovenous malformation drain-
ing vein physiology and determinants of transnidal
pressure gradients. The Columbia University AVM
Study Project. Neurosurgery.;35(3):389-395
109. Y
 oung WL, Pile-Spellman J, Prohornik I, Kader A,
Stein BM (1994) Evidence for adaptive autoregula-
tory displacement in hypotensive cortical territories
adjacent to arteriovenous malformations. Colum-
bia University AVM Study Project. Neurosurgery
34(4):601-610
110. Y
 uki I, Kim RH, Duckwiler G, Johan R, Tateshima S,
Gonzales N, et al (2009) Treatment of brain arterio-
venous malformations with high-flow arteriovenous
fistulas: risk and complications associated with en-
dovascular embolization in multimodality treatment.
J Neurosurg.;16 DOI: 10.3171/2009.9.JNS081588
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