an introduction to vascular neurosurgery

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AND SHOULD NOT BE PART OF THE BOOK WHEN PRINTED.]

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COORDINATOR:

IOAN ȘTEFAN FLORIAN, MD, PhD

VICTOR VOLOVICI, MD

CRISTINA-CATERINA ALDEA

IOAN-ALEXANDRU FLORIAN

Intraoperative photographs, CT, MRI, CTA, MRA were provided by

Professor Ioan-Ștefan Florian, MD, PhD, from his personal

collection.

Angiographies from Chapter 4 were offered by Lucian Mărginean,

MD, PhD.

Artwork: Ioan-Alexandru Florian

Rareș Mișcov

Desktop publishing and design: Adrian Zoican

CONTENTS

FOREWORD………………………....5

SECTION I:

Anatomy……………………..…...7

SECTION II:

Imaging in vascular lesions…….47

SECTION III:

Cerebrovascular disease….……63

SECTION IV:

Aneurysms and AVMs…………85

FOREWORD

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Vascular neurosurgery, while not the youngest subspecialty of neurosurgery, is by far the

most challenging and with an amazing evolution in terms of possibilities and options for the

treatment of vascular intracranial pathology.

Starting from very humble beginnings in the late 1700's it has evolved into one of

the most challenging domains that exists on the planet, with its specialists being able to

perform what is sometimes rightfully considered to be acts of magic inside the delicate

tissue of the brain with minimal or no damage. Aneurysms and intracranial vascular

malformations have been around as long as human history but it is only very recently that

they have also been recognized and treated. From the first use of a Cushing silver clip by

Dandy in 1935, the aneurysm clip has become a cornerstone and a symbol of what

neurosurgery is today. Even in the era of minimally invasive procedures, endovascular

treatment and progressively more aversion towards open surgery, good microsurgery still

remains the best, safest, most important manner to treat intracranial vascular pathology.

It is because of these and many other reasons that we decided to set up the second

edition of the Masterclass as a vascular-dedicated endeavour, to inspire and teach the

generation of future vascular neurosurgeons who are just now realizing where their loyalties

lie in this extraordinary field of ours.

We also thought it would be a welcome addition if next to the course participants

could receive a book detailing several more important aspects which will be discussed

during the course and this lies here before you in an electronic format.

We wish all the participants an open mind and to enjoy the second edition of the

Neurosurgical Masterclass in Cluj!

Professor Ioan Stefan Florian, MD, PhD

Cluj-Napoca, 28.02.2014 Victor Volovici, MD

Cristina-Caterina Aldea

Medial dissection of the Internal Carotid Artery in order to expose the optic chiasm –

anatomical relationships

CHAPTER 1 THE ARTERIAL ANATOMY OF THE BRAIN

VICTOR VOLOVICI

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THE CAROTID ARTERY AND THE ANTERIOR CIRCULATION

Operating succesfully in Neurosurgery requires an in-depth three-dimensional

anatomical knowledge, good knowledge of radiology and of the imaging options

used in diagnosis of the pathology to be operated upon and much practice in the

operating room.

The cerebrum receives blood flow from the two internal carotid arteries

and from the two vertebral arteries, namely from their terminal arteries, the

anterior, middle and posterior cerebral arteries, interconnected to form the so-

called circle of Willis (Figure 1.1) at the base of the cerebral hemispheres.

The Common Carotid artery arises from the brachiocephalic trunk on

the right side and from the aortic arch on the left side, resepctively, and courses

laterally to the trachea in the vagina carotica in the anterior portion of the neck

together with the internal jugular vein and the vagus nerve. It bifurcates into the

external and internal carotid arteries at the level of C4.

An article form Rhoton in 1981 provides an excellent anatomical study of

the carotid artery at a point in time where microsurgery for intracerebral

aneurysms, already pioneerd by Yasargil in the 60's, begun to take off at an

extremely rapid pace and in-depth microsurgical anatomical studies were required.

AN INTRODUCTION TO VASCULAR NEUROSURGERY

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.

Figure 1.1 – Circle of Willis

SECTION I: ANATOMY CHAPTER 1: THE ARTERIAL ANATOMY OF THE BRAIN

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The Internal Carotid (Figure 1.2) may be divided thus into several

segments, each with anatomic particularities and different approaches. It is not the

purpose of this very short review to go in-depth into, for example the Dolenc

approach to the cavernous sinus and its very complicated anatomy, so we shall

only present a quick run-throug of concepts aiding and laying the foundation even

for the study of cerebrovascular disease.

There are many modalities to divide the carotid artery into segments and

there is no international consensus, but a useful division to remember is as follows:

C1- cervical segment, C2- petrous segment, C3- cavernous segment,

C4- supraclinoid segment, which can be further divided into C4- clinoid segment,

C5- ophtalmic segment, C6- communicating segment, C7- choroidal segment.

Figure 1.2 – Carotid artery segments


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The divison into segments helps with the precise localisation of an

aneurysm in the course of the internal carotid and with anatomical correlations

with the digital subtraction angiography, allows planning of the operative

approach and establishes in one instance all anatomical relationships related to

one segment in particular. E.g. a lesion in the cavernous sinus automatically

implies an intimate relationship with cranial nerves III, IV, VI , V1 and V2, which

should be taken into consideration when plannin g the approach.

The cervical carotid, C1, does not present any branches and courses in

the carotid canal to become the petrous portion. C2 usually sends off 2 branches,

the tiny caroticotympanic and pterygoid arteries, which enter the tympanic

cavity via a foramen in the canalus caroticum and the pterygoid canal together

with the vidian nerve respectively.

The C2 portion then courses over the foramen lacerum- without passing

through it, to enter the cavernous sinus. Here C3 gives off inconstantly 4 branches,

the dorsal meningeal branch for the dura of the upper clivus, the tentorial artery

and the inferior hypophyseal artery. These are usually grouped in a meningo-

hypophyseal trunk, barely visible on the DSA, save for rare situations where

there is a dural fistula involving the a. meningea posterior. The last branch is the

infero-lateral trunk, which runs to the lateral wall of the cavernous sinus.

Inconstantly, an artery for the capsule of the pituitary has been described, known

as the McConell capsular artery.

The most relevant portion of the internal carotid is the intracranial

supraclinoid portion, after the emergence of the carotid from the cavernous sinus.

Here the artery gives off the 3 important branches which also divide this portion

into 3 segments, each with its own particular anatomical correlations, the

ophtalmic artery which represents the proximal boundary of the ophtalmic

segment, the posterior comunicating artery, setting the proximal boundary for

the communicating segment C6, and the anterior choroidal, as the proximal

boundary for the choroidal segment. In C7 the internal carotid suffers the

bifurcation in its terminal branches, the anterior and middle cerebral arteries.


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Before we move on to the terminal arteries of the internal carotid, we

need to have a short look at the other 3 important intracranial branches. The

ophtalmic artery arises under the optic nerve and pases anteriorly and laterally to

assume a superolateral position to the internal carotid, entering the optic canal

together with the optic nerve heading towards the orbit. It initially sits inferiorly to

the nerve, but then crosses over it to assume a medial position in the orbit. Its

exposure during surgery usually requires a so-called Dolenc approach, with

removal of the anterior clinoid process with the help of a 1-mm diamond drill. The

perforating arteries arising from the artery serve the stalk of the pituitary, the optic

chiasm and the optic nerves.

The next branch of the supraclionoid portion of the carotid is often not

encountered during her surgical exposure and may present itself in a variable

number, ranging from one relatively bigger trunk to 5 thin arteries, namely the

superior hypophyseal artery(ies). They supply the anterior lobe of the

pituitary, but not the infundibulum and the floor of the 3rd ventricle which owe

their blood supply to the next branch.

The posterior communicating artery, embirologically the origin of the

posterior cerebral artery, poses a series of problems with reagard to its enormous

variability and anatomical relationships. Aside from being a common site for

aneurysms(its point of origin from the internal carotid), it can range from being

hypoplastic to being the primary source of blood flow to the posterior circulation

in the case of a "fetal" PCom. It passes posteromedially to join the posterior

cerebral artery in the interpeduncular cistern. Its trajectory is in a subarachnoid

cisternal compartment limited medially by the pituitary stalk and infundibulum,

laterally by the medial surface of the uncus, superiorly by the optic tract and

floor of 3rd ventricle and inferiorly by the roof of the cavernous sinus and

dorsum sellae. As mentioned before, its exact trajectory is extremely variable and

not the subject of this review. About 4-14 perforating arteries arise from the

PCom, supplying blood to the infundibulum and to the floor of the 3rd ventricle.

The largest and most important branch is the premamillary artery, also known as

the "anterior thalamoperforating artery".


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The next and final collateral artery before the bifurcation of the ICA is the

anterior choroidal artery. It courses posteriorly and laterally under the optic

tract, entering the temporal horn through the inferior choroidal point posteriorly to

the uncus, which marks the beginning of the choroidal fissure. The AChA sends

off branches to the optic tract, crus cerebri, lateral geniculate bodies and uncus in

its cisternal segment. Furthermore, it provides numerous branches for the optic

radiation, globus pallidus, mesencephalon, thalamus, posterior limb of the internal

capsule. Inside the temporal horn it anastomoses with the lateral posterior

choroidal artery (PLChA).

Variably, 1-9 perforating arteries arise from the choroidal segment(C7) of

the carotid artery, and occupy the posterior half of the central region of the anterior

perforated substance.

The anterior perforated substance is also the landmark anterior to which

the carotid artery bifurcates into its terminal branches, the anterior and middle

cerebral arteries.

The Anterior Cerebral Artery (Figures 1.3 and 1.4) is the medial

terminal branch of the internal carotid. It courses on the medial side of the

hemispheres, providing vascularization mainly to the frontopolar region, part of

the superior frontal gyrus and the mesiofrontal structures, paracentral lobule

and precuneus and to deep structures. There are multiple systems which attempt

to divide the anterior cerebral artery in segments, and we find the angiographical

method most useful, as the it is easy to correlate the DSA findings with the

microsurgical anatomy encountered intraoperatively. There are, thus, 5 segments:

A1, extending from the bifurcation to the ACom(anterior communicating artery),

A2, extending from the ACom to the junction between the rostrum and the genu of

the coprus callosum, A3, extending from the genu of the corpus callosum to the

point where the artery turns sharply and posteriorly over the corpus callosum

following its course, A4 and A5, extending above the corpus callosum from the

genu to the splenium. The limit between A4 and A5 is a plane passing

posteriorly to the coronal suture and intersecting the A4- A5 segment, also called


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the horizontal segment. The A2-A3 segment is also known as the ascending

segment, and the distal portion of the anterior cerebral artery to the anterior

communicating is commonly known as the pericalosal artery. Of its many

branches, the discussion needs to fan out to the most important ones. Thus, 1-11

medial lenticulostriate perforators arise usually from the posterior aspect of A1 and

enter the medial half of the anterior perforated substance. The anterior

communicating artery ensures communication between the 2 A1 segments, which

are in only about 25% of equal calibre. It originates embriologically from a

multitude of vascular channels which will coalesce and form one communicating

channels in about 75% of cases, explaining the high degree of variability of the

ACom anatomy which needs to be properly diagnosed before the first incison is

made. The Acom may also present 1-4 perforators, supplying the infudibulum,

the anterior perforated substance, the subcallosal area and the preoptic areas

of the hypothalamus. A very important branch, the recurrent artery of

Heubner, appears in 78% of cases from the procimal A2 and is usually seen upon

retraction of the frontal lobe prior to the visualization of the A1 segment. It is the

largest and longest branch heading towards the anterior perforated substance,

initially accompanying M1 in the first medial part if the Sylvian fissure before

entering the anterior perforated substance in its full mediolateral extent. Last but

not least, the basal perforators, passing posteriorly to enter the optic chiasm and

lamina terminalis. It is also worth mentioning that the 2 medial branches the

orbitofrontal and frontopolar arteries usually arise from the A2 segment and that

most of the vascularization of the medial hemisphere coming from the anterior

cerebral artery usually only arises from the pericalossal artery and very rarely from

the calosomarginal artery.


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Figure 1.3 – Anterior cerebral artery – frontal view

Figure 1.4 – Anterior cerebral artery – sagittal view


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The second terminal branch of the internal carotid artery is the Middle

Cerebral Artery (Figures 1.5 and 1.6). It is divided into 4 segments, to allow for a

better microsurgical-radiological correlation. M1, or spehnoidal segment, M2, or

insular segment, M3, the opercular segment and M4, the cortical segment. The

M1 segment extends from the bifurcation of the internal carotid anteriorly to the

anterior perforated substance to the limen insulae. Anatomically, the proximal

segment is in relationship with the anteromedial uncus, the ala minor of the

sphenoid and the anterior perforated substance. The distal segment rests on the

planum polare, all the way to the apex of the insula of Reil called the monticulus.

M1 gives off 2 types of branches, the lateral lenticulostriate arteries which mostly

arise from its posterior aspect and the early branches usually temporopolar, which

arise before the bifurcation of M1, that occurs in 86% of cases before the limen

insulae. M2 or the insular segment extends from the limen insulae to the circular

or limiting sulcus of the insula. It most often appears as a superior and an inferior

trunk and at the edges of the limiting sulcus it fans out into the opercular

compartment as M3 branches. Extremely essential for operative exposure of the

middle cerebral artery is the relationship with the pars triangularis of the inferior

frontal gyrus. The genu of the middle cerebral artery is the sharp turn it makes at

the level of the monticulus, or insular apex, in order to pass from the basal surface

of the hemisphere to the lateral surface of the cerebrum. The genu is located a few

milimeters deep and ventral to the pars triangularis of the inferior frontal gyrus,

limited by the horizontal and ascending sulci. This relationship is useful for a rapid

intraoperative orientation: should the aneurysm be located in the vincinity of the

genu of the middle cerebral artery, then opening the fissure should start proximally

to the pars triangularis. If it is located at the level of the genu, then splitting the

sylvian fissure may start just proximally to the pars triangularis and if it is distal to

the genu then splitting may begin at the level of the pars triangularis, ensuring a

minimal exposure with good proximal control. The M3 or opercular segment has

an anatomical relationship with the frontoparietal operculum superiorly and the

temporal operculum inferiorly. An anatomical landmark of great importance is the

so-called M-point of Sylvian point, visible on the angiography. It is defined as the

point which is located behind the insula, above the medial end of the longest of the


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transverse temporal gyrus, the gyrus of Heschl. It displays on the angiography the

posterior end of the insula and the central core, atrium, thalamus and its endpoint

the pulvinar. The last segment is the M4 or cortical segment. It extends from the

opercula superiorly and inferiorly on the convexity, supplying a very large area

with blood.

Figure 1.5 – Middle cerebral artery – axial section


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Figure 1.6 – Middle cerebral artery segments

THE POSTERIOR CIRCULATION

To complete the Circle of Willis, we will now refer to the Posterior Cerebral

Arteries. These are actually the terminal branches of the Basilar artery, but they

are the direct link of the posterior circulation to the anterior circulation via the

previously described posterior communicating artery, subject to extreme

anatomical variability. Moreover, they are embirologically branches of the

internal carotid and only after birth do they develop as terminal branches of the

basilar, hence the need to present them after the anterior circulation. The posterior

cerebral artery is divided into 4 segments. The P1 segment reaches from the basilar

bifurcation in the interpeduncular cistern to the place where the PCom joins the

posterior cerebral artery. The P2 segment begins at the union of the PCom with

the PCA to the quadrigeminal cistern. This segment is further divided, in order to

aid operative planning into P2A and P2P segments. P2A begins at the union with


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the PCom and courses around the crus cerebri. At the posterior margin of the crus

begins the P2P and it courses in the ambient cistern to the tegmentum of the

midbrain, paralelly and inferiorly to the basal vein, inferolaterally to the lateral

geniculate bodies and pulvinar and medially to the parahypocampal gyrus, entering

the quadrigeminal cistern. The P3 segment begins under the pulvinar and ends at

the anterior limit of the anterior calcarine sulcus, being in most cases already

divided in its terminal branches, the calcarine and parieto-occipital arteries before

reaching this point. A point of interest on DSAs is the quadrigeminal point,

which marks the posterior limit of the mesencephalon on an angiography, defined

as the point where the 2 PCAs are closest to each other in the quadrigeminal

cistern. The P4 segment represents the cortical branches of the PCA. PCA gives

off the main branches in the shape of posterior thalamoperforating, direct

perforating, short and long circumflex, thalamogeniculate, MPChA and LPChA,

inferior temporal, parieto-occipital, calcarine and posterior pericallosal arteries.

The many and essential posterior thalamogeniculate arteries arise from P1 and

enter the brain through the posterior perforated substance and interpeduncular

fossa, supplying the posterior thalamus, hypothalamus, subthalamus, substantia

nigra, nucleus rubrum, oculomotor and trochlear nuclei, oculomotor nerve,

mesencephalic reticular formation, pretectum, posterior floor of 3rd ventricle and

posterior portion of the internal capsule. The direct perforating arteries mainly

arise from P2A and supply the crus cerebri. The short and long circumflex arteries

arise from P1 and supply the lateral geniculate body and the colliculi respectively.

The thalamogeniculate arteries arise from P2A and P2P equally. The medial

posterior choroidal artery (MPChA) usually arises from P2A, coursing laterally

to the mesencephalon, then turning sharply at the level of the pulvinar to proceed

laterally to the colliculi and epyphysis to enter the 3rd ventricle via the velum

interpositum and via the foramen of Monro in the choroid plexus of the lateral

ventricles. It supplies the crus cerebri, tegmentum, geniculate bodies, colliculi,

pulvinar, pineal gland and medial thalamic nuclei. On a lateral projection on a

DSA the MPChA is easiest recongizable by its shape resembling the number 3,

with the inferior curve being its sharp turn at the level of the puvinar and the

superior curve being the point where int crosses the colliculi before entering the


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velum interpositum. The lateral posterior choroidal artery (LPChA) usually

arises from P2P, passing directly laterally to enter the choroidal fissure to supply

the choroid plexus in the atrium and the temporal horn, and anastomosing with the

AChA. Inferior temporal arteries provide blood supply to the basal surface of the

temporal and occipital lobes, being made up of the hippocampal, anterior, middle

and posterior arteries, the former 2 usually arising from P2A and the latter 2

arising from P2P. The terminal branches of the PCA are the pariet-occipital and

calcarine arteries, each coursing in the homonymous fissure. The parieto-occipital

artery gives off the posterior paericallosal artery in 65% of the cases, providing

blood supply to the splenium of the corpus callosum.

In order to conclude the brief presentation of the blood supply of the

brain, essential for understanding the basics of cerebrovascular disease, we will

present the infratentorial circulation, beginning with the vertebral and basilar

arteries and proceeding to the essential 3 branches, the superior cerebellar artery

(SCA), the anterior inferior cerebellar artery (AICA) and the posterior inferior

cerebellar artery (PICA) – Figure 1.7. It is of interest to note the endeavour of

scholars such as Prof. Rhoton to find a logic in the extremely complicated

infratentorial circulation. As such, he describes the "rule of 3", as such the

brainstem presents 3 parts, the cerebellum 3 surfaces (petrosal, tentorial and

suboccipital), 3 cerebellar peduncles, 3 fissures (cerebellomesencephalic,

cerebellopontine, cerebellomedullary), 3 main arteries mentioned earlier, 3 venous

draining groups (petrosal, galenic and tentorial). As such, we define 3

neurovascular complexes: the superior complex, SCA, and cranial nerves III, IV,

V and mesencephalon, the middle complex, AICA, nerves VI, VII, VIII, pons and

inferior complex, PICA, IX, X, XI, XII and medulla.


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Figure 1.7 - Posterior fossa blood supply

The Vertebral Artery arises from the subclavian artery as one of the 2

main superior collateral branches. It courses medially and superiorly to reach the

lowest foramen transversarium, usually C6, after which it ascends through all

foramina in front of the cervical nerve roots. At C2 it deviates laterally to enter a

more laterally placed foramen transversarium of the atlas. It then passes behind

the lateral mass of the atlas and atlanto-condylar joint, being pressed into the

groove on the upper surface of the posterior arch of the atlas, coursing along the

floor of the suboccipital triangle, entering the vertebral canal by passing

anteriorly to the atlanto-occipital membrane in order to pierce the dura. Here, it

gives off the posterior meningeal artery, the posterior spinal artery, muscular

branches to the deep cervical musculature and very infrequently the PICA. The


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intradural aspect begins here, at the edge of the foramen magnum, where the dura

thickens to form a funnel-like structure around the artery. It is also bound by

fibrous dependencies of the dura with the first cervical nerve and the posterior

spinal artery exiting through this foramen with the vertebral artery. The intradural

portion is divided academically into 2 segments, the lateral medullary coursing

until the preolivary sulcus and the anterior medullary segment coursing until the

union with the VA on the opposite site in front of the pontomedullary sulcus to

form the basilar artery. This latter segment also rests on the clivus. The branches

that arise in this region from the vertebral artery are the posterior spinal, anterior

spinal, PICA and anterior and posterior meningeal arteries.

The Basilar Artery, created from the union of the vertebral arteries,

courses in a very shallow groove on the surface of the pons. Its length spans the

distance between the pontomedullary sulcus to the level of the emergence of the

3rd cranial nerves from the pedunculli cerebri. It may sometimes have a tortous

trajectory and may even deviate so laterally as far as the origin of the abducens or

of the facial nerve. After crossing the oculomotor nerves it divides in its terminal

branches, the posterior cerebral arteries, discussed earlier. It gives off pontine,

labyrinthine, AICA, SCA and posterior cerebral arteries. The pontine branches

are perforators that either enter the pons directly or navigate it circumferentially

on its lateral aspect and give off small vessels which penetrate the pons.

From superior to inferior, the first artery to be discussed, representing the

first neurovascular complex is the Superior Cerebellar Artery. It is closely

related to the cerebellomesencephalic fissure, the oculomotor, trochlear and

trigeminal nerves and the mesencephalon. They usually arise close to the basilar

apex, under the oculomotor nerve. In 75% of cases there is a point of contact with

it, 100% of cases have a point of contact with the trochlear. As it encircles the

brainstem it sometimes makes a caudal loop which can reach all the way to the

trigeminal nerve on its posterior or posteriomedial surfaces, causing the

neruovascular conflict leading to trigeminal neuralgia. The proximal SCA courses

medially to the free edge of the tentorium and after passing above the trigeminal

nerve it enters the cerebellomesencephalic fissure, where its branches fan out into


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the precerebellar arteries. After exiting the cerebellomesencephalic fissure, it is

once again medial to the free edge of the tentorium and its branches pass

posteriorly under the tentorial edge to be distributed to the tentorial surface of the

cerebellum. The SCA usually bifurcates into a rostral and a caudal trunk, and it

gives off perforating arteries tot he brainstem and cerebellar peduncles. The rostral

trunk usually supplies the vermis and surrounding paravermian areas, whilst the

caudal trunk supplies blood to the hemisphere on the suboccipital surface.

Academically, it is divided in several segments. The anterior pontomesencephalic

segment extends to the anterolateral margin of the brainstem. The lateral

pontomesencephalic segment loops caudally and sometimes reaches the Vth nerve

root entry and terminates at the anterior margin of the cerebellomesencephalic

fissure. The basal vein and PCA course parallel to this segment. The

cerebellomesencephalic segment can be found in the homonymous fissure, which

deepens medially and is deepest in the midline above the superior medullary

velum. It then fans out in the shape of cortical branches, with the rostral trunk

supplying the medial area and the caudal trunk supplying the lateral area of the

tentorial surface of the cerebellum. The branches of the SCA are perforating,

precerebellar and cortical. The perforating ones may be of a direct or circumflex

type, with the direct ones entering the brainstem directly and the circumflex

encircling the brainstem before entering it. The latter circumflex ones may also be

divided into long and short circumflex, with the short ones travelling less than 90

degrees around the brainstem. The perforators arise from the main, rostral and

caudal trunks, the most frequent type of which is circumflex. The precerebellar

arteries arise in the cerebellomesencephalic fissure to supply the deep cerebellar

grey matter. They are divided in a medial group that passes between the superior

medullary velum and the central lobule and a lateral group that passes between

the superior and middle cerebellar peduncles and the wings of the central

lobule. After leaving the cerebellomesencephalic fissure, the trunks of the SCA

give off hemispheric/vermian arteries. The hemispheric ones are usually divided

into medial intermediate and lateral, depending on the third of hemisphere which

the vascularize. The vermian branches, usually 2, supply blood to the median strip


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which borders the midline and a paramedian strip bordeing the hemispheric

surface.

More inferiorly, we encounter the Anterior Inferior Cerebellar

Artery(AICA). It usually arises from the lower third of the basilar artery,

constituting together with the abducens, facial and vestibulocochlear nerves and

the pons the second neurovascular complex, around the cerebellopontine angle. Its

anatomical relationships are with important structures related to many operations

of the posterior fossa, namely the pons, lateral recess, foramen of Luschka,

cerebellopontine fissure, petrosal surface of the cerebellum. After it arises from the

basilar artery, it encircles the pons near the abducens and the facial, sensing

branches to them and to the internal acoustic meatus. It then passes in relationship

to the flocculus, on the middle cerebellar peduncle and supplies blood to the

petrosal surface of the cerebellum. Near the facial-vestibulocochlear complex it

divides into a rostral and a caudal trunk. The former usually courses above the

flocculus and at the level of the middle cerebellar peduncle distributes itself to the

superior lip of the cerebellopontine fissure and to the superior part of the petrosal

surface of the cerebellum. The caudal trunk supplies the inferior petrosal surface of

the cerebellum, with tha adjacent flocculus and choroid plexus coming out of

Luschka. Academically, we divide AICA into several segments. The anterior

pontine ends at the level of the long axis of the olive, usually being in contact with

the abducens at this point. The lateral pontine segment passes through the CPA,

above, below or throught the facial nerve and is related to the internal acoustic

meatus, sometimes looping in to form an arterial loop going into the meatus itself.

It is moreover intimately in contact with lateral recess and the choroid plexus

from the foramen of Luschka. This is where AICA gives off its nerve-related

branches, which we will describe shortly. The flocculonodular segment begins

where the trunks pass above or under the flocculus to the middle cerebellar

peduncle and cerebellopontine fissure. The final segment is composed of the

cortical branches supplying the petrosal part of the cerebellum. The branches of

the AICA are subject to a great deal of variability, beginning with the place of

bifurcation, as the vascularized territory is significantly different when the main


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trunk splits proximally or distally to the facial-verstibulocochlear complex.

However, constantly the branches of the rostral trunk anastomose with the

branches of the SCA and those of the caudal trunk anastomose with those of the

PICA. It also gives rise to perforating arteries to the brain stem, choroidal arteries

to the choroid plexus and nerve-related arteries. The nerve-related branches stem

in the CP angle and are related to the facial-vestibulocochlear complex. These

branches are the labyrinthine artery, which enter the internal auditory canal

and supply the bone and dura of this canal, as well as give off vestibular, cochlear

and vestibulocochlear branches, supplying the organs of the inner ear. The

recurrent perforating arteries arise in the close proximity of certain nerves

which they follow and supply blood to until the meatus and then they make a sharp

turn and return to the root of the nerves to vascularize this area and the brainstem

around it. The subarcuate artery originates medially to the porus acusticus and

enters the subarcuate canal via the subarcuate fossa. It is amenable to

coagulation safely when opening the internal acoustic meatus, it supplies the

petrous bone in the vincinity of the semicircular canals. The subarcuate canal may

be a route of extension of infections in complicated cases of mastoiditis to the

meninges and superior petrosal sinus. The terminal cortical branches of the rostral

and caudal trunks of AICA supply the superior and inferior petrosal surfaces of the

cerebellar hemisphere respectively, anastomosing as described with branches of

the SCA and PICA, subject to a high degree of variability with respect to the exact

area of vascularization.

The final and most complex artery is the Posterior Inferior Cerebellar

Artery (PICA). Infratentorially, it represents together with the medulla, the

glossopharyngeus, vagus, accesory and hypoglossus nerve the inferior

neruovascular complex. It has the most complex, tortous and variable course of

all the arteries. It is related to the cerebellomedullary fissure, the inferior

cerebellar peduncle and the suboccipital surface of the cerebellum. It arises

from the vertebral artery near the inferior olive, laterally or anteriorly to it. As it

courses towards the anterolateral edge of the medulla, it passes rostrally, caudally

or between the rootlets of XII, and at the posterolateral margin of the medulla


26 | P a g e

oblongata it courses between the fibers of the IX, X and XIth nerves. After that it

encircles the cerebellar tonsil and enters the cerebellomedullary fissure and passes

dorsally to the lower half of the roof of the 4th ventricle. After exiting the fissure,

its cortical branches are distributed to the vermis and the hemisphere of the

suboccipital surface. Academically, it is also divided into segments, but these are

more complex than those described for the SCA and the AICA. The anterior

medullary segment extends posteriorly past the hypoglossus to the level of the

boundary between the anterior and lateral medulla (a line that passes through the

most porminent part of the inferior olive). The lateral medullary segment ends at

the level of origin for the IX, X and XIth nerves. While the first segment is subject

to variability because of variability in origin form the vertebral artery, the lateral

medullary segment is one of the most constant ones. The third segment is called

the tonsillomedullary segment and it extends to the caudal half of the tonsil. The

proximal portion of this segment puts PICA in a relationship with the lateral recess

after which is dives posteriorly to reach the inferior pole of the tonsil. It then

turns rostrally on the medial side of the tonsil, forming a caudal loop easily

recognizable on the DSA and helpful for orientation. The fourth segment is called

the telovelotonsillar segment, which also happens to be the most complex one. It

begins during PICA's ascent on the medial side of the tonsil towards the roof of the

fourth ventricle and ends where it exits the fissures in orde to supply the vermis

and the hemispheres. It is here that PICA usually exhibits a convex loop called the

cranial loop, also useful for orientation on the DSA. An important anatomical

relationship of this loop is that it is caudal to the fastigium, being located between

the cerebellar tonsil and tela choroidea below and the inferior medullary velum

above, with the apex of the loop usually situated over the inferior medullary

velum, sometimes extending all the way to the fastigium, but usually remaining

under it. Branches that arise in this complex segment supply the tela choroidea and

the choroid plexus of the fourth ventricle. The final segment is the cortical

segment, which begins when the trunks of PICA exit between the vermis and

tonsil medially and the hemisphere laterally, and gives off the terminal branches.

The PICA bifurcates into lateral and medial trunks before it exits to the surface of

the hemisphere. The medial trunk usually climbs the vermohemispheric fissure to


27 | P a g e

reach the vermis and the lateral trunk passes via the telovelotonsillary fissure to

reach the suboccipital cerebellar surface. The medial trunk gives off terminal

branches for the inferior vermis and adjacent parts of the tonsil and hemisphere.

The lateral trunk divides into a large hemispheric trunk which supplies blood to

the hemisphere and several smaller tonsillar branches for the tonsilla. The

bifurcation occurs on the medial part of the tonsil. While passing through the

tonsilomedullary fissure, the turnks give branches for the medulla and while

passing through the telovelotonsillar fissure branches arise for the dentate

nucleus. Perforating arteries occur within the three medullary segments and are

either direct or circumflex. They enter the brainstem and intermingle with those

that arise from the vertebral arteries, usually from the part distal to the orogin of

the PICA. Other collaterals are the choroidal branches, which supply the tela

choroidea and the plexus of the fourth ventricle, near the midline or the medial part

of the lateral recess. Most of these arteries arise in the tonsillomedullary and

telovelotonsillar segments and the part of the plexus not supplied by PICA is

supplied by AICA. The cortical branches are the terminal branches of PICA and

they provide blood to the suboccipital surface of the cerebellum. They are divided

into hemispheric, vermian and tonsillar groups, the vermian usually arising from

the medial trunk and the rest from the lateral trunk, as previously mentioned. Each

half of the vermis is divided, just as in the case of the AICA, into paramedian and

median segments and the hemisphere is also divided in medial, intermediate and

lateral segments.

This has been a brief review of the most important aspects of the

immenisty and complexity which is the vascular system of the cerebrum. Without

permanent study of CTs, angiographies, dissectioons, books and intraoperative

anatomy one will never be able to reach a satisfying level in order to become a

vascular neurosurgeon. It is therefore of the essence that these concepts to be

repeated over and over again until one is able to juggle the concepts without

difficulty. It is our belief that this is the only path to proficiency and mastery of

cerebrovascular operations, most often the most challenging in all of neurosurgery.

CHAPTER 2 CEREBRAL VENOUS BLOOD FLOW

CRISTINA C. ALDEA

28 | P a g e

C Cerebral Venous drainage patterns possess a high degree of variability not only

between different individuals but also when regarding the two hemispheres of a

given brain. These variations may pose limitations for detailed anatomic

understanding. However, normal anatomic variants characteristically display a

distinct set of common features (1).

Specific Anatomic and Physiologic Features

The cerebral venous system forms in the pia-arachnoid transitional area where

small venous channels drain the underlying brain parenchyma. These channels will

form the cerebral veins which will course through the subarachnoid space and

subarachnoid cisterns. The cerebral veins possess no valves and have thin walls

(owing to the absence of the tunica muscularis). Consequently blood flow within

these veins is possible in both directions and they have the capacity to remain

dilated and even become arterialized in certain pathological entities. The fact that

any change in the central venous pressure is transmitted to the intracranial

compartment is also explained by these two particularities with implications in

several pathological entities such as idiopathic intracranial hypertension (3). The

cerebral veins pierce the arachnoid membrane to cross the subdural space as

bridging veins in order to drain to the nearest dural venous sinus. The veins which

drain the central core and white matter course through the walls of the ventricles

and in the basal cisterns to collect into either the great vein of Galen, the basal

vein of Rosenthal or the internal cerebral vein. These in turn will drain into

dural venous sinuses.


29 | P a g e

In the jugular fossa, the sigmoid sinus will become the internal jugular

vein, which represents the major site of venous outflow from the intracranial

compartment. Other sites of venous outflow to the extracranial compartment are

the veins of the orbit and the venous plexuses around the vertebral arteries. The

diploe and scalp veins may act as collateral outflow pathways (2).

The diploic veins course between the external and internal tabulae of the

skull and connect the scalp veins with the underlying meningeal veins and dural

sinuses. Moreover these veins characteristically do not cross suture lines.

Damage to the diploic venous system may cause postoperative bleeding and may

impact the healing of the cranium after neurosurgical procedures. The parietal

bone harbors most of the diploic vessels whilst the squamous part of the temporal

bone presents no diploic veins. The anterior diploic system connects with the

superior sagittal sinus while the posterior diploic system displays connections

with the transverse and sigmoid sinuses. It is important to note that the point of

drainage for the frontal diploic vein is located near the supraorbital notch and that

the point of drainage of the anterior temporal diploic vein is located in the

pterional area. These vessels can be damaged during supraorbital, modified

orbitozygomatic, and pterional craniotomies (4).

The emissary veins connect the superficial veins with the underlying

dural sinuses by passing through the cranium. They pass through channels of

quite some variability. There are three commonly described groups: the parietal

emissary veins which connect the superior sagittal sinus with the overlying scalp

veins; the mastoid emissary veins which connect the transverse sinus with the

occipital and posterior auricular veins and passing through the mastoid foramen

and the anterior condylar emissary veins which connect the inferior petrosal sinus

with the suboccipital veins and passing through the hypoglossal canal (2).

The cerebral venous system can be didactically divided into a superficial

venous system and a deep venous system. The most important confluence point

SECTION I: ANATOMY CHAPTER 2: VENOUS BLOOD FLOW

30 | P a g e

between the superficial and deep venous systems is at the level of the straight

sinus. This sinus collects venous outflow from both great cerebral veins of Galen,

which are part of the deep cerebral venous system, as well as from superficial

veins draining the cerebral cortex. The key overlapping site of the extracranial

and intracranial venous systems is the cavernous sinus. At this level, venous

outflow from the ophthalmic veins is drained together with the venous outflow of

the sphenoparietal sinus, hypophyseal veins, the middle cerebral vein and

uncal vein (2). The cavernous sinus also receives venous drainage from the

pterygoid plexus, which lies outside the skull base through the foramen of

Vesalius, the foramen ovale and other foraminae innominata. Communication

between the intracranial and extracranial compartments is also aided by the

emissary and diploic veins.

DURAL VENOUS SINUSES

Dural venous sinuses are channels that form between two layers of dura. This

permits them to maintain their patency even if the intracranial pressure rises. As

the cerebral veins, they lack valves.

The superior sagittal sinus (Figure 2.1) courses along the midline

following the convexity of the calvarium. It extends from immediately posterior

to the foramen caecum all the way to the internal occipital protuberance where

it joins the transverse sinuses, the straight sinus and the occipital sinus to form the

confluence of sinuses. It receives blood from the inferior surface of the frontal

lobes and the superior portion of the medial and lateral surfaces of the frontal,

parietal and occipital lobes (5). The superior sagittal sinus drains to the left and

right transverse sinuses equally. When the drainage volume is not equal, the right

transverse sinus is usually the dominant one, receiving most of the venous outflow.

Lateral to the superior sagittal sinus are the venous lacunae. These are

enlarged venous spaces that communicate with the sinus through small openings.


31 | P a g e

They drain the meningeal veins. The bridging veins coursing towards the superior

sagittal sinus characteristically pass beneath these lacunae. Pacchionian

granulations responsible for the resorption of the cerebrospinal fluid protrude into

the floor and walls of these spaces, becoming more prominent with age. These

lacunae must be kept in mind whenever performing an approach in the parasagittal

area and procedures which involve cannulation of the lateral ventricle.

The inferior sagittal sinus courses along the posterior two-thirds of the

inferior edge of the falx cerebri. It joins the great cerebral vein of Galen to form

the straight sinus. The anterior pericalossal vein is the largest tributary of this

sinus.

The occipital sinus is inconstant. It is the smallest of the cranial sinuses

and may be duplicated. When it is present, it drains superiorly towards the

confluence of sinuses. Alternatively, it may drain inferiorly towards the sigmoid

sinus or it can connect with the marginal sinus (which is located around the

foramen magnum). The occipital sinus is most prevalent in the pediatric

population, diminishing in size with age (7).

The transverse sinus courses laterally in the tentorium cerebelli until it

turns inferiorly to become the sigmoid sinus. The transverse sinus receives venous

outflow from important supratentorial veins from the occipital and parietal lobes.

The vein of Labbé also drains into the transverse sinus. In addition, this sinus is

the draining point of some of the inferior cerebellar veins and the superior

petrosal sinus.

The superior petrosal sinus connects the transverse sinus with the

cavernous sinus. It receives the inferior cerebral veins, cerebellar veins and veins

from the tympanic cavity. The inferior petrosal sinus connects the cavernous

sinus with the internal jugular vein. It receives venous blood flow from the veins

of the pons, medulla oblongata and veins from the suboccipital surface of the

cerebellum. Internal auditory veins also drain into this sinus.


32 | P a g e

The sigmoid sinus represents the continuation of the transverse sinus. It

becomes the internal jugular vein in the jugular fossa. The sigmoid sinus may

also receive some venous channels from the pons and medulla oblongata.

The tentorial sinuses are located on each half of the tentorium cerebelli.

They are divided into a medial and a lateral group. The medial group of tentorial

sinuses collects the venous outflow of the superior cerebellar surface and drain

into the transverse sinus. The lateral group of tentorial sinuses receives the venous

blood from the basal and lateral surfaces of the parietal and occipital lobes.

They may drain in either the transverse or the straight sinus (6).

Figure 2.1 – Dural sinuses and main veins of the cerebrum


33 | P a g e

DURAL VENOUS SINUSES

Dural venous sinuses are channels that form between two layers of dura. This

permits them to maintain their patency even if the intracranial pressure rises. As

the cerebral veins, they lack valves.

The superior sagittal sinus courses along the midline following the

convexity of the calvarium. It extends from immediately posterior to the foramen

caecum all the way to the internal occipital protuberance where it joins the

transverse sinuses, the straight sinus and the occipital sinus to form the confluence

of sinuses. It receives blood from the inferior surface of the frontal lobes and the

superior portion of the medial and lateral surfaces of the frontal, parietal and

occipital lobes (5). The superior sagittal sinus drains to the left and right transverse

sinuses equally. When the drainage volume is not equal, the right transverse sinus

is usually the dominant one, receiving most of the venous outflow.

Lateral to the superior sagittal sinus are the venous lacunae. These are

enlarged venous spaces that communicate with the sinus through small openings.

They drain the meningeal veins. The bridging veins coursing towards the superior

sagittal sinus characteristically pass beneath these lacunae. Pacchionian

granulations responsible for the resorption of the cerebrospinal fluid protrude into

the floor and walls of these spaces, becoming more prominent with age. These

lacunae must be kept in mind whenever performing an approach in the parasagittal

area and procedures which involve cannulation of the lateral ventricle.

The inferior sagittal sinus courses along the posterior two-thirds of the

inferior edge of the falx cerebri. It joins the great cerebral vein of Galen to form

the straight sinus. The anterior pericalossal vein is the largest tributary of this

sinus.

The occipital sinus is inconstant. It is the smallest of the cranial sinuses

and may be duplicated. When it is present, it drains superiorly towards the

confluence of sinuses. Alternatively, it may drain inferiorly towards the sigmoid


34 | P a g e

sinus or it can connect with the marginal sinus (which is located around the

foramen magnum). The occipital sinus is most prevalent in the pediatric

population, diminishing in size with age (7).

The transverse sinus courses laterally in the tentorium cerebelli until it

turns inferiorly to become the sigmoid sinus. The transverse sinus receives venous

outflow from important supratentorial veins from the occipital and parietal lobes.

The vein of Labbé also drains into the transverse sinus. In addition, this sinus is

the draining point of some of the inferior cerebellar veins and the superior

petrosal sinus.

The superior petrosal sinus connects the transverse sinus with the

cavernous sinus. It receives the inferior cerebral veins, cerebellar veins and veins

from the tympanic cavity. The inferior petrosal sinus connects the cavernous

sinus with the internal jugular vein. It receives venous blood flow from the veins

of the pons, medulla oblongata and veins from the suboccipital surface of the

cerebellum. Internal auditory veins also drain into this sinus.

The sigmoid sinus represents the continuation of the transverse sinus. It

becomes the internal jugular vein in the jugular fossa. The sigmoid sinus may

also receive some venous channels from the pons and medulla oblongata.

The tentorial sinuses are located on each half of the tentorium cerebelli.

They are divided into a medial and a lateral group. The medial group of tentorial

sinuses collects the venous outflow of the superior cerebellar surface and drain

into the transverse sinus. The lateral group of tentorial sinuses receives the venous

blood from the basal and lateral surfaces of the parietal and occipital lobes.

They may drain in either the transverse or the straight sinus (6).


35 | P a g e

SUPRATENTORIAL VENOUS SYSTEM

Superficial Venous System

The superficial venous system drains the cortical surfaces of the cerebral

hemispheres. The cortical veins collect into bridging veins that carry the venous

blood through the subdural space to the nearest sinuses. It covers a depth of 1-2 cm

below the cerebral cortex. These veins are didactically divided into four groups:

superior sagittal, sphenoidal, tentorial and falcine.

The superior sagittal group is formed by the bridging veins that drain

the medial and lateral aspects of the frontal, parietal and occipital lobes. Part of

the orbital surface of the frontal lobe is also drained by this group of veins. This

group delivers blood to the superior sagittal sinus. The veins enter the sinus either

directly or through the meningeal sinuses adjoining the superior sagittal sinus.

The sphenoidal group of veins drains the cortical surfaces near the

Sylvian fissure corresponding to the frontal, temporal and parietal lobes. This

group carries blood to the sinuses on the inner part of the sphenoid bone: the

sphenoparietal or the cavernous sinus.

The tentorial group serves the basal and lateral aspects of the temporal

lobe, the basal surface of the occipital lobe and also serves as a draining point for

the vein of Labbé.

The falcine groups’ anatomical drainage territory corresponds to that of

the limbic lobe. The venous blood is driven towards the inferior sagittal sinus or

the straight sinus. This may happen directly or via the deep cerebral veins.

There are two major anastomotic veins on the lateral surfaces of the

cerebral hemispheres: the vein of Trolard and the vein of Labbé. The vein of

Trolard (the superior anastomotic vein or the frontoparietal vein) connects the

superior sagittal sinus to the veins coursing along the Sylvian fissure. The vein of

Labbé (the inferior anastomotic vein or the temporooccipital vein) connects the


36 | P a g e

veins adjoining the Sylvian fissure with the transverse sinus. Together with two

other anastomotic veins (the vein of Rolando or the parietal vein and the vein of

Sylvius) they anastomose at the level of the insula (1). These four veins share a

close relationship with one another, the smaller one is, the larger the other. It is

also important to keep in mind the fact first demonstrated by di Chiro in 1962,

namely that the vein of Labbé tends to be the dominant one in the dominant

hemisphere whilst the vein of Trolard tends to be more dominant the opposite side

(8).

Deep Venous System

This system drains the central core and white matter. Venous blood from these

regions is first collected into the deep cerebral venous system (internal cerebral

vein, basal vein of Rosenthal, great vein of Galen) and is eventually drained into

the straight sinus.

Thus, the straight sinus becomes a crucial meeting point between the

superficial and deep draining systems of the brain. This sinus originates at the

conjuncture of the inferior sagittal sinus and the great veins, behind the splenium

of the corpus callosum. It drains into the transverse sinus.

The internal cerebral vein originates behind the foramen of Monro and

courses posteriorly in the velum interpositum. It exits the velum above the pineal

body, enters the quadrigeminal cistern and joins the great vein of Galen. The

velum interpositum is a thin membranous partition in the roof of the third

ventricle. Between its’ folds many ventricular veins (among others, the

thalamostriate vein) course to reach the internal cerebral vein.

The basal vein of Rosenthal presents many anatomical variations. It

forms below the anterior perforated substance and courses posteriorly, between the

midbrain and temporal lobe to reach the vein of Galen. It drains the basal surfaces

of the cerebral hemispheres and is thus by didactic definition a superficial vein. It

is named together with the deep cerebral veins owing to its location.


37 | P a g e

The great vein of Galen passes posterosuperiorly behind the splenium of

the corpus callosum in the quadrigeminal cistern. Although only 1-2 cms in

length, it receives not only the basal and internal veins but also some of the veins

of the posterior fossa. It drains into the anterior end of the straight sinus.

INFRATENTORIAL VENOUS SYSTEM

Posterior Fossa Veins

The posterior fossa veins are best understood when cognitively linked with the two

main structures in the posterior fossa that they drain: the cerebellum and the

brainstem.

The cerebellar veins are named after the cerebellar structures which they

serve or the fissures where they course in.

The major veins related to the surface of the brainstem are named

according to their relationship to the mesencephalon, pons or medulla oblongata

and according to their course, either longitudinal or transversal. These medullary

veins also act as collecting veins for the small cerebellar veins.

The veins of the posterior fossa can be didactically divided into three

major groups according to the dural sinuses which receive their venous output: the

petrosal or anterior group, which drains to the superior and inferior petrosal

sinuses; the galenic or superior group, which collects into the great vein of Galen

and the tentorial or posterior group which gives its output to the sinuses adjacent

to the confluence of sinuses (6).

The petrosal group of veins is composed of five groups of veins: firstly

the veins which drain the anterior part of the brainstem, namely the anterior

pontomesencephalic vein, the transverse pontine vein, the lateral pontine vein,

the anterior medullary vein and the parenchymal perforating veins; secondly the


38 | P a g e

brachial veins, which course across the lateral aspect of the precentral cerebellar

fissure; thirdly the superior and inferior hemispheric veins and the veins of the

great horizontal fissure, which drain the superior and inferior surfaces of the

cerebellar hemispheres; and fourthly the veins which lie on the cerebellar side ( the

medial tonsillar vein) and the veins which lie on the medullary side (the retro-

olivary vein and the vein of the inferior cerebellar peduncle). The fifth group

consists of the vein of the lateral recess of the fourth ventricle.

The galenic group is composed of cerebellar tributaries (the precentral

cerebellar vein and the superior vein) and of mesencephalic tributaries (the

median anterior, the lateral anterior and lateral pontomesencephalic veins, the

lateral and posterior mesencephalic vein, the peduncular vein and the tectal

vein).

The tentorial group consists of the inferior vermian vein and the

superior and inferior hemispheric veins (6).

REFERENCE

1. Huber, Peter: Cerebral Angiography, Translated by George Bosse. Foreword by Hugo

Krayenbuhl and M. Gazi Yasargil- 2nd completely revised edition – Stuttgart, New-

York- Thieme, 1982

2. Morris Pearse. : Practical Neuroangiography, Lippincott Williams and Wilkins, 2007

3. Bradac, Gianni Boris: Cerebral Angiography-Normal Anatomy and Vascular

Pathology, Springer, 2011

4. García-González U, Cavalcanti DD, Agrawal A, Gonzalez LF, Wallace RC, Spetzler

RF, Preul MC: The diploic venous system: surgical anatomy and neurosurgical

implications. Neurosurg Focus. 2009 Nov;27(5)

5. Rhoton AL Jr. : The Supratentorial Cranial Space. Microsurgical Anatomy and

Surgical Approaches. Neurosurgery 51[Suppl 1]:159–205, 2002

6. Rhoton AL Jr: The Posterior Fossa Veins. Neurosurgery, Vol. 47, No. 3, September

2000 Supplement


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7. Ayanzen R.H., et al : Cerebral MR Venography: Normal Anatomy and diagnostic

pitfalls. AJNR 2000 21: 74-78

8. Di Chiro G : Angiographic Patterns of Cerebral Convexity Veins and Superficial Dural

Sinuses. AJR Am J Roentgenol Radium Ther Nuc Med :87. 301-321, 1962.

9. Duvernoy, Henry: Human Brain Stem Vessels-Second Edition, Heidelberg-

Springer,1999

10. Osbron, Anne: Diagnostic Cerebral Angiography, Lippincott William and Wilkins,

1980

11. M.G. Yasargil: Microneurosurgery Vol.2, Thieme, 1994

12. Seeger, Wolgang: Microsurgery of Cerebral Veins, Springer-Verlag/Wien, 1984

13. Yasargil MG, Damur M. Thrombosis of the cerebral veins dural sinuses. In: Newton

TH, Potts DJ, eds Radiology of the Skull and Brain: Angiography St. Louis: Mosby-

Year Book; 1974;2:2375-2400

14. Browning H. The confluence of dural venous sinuses. Am J Anat 1953;93:307-329

15. Jin Wang. et al: Evaluation of the anatomy and variants of internal cerebral veins with

phase-sensitive MR imaging. Surgical & Radiologic Anatomy . Aug2010, Vol. 32

Issue 7, p669-674

16. Rhoton AL Jr: The Cerebral Veins. Neurosurgery. 2002 Oct;51(4 Suppl)

CHAPTER 3 SUBARACHNOID SPACE AND THE CEREBROSPINAL FLUID


40 | P a g e

INTRODUCTION

The meninges are three sequential membranous layers that cover the brain and

the spinal cord. They are named as follows:

The dura mater (L., tough mother) the outermost layer;

The arachnoid, beneath the dura;

The pia mater (L., tender mother), directly paving the surface of the brain

and spinal cord.

While the intracranial dura coats the bone through powerful adhesions,

the spinal dura is separated from the walls of the medullary canal. In truth, what

is considered the outer portion of the intracranial dura is actually the periosteum.

The genuine dura mater is the subjacent layer, closely adhering to the arachnoid

and forming the dural sinuses and the dural septa (the falx cerebri, falx cerebelli,

and tentorium cerebelli).

Both the arachnoid and the pia mater derive from the same mesenchymal

strata enveloping the brain. Therefore, they are commonly referred to as the pia-

arachnoid, with the former being the visceral portion, and the latter the parietal

portion of the same layer. Proof of this is the numerous trabeculae that bridge the

two within the so-called subarachnoid space.

The cerebrospinal fluid (CSF) is a clear, colorless fluid that fills up the

cerebral ventricles and the subarachnoid space. Only a tenth of its volume is found

within the ventricular system, the rest flowing in the subarachnoid space. CSF is


41 | P a g e

mostly produced in the choroid plexuses of the lateral, third and fourth ventricles,

and to a smaller degree in the spinal cord.

The importance of the subarachnoid space stems not only from the

circulation of the CSF, but also from the inclusion of the main vasculature of the

brain. Any injury brought onto the vessels supplying or draining the cerebral tissue

will most likely reverberate as a subarachnoid space hemorrhage. This chapter

is therefore dedicated to the anatomy of this space, as well as the physiology of the

cerebrospinal fluid.

THE ARACHNOID

The arachnoid is a slender and avascular membrane that borders the inner

surface of the dura, without being properly attached to it. It is weaved by fibrous

tissue and extends to the pia mater via subtle weblike trabeculae (from which it

derives its name). These trabeculae are composed of loose connective tissue fibers

including elongated fibroblasts and serve to anchor the blood vessels supplying

the brain. Underneath this layer of the meninges lies the subarachnoid space.

THE PIA MATER

The pia mater is also a subtle membrane comprised of connective tissue. Unlike

the arachnoid, however, it does contain blood vessels. It lies on the surface of the

brain and the spinal cord directly, closely following every nook and cranny. The

only regions where the pia is absent are the natural orifices between the

subarachnoid space and the fourth ventricle (foramen of Magendie and the

foramens of Luschka). The pia mater is also the continuation of the perivascular

connective tissue sheath of the blood vessels supplying these nervous structures.

SECTION I: ANATOMY CHAPTER 3: SUBARACHNOID SPACE AND THE CEREBROSPINAL FLUID

42 | P a g e

Two layers compose this membrane: the pial intima situated deeply, and

the epipial layer that is superficial. The former penetrates the cerebral

parenchyma alongside blood vessels, whilst the latter continues the arachnoid

trabeculae. The subarachnoid space extends with the aforementioned blood vessels

as a perivascular space containing CSF, known as the Virchow-Robin space.

As a notice, both surfaces of the arachnoid, the inner surface of the pia,

and the weblike trabeculae are covered with a thin squamous epithelial layer. Both

the arachnoid and the pia mater fuse around the opening for the cranial and spinal

nerves as they emerge from underneath the dura.

SUBARACHNOID SPACE AND CISTERNS

The subarachnoid space is the only gap between the meningeal layers that is

constantly filled with fluid. As the arachnoid does not follow the contour of the

brain as intimately as the pia, an anatomic space is formed between the two. As a

result, subarachnoid space does not have the same depth as it surrounds the brain.

The more shallow portions are those respective to the gyri, while the depth

increases at the level of the brain sulci. At the base of the brain (adjacent to the

cerebral peduncles, in front of the brainstem, around the optic chasm and so forth),

the distance between the arachnoid and the pia mater is at its greatest, thus forming

the subarachnoid cisterns.

There are two types of cisterns, according to symmetry: median cisterns,

which are odd in number and situated along the median line, and lateral cisterns,

paired and placed symmetrically on both sides of the brain.

The median subarachnoid cisterns are as follows:

The cerebellomedullary cistern (cisterna magna) is the largest. It is situated

between the cerebellum and the medulla oblongata, continuous with the

fourth ventricle via the foramens of Luschka and the foramen of Magendie.


43 | P a g e

Found within it are the vertebral arteries, the origin of the PICA, cranial

nerves IX through XII, and the choroid plexus that protrudes from the fourth

ventricle through the foramens of Luschka.

The pontine cistern surrounds the pons anteriorly. It is most notable for

containing the basilar artery, along with the origins of the AICA and the

SCA from both sides, as well as the sixth cranial nerve.

The interpenduncular cistern, as its name suggests, lies between the two

cerebral peduncles. It is here that the basilar artery branches, forming the

posterior portion of the Circle of Willis. Also included are the PCoA, the

basal vein of Rosenthal, and the third cranial nerve.

The retrochiasmatic cistern is located just posteriorly to the optic chasm

and sets the continuation between the interpeduncular and prechiasmatic

cisterns.

The prechiasmatic cistern contains the origin of the ACA, the anterior

portion of the optic chasm and the intracranial segment of the optic nerves,

and the pituitary stalk.

The lamina terminalis cistern is situated anteriorly and superiorly to the

prechiasmatic cistern, merely rostral to the third ventricle. Found here are

arteries comprising the anterior portion of the Circle of Willis (the A1 and

proximal A2 of the ACA, and the ACoA), as well as the hypothalamic

arteries, the origin of the fronto-orbital arteries, and the recurrent artery of

Heubner (a branch arising from the proximal A2 or distal A1 and supplying

segments of the caudate nucleus, internal capsule, putamen, and septal

nuclei).

The superior cistern, or ambient cistern as it is also called, is located around

and dorsal to the midbrain. Its importance derives from containing the great

vein of Galen, the PCA, the SCA, the posterior pericallosal arteries, and the

fourth cranial nerve.

The lateral subarachnoid cisterns are as follows:


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The cerebellopontine cisterns are situated in the angles formed between

the pons and the cerebellum. On each side, they contain the AICA, cranial

nerves V, VII and VIII, and the petrosal vein.

The lateral cisterns of Sylvius are found in the fissures (bearing the same

name) between the frontal and temporal lobes and they include the MCA as

well as the medial cerebral vein.

The carotid cisterns are located between the internal carotid arteries and

the respective optic nerve. Aside from the ICA, they contain the origin of

the PCoA.

In the proximity of the superior sagittal sinus, the pia mater and the

arachnoid send out small processes that pass through the dura and protrude into the

superior sagittal sinus. These are known as the arachnoid granulations of

Pacchioni. Although variable in quantity and placement, these formations have the

common purpose to drain the CSF from the subarachnoid space into the venous

system. This is achieved through the pressure gradient between the two

compartments, the venous system having the lower value.

The arachnoid villi are microscopic extensions of these granulations.

They are comprised of single-layered epithelium on the outside, a network of

connective and elastic tissue fibers on the inside, and a thin outer limiting

membrane in between.

The granulations of Pacchioni tend to increase in size and calcify with

age. The effect of these alterations on normal function is not fully understood. A

subarachnoid hemorrhage may lead to scarring of the granulations, with poor

CSF absorption as a consequence.


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THE CEREBROSPINAL FLUID

As briefly stated above, CSF is a clear, colorless, and virtually acellular fluid that

occupies the most of the subarachnoid space and ventricles. In normal adults, the

total amount of CSF contained is approximately 125-150 ml, the majority of

which (90%) is situated solely in the subarachnoid space. All of the plasmatic

components (for example potassium, glucose, proteins, and especially sodium

chloride) are found within, however in different quantities.

The circulation rate of CSF is around 500-700 ml per day. The main sites

of production are the choroid plexuses found in every ventricle (and to some

extent the cisterna magna as well). A choroid plexus consists of numerous villi,

each one made of a single layer of cuboidal epithelial cells overlaying a highly

vascularized core of connective tissue. Plasma is processed by these cuboidal cells

and diffuses into the ventricles as CSF. This newly formed fluid escapes from the

ventricle system through the foramens of Luschka and the foramen of

Magendie, regardless from which of the choroid plexus it derives. Once inside the

cerebellomedullary cistern, CSF flows throughout the entire subarachnoid space,

bathing the brain and the spinal cord alike. A noteworthy difference between

production and drainage of CSF is that, while drainage ensues passively (at the

arachnoid granulations) in virtue of hydrostatic pressure gradient, production is

dependent on sodium-potassium ATPase and carbonic anhydrase.

CSF has multiple roles in protecting the cerebrospinal axis. As any

liquid, it acts as a mechanical dampener, diminishing traumatic forces that may

harm the brain. Also, by completely immersing the brain, it physically reduces its

weight from 1500 grams to a mere 50. Aside from mechanical protection, CSF

grants thermal stability, thus assuring optimal functionality of the nervous

system.

Cerebral nutrition is also a role provided by CSF, as well as discarding

many of the neuronal catabolism products and hematologically disseminated

pathogenic agents. Since the intracranial cavity of the adult is inextensible, any


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increase of intracranial pressure may damage the brain. CSF volume is the major

compensatory mechanism for intracranial pressure, any excessive production or

reduced drainage being able to cause possibly grave and irreversible injuries. As

such, internal hydrocephalus is caused by disproportionate accumulation of CSF

within the ventricles, whereas external hydrocephalus is the result of poor

absorption through the arachnoid granulations. Either of them may be the

complication of a subarachnoid space hemorrhage.

REFERENCE

1. Sido FG. Tratat de Neuroanatomie Funcțională și Disecția Nevraxului. Second

edition. Casa Cărții de Știință, 2007; VII: 632-45

2. Ross MH, Pawlina W. Histology, a Text and Atlas. Sixth edition. Lippincott Williams

& Wilkins, 2011; 12: 383-5

3. Drake RL, Vogl AW, Mitchell AWM. Gray’s Anatomy Pentru Studenți. Second

edition. Churchill Livingstone, 2010; 8: 830-4

4. Wang PP, Avellino AM. Hydrocephalus in Children. In: Rengarchary SS, Ellenbogen

RG. Principles of Neurosurgery. Second Edition. Elsevier Mosby 2008; 8: 117

5. Dănăilă L, Ștefănescu F. Anevrismele Cerebrale. Editura Academiei Române, 2007;

3: 45

Left Frontal Spetzler Martin Grade 3 AVM- venous phase demonstrating superficial

drainage into the superior sagittal sinus

CHAPTER 4

IMAGING OPTIONS IN CEREBRAL VASCULAR LESIONS

CRISTINA C. ALDEA, LUCIAN MĂRGINEAN

48 | P a g e

COMPUTED TOMOGRAPHY (CT)

A patient with clinical diagnosis of stroke should immediately undergo an

emergency non-enhanced CT scan. This is done primarily to differentiate

between haemorrhagic and ischemic stroke. If an ischemic stroke is found, the

CT can point out whether the cause is an arterial or a venous infarction. If

intracranial hemorrhage is confirmed, this investigation permits localization of the

bleeding (table 1) and establishes whether the cause is vascular or non-vascular

(tumor, infection).

Intracranial hemorrhage

Intraaxial hemorrhage Extraaxial hemorrhage

Intracerebral

Hemorrhage

Intraventricular

Hemorrhage

Epidural Hemorrhage

Basal ganglia

Hemorrhage

Lobar Hemorrhage

Pontine

Hemorrhage

Cerebellar

Hemorrhage

Subdural Hemorrhage

Subarachnoid Hemorrhage

Table 4.1: Classification of Intracranial Hemorrhage Based on its Location

CT is ideal in emergency settings because of its cost-time efficiency and

its high sensitivity in detecting acute blood in the intracranial compartment. Acute

blood is markedly hyperdense in comparison with normal brain parenchyma;


49 | P a g e

consecutively if the amount of hemorrhage is large enough and the scan is

performed early, the diagnosis is seldomly missed. In case of spontaneous

intracerebral hematoma, the hematoma appears on CT as a markedly hyperdense

area surrounded by a ring of low density (corresponding to the area of perifocal

edema). At 7-10 days from the onset of the hemorrhage the hyperdensity of the

blood attenuates from the periphery towards the center of the hematoma. If the

hematoma is small, it will become izodense in 2-3 weeks and in 2 months if it is

larger in size. After 2-4 months the space occupied by the hematoma will be

replaced by a liquid cavity. In case of an ischemic stroke, the region corresponding

to the territory of the obstructed vessel appears hypodense in comparison with

normal brain parenchyma (3) .

Image 4.1: Left Lobar Hemorrhage on non-e. CT

SECTION II: IMAGING IN VASCULAR LESIONS

CHAPTER 4: IMAGING OPTIONS IN CEREBRAL VASCULAR LESIONS

50 | P a g e

Clinical suspicion of subarachnoid hemorrhage is always followed by

investigations which permit confirmation of the clinical diagnosis and establishing

the underlying cause (the source of hemorrhage). CT provides information about

the location and type of intracranial hematoma (if it exists), the coexistence of

hemorrhage in other intracranial compartments (e.g. acute subdural hematoma),

size of the ventricles (literature data reports the incidence of acute hydrocephalus

following SAH in the range of 15 to 31 % (5,6) ), the presence of ischemic

lesions (due to vasospasm), the amount of SAH (important prognostic factor for

vasospasm and pretruncal hemorrhage), the location of the aneurysm in 70 % of

cases (e.g. ACoA aneurysm- predominantly interhemispheric hemorrhage, ACM

and ACoP – hemorrhage in Sylvian fissure) and it may point out the source of

bleeding in case of multiple intracranial aneurysms.

SAH appears as hyperdense substance filling the normally hypodense,

CSF- filled subarachnoid spaces. These findings are most visible in the larger

subarachnoid spaces such as the suprasellar cistern and the Sylvian fissure.

Blood in these two spaces appears as the characteristic “star-sign” on the CT-scan.

Non-contrast CT scan detects SAH in 95% of cases in the first 48 hours

from aneurysmal rupture. After 5 days, 58% of patients have normal CT scans (1) .

CT can confirm SAH but can rarely detect the underlying cause. If the

source of bleeding is not found, the patient must undergo a CTA and afterwards, if

there is still no certitude about the source of bleeding, an angiography. If the

angiography is also negative, an occult aneurysm or other cause of SAH must be

considered.

Contrast enhanced CT is performed for differential diagnosis with other

intracranial processes or if the examination is done late after the onset of the

bleeding. Between the 1st and 6th week a ring enhancement can be observed, this

disappears in 2-6 months and is due to the peripheral hypervascularisation of

the hematoma and damage to the blood-brain barrier.


51 | P a g e

The diagnosis of AVMs is dependent on imagistic studies. These studies

will confirm the existence, the characteristics, dimensions and will identify the

afferent and efferent vascular components of the malformation.

Clinical symptoms of AVMs are highly suggestive. Most patients present

with ictal debut (bleeding of AVM) consecutive to an epileptic fit without family

history of epilepsy or previous seizure history or pregressive neurologic deficit.

All these symptoms pointing towards an expansive intracranial process must be

investigated through an emergency CT scan (hemorrhagic the lesion or not). This

investigation provides data regarding the localization of the AVM, its

dimensions, and, if it has ruptured, the location of the hematoma.

On non-contrast enhanced (or native) CT, the AVM appears as a

hyperdense lesion. It can be located anywhere in the brain and is usually observed

as a triangular formation with the base of the triangle oriented towards a

ventricle. Other aspects may be encountered, the form and extent of AVMs being

extremely variable. Small calcifications at the level of lesion or in perilesional

area may be noted. Contrast enhanced CT will contour the AVM, as well as its

feeding arteries and draining veins. In case of a ruptured AVM the dimensions and

the extent of hemorrhage can be evaluated. The lesion itself is difficult to

visualize on native CT, but enhancement will make the lesion and/or its tributary

vessels visible, if the hematomas effect is not that huge to mask the AVM.

If the AVM or the hematoma resulting from its rupture was confirmed

with CT and the clinical data also indicates a vascular malformation (young patient

without significant history of hypertension, suggestive localization) will oblige to

continue the investigations in order to precisely characterize the lesion. CT is

also a helpful aid in postoperative evaluation of patients, when clinical evolution is

not favorable or for follow up of the lesion in time.

Cavernomas appear on CT as hyperdense lesions (because of their

impregnation with hemosiderin). They have an inhomogeneous, well contoured,



52 | P a g e

round shape. Some may present calcifications and/or contrast enhancement

(tardive, due to the low flow inside the lesion).

COMPUTED TOMOGRAPHY ANGIOGRAPHY (CTA)

CTA is used to search for an underlying vascular cause of a bleeding prior

confirmed by conventional CT. It is especially useful in SAH and

intraparenchymal hematoma where primary hemorrhage is less likely based on

patient history.

Some centers report a sensibility of 98% of detection of aneurysms up to

2,2 mms (1). A number of authors advocate that CTA should be the most

important method of evaluation and preoperative planning both for aneurysms and

for AVMs (2) . The advantages of CTA are many: it is fast and non-invasive, it

offers the possibility of three dimensional evaluation of structures with digital

subtraction, which excludes the artifacts caused by bony structures (e.g. osseous

subtraction shows ACoP aneurysms), it allows the morphologic reconstruction of

the aneurysm and is not dependent on the permeability of the parent vessel or by

the aneurysmal sac. It is also an important aspect that CTA is readily available in

emergency conditions which allows immediate precise diagnosis and surgical

treatment .


53 | P a g e

Image 4.2: CTA reconstruction demonstrating a left MCA aneurysm

MAGNETIC RESONANCE IMAGING (MRI)

MRI is requested particularly in search of an underlying pathology, especially if a

tumor is suspected. Identifying the hemorrhage on MRI is challenging because the

blood changes in its appearance based on the sequence, the size and location of

bleed and the time elapsed from the onset of the hemorrhage. These parameters

modify the type and distribution of paramagnetic substances in the affected brain

parenchyma.

In the first 48 hours after the hemorrhage MRI has low sensibility for

detecting the acute blood. This investigation offers useful information after 4-7

days. MRIs most important aid is that it is of help in detecting SAH after 10-20

days from the onset. After this interval it can detect the source of the hemorrhage



54 | P a g e

and it can point towards the location of an aneurysm, if this is the cause of the

bleeding. The fact that the pathologic modifications remain visible for a long time

period is very useful in multiple intracranial aneurysms (1) .

Image 4.3: MRI demonstrating 2 right MCA aneurysms

In case of a previously confirmed AVM on CT, performing an MRI offers

a helpful aid. It is a high accuracy non-invasive investigation, it demonstrates the

exact dimensions and the relationship of the lesion with the surrounding neural

structures. On MRI an AVM appears as a tangle of serpentine curvilinear

hypointense tubules. The high flow velocity inside the lesion may mask

Gadolinium enhancement. AVMs typically do not present perilesional edema.

This fact allows the differential diagnosis with a tumor with recent hemorrhage.

Often, in complementing the CT with help of the MRI information is gained

regarding the microanatomy of the nidus, feeding arteries and draining veins.

Association with MRA completes the anatomic details and offers invaluable

information for planning the surgical approach.

MRI is the gold standard for the diagnosis of cavernomas. They appear

as inhomogeneous, well circumscribed lesions with a characteristic “salt and

pepper” appearance. They may be surrounded by a ring of low signal because of


55 | P a g e

the peripheral deposits o hemosiderine. Cavernomas are not contrast enhancing

lesions.

Image 4.4: Typical Appearence of Cavernoma on MRI in T2 sequence

MAGNETIC RESONANCE ANGIOGRAPHY (MRA)

Multicenter studies demonstrated that MRA routinely detects aneurysms as small

as 3mms in diameter (1,6). With this method the morphology of aneurysms can

accurately be studied. Its major advantage is that it offers the possibility of three

dimensional study of the aneurysm and the surrounding neural structures. This is

a major advantage also in the preoperative planning preceeding AVM surgery.

MRA can also be used to complement angiographic studies, especially in

cases when angiography failed to locate the source of the hemorrhage despite the

CT being very suggestive for aneurysmal rupture. In elderly patients and in those

allergic to iodinated contrast material used in both CT and angiography, MRA

remains the only diagnostic option.

MRA allows “watchful waiting” in case of aneurysms or AVMs found

incidentally, and helps the therapeutic decision by monitoring the evolution of the



56 | P a g e

lesion. It can also be performed as a screening test in patients with first degree

relatives with cerebral aneurysms. This category of patients have a high risk for

developing cerebral aneurysms themselves.

Image 4.5: MRA reconstruction demonstratin a right occipital AVM

ANGIOGRAPHY

Catheter angiography is an invasive procedure which is only performed in cases

in which an underlying vascular abnormality is clinically suspected, but the

previously performed CTA was failed to identify the underlying cause. It is also

used in cases where further details about a previously identified lesion are needed

or if the further endovascular treatment of the identified lesion is desired.

In the past, in the absence of non-invasive imaging procedures like CT

and MRI, angiography was used as a method for investigating intracerebral

hematomas, midline shifting of vessels (particularly veins which are more


57 | P a g e

adherent to the surrounding brain parenchyma than arteries) being an indicator of

an intraparenchymal hematoma and its mass effect (4).

Today, angiography is still considered to be the gold standard in

evaluating cerebral aneurysms. Angiography demonstrates the source of the

bleeding, in up to 80-85% of cases and it also shows the presence of vasospasm

(narrowed vessels).

Typically, a four-vessel angiography is carried out in every patient

(examining the two internal carotid arteries and the two vertebral arteries). This

is done in order to detect other possible aneurysms and the stat of the collateral

circulation. In performing an angiography the vessel with highest suspicion of

harboring the aneurysm is the first to be examined, in case the procedure has to be

prematurely abandoned. Before concluding the angiography it is necessary to

study the emergence of the PICA bilaterally and the flow in the ACoA (3).

Image 4.6: Aneurysm of the Carotid Artery



58 | P a g e

In case of a previously demonstrated AVM, angiography provides

information on the flow velocity inside the lesion and additional information

regarding its anatomic relationships.

Using high velocity imaging, image zoom and different angles details

about the AVM feeders, draining veins and nidus can be obtained. Regarding the

flow dynamics inside the lesion, angiography is the sole investigation that can be

implied. If the chosen treatment modality is not endovascular obliteration of the

lesion the angiographic evaluation should be performed as close to the operative

moment as possible, because AVMs have the tendency of modifying their

dimensions and draining trajectories, especially if the initial presentation was

bleeding. Supplementary feeders or draining veins may appear which were either

masked by the hematoma in the acute phase or thrombosed. The four vessel

angiography allows identification of clinically silent lesions. It is important to

note that not every AVM can be identified with routine angiography.

Angiographically occult AVMs are small, high velocity lesions with partial

thrombosis at the level of the nidus.

Cavernomas are the classic prototype of angiographically occult

lesions. The site of the cavernoma appears as an avascular region with a high

density of capillaries. This is due to the fact that the cavernoma does not possess

feeding vessels and that the blood stagnates inside the lesion. Consequently

angiography is not used in their diagnosis and endovascular techniques cannot be

applied in their treatment.

Complications of angiography may include ischemic events; alteration of

the patients neurologic status after 24-72 hours; high intraluminal pressure

changes during the injection of the contrast agent which may precipitate

aneurysmal rupture; systemic hypertension; vasospasm; complications at the site

of catheterization (hematoma, pseudoaneurysm).


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Image 4.7: Left Frontal Spetzler Martin Grade 3 AVM – arterial phase

demonstrating the feeding arteries from the left ACA



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Image 4.8: Left Frontal Spetzler Martin Grade 3 AVM- venous phase

demonstrating superficial drainage into the SSS

REFERENCE

1. Florian IS, Perju-Dumbravă L. Opțiuni Terapeutice în Accidentele Vasculare

Hemoragice. Editura Medicală Universitară „IuliuHațieganu” Cluj-Napoca 2007

2. Morris Pearse. : Practical Neuroangiography, Lippincott Williams and Wilkins, 2007

3. Osbron, Anne: Diagnostic Cerebral Angiography, Lippincott William and Wilkins,

1980

4. Huber, Peter: Cerebral Angiography, Translated by George Bosse. Foreword by Hugo

Krayenbuhl and M. GaziYasargil- 2nd completely revised edition – Stuttgart, New-

York- Thieme, 1982

5. Woernle CM, Winkler KM, Burkhardt JK, Haile SR, Bellut D, Neidert MC, Bozinov

O, Krayenbühl N, Bernays RL:Hydrocephalus in 389 patients with aneurysm-


61 | P a g e

associated subarachnoid hemorrhage, J ClinNeurosci. 2013 Jun;20(6):824-6. doi:

10.1016/j.jocn.2012.07.015. Epub 2013 Apr 4

6. Pierot L, Portefaix C, Rodriguez-Régent C, Gallas S, Meder JF, Oppenheim C: Role of

MRA in the detection of intracranial aneurysm in the acute phase of subarachnoid

hemorrhage. J Neuroradiol. 2013 Jul;40(3):204-10

Main aneurysm sites

CHAPTER 5 SUBARACHNOID SPACE HEMORRHAGE


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INTRODUCTION

The term subarachnoid space hemorrhage (SAH) denotes the extravasation of

blood in the space between the pial and arachnoid membranes of the meninges. It

can be either spontaneous, or as a result of trauma. However, the more common

usage of this term indicates non-traumatic hemorrhage (as a consequence of either

aneurysmal or arteriovenous malformation rupture). From a quantitative point

of view, SAH can range from insignificant to a massive amount. The blood may

originate from a vessel situated in the subarachnoid space (mostly arteries, while

veins rupture in the case of arteriovenous malformations), or from a parenchymal

hemorrhagic lesion that invades the ventricle system or lacerates the pia mater.

The arachnoid is a thin meningeal membrane weaved of fibrous tissue. It

stands underneath the dura mater and, although not attached, the two layers

strongly adhere to one another. On the other hand, the pia mater is more reclusive

in relationship with the arachnoid, and the weak bonds between the two are

comprised of fibrous trabeculas and connective tissue. As a result, a seemingly

virtual space is formed, namely the subarachnoid space.

The subarachnoid space houses cranial nerves and the main vessels

(including the arterial Circle of Willis). It can be divided into numerous chambers,

known as cisterns. The cerebrospinal fluid (CSF) originating from the ventricle

system passes through the medial foramen of Magendie and the two lateral

foramens of Luschka (belonging to the fourth ventricle) and into the cisterna

magna (the largest of cisterns, as its name suggests). From here on, the CSF can

either flow inferiorly into the spinal subarachnoid space, or anteriorly and laterally

into the other subarachnoid cisterns. Subarachnoid vessels resting in the cerebral


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sulci send (or receive) branches into (or from) the parenchyma. These branches are

also included in a narrow continuation of the subarachnoid space, a perivascular

space filled with CSF, commonly referred to as the Virchow-Robin space.

Subarachnoid space hemorrhages account for a small number of strokes,

most of which are caused by aneurysmal rupture. Patients with arteriovenous

malformations or an unknown cause of SAH usually have a higher outcome than

patients harboring aneurysms. The most dreaded complication of SAH is

vasospasm, aggravating cerebral perfusion in an already damaged brain. It is

obvious why the causes of SAH need to be researched quickly and thoroughly, and

why treatment must be established to minimize not only the hemorrhage itself, but

the effects of vasospasm as well.

CLASSIFICATION (CLINICAL GRADING)

Clinical grading is essential in determining the patient’s condition on arrival, the

prognostic and possibilities of treatment. The Hunt and Hess Grade and the

Fisher Grade are detailed below. The Hunt and Hess grades are given in

accordance to the patient’s symptomatology and the Fisher Grade classifies the

appearance of SAH on CT scan.

A common rule is shared by these grading scales: the lower the grade,

the better the outcome. In the Hunt and Hess system, grades I-III are generally

associated with a favorable prognostic, while grades IV and V imply a poor

scenario. Patients diagnosed with a higher score generally require stabilization to

grade III before surgery can be performed. This system correlates well with patient

outcome. Fisher Grade has been shown to accurately predict the likelihood of

symptomatic cerebral vasospasm.

SECTION III: CEREBROVASCULAR DISEASE CHAPTER 5: SUBARACHNOID SPACE HEMORRHAGE

66 | P a g e

Grade Description

I Asymptomatic / mild headache / slight nuchal rigidity

II Moderate to severe headache and nuchal rigidity / no deficits other

than cranial nerve palsy

III Drowsiness / confusion with mild focal neurologic deficit

IV Stupor, moderate to severe hemiparesis, early decerebration and

vegetative state

V Deep coma, decerebration, moribund state

Table 5.1: Hunt and Hess’s Grading of SAH

Grade Appearance of Blood on Head CT Scan

I No blood detected

II Diffuse deposition / thin layer with all vertical strata of blood (in

interhemispheric fissure, insular cistern, or ambient cistern) less

than 1 mm in thickness

III Localized clots and/or vertical strata of blood 1 mm or more in

thickness

IV Intracerebral / intraventricular clots with diffuse or no

subarachnoid blood

Table 5.2: Fisher’s Grading

Because a recent grading scale has gained widespread usage among

neurosurgeons, it should be mentioned. The World Federation of Neurologic

Surgeons (WFNS) has established a SAH grading scale based on the on-

admission Glasgow Coma Scale of the patient, associated with the presence of the

motor deficit.


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EPIDEMIOLOGY

Aneurysmal rupture stands at an annual rate of 12 cases per 100,000 population.

This is especially the case of patients in the 5th

or 6th

decades. The risk is higher

in Afro-Americans than in Caucasians and the incidence of SAH is greater in

women. SAH from aneurysmal rupture is a prominent cause of maternal

mortality (up to 25% of maternal deaths), being expressly heightened in the third

trimester of pregnancy.

Although mortality rates have decreased in the last 30 years, SAH still

stands as an overwhelming neurologic problem, with an estimated 10-15% of

patients dying before ever reaching the hospital. Death occurs in about 25% of

patients within the first 24 hours, regardless of medical attention received. Nearly

half of the affected individuals do not survive over 6 months, and a third of those

who endure have major, irreversible neurologic deficits.

ETIOLOGY

Traumatic head injury is by far the leading cause of subarachnoid hemorrhage.

In the case of spontaneous (or non-traumatic) SAH, rupture of saccular

aneurysms account for 80% of instances, while the rest result from the rupture of

mycotic aneurysms, arteriovenous malformations, neoplasm, or cortical

thrombosis. A lacerated intraparenchymal hematoma may also result in the

presence of blood in the subarachnoid space.

Both congenital and acquired factors are believed to take part in the

etiology of SAH. This is particularly emphasized by the association of aneurysms

with specific congenital diseases (Marfan syndrome, Ehlers-Danlos syndrome,

polycystic kidney disease, coarctation of the aorta, fibromuscular dysplasia).

Also, patients harboring multiple aneurysms have a significantly higher risk of

SAH. Aside from these, any acquired cause of aneurysmal rupture (factors that

brusquely heighten arterial hypertension) is considered an etiologic factor.


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PATHOPHYSIOLOGY

The blood escaping from an aneurysmal breach can vary from minute warning

leaks to massive amounts that lead to death. In most instances, probability of

rupture is directly proportional to the size of the aneurysm (based on La Place’s

Law stating that the larger the vessel radius, the larger the wall tension required to

withstand a given internal fluid pressure). Therefore, aneurysms with a diameter of

up to 5 mm have only a 2% chance to rupture, 40% of those with diameters

between 6-10 mm are already bleeding upon discovery. Paradoxically, large and

giant aneurysms rupture less frequently, so the rule seems to apply only to small

aneurysms (below 12 mm).

The consequences of SAH may change with the location of the bleed,

volume of CSF space, patient age, premorbid conditions (if present), cerebral

metabolism, systemic dysfunctions and electrolyte disturbances. Hypertension is

not only a cause of HAS of aneurysmal origin, but also a leading factor in

aneurysmal development. Because of hypertension, blood is released into CSF

space under high pressure, this in itself being able to engender damage to local

tissues. High flow rates of aneurysms with wide breaches produce large volume

SAH in a short amount of time. In this scenario, intracranial pressure rises

abruptly. Conversely, an aneurysm with a continuous leak may gradually escalate

SAH, progressively increasing intracranial pressure and slowly worsening the

clinical Grade of the patient. Blood extravasation elevates intracranial pressure,

while the presence of blood can irritate the meningeal layers. Its toxic effects can

result in global ischemia, mitochondrial respiration alterations with lactic

acidosis and cellular membrane ATPase dysfunction, and disturbances in calcium

and potassium serum levels.


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Figure 5.1 – Aneurysm rupture

Cerebral perfusion is altogether reduced following SAH, and even more

so in the case of cerebral vasospasm. The cerebral metabolic rate of oxygen is

also significantly diminished. These values remain decreased for a few weeks after

this event, possibly foreshowing cerebral infarction. Autoregulation suffers

impairment (causing vasomotor paralysis), as evidenced by alterations in systemic

blood pressure and partial pressure of carbon dioxide.

CLINICAL FEATURES


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Sudden onset of excruciating headache is the central feature of SAH. It is

described appearing as a “bolt out of the blue” (hence named thunderclap

headache) and patients refer to it as the “worst headache of my life”. Some

individuals present with warning bleeds that trigger cephalgia of variable

intensity and possibly associated with nausea, vomiting, and giddiness. This

warning hemorrhage is exceedingly important to identify on time to prevent a

catastrophic SAH.

Sudden loss of consciousness (LOC) occurs as intracranial pressure

exceeds cerebral perfusion pressure. It affects 45% of patients and the severity

varies from a state of drowsiness and mild confusion to deep coma. The amount

of bleeding and the location of the aneurysm have a strong influence on the

duration of the comatose state.

Meningeal irritation syndrome (nuchal rigidity and pain, photophobia)

is caused by the presence of blood and its irritative effect in the subarachnoid

space. It is highly evocative and can occur in as many as two thirds of patients,

although only after a delay of several hours following the rupture event.

Visual loss manifests as a consequence of venous hypertension and

disruption of retinal veins and retinochoroidal anastomoses. The mechanism of

this is either compression, or increase of the intracranial pressure. Three types of

ocular hemorrhages have been described: subhyaloid (pre-retinal), intra-retinal,

and vitreous (the so-called Terson syndrome). Visual loss may spontaneously

resolve in 6-12 months, or may lead to irreparable visual deficit.

Among the focal neurologic deficits described, mono- and hemiparesis,

diplopia, and extraocular movement impairment are the most common. 3rd

cranial nerve palsy (the eye is angled “down and out”) is most likely the result

of compression from a Posterior Communicating Artery aneurysm.


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MANAGEMENT STRATEGIES

First of all, it is recommended that all patients suffering from SAH (regardless of

their clinical condition) should be admitted into the intensive care unit until the

etiology of hemorrhage is identified. Patients must not be allowed out of bed and

mobilization should be reduced to a minimum (just enough to prevent deep

venous thrombosis). Limited visitors and external stimulation (including

lighting) are also highly suggested. Nevertheless, it is mandatory to maintain

frequent neurologic evaluation, analgesia (but cautiously), pulse, hematocrit and

oxygen monitoring. Fluid intake should also be regulated.

Proper history of the patient, physical examination and assessing

Airway, Breathing and Circulation (properly coined the medical “ABC”) are

obligatory, since treatment is based on these variables. Endotracheal intubation

should be performed for comatose patients and those unable to protect their

airway. Intratecal thrombolytics such as recombined tissue plasminogen

activator (rtPA) may be required to reduce the risk of rebleeding. Because the

patient should be kept abed, placing a Foley catheter for urine output is

recommended.

The traditional medical treatment consisted of strict blood pressure

control with antihypertensive therapy and fluid restriction. Nowadays,

antihypertensive agents are advocated only when mean arterial pressure surpasses

130 mmHg, as the traditional treatment was incriminated for having high

mortality and morbidity rates. Arterial pressure should be kept at optimal levels, so

that cerebral perfusion is not affected. Most clinicians avoid using nitrates

(nitroglycerin), which increase intracranial pressure. Instead, the agents of

choice in patients without contraindications are beta-blockers, easily titrated and

have little if no influence on intracranial pressure. Calcium channel blockers

(nimodipine) do have a tendency to increase intracranial pressure, although not as

much as nitrates. The advantages of Triple H therapy (hypertension, hypervolemia

and hemodilution) are controversial.


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An angiogram can reveal the site of rupture, although some studies

debate on whether the use of angiographic dye may cause cerebral vasospasm. If

intracranial pressure is well controlled and, in general, the age of the patient is

under 65 years, a craniotomy can be performed immediately. Is preferable to

remove large flaps of bone, as to avoid brain herniation and strangulation. In

elderly patients who present with co-morbidities, or improperly controlled

intracranial pressure, the prospect of endovascular approach can be considered.

The treatment of complications ensuing SAH will be presented in the following

chapter.

REFERENCE


Hemoragice. Editura Medicală Universitară „Iuliu Hațieganu” Cluj-Napoca 2007;

2.2.3: 107-116


4: 73-85

3. Kato Y, Sano H. Subarachnoid Hemorrhage. In: Kalangu KKN, Kato Y,

Dechambenoit G. Essential Practice of Neurosurgery. Access Publishing Co., Ltd,

2009; IV.3: 446-458

4. Becske T, Lutsep HL. Subarachnoid Hemorrhage. Medscape Reference. Cited 11th

Jan 2014

5. Greenberg MS. Handbook of Neurosurgery. Seventh Edition. Thieme, 2010; 30:

1034-1044

CHAPTER 6 COMPLICATIONS OF SUBARACHNOID SPACE HEMORRHAGE


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INTRODUCTION

Complications following SAH can be divided into two categories, neurological

and medical. Although it was believed that the elevated mortality and morbidity

rates of SAH were assigned to neurologic complications, recent evidence tends to

confer medical complications a much more substantial role than before. Usually,

the poorer the patient’s state on admission means the higher the probability to

develop complications.

1. Neurological complications:

Rebleeding

Hydrocephalus

Seizures

Vasospasm

2. Medical complications:

Cardiovascular dysfunction

Hypertension

Hyperglycemia

Hyponatremia

Deep Venous Thrombosis (DVT)

Pulmonary dysfunction

Gastrointestinal dysfunction

The two most dreaded of these are definitely rebleeding and

vasospasm. The most scarring and disabling of all, these two have the highest

mortality rates of all SAH complications. The majority of authors therefore


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recommend a more assertive approach toward these patients, starting with

admission in intensive care, even should their general condition be good.

A. NEUROLOGICAL COMPLICATIONS

REBLEEDING

The incidence of rebleeding is greatest within the first 2 weeks, the peak looming

between the initial 24-48 hours and affecting about 4% of the patients. Afterward,

the incidence hovers at around 1.5% per day, thus 12-20% of individuals present

with rebleeding in the later 12 days and 50% in the following 6 months. Mortality

stands at staggering 50% within the first month. A high grade on the Hunt and

Hess scale indicates a great chance of this complication. The best chance for the

patient is either immediate surgical clipping of the ruptured berry aneurysm, or

endovascular obliteration, the choice depending on the location and neck of the

aneurysm, and, of course, hospital staff experience and availability.

Patients who have survived the initial SAH have a greater chance of

redeveloping SAH than the general population. Even though the aneurysmal cause

is identified and properly treated, the long-term risk of re-rupture remains.

Therefore, efficient screening for new aneurysms in these patients is enormously

worthwhile.

HYDROCEPHALUS

Hydrocephalus can either be an acute or a delayed complication of SAH. An

obstructive mechanism of acute post-SAH hydrocephalus is considered, with the

greatest implications being the impediment of CSF flow through the Sylvian

aqueduct, the fourth ventricle, or absorption through the arachnoid

SECTION IIi: CEREBROVASCULAR DISEASE

CHAPTER 6: COMPLICATIONS OF SUBARACHNOID HEMORRHAGE

76 | P a g e

granulations. The onset is within the first 24 hours, although it can be postponed

to as much as one week.

Risk factors that precipitate the development of hydrocephalus include

increased age of the patient, radiologic factors (intraventricular hemorrhage,

diffuse SAH and intraparenchymal hematoma), use of antifibrinolytic drugs,

arterial hypertension, seizures, loss of consciousness, and certain locations of

aneurysms (especially those involving the posterior cerebral circulation).

Among the most evocative clinical features are abrupt mental status changes, such

as lethargy, stupor, or coma. The most lethal alterations are brainstem

compression and occlusion of blood vessels.

Nearly half of cases of acute post-SAH hydrocephalus resolve

spontaneously. In case sudden improvement does not occur, ventriculostomy is

the recommended course of action. Precautions must be taken in order to avoid

sudden decrease of intracranial pressure (which may itself increase the risk of

rebleeding) or infections.

Chronic or delayed hydrocephalus is caused by increased adhesion

between the arachnoid and the pia mater, and the scarring of the arachnoid

granulations of Pacchioni. It occurs in 3 weeks following SAH and manifests with

incontinence, gait instability, and progressive cognitive dysfunction. Half of

patients may require permanent ventricular drainage in order to achieve

amelioration.

SEIZURES

Rupture of aneurysms situated in the middle cerebral artery territory typically

results in seizures. These appear in 13-24% of patients within the first 24 hours

and can be partial, generalized or complex-partial. Seizures are inherently a risk

factor for rebleeding, as they may lead to hypertension, increased cerebral blood

flow, and elevated intracranial pressure.


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Since phenytoin can attain rapid therapeutic concentration through

intravenous load and does not cause alterations in consciousness, it is the agent

of choice in treating this complication. Long-term anticonvulsants are not

recommended if the patient is without a history of seizures prior to SAH.

CEREBRAL VASOSPASM

Cerebral vasospasm is the most severe, and therefore most feared, complication

following SAH of aneurysmal origin. Rarely, it can also occur after trauma, in

which case hemorrhage may or may not be present. Vasospasm has two

definitions:

1. Delayed Ischemic Neurological Deficit (DIND), also known as

symptomatic vasospasm, is characterized by decreased level of

consciousness with focal neurological deficits. As its name suggests, a

variable time gap stands between the onset of SAH and the neurologic

deficit.

2. Radiographic vasospasm, or angiographic vasospasm, is described as

arterial lumen narrowing shown on angiography, with slowing of contrast

filling.

These two entities may coexist, or appear independently. Most patients

(20-70%) present with radiologic vasospasm, while only a fraction (20-30%)

develop neurological deficit.

From a clinical standpoint, vasospasm may be indistinguishable from

rebleeding or delayed hydrocephalus. It is usually insidious and manifests with

general symptoms such as decrease in level of consciousness, meningeal signs and

confusion, and focal symptoms, for example headache, focal motor deficit and

cranial nerve palsy.

Depending on the location of the ruptured aneurysm (or cause of SAH),

two syndromes have been described:



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Anterior Cerebral Artery (ACA) syndrome, essentially comprised of

frontal lobe deficit (apathy, confusion, attention deficit, bradypsychia,

urinary incontinence);

Medial Cerebral Artery (MCA) syndrome, as evidenced by hemiparesis,

aphasia and apraxia (inability to perform complex movements).

Vasospasm has a typical onset on the 3rd

day after SAH has occurred, but

no later than 17 days following hemorrhage. This, however, depends on whether

the patient has had a prior SAH. In patients with previous SAH, the day of onset

is nearer to the earlier limit, while the patients experiencing the first SAH

develop vasospasm closer to the later limit of the interval. The culmination of

vasospasm is around days 6-8 after hemorrhage and the resolution is usually on the

12th

day.

Pathophysiology is still disputed. There are many theories regarding the

narrowing of arteries, although studies in humans and animals have revealed that it

is not the result of architectural thickening of the vessel walls (thus disaffirming

the hypothesis of endothelial proliferation). Most likely, vasospasm is actually a

multifactorial, profound vasoconstriction as a response to vasoactive substances

(noradrenaline, prostaglandins, plasmin, fibrin degradation products, angiotensin,

or serotonin) in the subarachnoid space. Presently, the most studied etiologic

factors are hemoglobin and endothelin. Inflammation and immunoreactive

processes might also be incriminated.

Among the known risk factors of vasospasm are as follows:

1. High Hunt and Hess grade on admission

2. Placement and number of blood clots (high Fisher Grade)

3. Clinically severe SAH

4. Large volume of blood in the subarachnoid space

5. Female sex

6. Age less than 35 and more than 65 years

7. Smoking

8. Arterial hypertension


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9. Hypovolemia

10. Location near the proximal 9 cm of ACA or MCA

11. Incomplete Circle of Willis

12. Angiographic dye administration (controversial)

Diagnosis of vasospasm is by method of exclusion of other causes of

neurological deficit, which are rebleeding, hydrocephalus, cerebral edema,

seizures, cerebral hypoxia, sepsis, and metabolic disturbances (hyponatremia).

Transcranial Doppler (TCD) is a non-invasive method for diagnosing cerebral

vasospasm. Whenever vasospasm is present, the velocity of blood flow increases

(above 200 cm/s), which is detected by the TCD. MCA is the most often used

vessel in this purpose. Increased blood flow may yield false negative results,

which should be taken into consideration.

Prevention of vasospasm is primarily achieved trough early surgery (by

evacuation of clots, ventricular drains of blood and reducing the chances of

rebleeding), although tempestuous handling of vessels may actually increase the

chance of vasospasm. Avoidance and treatment of hypertension, hypovolemia,

infection and anemia may also alleviate the severity of this complication.

Early surgical treatment of rebleeding represents the most important

method of prevention of vasospasm. Conversely, aneurysmal clipping can

essentially increase the risk of vasospasm by aggressive behavior toward arteries.

The risk of this complication can be diminished through intraoperative irrigation

of the subarachnoid space with thrombolytic substances (such as urokinase,

recombined tissue Plasminogen Activator, papaverine and, more recently,

nicardipine). In the case of refractory vasospasm affecting larger vessels, Trans

luminal Balloon Angioplasty can be used to dilate the narrowed arteries. Cervical

sympathectomy has fallen into desuetude.

Medical management targets vasospasm, with the additional goal of

granting neuroprotection. At the core of this method lies the Triple-H therapy,

represented by hypertension, hypervolemia and hemodilution, which has



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promising results. Calcium channel blockers (such as Nimodipine and

Nicardipine) are also used due to their smooth muscle relaxation effect and their

neuroprotective action (Nimodipine especially). Other neuroprotective agents are

NMDA receptor antagonists (Nuedexta) and Free Radical scavengers

(antioxidants).

Patient monitoring should include maintenance of systolic pressure

above 120 mmHg, isotonic substance perfusions and normal maintenance of

systemic vascular resistance. Electrocardiography may be performed for elderly

patients. Careful monitoring of the side effects of medical treatment is also

mandatory.

B. MEDICAL COMPLICATIONS

CARDIOVASCULAR DISFUNCTIONS

Arrhythmias occur in the initial stages of SAH and can affect as many as 90% of

patients. They are the result of subendocardial and myocardial infarction, and

coronary vasospasm due to high levels of systemic and myocardial noradrenalin

(released as a response to stress and pain during SAH) and potassium depletion.

Mostly benign, only those associated with hypokalemia are considered life

threatening.

The most common examples of arrhythmias following SAH include:

Premature ventricular complexes

Bradyarrhythmias

Supraventricular tachycardia

Ventricular flutter

Ventricular fibrillation

Torsade de Pointes


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Treatment of this complication is rather difficult. The Triple H therapy

employed to prevent secondary cerebral infarction may actually exacerbate an

already existent myocardial ischemia. Contrariwise, myocardial infarction therapy

(such as nitrates) may in fact increase intracranial pressure, lower cerebral

perfusion pressure, and aggravate cerebral ischemia. Some patients may require

insertion of a pacemaker in the event of sustained bradycardia. However this may

also decrease cerebral perfusion pressure.

HYPERTENSION

Arterial pressure may increase prior to aneurysmal rupture as a response to stress

factors, or after this event as a means to compensate for the decrease in cerebral

perfusion pressure. The latter situation is known as the Cushing phenomenon.

Mild sedation might prove sufficient in the maintenance of arterial

pressure, whereas antihypertensive medication may only be given should

sedatives fail. The true purpose of treating hypertension is not a rapid decrease in

arterial pressure, but preserving a balance between maintaining cerebral perfusion

pressure and diminishing the risk of vasospasm and rebleeding.

HYPERGLYCEMIA

This complication arises mostly because of stress and mainly affect elderly

patients with already manifest diabetes mellitus. Increased glycaemia may alter the

state of consciousness and trigger partial or generalized seizures.

Cortisone therapy would likely worsen hyperglycemia. Recommended

treatment should aim for dehydration correction, since the benefits of insulin are

disputed in these cases.



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HYPONATREMIA

Hyponatremia is the most common and most important of the hydrolytic

disturbances following SAH. It occurs in 35% of patients, with a peak incidence

between days 2-10 after the event. The exact mechanism is still uncertain, however

elevated levels of antidiuretic hormone (ADH) and atrial natriuretic factor

(ANF) have been incriminated.

ADH levels increase when plasma osmolality is high (as a consequence

of hyperglycemia, for instance), thus resulting in hypervolemia with an apparent

decrease in serum sodium levels (although technically there is no urinary loss of

sodium in this case). On the other hand, ANF secretion is stimulated by increased

intravascular volume and blocks sodium reabsorption in the distal ducts of the

nephrons. It is important to clinically differentiate between the two causes. In

inappropriate secretion of ADH (SIADH), the patient presents with

hypervolemia and fluid retention, whereas cerebral salt wasting syndrome

(CSW) manifests with hypovolemia and requires an additional supply of liquids.

Anterior circulation aneurysms are likely to result in diabetes

insipidus (since perforating arteries from this level provide for the hypothalamus).

This may remit in a matter of days up to weeks, yet some patients need intranasal

administration of desmopressin as diabetes insipidus may become permanent.

DEEP VENOUS THROMBOSIS

The incidence of DVT is 2%, with half of these patients developing pulmonary

thromboembolism. Therefore, prevention must be achieved by any means

necessary.

Intermittent compression of the inferior limbs and passive movement

exercises are the most favorable prophylactic measures, however anticoagulant

therapy is expressly prohibited in the case of an unclipped aneurysm.


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PULMONARY DYSFUNCTIONS

These complications are the most life threatening, affecting nearly half of the

patients with SAH. Pulmonary edema is of neurogenic origin and occurs after

acute neurological injuries that determine an increase of intracranial pressure. It

is caused by an alteration in pulmonary capillary permeability. Although its

incidence lessens with the time elapsed since SAH, it makes way for pneumonia

and thromboembolism.

Treatment of acute pulmonary edema may comprise of gentle diuresis,

dobutamine, and positive end-expiratory pressure. Triple H therapy is not

associated with neurogenic pulmonary edema, however it may be the cause of

fluid overload.

DIGESTIVE DISFUNCTIONS

Upper gastrointestinal bleeding arises from stress gastritis and mucosal ulcers

formed as result of elevation in intracranial pressure. These bear the name of

Cushing ulcers. They affect a significant number of patients with SAH (around

4%).

As a rule, all medical and surgical centers administer antacids and

antihistamines as prophylaxis. However, there is no study that supports the

efficacy of this treatment.



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REFERENCE



2.2.3: 107-116; 2.6: 149-158


4: 73-85; 8: 129-130

3. Kato Y, Sano H. Subarachnoid Hemorrhage. In: Kalangu KKN, Kato Y,

Dechambenoit G. Essential Practice of Neurosurgery. Access Publishing Co., Ltd,

2009; IV.3: 446-458

4. Mally R. Cerebral Vasospasm. In: Kalangu KKN, Kato Y, Dechambenoit G.

Essential Practice of Neurosurgery. Access Publishing Co., Ltd, 2009; IV.4: 472-476

5. Becske T, Lutsep HL. Subarachnoid Hemorrhage. Medscape Reference. Cited 12th

Jan 2014

6. Kassel NF, Shaffrey ME, Shaffrey CI. Cerebral Vasospasm Following Aneurysmal

Subarachnoid Hemorrhage. In: Apuzzo MLJ. Brain Surgery. Churchill Livingstone,

1993; Vol.1, 27: 847-856

Resection of a temporal lobe AVM situated on both sides of the vein of Labbe, with

anatomical and functional preservation of the aforementioned vein

CHAPTER 7 CEREBRAL ANEURYSMS - GENERAL ASPECTS


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INTRODUCTION

Cerebral aneurysms are pathologic focal dilatations of the blood vessels

comprising the cerebral circulation. This implies a thinning of all the layers of the

vessel wall, representing its point of minimal resistance.

Numerous factors have been incriminated in the development of

aneurysms, although not one can be declared the sole cause of their manifestation.

Thus, careful evaluation of all the risk factors and predispositions is crucial. Their

frequency, however, is nearly impossible to determine.

One of their main features, and also most perilous, is their propensity to

rupture. This often leads to the dreaded subarachnoid space hemorrhage

(SAH), with diffuse or focal forms of vasospasm resulting in the infarction of the

cerebral parenchyma.

Clinical presentation is mostly nonspecific, raging from a silent and

asymptomatic state, to mild headache, to even uncommon onsets of sudden death.

Though a SAH of an aneurysmal origin usually has characteristic historical

features, the pattern of symptoms differs with the size and placement of the

aneurysm itself.

All things considered, it is obvious why this subject has been considered a

challenge for neurosurgeons across the ages and why so many efforts were made

into understanding, diagnosing and treating cerebral aneurysms. The last decade

alone brought along considerable progress in these fields.


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CLASSIFICATION

Based on morphology, aneurysms can be divided as follows:

Saccular (berry or congenital, Figure 7.1) represent the majority (90%) of

all intracranial aneurysms and are usually placed at the branching points of

subarachnoid conducting arteries. In most cases (85-95%), saccular

aneurysms are situated in the anterior circulation. Rupture is frequent

within this variant, accounting for 70-80% of spontaneous SAH.

Figure 7.1 – Saccular aneurysm

Dolichoectatic (fusiform) aneurysms (Figure 7.2) are elongated

outpouchings of proximal arteries, having mainly an arteriosclerotic origin.

They are by far fewer than the saccular type (only 7%) and are generally

less likely to rupture. They predominantly affect the vertebrobasilar

circulation.

SECTION IV: ANEURYSMS AND AVMs CHAPTER 7: ANEURYSMS – GENERAL ASPECTS

88 | P a g e

Figure 7.2 – fusiform aneurysm

Mycotic (infectious) aneurysms are stationed peripherally, being the least

common type (0.5% of all cases). They are secondary to vascular wall

infection, due to hematogenous dissemination (for example, from a site of

infectious endocarditis). Frequently, infectious aneurysms are multiple.

Their high rate of rupture is noted.

The diameter of an aneurysm may vary from a few millimeters (below 5

mm it is considered a microaneurysm) to a few centimeters. Small aneurysms


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range from 5 to 12 mm. A large aneurysm has a diameter between 12 and 25 mm,

while a giant aneurysm surpasses the higher limit (Figure 7.3)

Figure 7.3 – Giant aneurysm


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EPIDEMIOLOGY

The actual prevalence of aneurysms in the general population is problematic to

estimate, since autopsy series differ in terms of age of the individuals assessed.

Most authors agree on an average of 5% of the general populace. Around half of

these aneurysms eventually rupture. It is unmistakable, however, that the

frequency of aneurysm detection increases with age.

Peak incidence of rupture varies between the fifth and seventh decades of

life, with only 2% of pediatric patients presenting intracranial aneurysms and a

significantly lower risk of bleeding. The great majority of aneurysms are

asymptomatic until this event.

Aside from age, aneurysm size has been repeatedly found as a

contributing factor of rupture. Thus, an aneurysm with a diameter between 4 and

7 mm has the maximum risk, while the giant variants seem to have a much less

pronounced tendency (possibly due to a thrombus reinforcing the thin vessel wall).

Most of cerebral aneurysms are situated in the anterior portion of the

Circle of Willis. Although it is debated whether this is a cause of limited diagnoses

rather than the actual prevalence.

Gender distribution of aneurysms tends to favor women, with a male to

female ratio of 1:1.6. This may suggest a hormonal determinism in their

development. Most of the aneurysms in men are situated either in the anterior

communicating artery (ACoA), or the anterior cerebral artery (ACA), while the

most common site in women is at the junction of the internal carotid artery (ICA)

with the posterior communicating artery (PCoA). Giant aneurysms are three

times more often in women and the prognosis for aneurismal SAH is also worse

for this sex.

Survival ratio after the firs episode of rupture is merely 50%. Only a

third of these patients may present an adequate long-term prognosis.


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ETIOLOGY

The cause of aneurysmal development is as of yet shrouded in mystery. The

pathogenesis is inherently tied to cerebrovascular structure aberrations and a

multifactorial etiology is currently widely accepted. Three types of factors are

involved in aneurysmal manifestation: A. risk factors, B. adjuvant factors and C.

rupture-triggering factors.

A. In comparison to extracranial arteries, the intracranial vessels present a thicker

internal elastic lamina, despite lacking the external elastic lamina. Also, the

muscular media has fewer muscle fibers, while the elastic tissue is sparser within

the media and the adventitia. The fibrous adventitia has the greatest input in

maintaining the structural integrity of the vessel wall. Despite this, the

subarachnoid space does not confer the same support as conjunctive tissue does.

Thus a genetic predisposition may be assessed. More recently, a substantial genetic

contribution to sporadic intracranial aneurysms has been discovered (Alg et al).

The researchers identified 19 single-nucleotide polymorphisms (SNPs) associated

with this disease, the most important of which were on chromosomes 9, 8 and 4.

The genes involved are related to vascular endothelial maintenance.

While atherosclerosis has been definitely impeached in the genesis of

dolochoectatic aneurysms, many authors associate this factor with hypertension

(along with a possible familial inheritance pattern) to the origin of saccular

aneurysms. The embolic factor has been tied to atrial myxoma (causing

neoplastic aneurysm formation).

The infectious factor determines the appearance of mycotic aneurysms,

typically in the distal branches of the middle cerebral artery (MCA). This suggests

the embolic origin of this type of lesion. Direct extension from arterial lumen to

adventitia of septic emboli containing Staphylococcus aureus or Streptococcus

viridans is thought to lead to wall degradation, thus causing mycotic aneurysms.


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Last, but not least, craniocerebral trauma may hold a key role in

instigating these lesions. In this case, aneurysms affect the peripheral cortical

branches as a result of the contact with the edge of the falx cerebri or skull

fracture. While not true aneurysms (due to the absence of all layers of the vessel

wall), traumatic dissecting aneurysms are generally located at the skull base and

are a consequence of the expansion of intramural hematomas.

Recent studies highlighted a direct relationship between aneurysmal

rupture and the intensity of apoptosis within the aneurysmal wall 1 or 2 days prior

to rupture itself.

B. Recurrently cited adjuvant factors are as follows:

Smoking (apparently the most important of all)

Pregnancy and labor (presence of aneurysms during late pregnancy and

childbirth commonly leads to rupture)

Oral contraceptives

Alcoholism

Drug abuse

Exaggerated food consumption

C. A few authors describe rupture-triggering factors, circumstances causing rapid

heightening of arterial tension:

Defecation

Coitus

Stress

Lumbar puncture

Cerebral angiography


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Intracranial aneurysms have been repeatedly associated with systemic

conditions and intracranial vascular malformations, among which:

1) Autosomal dominant inherited polycystic kidney disease (ADPKD)

2) Coarctation of the aorta

3) Fibromuscular dysplasia (intra- and extracranial alike)

4) Marfan syndrome

5) Ehlers-Danlos syndrome (type IV especially)

6) Arteriovenous malformations

7) Osler-Weber-Rendu syndrome

8) Tuberous sclerosis

9) Systemic lupus erythematosus

10) Sickle cell anemia

11) Von Recklinghausen disease

12) Moyamoya syndrome (explained in its respective chapter)

MORPHOLOGY

Typically, an aneurysm is comprised of three elements: the neck, which connects

it to the originating artery (it is also the site for clipping); the body (or the sac),

making up the majority of the aneurysm itself; the fundus, or the distal portion

(usually the point of minimal resistance, most likely to rupture). As previously

mentioned, saccular aneurysms represent the net majority and this description is

mostly suited for them. There are four rules regarding saccular aneurysm

anatomy, crucial to surgical approach:

1) They usually arise at the branching point of an artery;

2) They may also appear at the turning point of an artery, on its convex

portion;

3) They develop on the presumed trajectory of the blood flow had the

branching point or turn not existed;


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4) A constant feature is the perforating vessels that reside at the aneurysmal

point of origin. These must be preserved at all costs!

Fusiform (dolichoectatic) aneurysms are, as their name suggests,

elongated dilatations in the vascular wall, sometimes tortuous, innately deprived

of a true aneurysmal neck. They frequently contain a laminated thrombus. SAH

through rupture may occur, however these lesions more often exert mass effect on

cerebral parenchyma, with brainstem compression and cranial neuropathies.

Sometimes, their presence may result in the obstruction of cerebrospinal fluid

outflow.

Mycotic aneurysms are usually multiple and located at the distal

branches of the MCA. While meager in size, their propensity to bleed is

alarming. Because of these qualities, clipping is not recommended, if not entirely

impossible.

There are five major sites, accounting for almost 90% of all aneurysmal

placements:

1) The point of emergence of the PCoA from the ICA

2) The AcoA

3) The branching point of the ICA

4) The MCA point of bifurcation

5) The junction between the PCA and the basilar artery

Histologically, brownish pigmentation (hemosiderin) and fibrous

adhesions surrounding the adjacent brain parenchyma can be seen in gross

postmortem examinations. Shape and size may change after the onset of death.

Aneurysmal calcifications and intraluminal thrombus may also be sighted.


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Figure 7.4 – Localisation of aneurysms


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Microscopically, the thinned wall of an aneurysm might present all layers

of normal intracranial vessel wall. However, the internal elastic lamina may be

deteriorated and fragmented, while the tunica media may all the while be entirely

absent. Phagocytes laden with hemosiderin and lymphocytic infiltration may also

be present. An infected embolus adhering to a necrotic arterial wall within a

mycotic aneurysm is not uncommon. In this instance, the intima and internal

elastic lamina may be intensely affected, with an inflammatory infiltrate comprised

of polymorphonuclear cells, lymphocytes and macrophages. Vasospastic arteries

may display sarcolemmal destruction and myofilament fragmentation.

Figure 7.5 – comparrison between aneurysm wall structure (upper arrow)

and normal arterial wall structure (lower arrow)


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NEUROLOGY

Since most aneurysms are clinically silent prior to rupture, symptoms usually

describe the event of an acute SAH. Even though SAH of aneurysmal origin has

distinctive historical features, these may vary with placement, shape and size of

the aneurysm itself. The most typical symptoms of cerebral aneurysms and SAH

are along these lines:

Severe acute headache, it is commonly reported as “the worst headache

ever”. Pain can also be caused by aneurysmal expansion, intramural

hemorrhage or thrombosis and it may or may not accompany SAH. In most

neurosurgeons’ experience, there is a history of a warning leak a few days

before the onset of rupture (in ¼ up to ½ patients). Though these may be

mild, sudden headache or minor focal neurologic deficit should rouse the

physician’s awareness.

Facial pain can be caused by cavernous carotid aneurysms.

Alterations in consciousness, brought on by the sudden elevation of

intracranial pressure (possibly rupture-related) and a swift decline of cerebral

arterial perfusion pressure, may range from confusion, to mild impairment, to

even syncope in 50% of cases.

Palsy of the third cranial nerve (the eye is infraducted and abducted, or

“down and out”), particularly with a fixed dilated pupil and palpebral ptosis,

is pathognomonic for PCoA aneurysms. It requires diagnostic studies to

exclude a posterior carotid wall aneurysm or a distal basilar aneurysm.

Focal or generalized seizures occur within 24 hours of the onset of rupture

in up to 25% of patients.

Visual loss, blurred vision or diplopia may be manifest.

Weakness, hemisensory loss, language disturbances, memory loss, attention

deficit and olfactory disturbances are focal deficits produced by hemorrhage

or ischemia, although more commonly associated with giant aneurysms.

Photophobia, sonophobia or stiffness of the neck (caused by meningeal

irritation) may also be present.


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Autonomic disturbances such as fever, nausea, vomiting, diaphoresis and

chills are a result of blood degradation products being accumulated in the

subarachnoid space. Cardiac arrhythmias might have a different trigger.

Respiratory dysfunction and cardiovascular instability herald brainstem

compression.

Pituitary function may be altered due to intrasellar aneurysms.

The presentation of a traumatic aneurysm may be belated, with intracranial

hemorrhage or recurrent epistaxis.


First of all, it should be emphasized that there is no such thing as two clinically

identical patients. Therefore, the most effective way to approach a patient is not

simply objectivizing the superfluity of diagnostic information, but to employ a

subjective medical “sense” for the patient’s neurologic and systemic status.

Because the risk of rebleeding is at its highest within the first 48 hours

after the initial rupture, the surgical strategy is to minimize this threat by securing

the ruptured aneurysm as soon as humanly possible. Alas, the possibilities of

referring to neurosurgical centers are not the same for all patients; thus, many

arrive at least one or two days following the bleeding incident. This aside, it is not

always in the patient’s best interest to undergo surgery at night, citing the fatigue

of the neurosurgeon and the possibly suboptimal operating room staff. Last, but

not least, not aneurysms are alike, just as the patients are not. While some may

tolerate extensive retraction and dissection, those in poorer conditions may worsen

with hasty surgery. In this situation, it would be best if the brain was permitted a

few days to recover and even palliative endovascular approach might prove

attractive.

Prehospital care should include a thorough evaluation of vital signs and

neurological status. Endotracheal intubation and intravenous access may be


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necessary. The prevention of complications and supportive measures are the key

objectives of medical therapy for patients in the periprocedural period or poor

surgical candidates.

Prior to definitive aneurysm treatment, medical approaches imply the

control of hypertension, calcium channel blocker administration and seizure

prevention.

Following surgical or endovascular treatment, blood pressure must be

maintained higher as to lessen the complications of vasospasm. Antifibrinolytic

therapy (-aminocaproic acid) was introduced more than two decades ago, aiming

to prevent or delay rebleeding. However, cerebral ischemia resulting from

vasospasm proved more frequent if antifibrinolytics were used than if they were

not.

Pressors remain a pillar in the therapy of aneurysms. Their safety and

efficacy appear to be profusely enhanced by volume expansion, the combination of

hypertension and hypervolemia having the greatest outcome in the medical

treatment of symptomatic vasospasm.

Mainly, there are two major invasive strategies in the treatment of

cerebral aneurysms. Surgical therapy focuses on excluding the aneurysm from

the cerebral circulation and reducing mass effect on neighboring structures.

Numerous approaches have been developed and perfected to suit the location and

the anatomy of the lesion. In this purpose, a surgical clip (Yașargil clip) is placed

across the neck of the aneurysm, preserving the parent vessel and eliminating any

aneurysmal rest that may develop afterward. Endovascular techniques, on the

other hand, are an alternative that may be employed even in the onset of acute

aneurysmal SAH. They also allow parent vessel preservation and rely on

electrolytically detachable platinum coils (Guglielmi detachable coils, or GDC),

pliable stents (self-expanding or balloon-expandable), balloons or glue. GDC may

be deployed within the lumen of the aneurysm, promoting thrombosis and eventual

obliteration (See the following chapters for further details).


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REFERENCES



2.1: 91-102

2. Liebeskind DS, Lutsep HL. Cerebral Aneurysms. Medscape Reference, cited Dec

2013

3. Batjer HH, Chandler JP, Getch CC, Gravely L, Bendok BR. Intracranial Aneurysm.

In: Rengarchary SS, Ellenbogen RG. Principles of Neurosurgery. Second Edition.

Elsevier Mosby 2008; 14: 215-239

CHAPTER 8 ANEURYSMS OF THE POSTERIOR CIRCULATION

VICTOR VOLOVICI

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EPIDEMIOLOGY, TREATMENT, PROGNOSIS

The incidence of subarachnoid hemorrhage is estimated at 10-15 cases per 100

000, with major geographical, ethnic and gender variations[1]. Although a

common incidental finding at postmortem examination, with prevalence ranging

from 1% to 6% in large autopsy series[2,3] it is also estimated that per year 50%

or more from the patients with an SAH secondary to a ruptured intracranial

aneurysm die or are severely disabled, corresponding to about 14.000 people[2].

The outcome depends on various factors, 6 of which are the most relevant, age,

accessibility to a care facility, patient’s clinical status as described by the Hunt

and Hess and WFNS grading scales, the amount of intracerebral hemorrhage

according to Fisher’s grading scale, aneurysmal location and the presence of

vasospasm.

Aneurysms of the posterior circulation are estimated at 8-15% of all

intracranial aneurysms, according to multiple authors[6,8,9]. They are most

frequently located at the top of the basilar artery or at the junction of the

vertebral artery and the ipsilateral posterior inferior cerebellar artery[5,6]. In

20-30% of patients there were multiple aneurysms, usually 2 or 3, with as many as

13 described in one single patient[5,6,7,10].

Schievink and collaborators describe in the 1997 review published in the

New England Journal of Medicine that of the patients with spontaneous

subarachnoid hemorrhage approximately 12% die before reaching a hospital,

40% die within 30 days from the rupture and ~30% of the survivors are left

with severe neurological disability. Mayberg and colleagues describe in 1994 in

the guidelines for the management of aneurysmal subarachnoid hemorrhage that 5-


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15% of patients presenting with clinical symptoms of a stroke actually have a

subarachnoid hemorrhage and that the advice for this group of patients is early

treatment as early as 24-72 hours because of the high risk of repeat rupture

within the first 2 weeks after the subarachnoid hemorrhage episode[11].

SURGICAL OPTIONS

Some of the most burdensome lesions that a cerebrovascular neurosurgeon has to

face are posterior circulation aneurysms[26]. As stated earlier, disparaging

anatomy, lengthy complicated approaches and prolonged operation and ischemia

time all factor in to provide a considerable challenge for even the most skilled

neurosurgeon[14,15]. As with all intracranial aneurysms, a thorough plan has to be

thought out preoperatively and intraoperatively, a thorough and deep knowledge of

neuroradiology has to be employed for this purpose, and one must also make

judicious use of intraoperative monitoring, angiography, Doppler, whilst bearing

in mind proximal control, preservation of perforators and sharp dissection, to name

a few precepts[25].

There are 4 “classical” preferred approaches to posterior circulation

aneurysms, as well as combinations of these: the pterional approach, transpetrosal

approaches, retrosigmoid approach and extended far-lateral approach[25].

Lawton, Spetzler and collaborators divide posterior circulation aneurysms

in 3 groups with respect to their relationship to the basilar artery, as follows:

The first is the the upper basilar zone comprising the upper 2/5 of the basilar

artery, approached via an pterional approach [23].

SECTION IV: ANEURYSMS AND AVMs CHAPTER 8: ANEURYSMS OF THE POSTERIOR CIRCULATION

104 | P a g e

Figure 8.1 - Periosteum removal for craniotomy.

The second area of interest is the midbasilar zone, the middle fifth of the

basilar artery. These are approached via transpetrosal-type approaches: the

retrolabyrinthine approach, which spares the semicircular canals and cochlea,

and provides access to the neck of the basilar aneurysm, the translabyrinthine

approach, which implies sacrificing hearing and the elimination of semicircular

canals [29] and the transcochlear approach, which although offers a broad and

elegant exposure of the brain stem and clivus, does so at the expense of the most

part of the petrous bone, cochlea and extended manipulation of the facial nerve

[13,14]. For aneurysms involving the AICA the retrosigmoid approach is the most

widely used [25].

The third area of interest with respect to the basilar artery is the

vertebrobasilar zone, involving the lower 2/5 of the basilar artery as well as the

intradural part of the vertebral artery. These lesions are commonly approached via

a far-lateral approach [30,31], whereby classically 1/3 of the occipital condyle

would be drilled away and the foramen magnum would be resected laterally


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towards it while also removing the arc of C1 all the way to the anterior sulcus of

the vertebral artery. Experience has taught that it is also safe to drill 1/2 to 2/3 of

the condyle without sacrificing stability [25,30].

In selected cases where a giant aneurysm of the area needs to be

microsurgically treated, combinations of the aforementioned approaches may be

required, for example a combined far lateral- transpetrosal approach, in which

both the tentorium and the sinus sigmoideus are both sectioned to provide a wide

exposure of the antero-lateral brainstem [32,33].

Figure 8.2 - X-shaped or Y-shaped dura mater incision offers a wide

surgical field.


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Figure 8.3 - PICA aneurysm clipping performed while avoiding

damage to the cranial nerves and arterial perforators.

ENDOVASCULAR OPTIONS

As stated earlier, after the first experiments with “Hunterian” balloons as means of

occluding the parental artery[18, 19]. After the revolutionary invention of Guido

Guglielmi in 1991, the platinum detachable coils[35, 36], experiments began to be

more focused on the patient group deemed “too difficult to clip”: anatomically

undesirable location, poor neurological status, advanced age and poor overall

prognosis. Vinuela reports in the first multicenter study using coils in 1997 403

patients, 57% of which had posterior circulation aneurysms[22], as opposed to the


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regular 8-15%[8]. The breakthrough moment for the endovascular treatment of

aneurysms came after the publication in 1997 of the study by Raymond en

colleagues where 23 basilar tip aneurysms were treated by coiling and prevented

rebleeding, with mortality and poor outcome rates of 8.7% each and one death and

one minor permanent deficit as a direct result of endovascular treatment[38]. The

largest series of basilar tips aneurysms ever published, by Peerless and colleagues

in 1994 also had a mortality rate of 8% and a morbidity rate of 9.7%, which were

both linked, as in the case of the coiling procedures, to initial or recurrent bleeding,

vasospasm or technical complications. However, this series of patients was very

large, comprising 1767 vertebrobasilar aneurysms[37].

The studies reviews by Lozier et al regarding the endovascular treatment

of basilar apex aneurysms had diverse indications for coiling, failed clipping, poor

neurological status, physician or patient preference and anticipated surgical

difficulty on preoperative scans[9, 45-49], with a preponderance for the latter as

main reasons, namely anticipated operative difficulty and personal preference. The

size of the aneurysm was small(<10 mm) in 57.5% of cases, large(11-25 mm) in

34.6% of cases and giant(>25 mm) in 7% of cases, with 60.1% of them exhibiting

a broad neck(>4 mm). The Hunt and Hess score upon admittance was in 33.2% of

cases grade 1, in 31.4% grade 2, in 22.1% grade 3, in 8% grade 4 and in 4% of

cases grade 5. 220 aneurysms were treated with GDC coils. Of these, on analysis

of the immediate postprocedural angiography 100% occlusion was achieved in

43.2% of cases, 90-99% occlusion in 44.6% of cases and less than 90% occlusion

in 12.3%. The overall complication rate procedure-related was 14%(32 cases), the

most relevant being coil protrusion 9 cases(3.9%), parent artery thrombosis 9

cases(3.9%) and aneurysm rupture 7 cases(3.1%). Of these, 2 patients suffered

considerable neurological deterioration with a poor outcome and 2 patients

expired.

Subsequent articles, so far as 2013 confirmed the findings of Lozier et al

and despite the evolution of techniques figures hover around the same point[57].


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Even after 10 years, with the experience gathered and in spite of all new

techniques, a retrospective study performed by Tykocki et al in 2013 on 63

posterior circulation aneurysms, reveals similar figures[58]. 51 of these aneurysms

were ruptured and 12 unruptured. Complete occlusion was achieved in 36 (57.1%),

incomplete in 15 (23.8%), and partial in 12 (19%) patients. In patients with the

neck size of 1-2 mm the complete occlusion was in 75% (24/32) andincomplete in

12,5% (4/32). A neck size of 2-4 mm corresponds to obliteration rates of 38.7%

(12/31) complete occlusion and 29% (9/31) incomplete occlusion. The predictor of

total occlusion in Probit and linear regression models consisted of only one

independent variable, the narrow neck size. In this study there were no aneurysms

commonly regarded as broad-necked(>4 mm)[58], which could be considered a

selection bias.

As mentioned earlier, the most frequent localization of aneurysms of the

posterior circulation besides the basilar apex is the superior cerebellar artery,

13.5%[9]. Studies on other localizations are relatively scarce and are limited to

single-center experiences with small numbers of patients. Haw et al publish one

such study in 2004 in which 12 superior cerebellar artery aneurysms were treated

by endovascular coiling in eleven patients between 1992 and 2001[59]. 7 patients

presented with subarachnoid hemorrhage, 2 with neurologic deficit, and 2 with

unruptured aneurysms. 6 patients had a complete obliteration and 6 an incomplete

obliteration, with no further subarachnoid hemorrhage occuring during the follow-

up period(duration of follow-up between 6 and 119 months, mean follow-up 50

months). Procedural morbidity was one superior cerebellar artery infarct with good

recovery, and the outcome was satisfying, with 9 out of 11 patients on follow-up

were performing at Glasgow Outcome Scale (GOS) 5. One patient with GOS 3

presented with a poor grade subarachnoid hemorrhage and the other patient with

GOS 4 presented with a parenchymal hemorrhage due to an arteriovenous

malformation[59].


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RANDOMIZED TRIALS

The four trials which will be reviewed are the Helsinki prospective study of 1999,

the ISAT study of 2002, the ISUIA trial of 1998 and the Barrow Ruptured

Aneurysm Trial results of 2013.

The first randomized clinical trial which compared microsurgery with

endovascular procedure was published by Hernesniemi and his collaborators in

1999, and included 109 patients with SAH and an aneurysm which could be

treated by either method. The follow-up was clinical at 3 months, angiography at

3, 6, and 12 months and neuropsychological testing at 3 and 12 months. The

relevant figures show a technical mortality of 4% in the surgery group and 2% in

the endovascular group, with better initial angiographical results for posterior

circulation aneurysms in the endovascular group(11 patients, p=0.045)[65].

In 2002 in the Lancet Molyneux et al published the International

Subarachnoid Aneurysm Trial(ISAT)[66], providing level I evidence on the

subject. The study was a randomized prospective trial which enrolled 2143

patients with aneurysms which could be treated by either option, 1070 of which

were included in the clipping group and 1073 included in the coiling group. Over

90% of these aneurysms were under 6 mm and the majority involved the anterior

cerebral artery(50.5%), followed in frequency by the internal carotid(with the

posterior communicating included in this group). For the purposes of this review

we find in the study a figure of 2.7% posterior circulation aneurysms. When

compared to the normal 8 to 15%[6], we are faced with a selection bias of the

adjudicating committee, where there was unanimity among neuroradiologists and

neurosurgeons that most of the aneurysms needed to be treated by enodvascular

techinques. The overwhelming majority of patients were in excellent clinical

condition prior to the intervention. Follow-up involved using the modified Rankin

scale(mRS) at 2 months and 1 year. The study was halted when an interim analysis

revealed significantly better (p=0.0019) death and disability rates in the

endovascular group, where 30.6% of the patients treated microsurgically(243 of

793) had expired or were dependant at 1-year follow-up, compared with


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23.7%(190 of 801) in the endovascular group. A risk reduction for death and

dependancy of 22.6% and an absolute reduction of 6.9% for the endovascular

option[66].

The ISUIA(International Study of Unruptured Intracranial Aneurysms)

study published in the New England Journal of Medicine in 1998[67] explored a

different, subtly more complex issue: that of the treatment options for unruptured

aneurysms, which far outnumber those presenting with subarachnoid hemorrhage,

basing their discussion of the following key-point: what variables can predict the

moment of rupture for an aneurysm. The strongest predictors are thus the size of

the aneurysm, the location and the patient's gender and history(herein included

previously ruptured aneurysms). 1449 patients with 1937 were retrospectively

studied. The cohort was split in 2 groups: Group 1, 727 patients, no history of

SAH and Group 2, 722, with a history of a previously ruptured and treated

aneurysm, which presented another, unruptured, one.

For Group 1 the rupture rate was proven to be 0.05% per year with aneurysms

under 10 mm in diameter, and 1% per year for aneurysms over 10 mm in diameter.

Giant aneurysms posed a significantly higher risk, experiencing a 6% rupture rate

in the first year. As well as size, location was also a predictor for rupture: posterior

circulation aneurysms tend to rupture regardless of size.

Group 2 already had a history of SAH with a treated aneurysms and had another,

not ruptured aneurysm. Here the risk for rupture was 0.5% per year for aneurysms

less than 10 mm in diameter and less than 1% for aneurysms over 10 mm in

diameter. Size was in this group not an independent risk factor, but location and

age were, with basilar tip aneurysms showing a 5.1 relative risk and older age a 1.3

relative risk.

There is a discrepancy between the rupture rates encountered in clinical

practice and the rates exposed by the ISUIA study[6,67]. Thus, the same

investigators published in 2003 a prospective study following a larger cohort

recently, 4060 patients being assessed, 1692 without aneurysmal repair, 1917 had

open surgery, and 451 had endovascular procedures. The critical size for rupture


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was deemed 7 mm, with an evident higher risk for rupture of posterior circulation

aneurysms relative to that of anterior circulation aneurysms.

The results of the ISAT study of 2002 have to be viewed in light of the

new prospective randomized study carried out on 471 patients at The Barrow

Neurological Institute by Spetzler and his collaborators, the 3-year follow-up being

published in 2013[68]. 238 patients were assigned to clip occlusion and 233 to

coil embolization, with no exclusions based on anatomical criteria. Crossovers

were possible based on the physician's preference and evaluation and/or the

patient's wish and it is very interesting to note that of the 170 patients who had

been originally assigned to coiling, 64 (38%) crossed over to clipping, whereas 4

(2%) of 179 patients assigned to surgery crossed over to coiling. There was on the

6 months' 1 year and 3 year follow-up no significant difference in outcome

between anterior(339 cases) and posterior(69 cases) circulation aneurysms. The

only concern was raised by posterior circulation aneurysms: there was a

significantly better outcome in the coiling group than in the clipping group which

persisted at 3-year follow-up, but these figures have to be viewed taking into

considerations that the 3 groups are strongly inhomogeneous: anatomical matching

differs strongly, with for example 18 of the 21 posterior inferior cerebellar artery

cases being assigned to clipping.

CONCLUSION

It is easy to draw drastical conclusions based upon, for example, the ISAT study,

and say that all aneurysms need to be coiled or to take another extremist stand and

deem all aneurysms suitable for clipping based on the experience of renowned

centers with incommensurable experience in the microsurgical treatment of such

diseases. It is clear that there is a place for endovascular techniques in the

treatment of intracranial aneurysms, even with the recurrence rates and

reintervention rates. The question is if the patient who is admitted with an SAH or

the patient who discovered as a chance finding an aneurysm should be primarily

referred to the endovascular specialist or to the neurosurgeon (or to a vascular


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neurologist, who, in turn runs a multidisciplinary team) and in this respect it seems

rather evident that a multidisciplinary team is needed where the neurosurgeon the

lead role plays and the final word enounces for any given case. Moreover, it is

very easy to dismiss posterior circulation aneurysms as "coilable, with few

exceptions", when studies such as the one by Krisht in 2007[73] clearly show that

is not only endovascular techniques who are evolving, but also microsurgical ones,

with excellent results(no procedure-related mortality, mRS 0-2 in 92.8% of cases

for basilar apex aneurysms, traditionally considered a per excellence coilable

aneurysm). It should be evident, thus, that microsurgery has to continue to evolve

in providing the medical world with new techniques and new solutions for old

problems in the case of posterior circulation and should not, under any

circumstance, take a step back to allow coiling to automatically be the treatment

of choice for this anatomical location, but rather to set the tone and the standard of

care with respect to these lesions.

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39. Murayama Y, Malisch T, Guglielmi G, et al. Incidence of cerebral vasospasm after

endovascular treatment of acutely ruptured aneurysms: report on 69 cases. J

Neurosurg 1997; 87(60):830-835

40. Raymond J, Roy D, Bojanowski M, Moumdjian R, L'Esperance G. Endovascular

treatment of acutely ruptured and unruptured aneurysms of the basilar bifurcation. J

Neurosurg 1997;86(2):211-219

41. Phillips LH. The unchianging pattern of subarachnoid hemorrhage in a community.

Neurology 1980;30:1034-1040

42. Eskridge JM, Song JK. Endovascular emoblization of 150 basilar tip aneurysms with

Guglielmi detachable coils: results of the Food and Drug Administration multicenter

clinical trial. J Neuruosurg 1998;89(1):81-86

43. Schievink WI, Wijdicks EF, Parisi JE, Piepgras DG, Whisnant JP. Sudden death from

aneurysmal subarachnoid hemorrhage. Neurology 1995;45(5):871-874

44. Vallee JN, Aymard A, Vicaut E, Reis M, Merland JJ. Endovascular treatment of

basilar tip aneurysms with Guglielmi detachable coils: predictors of immediate and

long-term results with multivariate analysis 6-year experience. Radiology 2003;

226(3):867-879

45. Tateshima S, Murayama Y, Gobin YP, Duckwiler GR, Guglielmi G, Vinuela F.

Endovascular treatment of basilar tip aneurysms using Guglielmi detachable coils:

anatomic and clinical outcomes in 73 patients form a single institution. Neurosurgery

2000;47(6):1332-1339 discussion 1339-1342

46. Gruber DP, Zimmerman GA, Tomsick TA, van Loveren HR, Link MJ, Tew JM Jr. A

comparison between endovascular and surgical management of basilar apex

aneurysms. J Neurosurg 1990;90(5):868-874

47. McDougall CG, Halbach VV, Dowd CF, Higashida RT, Larsen DW, Hieshima GB.

Enodvascular treatment of basilar tip aneurysms using electrolytically detachable

coils. J Neurosurg 1996;84(3):393-399

48. Bavinzki G, Killer M, Gruber A, Reinprecht A, Gross CE, Richling B. Treatment of

basilar artery bifurcation aneurysms by using Guglielmi detachable coils: a 6-year

experience. J Neurosurg 1999;90(5):843-852

49. Klein GE, Szolar DH, Leber KA, Karaic R, Hausegger KA. Basilar tip aneurysm:

endovascular treatment with Guglielmi detachable coils - midterm results. Radiology

1997;205(1):191-196

50. Steiger HJ, Medele R, Bruckmann H, Schroth G, Reulen HJ. Interdisciplinary

management results in 100 patients with ruptured and unruptured posterior circulation

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51. Uda K, Murayama Y, Gobin YP, Duckwiler GR, Vinuela F. Enodvascular treatment

of basilar apex aneurysms with Guglielmi detachable coils: clinical experience with

41 aneurysms in 39 patients. J Neurosurg 2001;95(4):624-632

52. Lempert TE, Malek AM, Halbach VV, et al. Endovascular treatment of ruptured

posterior circulation cerebral aneurysms. Clinical and angiographic outcomes. Stroke

2000;31(1):100-110

53. Nicholas DA, Brown Rd Jr, Thielen KR, Meyer FB, Atkinson JL, Piepgras DG.

Endovascular treatment of ruptured posterior circulation aneurysms using

electrolytically detachable coils. J Neurosurg 1997;87(3):374-380

54. Birchall D, Khangure M, McAuliffe W, Apsimon H, Knuckey N. Endovascular

treatment of posterior circulation aneurysms. Br J Neurosurg 2001;15(1):39-43

55. Pierot I, Boulin A, Castaings L, Rey A, Moret J. Selective occlusion of basilar artery

aneurysms using controlled detachable coils: report of 35 cases. Neurosurgery

1996;38(5):948-953 discussion 953-954

56. Le Roux PD, Winn HR. Management of cerebral aneurysms. How can current

management be improved? Neurosurg Clin N Am 1998;9(3):421-433

57. Jennett B, Bond M. Assesement of outcome after severe brain damage. Lancet

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58. Tykocki T, Nauman P, Kostkiewicz B. Endovascular embolization of ruptured and

unruptured posterior circulation aneurysms. A multi-factor analysis. Turk Neurosurg.

2013;23(1):25-3

59. Haw C, Willinsky R, Agid R, TerBrugge K. The endovascular management of

superior cerebellar artery aneurysms. Can J Neurol Sci. 2004 Feb;31(1):53-7

60. Jin SC, Park ES, Kwon do H, Ahn JS, Kwun BD, Kim CJ, Choi CG. Endovascular

and microsurgical treatment of superior cerebellar artery aneurysms. J Cerebrovasc

Endovasc Neurosurg. 2012 Mar;14(1):29-36

61. Milosevic Medenica S. Endovascular treatment of wide-neck, ruptured and

unruptured aneurysms without supporting devices. A single center experience.

Neuroradiol J. 2013 Feb;26(1):97-105

62. Mukonoweshuro W, Laitt RD, Hughes DG. Endovascular treatment of PICA

aneurysms. Neuroradiology 2003;45(3):188-192

63. Yonas H, Agamanolis D, TakaokaY, et al. Dissecting intracranial aneurysms. Surg

Neurol 1977;8:407-415

64. Rabinov JD, Hellinger FR, Morris PP, Ogilvy CS, Putman CM. Endovascular

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65. Vanninen R, Kovisto T, Saari T, Hernesniemi JA, Vapalahti M. Ruptured intracranial

aneurysms: acute endovascular treatment with electrolytically detachable coils- a

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66. Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial

Collaborative Group(ISAT). ISAT of neurosurgical clipping versus endovascular

coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial.

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67. International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured

intracranial aneurysms- risk of rupture and risks of surgical intervention. N Engl J

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68. Spetzler RF, McDougall CG, Albuquerque FC, Zabramski JM, Hills NK, Partovi S,

Nakaji P, Wallace RC. The Barrow Ruptured Aneurysm Trial: 3-year results. J

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69. Wiebers DO, Whisnant JP, Huston J III, et al; International Study of Unruptured

Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: natural

history, clinical outcome, and risks of surgical and endovascular treatment. Lancet

2003;362(9378):103-110

70. McCormick WF, Acosta-Rua GJ. The size of intracranial saccular aneurysms. An

autopsy study. J Neurosurg 1970;33(4):422-427

71. Juvela S, Porras M, Poussa K. Natural history of unruptured intracranial aneurysms:

probability and risk factors for aneurysm rupture. J Neurosurg 2000;93(3):379-387

72. Hacein-Bey L, Connolly ES Jr, Mayer SA, Young WL, Pile-Spellman J, Solomon

RA. Complex intracranial aneurysms: combined operative and endovascular

approaches. Neurosurgery. 1998 Dec;43(6):1304-12; discussion 1312-3

73. Krisht AF, Krayenbuhl N, Sercl D, Bikmaz K, Kadri PA. Results of microsurgical

clipping of 50 high complexity basilar apex aneurysms. Neurosurgery 2007

Feb;60(2):242-250 discussion 250-252

CHAPTER 9 SURGICAL MANAGEMENT OF INTRACRANIAL ANEURYSMS

IOAN-ȘTEFAN FLORIAN, CLAUDIU POPA, IOAN-ALEXANDRU FLORIAN

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INTRODUCTION

The purpose of surgical treatment of intracranial aneurysms is preventing

aneurysmal enlargement and/or rupture while at the same time preserving the

integrity of normal vasculature, cranial nerves and cerebral parenchyma.

Usually, this objective is achieved by placing a clip at the neck of the aneurysm.

SURGICAL EXPOSURE

The ideal surgical exposure involves adequate brain relaxation and a sufficiently

wide bone opening. The former is vital in certain placements of aneurysms, such

as ACoA or basilar apex aneurysms. However, when aneurysms are more easily

accessible (as is the case of MCA and PCoA aneurysms), brain relaxation is not as

important. Methods for realizing brain relaxation are:

Hyperventilation

CSF drainage, which offers a dry surgical field and helps removing

blood and fibrin degradation products. This is realized through:

o Ventriculostomy: the ventriculostomy catheter can be placed pre- or

intraoperatively and may have a number of complications (seizures,

bleeding at point-of-insertion, infection, heightened risk of

vasospasm)

o Lumbar drainage: this is performed usually after anesthesia as to

avoid inducing arterial hypertension. In our unit, we use two types of

lumbar drainage:


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Through a lumbar puncture needle, which offers swifter

decompression, but can cause aneurysmal rupture. This drainage

method implies removing the needle only after lifting the

craniotomy flap. Drainage is allowed only up to 20-30 ml of CSF,

resulting in moderate brain relaxation and avoiding aneurysmal

rupture.

Through a drainage catheter, which grants a slower decompression,

but has the advantage of removing large amounts of CSF through a

Touhy 16 needle. On the one hand, there is a risk to abruptly

decompress the brain and rupture the aneurysm if this maneuver is

performed before surgery. On the other, catheter drainage provides

an adequate postoperative control of the aspect of CSF, avoids

painful repeated lumbar punctures, and offers protection against

fistulas in the event of an accidental opening of the frontal sinus.

Accidents reported in this maneuver are: aneurysmal rupture (0.3%),

chronic lumbar pains, drainage malfunction (5%), drainage fracture

in the subarachnoid space and consecutive CSF fistula, headache,

infection, neuropathy, and epidural spinal hematoma.

Intracisternal drainage: in our opinion, this is the most effective method of

intraoperative brain relaxation. Opening the basal cisternae and the Sylvian

valley, and extracting the occasional blood clots allows surgical comfort and

sufficient brain relaxation in the great majority of cases.

Administration of diuretics: Mannitol and Furosemide may, in theory,

elevate the risk of rupture.

CRANIOTOMY

The bone opening (craniotomy) must be:

Utterly adapted to the location, size and morphology of the aneurysm;

Able to reveal the Circle of Willis as basally as possible, thus reducing

the traction suffered by the brain;

SECTION IV: ANEURYSMS AND AVMs

CHAPTER 9: SURGICAL MANAGEMENT OF INTRACRANIAL ANEURYSMS

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Spacious enough for the surgeon to explore the main blood vessels and to

allow ample room in case of unforeseen events (aneurysmal rupture or

detachment, lesion of the proximal artery and so forth)

The classical pterional flap described by Yașargil is the pathway most

authors employ in the case of anterior circulation aneurysms, as well as the

majority of basilar apex aneurysms. We utilize a slightly modified pterional

craniotomy (frontal-temporal) for anterior circulation and supraclinoid basilar

aneurysms. We also used this approach to treat multiple bilateral aneurysms, with

one exception (in which case the bleeding emerged from the distal segment of A2

and we were required to use a bifrontal-pterional approach).

The indications for frontal-temporal approach are suprasellar and

parasellar lesions. On a sagittal plane, this approach can extend from the anterior

planum sfenoidale to the basilar artery level. On a frontal level, it can range

from the sellar diaphragm to a perpendicular level 1.5-2 cm away from it. Based

on the majority of authors and their reports, the greatest disadvantage of the

pterional approach is compromising the visibility of the contralateral optical nerve

and internal carotid artery. In our surgical experience, however, this disadvantage

persists only concerning the visibility of aneurysms of the contralateral PCoA and

anterior choroidian artery. This said, we have had only two cases of multiple

aneurysms in which we succeeded in clipping a contralateral PCoA aneurysm.

Using this approach, even the opposite MCA bifurcation may be accessed.

This type of craniotomy offers lateral subfrontal and Sylvian valley

access of aneurysms. Interstitial spaces of access are the interoptic-carotid,

ineroptic-chasm, suprachasmatic translaminaterminalis, and supracarotid

spaces, and the triangle made by the carotid artery and the oculomotor nerve. By

enlarging the craniotomy posteriorly (“half-and-half”), one can even clip

aneurysms near the basilar apex (superior cerebellar, posterior inferior cerebellar,

and posterior-superior-oriented basilar apex aneurysms).

Patient positioning. Generally, dorsal decubitus with a soft support of

the ipsilateral shoulder is recommended.


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The scalp incision starts at approximately 1 cm anterior to the tragus, just

above the zygomatic arch. Based on the location of the aneurysm, a slightly

anterior-driven incision will be performed. This allows a trepanation hole to be

placed above the middle of the superciliary arch (Figure 9.1)

Figure 9.1 - Frontal craniotomy incision. In this case, an anterior frontal

extension of the incision was performed to assure larger access of the

subfrontal region.

To preserve the frontal branch of the facial nerve, we perform an

interfascial dissection, exposing the flap on its entire surface and inferiorly until

this reaches the zygomatic arch (Figure 9.2).



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Figure 9.2 - Interfascicular dissection of the cutaneous flap.

Figure 9.3 - Bone flap periosteum removal.

We have modified the classical method of craniotomy, described as

having 4 burr holes, by placing the anterior hole above the middle of the

supraorbital margin. The so-called “key-hole”, the most important of the four, is


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positioned at the orbital-frontal angle. The second hole is made at the middle of

the coronal suture. The third one is made in the mediotemporal region and the

fourth in the temporal fossa, as low as possible (Figure 9.4).

Image 9.4 - Burr hole placement.

Once the bone flap is lifted, resection of the sphenoid wing is performed,

as close to the anterior cranial fossa as possible. Simultaneously, subtemporal

craniotomy is executed. The importance of this maneuver is great, since it

provides a large access toward deep structures while also diminishing the need for

brain retraction (Figure 9.5).

Decompressive lumbar puncture is usually practiced before opening the

dura mater. Its effects are almost immediate, the brain becoming pulsatile. Thus,

the tension in the dura mater decreases and the epidural space broadens.



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Figure 9.5 - Resection of the external 1/3 of the sphenoid wing.

DURA MATER INCISION

The dura mater is incised in an arch, from the posteriormost trepanation hole to

the anteriormost, at a distance of 2 cm from the sphenoid bone. The dural flap is

suspended inferiorly while the rest of the dura mater is left in its place, thus

protecting the brain (Figures 9.7 and 9.8).


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Figures 9.7 & 9.8 - Arcuate opening of the dura mater.



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DISSECTION

For adequately exploring the optochiasmatic region, opening the Sylvian valley is

mandatory. This operation may sometimes be challenging due to extant arachnoid

adhesions. Opening the Sylvian valley is simplified firstly by decompressive

lumbar puncture (performed earlier), and secondly by the aperture of the

pericarotid cistern deep within this valley. We begin opening the valley just above

the optic nerve, at the site where the arachnoid is further from the cortex,

regardless of whether this space is situated more laterally or medially. Afterward,

we dissect the valley until obtaining a sufficiently wide breach, extending it both

laterally and medially. At first, we do not employ any surgical instruments other

than a fine aspirator and a pair of microsurgical scissors. This way, we avoid

generating any decubitus lesions of the basal surface of the brain. Once we make a

small breach within the cistern, spontaneous CSF evacuation is achieved through a

soft tampon applied at the tip of the aspirator. Thus, an additional brain relaxation

is accomplished. By now the brain is suitably relaxed as to permit continuing the

dissection.

From this point on, the dissection may resume toward the location of the

aneurysm. For ACoA aneurysms, we dissect medially, whereas for aneurysms

involving the PCoA and choroidal arteries we continue laterally from the ICA

(Figures 9.9, 9.10, 9.11 and 9.12)

Regarding ICA bifurcation aneurysms, dissecting along this artery itself is

required. We usually focus on the lateral portion of the Sylvian valley, which we

dissect medially. The reason for this is to circumvent any chance to apply

excessive traction on the frontal lobe, traction that may detach a thrombus off the

ICA bifurcation aneurysm. Once the valley is entirely open, the ICA bifurcation is

visible. Above this element, the neck of the aneurysm can be distinguished, and

then dissected and isolated from the surrounding perforating vessels.


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Images 9.9 & 9.10 - Anatomic relationships include the optic nerve,

which is the first to appear in the surgical field. Careful dissection of

the arachnoid permits the visualization of the ipsilateral ICA, situated

on a deeper plane than the optic nerve (with which it forms the optico-

carotid triangle).



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Figures 9.11 & 9.12: Medial dissection permits total exposure of the

optic chasm, the contralateral A1 segment, as well as the contralateral

ICA. Continuation of the dissection allows access of the contralateral

M1 bifurcation.

Concerning MCA aneurysms, we recommend dissecting the ICA laterally

toward the bifurcation, as well as the initial portion of the MCA, so as to attain


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proper access of the vessel proximal to the aneurysm. Lateral dissection of the

valley can then be resumed, thus allowing for a shorter and relatively safer path

toward the aneurysm. Should intraoperative rupture of the aneurysm occur, we

discourage applying the temporary clip on the initial portion of the MCA longer

than 2-3 minutes (even if proximal control of this artery is attained). This amount

is usually more than enough to identify the M1 proximal to the aneurysm, where

the temporary clip may be reapplied for longer periods of time (8-10 minutes).

Basilar apex aneurysms can be approached through the

interopticocarotid triangle. Because the first aneurysmal component that “pops

up” in the surgical field is the fundus, access to this type of aneurysm raises a

number of difficulties. In the case of rupture, the situation may become dire, since

applying a temporary clip on an undissected and unisolated basilar artery is

performed at random and with the risk of affecting small-caliber vessels. These

vessels may be vital from a functional standpoint. Therefore, controlled

hypotension is recommended in this scenario (60-70 mmHg), along with placing a

clip on the dome of the ruptured aneurysm (to reduce the hemorrhage), and

dissecting and isolating the aneurysmal neck. Once the neck is in reach and as long

as the conditions are optimal, a permanent clip may then be applied.

CLOSURE

Closure is unexceptionally performed after rigorous hemostasis. This requires not

only frequently used hemostatic materials (such as Surgicel and Gelfoam), but also

a great amount of patience.

In all of our cases, we have used periosteum patch plasty to close the

dura mater. The periosteum is the most readily available material, as well as the

one having the greatest plasticity and tissue tolerance.

Nonresorbable threads are utilized to close the anatomic layers.

Subgaleal external drainage for a 48-hour period is, in our opinion, mandatory.



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We have employed this approach for 220 out of our 224 surgically treated

cases. The other types of opening will be presented in the chapters committed to

the anterior and posterior circulation aneurysms respectively.

INTRAOPERATIVE CEREBRAL PROTECTION

From a pathophysiological perspective, cerebral metabolism changes occur when

the cerebral metabolic rate of oxygen consumption (CMRO2) falls under a

certain threshold, due to an occluded artery. The territory supplied by said artery is

comprised of an ischemic tissue core, where neurons die in mere minutes, and a

penumbra (where marginal oxygenation is maintained, usually through the

leptomeningeal vessels). It may take up to several hours for the cells in the

penumbra to suffer irreversible damage. Cerebral protection against ischemia is

achieved by raising cerebral tissue tolerance to hypoxia. Protective agents act

through either preserving CMRO2 (Calcium channel blockers, free radical

scavengers, or Mannitol), or reducing CMRO2 by lowering neuronal electric

activity (barbiturates, Etomidate, or Isoflurane) or decreasing neuronal

maintenance energy (hypothermia remains the sole factor that can achieve this

purpose). Hypothermia has four grades:

Mild hypothermia, with core temperature down to 33OC may have

beneficial effects;

Moderate hypothermia, with temperatures between 32.5 and 33OC has been

used for head trauma;

Deep hypothermia from 32 to 18OC allows the brain to tolerate circulatory

arrest for up to 1 hour;

Profound hypothermia, with temperatures lower than 10OC, permits several

hours of complete ischemia (although this has unconfirmed clinical efficacy)

Adjunctive cerebral protection techniques: Systemic hypotension is

usually employed during manipulation and dissection of the aneurysm and has two

theoretic purposes, namely reducing aneurysmal turgor (to facilitate clip closure


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especially in the case of atherosclerotic neck) and diminishing transmural pressure

(to decrease the risk on intraoperative rupture). Some surgeons avoid this method

because of possible systemic hypoxia injuries.

“Focal” hypotension is achieved through the use of temporary clips,

specifically devised to avoid intimal injury of the vessel. These are placed on the

parent arteries, upstream of the aneurysm. Systemic hypertension may be

adjoined with this method to increase collateral flow. The proximal segment of the

ICA can sometimes tolerate an hour or more of occlusion, although perforator-

bearing portions of the MCA and the basilar apex may only abide several minutes

of temporary clipping. Among the most noted complications are intravascular

thrombosis and thromboembolism subsequent to removing the clip.

Some authors deem the use of temporary clips as being necessary in these

following cases: giant aneurysms, calcified neck, slender and fragile domes,

adhesion of dome to vital structures, perforators that arise from the vicinity of

the neck, and intraoperative aneurysmal rupture. Likewise, heparin might be used

to prevent thrombosis, whereas Thiopental, Etomidate, and Propofol may be

utilized when temporary clipping surpasses 10 minutes (so as to reduce neuronal

metabolism).

Circulatory arrest is used in conjunction with deep hypothermia. This

technique may be employed for patients harboring large aneurysms with

atherosclerosis and/or thrombosis and when the aneurysmal dome adheres to vital

cerebral structures.

ANEURYSMAL REST

Aneurysmal rest refers to the case in which clipping of the entire neck is not

feasible, leaving a free triangular-shaped section. This is not entirely harmless,

retaining a tendency to rupture throughout the years even at dimensions of 1-2

mm. The classification of aneurysmal rest is accredited to Drake (1967). More



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recently, Sidou et al. have proposed a new method of classification that may also

present reasons for additional clipping. Other surgeons encourage the necessity of

careful planning concerning adequate therapy of these aneurysmal rests:

endovascular approach, or direct surgical treatment. The incidence of

rebleeding in these cases stands at 3.7%. Postoperative follow-up must include

seriate angiography examinations. Any and all signs of aneurysmal rest growth

sanction either surgical or endovascular approach. A rebleeding incidence of 25%

has been cited at a 10-year postoperative follow-up of patients presenting with

aneurysmal rest.

ANATOMIC PRINCIPLES OF SURGICAL APPROACH

1) The parent vessel of the aneurysm must be exposed proximally to establish

blood flow control in the event of intraoperative aneurysmal rupture.

2) If possible, the main ipsi-/contralateral main vessel must be dissected

before the aneurysmal neck.

3) Dissection of the neck should precede fundus anatomization.

4) Before placing the permanent clip, all perforators must be separated from

the aneurysmal neck.

5) In the case of intraoperative rupture, certain objectives must be met:

tamponing, temporary occlusion, and lowering arterial pressure.

6) The permeability of large vessels and perforators should be confirmed

immediately after inserting the clip.

7) Bipolar coagulation can adjust the diameter of a large neck.

INTRAOPERATIVE ANEURYSMAL RUPTURE

Intraoperative aneurysmal rupture (IAR) is an undesirable event that should be

prevented and considered as integrating part of the surgical treatment of ruptured

intracranial aneurysms. Authors report an IAR incidence between 18 and 40%.

The epidemiology is on a continuous decline especially as a result of increasing

worldwide surgical experience and a greater expertise of rupture probability


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factors. If we consider that this risk peaked at 50% in the pre-microscopic age,

current data reveals that the number might have actually dropped to around 8.6%.

Morbidity and mortality of aneurysms increase with rupture by 20-25%.

This complication is exceptionally more threatening the earlier it occurs, during

anesthesia or opening of the dura mater. The aims of the neurosurgeon in this

scenario are: hemostasis, avoiding further aneurysmal damage, preventing

accidentally injuring main vessels and perforators, and clipping the aneurysm.

Precluding aneurysmal rupture involves certain measures: positioning the

patient in a way such that cerebral reduction is minimized, careful induction of

anesthesia, preventing hypertension during the “painful” stages of surgery, and

incision or head support fixation; eradicating the causes of transmural pressure

increase; simplification of access and aneurysmal dissection through a sufficiently

wide craniotomy and brain relaxation; using sharp instruments and dissecting

carefully so as to reduce the risk of extensive aneurysmal damage. Any method

that decreases cerebral retraction can lower the risk of rupture. Tempestuous

cerebral retraction in the initial phases of surgery can induce additional stress upon

the aneurysmal fundus and lead to overwhelming rupture and hemorrhage.

Lumbar or external ventricular drainage also assist in brain relaxation.

Some authors recommend cannulation of the frontal lobe as soon as the dura mater

has been opened (no occurrence of IAR in a series of 1500 patients who underwent

this maneuver), while also oppose lumbar drainage (which decreases intracranial

pressure in a chaotic manner). Frontal lobe cannulation also allows for better

control over intracranial pressure reduction.



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Operative stage Characteristics and treatment procedures

Initial exposure Rare. Cerebral mass becomes tensioned.

Causes:

Vibrations during drilling;

Intramural pressure growth upon opening the

dura;

Painful-phase hypertension;

Measures:

Decreasing arterial pressure;

Applying temporary clip, or ICA compression;

Frontal/Temporal cerebral resection.

Aneurysm

dissection

Causes:

Blunt surgical instruments: proximally from the

neck, difficult to control;

Sharp surgical instruments: minimal fundus

lesions;

Measures:

Damage caused by blunt instruments: temporary clip,

or lesion microsuture;

Damage caused by sharp instruments: tamponing,

suction, or coagulation.

Applying the clip Causes:

Insufficient aneurysmal exposure (blunt injury);

Flaws of the clip.

Based on Mark S. Greenberg, 2006.

Table 9.1: Characteristics of IAR

The phase of aneurysmal neck microdissection is associated with the highest

occurrence of IAR prior to applying the clip. Currently, there is a consensus


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regarding the use of sharp surgical instruments, which generate much more easily

controllable lesions.

In the event of early surgical phase aneurysmal rupture (preceding

aneurysmal microdissection), regional corticotomy might be sanctioned.

Sometimes, frontal or temporal lobectomy may be required to attain control over

the hemorrhage. The reasons for early IAR appear to be inadequate management

of arterial pressure, technical aspects that are correlated to lifting the craniotomy

flap, or uncontrolled drainage of CSF.

The basic rule of microdissection is obtaining proximal and distal

vascular control in its initial stages. In some cases, this may consent extracranial

exposure of vessels (for example, the cervical segment of the ICA, or the atlas

portion of the vertebral artery). This method of external compression of the

cervical ICA (performed by the anesthetist during aneurysmal rupture) seems to

subject the patient to unnecessary additional risks, as well as creating a low-

visibility surgical field.

Another aspect that should be taken into consideration is the path chosen

by the neurosurgeon to expose and dissect the region through the subarachnoid

space. If feasible, dissection must follow the natural anatomic path toward an area

concealed by a blood clot. Tempestuous aspiration of said clot ought to be

avoided, instead utilizing sharp instruments.

Temporary arterial occlusion is believed by most surgeons to be one of

the paramount measures in both prevention and control of aneurysmal rupture.

This maneuver can be coupled with the administration of certain agents that

protect the brain from ischemia.

In our practice, we apply temporary clips only in case we anticipate a

challenging dissection: giant aneurysms, polylobated aneurysms, or lesions that

have recently bled. Emergency surgical treatment builds the foundation for

aneurysmal rupture, while generally impressive cerebral edema makes for difficult



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brain retraction. This is the reason why, in case of early IAR (during induction,

craniotomy, or the initial stages of dissection), first and foremost we dissect the

ICA and apply a temporary clip at this level (preferably distal to the emergence of

the anterior choroidal artery). In some cases, this desideratum is not possible and

therefore the temporary clip is placed on the ICA just laterally to the optic nerve,

offering some measure of surgical comfort. The time gap is no longer than 8-10

minutes, however repeatedly removing and reapplying the clip (also in 8-minute

intervals) may allow for successful dissection of the ruptured aneurysm. A

permanent clip is then placed at the aneurysmal neck in 20-25 minutes at most.

The challenges that may arise as a result of rupture are a hemorrhagic

microsurgical field, accidental occlusion of the parent vessel or the perforators,

and substantial blood loss. Each and every location of intracranial aneurysms has

its own unique features concerning regional anatomy. These features can be used

in conceiving a targeted surgical approach, so as to effectively avoid or amend

aneurysmal rupture.

Ophthalmic artery IAR can be problematic to manage in the situation of

deficient proximal exposure and aneurysmal placement below the optic nerve or

the anterior clinoid process. This type of IAR is usually early, due to adhesions

between the aneurysmal dome and the optic nerve, although rupture can also

occur during neck dissection and clipping. Therefore, some authors support the

necessity of cervical ICA exposure before craniotomy, a method that can be useful

in the event of performing intraoperative angiography. In a few cases of surgically

treated ophthalmic artery aneurysms, resection of the anterior clinoid and

eventually opening the optic canal on a length of 2-3mm were sufficient for

aneurysmal clipping, rendering cervical ICA exposure unnecessary.

PCoA aneurysms have a more pronounced tendency to rupture because

of the adhesions between the aneurysmal dome and the medial surface of the

temporal lobe, or the anterior choroid artery. Thus, bleeding happens at the time of

temporal lobe retraction, or neck microdissection and clipping. In the last

scenario, clipping should be paused while temporary occlusion is initiated. This is


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the exact reason why we start the dissection in the subfrontal region, above the

optic nerve. From this level, we begin isolating and dissecting the ICA,

establishing vigilant proximal control. In the case of a subtentorially extended

aneurysm, any sudden movement can lead to rupture and therefore applying a

temporary clip on the ICA may be the necessary course of action.

There are three possible circumstances in which ACoA aneurysms

rupture: in the initial stages of microdissection (rough retraction of the frontal

lobe must be avoided, especially in the anteriorly or posteriorly oriented variants

which adhere to the optic chasm or the floor of the anterior fossa), microdissection

of an aneurysmal neck arising at the origin of the A2 (temporary occlusion of both

A1 segments is required), or the final stages of neck dissection (which necessitates

temporary bilateral occlusion of both the A1 and the A2). Resection of the gyrus

rectus proves highly useful, mostly succeeding the dissection of both A1

segments. The anatomy of these aneurysms is generally complex and angiographic

exploration does not always yield adequate coordination. On the other hand,

frontal lobe traction may alter normal anatomic rapports. These are the motives for

which we recommend proximal control on both A1 segments in all cases of ACoA

aneurysms. In the event of rupture, clipping will take place as near to the neck as

possible, firstly on the same side, and, should this not generate sufficient

hemorrhage reduction, a second clip will be placed on the contralateral A1.

ICA bifurcation aneurysms are in most cases adherent to the inferior

surface of the frontal lobe and have a higher leaning toward rupture than

aneurysms of the same caliber and different location. Frontal lobe retraction can be

limited if the ipsilateral Sylvian valley is dissected. Temporary occlusion is

performed above the origin of the anterior choroidal artery, which is a terminal-

type artery and can only endure occlusions of up to 15 minutes. A1 temporary

occlusion is executed if the ACoA receives blood flow from both A2 segments.

MCA aneurysms rupture either early during Sylvian valley dissection

procedures (when a second aspirator, dissection, and clipping of the M1 are

required), or during neck microdissection (in this scenario, we recommend



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temporary clips placed on both the M1 and the M2). Although, in theory, these are

much more easily approached, MCA aneurysms raise a series of difficulties

regarding valley dissection (the arachnoid can sometimes be thickened and

adherent, especially when hemorrhage occurred more than 14 days prior to

surgery), large aneurysmal neck, the emergence of the M2 segments on a long

portion of the neck, and the occasional presence of a trifurcation. All of these

features, along with a diminished occlusion tolerance of the M2, are decisive in

labeling the MCA as a challenging placement for aneurysms.

One of the most demanding complications of surgery is early rupture of a

basilar apex aneurysm. Consequently, adequate craniotomy is essential, as well

as CSF drainage, large basal exposure, and proximal vascular control (basilar

artery, superior cerebellar artery, PCA). Rupture occurs either during initial

dissection, or while clipping (in both cases, temporary occlusion and additional

aspiration are used).

Considering the anatomic features of the region, aneurysms affecting the

inferior portion of the basilar artery, PICA, or AICA are prone to rupture. Hence,

proximal arterial control and temporary clipping must be performed as soon as

possible during dissection.

Translated by Ioan-Alexandru Florian from: Florian IS, Perju-Dumbravă L.

Opțiuni Terapeutice în Accidentele Vasculare Hemoragice. Editura Medicală

Universitară „Iuliu Hațieganu” Cluj-Napoca 2007

CHAPTER 10 ARTERIOVENOUS MALFORMATIONS


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INTRODUCTION

Among the non-neoplastic cerebral lesions, arteriovenous malformations

(AVMs) account for the majority of hemorrhagic strokes below the age of 35

years. AVMs are also the main cause of neurologic deficit or mortality in young

adults. Therefore, well-defined diagnostic and treatment algorithms are substantial

in the management of AVMs.

William Hunter received credit for providing many important early

concepts on extracranial arteriovenous malformations in his 1762 monograph. His

descriptions formed the basis for the analyzing conflicting theories regarding the

pathophysiology and development of AVMs. In the mid 19th

century, Rokitansky

was the first to comprehensively portray angiomas of the intracranial cavity.

However, in his opinion, these were vascular tumors. Not long after, Virchow and

others polished Rokitansky’s description so as to include a somewhat rudimentary

classification of arterial, venous, arteriovenous and cystic angiomas, as well as

telangiectasias. It was Virchow who postulated that only a small percentage of

these lesions were neoplastic, and that the rest were, in fact, congenital anomalies.

The first well-documented case of a successful AVM excision was

performed in 1889 by Pean, a French general surgeon. The patient was a 15-year-

old boy who presented left-sided seizures and a right-sided fronto-parietal lesion,

namely an AVM. Afterward, Cushing and Dandy contributed to the history of

AVM treatment with their individual series of 14 and 15 cases, respectively.

Even so, the most important event in the treatment of AVMs to this day is

considered to be the development of intracerebral angiography. The

development of embolization and endovascular procedures represent other

milestones in the treatment of these lesions, as does the progress of neuroimaging.


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Today, functional mapping and frameless stereotaxis assist the

localization of AVMs. Endovascular procedures are perpetually improved,

although regardless of these advancements some patients are currently beyond any

assistance. Also, there are still numerous questions left unanswered concerning

AVM from both a medical and a scientific point of view. Yasargil and colleagues,

who have written a comprehensive review on historical developments of AVMs,

assure us that these dilemmas have existed ever since their discovery. That is

precisely why AVMs are in a “neurosurgical spotlight”, as not only diagnosis and

excision are key aspects of their treatment, but understanding them as well.

CLASSIFICATION

An exact description of AVMs is challenging, since their characteristics depend on

the quality of the post-mortem specimen. They differ in terms of bleeding

tendency as well as growth rate. McCormick defines four types of vascular

malformations:

1. True arteriovenous malformations share a common pathology, which is

direct arterial shunting into draining veins without the interposition of

capillaries. Most vessels within an AVM resemble veins in morphology,

although transitional vessels have also been described. Focal lesions are

usually compact, with no intervening neural tissue, while diffuse AVMs

include cerebral parenchyma between abnormal vessels. However, their

tendency to bleed depends on the histology and pathology of these lesions,

and not so much on their morphology. Hemosiderin deposits and atypical

gliotic tissue can be identified through microscopic examination after a

bleeding event. Consequently, thrombosis and reparative fibrosis (and in

some cases calcifications) ensue after these microhemorrhages. AVMs may

or may not be singular or associated with other vascular lesions. While

venous malformations do not present a clinical correlation, arterial

aneurysms have important clinical and surgical implications. These arterial

SECTION IV: ANEURYSMS AND AVMs CHAPTER 10: ARTERIOVENOUS MALFORMATIONS

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aneurysms have been categorized as intranidal, flow-related, or unrelated to

the AVM nidus itself. The intranidal aneurysms add to the risk of bleeding of

the AVM, whereas patients with flow-related aneurysms may present

hemorrhage from either lesion.

2. Venous malformations are composed of anomalous veins parted by normal

neural parenchyma. These malformations may represent a single tortuous,

profoundly dilated vein, or several veins converging at a single point. An

invariable trait is the absence of arterial input. They have been described as

the most frequent type revealed by autopsy. The venous phase of an

angiogram shows their characteristic appearance described as caput

medusae. On contrast-enhanced CT and conventional MRI, venous

malformations appear as linear signals in unusual locations. These lesions are

considered clinically benign, any hemorrhage arising from one being

secondary to a neighboring cavernous malformation.

3. Cavernous malformations are comprised of cystic vascular spaces

belonging to sinuous vessels, lined by a single endothelial layer. Recently it

has been discovered that the endothelial cells lack tight junctions. The

ensuing compact mass leaves no room for neural parenchyma to develop

within. Gross examination reveals well-circumscribed focal areas of reddish-

purple discoloration. Diameters tend to vary, reaching up to a few

centimeters. Hemorrhage leads to hemosiderin deposits, reactive gliosis and

possibly calcification. Since these lesions are in want of direct arterial input,

conventional angiography renders them almost undetectable. They are,

however, visible on MRI, having a specific appearance and heterogeneous

pattern.

4. Capillary telangiectasias are formed entirely by capillary-type blood

vessels. They closely resemble normal capillaries and, as opposed to

cavernous malformations, are surrounded by normal cerebral parenchyma.


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They seldom leave sequelae such as thrombosis or bleeding, despite their

frequent occurrence in the pons. Because of their low propensity to bleed,

capillary telangiectasias do not present a hemosiderin rim. It has been

considered1 that capillary telangiectasias are in fact nascent forms of

cavernous malformations, as both were present in the same patients, along

with what they described as intermediary forms.

A fifth category has been considered, that of direct arteriovenous

fistulae, presenting an undeviating connection between one or more arteries and a

vein. The interposing nidus is absent. Blood flow occurs at high pressures. Such

examples are the vein of Galen aneurysm, dural aneurysms and the carotid-

cavernous fistula.

The Spetzler-Martin grading scale is currently the most employed. It

takes into account the size, placement and drainage method of the AVM.

Obviously, this classification offers precious data on prognosis, evolution and

treatment indications, albeit being considered somewhat rudimentary.

AVM size

Small (<3 cm) 1 point

Medium (3-6 cm) 2 points

Large (>6 cm) 3 points

Adjacent cerebrum

eloquence

Ineloquent 0 points

Eloquent 1 point

Venous drainage Superficial 0 points

Deep 1 point

Table 10.1: Spetzler-Martin grading scale, with score for every criterion

An eloquent cerebral portion, through its lesions, leads to neurologic

motor or sensory deficit, or superior integration function deficit. The score given

1 Rigamonti et al, 1991


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by this classification can have a value between 1 and 5, thus defining the Spetzler-

Martin grade. As such, a medium-sized AVM in an ineloquent cerebral area with a

deep venous drainage has a grade III on the Spetzler-Martin scale. But so does a

small AVM affecting an eloquent cerebral area (for example the parietal lobe) and

a deep venous drainage.

In conclusion, grades I and II usually have a low mortality and morbidity

rate, while a grade V AVM may be considered inoperable, with severe neurologic

deficit. It is clear why this classification is not merely useful, but also imperative

before initiating the treatment of the patient.

EPIDEMIOLOGY

The true epidemiology and natural history of AVMs is difficult to determine, due

to the heterogeneity of patient populations and variable institutional bias towards

treatment. International detection rates range from 0.9 to 1.2 per 100,000 person-

years, however the true number of these lesions is thought to be far greater. It is

considered that approximately 0.1% of the global populace harbors at least one

AVM, most of which belong to the clinically benign types. Only 2% of AVMs are

multiple lesions.

As previously mentioned, AVMs are the main cause of hemorrhagic

stroke episodes under the age of 35 years and the most frequent cause of

neurologic deficit or mortality of individuals under 20 years of age. Death occurs

in 10-15% of patients who present hemorrhage, while morbidity occurs in 30-50%.

In population-based studies, 38-70% of intracranial AVMs initially present with

hemorrhage. Initial presentation may be indiscernible from other causes of

hemorrhage. The risk or rebleeding is high, especially during the first year after the

initial hemorrhage. Features associated with the risk of bleeding are the male

gender, an AVM of small size, posterior fossa or basal ganglia location, deep

venous drainage, reduced number of draining veins, high pressure in feeding


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arteries (as measured during angiography) and arterial aneurysms (whether

intranidal or flow-related).

The neurological deficit in an AVM-related hemorrhage is usually less

severe than that caused by a non-AVM-related hemorrhage. Recovery tends to be

better, as a result of both the young age of patients and the functional

reorganization of the cerebral parenchyma in patients with AVMs.

Seizures and epilepsy (focal or secondarily generalized) that are

unrelated to hemorrhage occur as the principal symptom in 15-40% of patients

presenting an AVM. The young age of patients, large AVM diameter, location in

the temporal lobe and feeders from the middle cerebral artery (MCA) are usually

associated with seizures. Anticonvulsivants comprise the standard treatment.

AVMs rarely lead to headache, however this may be the presenting

symptom for 4-14% of patients. Headache may be typical for migraine, or (less

specifically) more generalized.

MORPHOLOGY

The morphologic characteristics of an arteriovenous malformation are the arterial

inflow, the nidus and the venous drainage.

1. The arterial inflow consists of one or more arteries that supply the AVM

with arterial blood. They derive from the normal arterial circulation of the

cerebrum, however the vessel wall structure may present alterations. Blood

pressure in these abnormal arteries is lower than normal as a result of the

absence of peripheral resistance of the blood flow, normally generated by

capillary networks. As is the case with AVMs, the abnormal arteries drain

directly into low-pressure veins, causing the atrophy of the tunica media and

the adventitia. A high blood flow in these arteries may cause aneurysmal


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dilation, which in turn may lead to subarachnoid or intraparenchymal

hemorrhage.

2. The nidus is the main component of the AVM, the “body”, so to speak. It is

mainly an entanglement of abnormal, tortuous vessels that present variable

trajectories, calibers and lengths. Normal neural tissue usually cannot be

identified within the nidus. It is instead replaced by hemosiderin-impregnated

gliosis tissue, along with possibly thrombosis and even calcification.

Intranidal aneurysms possess a risk of rupture, adding the overall risk of

bleeding from the AVM itself. The size of the nidus can vary from just a few

millimeters to several centimeters (reaching even to an entire hemisphere), as

is the case of giant AVMs. Arteriovenous malformations tend to enlarge

where the arterial inflow is heightened, by engaging additional veins.

3. The venous drainage concludes the malformed arteriovenous route by

routing the arterial blood (that has not participated in nutrient and oxygen

exchange) into the venous circulation. Since the pressure in these particular

veins is higher than normal, it may lead to the vascular steal phenomenon,

depriving adjacent cerebral tissue of blood supply. Drainage can take place

into the dural sinuses (constituting superficial drainage), or the deep veins.

Arterialization is a process suffered by many of the drainage veins,

becoming larger in diameter (sometimes even aneurysmal in appearance)

with thickened walls, a tortuous trajectory and can occasionally be pulsatile.

Although capillaries are absent within the AVM, a proliferation of

capillaries can be noted at the periphery of the malformation itself. As previously

stated, aneurysms may be identified inside or associated with the AVM. They can

be of the following types: intranidal, flow-related or unrelated to the malformation.

As placement, AVMs can be found anywhere in the cerebrum, but also

intramedullary. The majority is located supratentorial, especially at the branches

of the MCA.


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PATHOGENESIS

Regarding the pathogenesis of AVMs, two hypotheses have been widely

discussed: embryonic agenesis of the capillary system and retention of

primordial vascular connections between arteries and veins. However, capillary

network agenesis would most likely result in brains lacking capillaries entirely, not

just focally. This is the reason why a different etiology must be incriminated.

AVMs are most likely the result of a combination of factors: the arrest of capillary

development in a certain area and the induced development of dysplastic vessels

from primordial vascular connections (although the latter mechanism is still

debated).


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There are several similarities between the morphology of an AVM and

that of an anastomotic plexus of a developing vasculature in the embryo. As such,

it has been hypothesized2 that AVM development begins during the sequential

formation and absorption of surface veins of the human embryotic growth.

Discordance between formation and absorption can potentially result in such an

anomaly. For example, the absence of the middle cerebral vein or its unsuccessful

communication with the cavernous sinus in patients harboring AVMs may signify

a late embryological development of that particular vein.

Aside from this, there are a few other embryological variants that tend to

correlate to arteriovenous malformations:

The entry of the superior ophthalmic vein into the cavernous sinus through

the inferior orbital fissure (rather than the superior one);

The relative infrequency of hemorrhage tied to the inferior petrosal sinus

fistula;

The occurrence of hemorrhage associated with a superior petrosal sinus

fistula;

The relative infrequency of blood backflow through the middle cerebral

vein in relation to a large cavernous sinus fistula;

A fusion deficit of the paired internal cerebral veins (which would explain

vein of Galen aneurysms).

Type 1 hereditary hemorrhagic telangiectasia (HHT), also known as Osler-

Weber-Rendu disease, has an autosomal dominant determination and is

represented by vascular dysplasia in multiple organs: cerebrum, gastrointestinal

duct and annexes and lungs. The AVMs concerning these cases have been reported

predominantly in adults. It is thought that mutation in the endoglin gene (on

chromosome 9) is the cause of this disease. Endoglin is a membrane glycoprotein

with a fundamental role in angiogenesis. Its level is reduced in the normal blood

vessels of these patients. HHT type 2 is caused by a mutation in the activin

receptor-like kinase gene (on chromosome 12) and is also autosomal dominantly

2 Mullan et al, 1996


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transmitted. However, the involvement of the endoglin gene in causing AVMs has

not been accurately demonstrated.

PATHOPHYSIOLOGY

The physiology of AVMs and the adjacent cerebral tissue can be affected by a

series of factors, including the size and location of the AVM itself, associated

vascular anomalies and the presence of hemorrhage. The key components to AVM

physiology models count the feeding artery of the lesion, the surrounding brain

(normally served by the same artery), and the arteriovenous shunt facilitated by the

AVM.

The unmediated connection between arteries and veins leads to the

abolition of peripheral capillary resistance. This in turn, eases blood flow

within these vessels, allowing for a higher velocity flow. As the arteriovenous

shunt becomes more pronounced, it will diverge blood flow towards the shunt

itself. This results in a reduction of cerebral perfusion in the vascular network

supplied by the feeding artery. This phenomenon is known as vascular steal and it

is inversely proportional to the hemodynamic resistance of the AVM. In normal

conditions, cerebral autoregulation would allow dilation of nutrient arterioles,

thus accommodating the reduced blood flow to the neighboring parenchyma.

However, long exposure to reduced perfusion pressures may result in permanent

dilation of the nutrient arterioles, which become pressure-dependent and passive

networks. Neither autonomic dilation nor constriction inputs function in this event.

Ischemia in the affected region occurs when the reduction in nutrient artery flow

exceeds the capacity for compensatory vasodilatation.

The nidus is also a site for important modifications. With the exception of

venous malformations and capillary telangiectasias, functioning brain parenchyma

is absent, being replaced by gliosis tissue (with calcifications and hemosiderin

impregnation). Blood vessel walls may also present with calcifications, hyalinosis,


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and aneurysmal dilation as a result of increased velocity and pressure of blood

flow.

AVM vessels are tortuous and entangled, showing intermediary

characteristics between arteries and veins. The size of the nidus is directly

influenced by flow and pressure. The higher the pressure and the flow, the larger

the diameter and the length of the vessels become. However, the most significant

mechanism of AVM growth is represented by the recruitment of additional

vessels. This is believed to cause the progressive neurologic deficit in AVM

symptomatology. Because of the high-velocity blood flow through vessels with

varying calibers, the flow becomes turbulent, non-laminar. This might lead to

murmurs perceived by the patient, or heard through the auscultation of the eye.

Drainage veins present a higher-than-normal blood pressure that is

conveyed to the tributary veins. This phenomenon leads to the adaptation of the

vessel walls, namely arterialization. High pressure and vessel dilation may lead to

headache that is resistant to analgesics and frequently pulsatile. The presence of

AVMs in small children can even be the source of cardiac pathology, such as

congestive heart failure.

HISTOPATHOLOGICAL FEATURES AND MOLECULAR BIOLOGY

Cavernous malformations regularly have a poor blood supply through very

small arteries. It is believed that capillary telangiectasias and cavernous

malformations are variations of the same entity (the former being the early

evolution stage of the latter). The veins in vascular malformations possess

thickened and hyalinized walls, almost completely deprived of smooth muscle

and elastic tissue. These veins are generally interspersed with normal brain

parenchyma. In some situations, cavernous malformations have been shown to

drain directly into venous malformations.


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As opposed to cavernous malformations, true AVMs exhibit mature

vessel wall features, as well as a high bloodflow profile. These grant a tendency

to vascular recruitment, vein arterialization and adjacent brain tissue gliosis.

Immunohistochemistry revealed that cerebral AVMs present with actin and

myosin heavy-chains staining within vessel-wall media. SM2, a marker for the

contractible phenotype of smooth muscle cells, has also been found in the venous

components of AVMs, suggesting arterialization of these components.

The dynamic features of AVMs may be explained through recent

findings, such as the increased expression of growth factors (including Vascular

Endothelial Growth Factor, Fibroblastic Growth Factor and Transformation

Growth Factor-1) and their receptors, positive DNA fragmentation, high levels

of endothelial turnover and imbalance of matrix metalloproteinases and their

respective tissue inhibitors, as well as angiopoetin and its receptor (Tie-2). Cell

death through apoptosis is also detected in the affected vessel walls. These

findings imply that AVMs are not inert vascular anomalies, but biologically active

and dynamically changing vascular pathologies.

The perinidal brain parenchyma suffers not only neural dysfunction, but

also neural loss as a result of the disturbed circulation around the AVM itself. A

pathologically dilated capillary network is located in the vicinity of the AVM,

connected to the malformation. Also, the absence of blood-brain barrier in these

afflicted vessels has been described.

CLINICAL PRESENTATION

AVMs are generally silent from a clinical perspective. As such, diagnosis is made

at the time when the first presenting event has occurred, usually a seizure or a

hemorrhage.

Intracranial hemorrhage is evidently the most common presenting

symptom (between 50 to 75% of cases) for patients with intracranial AVMs.


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Although subarachnoid and intraventricular hemorrhages may also occur, the

most often are the intracerebral hemorrhages, due to the location of the

AVM inside the parenchyma. Intraventricular hemorrhage from an AVM has

significant differences from that of a ruptured aneurysm. First, the blood

originates from (possibly arterialized) venous channels carrying blood with

arterial pressure, and not actual arteries. Second, vasospasm is rarely

associated in these instances. And last, survival and recovery rates are

much higher than those of a ruptured aneurysm, patients improving overtime

as the parenchymal clot resorbs.

Seizures are the second most frequent symptom related to supratentorial

AVMs, affecting 25 to 50% of patients without obvious hemorrhage. The

presence of a seizure disorder alone does not warrant radical surgical

treatment of true AVMs or cavernous malformations, since effective medical

management is sufficient in controlling AVM-induced epilepsy.

Headaches are a common symptom in patients harboring AVMs, however

rare in other vascular lesions without the evidence of hemorrhage. The

headache disorder is usually unilateral and similar to classical migraine

headaches, with the notable difference being that the pain does not shift

from side to side. However, auras, visual symptomatology and severe

debilitating intermittent headaches have also been described in patients

with AVMs. Patients most prone to developing a migraine-like headache

disorder of this cause harbor AVMs in the occipital lobe.

Arterial steal is a rare, nevertheless important symptom. It is most relevant

in patients who develop progressive neurological deficits without

hemorrhage over the course of many years, as a result of high-flow AVMs.


Treatment planning for AVMs depends on the risk of subsequent hemorrhage.

Although seizure disorder is also an important factor in deciding medical or

surgical management, it alone cannot be the basis of radical surgical excision. The


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historical and angiographic features of the individual patient establish the risk of

hemorrhage. Therapeutic alternatives include:

1. Operative resection or obliteration: Surgical treatment is the most

definitive and grants the best chance of an immediate cure. The least

important factor in deciding surgical approach is probably the presenting

symptom. The age of the patient, however, is significant. Non-symptomatic

patients over the age of 55 years present surgical risks equal to those of

allowing the lesions to develop naturally in the course of the lifetime.

Therefore, the risk of operative intervention in these patients is generally not

justified. Also crucial is the location of the AVM. Lesions in the basal

ganglia or brainstem should be treated surgically only in young patients

with symptomatic hemorrhage and important neurologic deficit. AVMs

situated in the medial hemisphere are also an operative challenge. As

opposed to these, small polar lesions can be treated even in older patients. As

previously stated, the Spetzler-Martin grading scale discriminates vascular

malformations on size, venous drainage and neurological eloquence of the

adjacent cerebral tissue. Surgical extirpation is highly recommended for

grades I and II, whereas grades IV and V are usually not amenable to this

approach alone. AVMs may be approached with craniotomy over the

cerebral convexity, through the base of the skull, or through the ventricular

system. The first step in resection in the isolation and ligation of the

arterial feeders. The nidus follows, while the draining veins are left for

last, so as not to increase the pressure while resecting the nidus.

2. Embolization: Endovascular embolization is an important adjunct that has

known rapid improvement concerning safety and efficacy. The procedure is

facilitated by the access through the femoral artery and fluoroscopic

guidance of a catheter into the feeding artery of an AVM. The arterial supply

of the lesion is occluded through the controlled use of embolic materials


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(such as wire coils, particulate slurries, pellets, small balloons or acrylate

glue). This method is almost never appropriate as the sole treatment, as a

partially treated AVM has a higher tendency to bleed than an untreated

lesion (through the increase of pressure inside the nidus). Embolization may

be performed in a single-stage, as well as a multistage approach, although

single-stage embolization offers higher safety and efficacy, despite the

apparent aggressiveness.

3. Radiosurgery: After Cushing and Bailey first described radiation therapy for

patients with AVMs, great progress has been achieved in both improving

target resolution and associated reduction in treatment morbidity. Proton

beam, gamma knife and linear accelerator methods are used to deliver

high-energy radiation to a well-defined volume containing the AVM nidus.

Thus, the malformed blood vessels undergo gradual sclerosis over the

course of 1-2 years, obliterating the AVM. During this period, the patient is

not free from the risk of hemorrhage. The gamma knife instrument is

expensive and therefore not widely available. Proton beams and linear

accelerators are more readily available and can be easily interfaced with

standard CT and angiographically directed stereotactic equipment. Proper

dosimetry diminishes side effects to moderate occurrences of mild radiation

necrosis. However, studies also reveal that neurological sequellae may

develop following radiosurgery. Regardless of the stereotactic method

employed, radiosurgery is not effective for AVMs with a diameter larger

than 3 cm.

As a rule, venous malformations and capillary telangiectasias do not require

therapeutic intervention due to their harmless nature. Incidentally discovered

cavernous malformations are best left untreated, unless they present with

hemorrhage. Medical care is recommended for older patients or individuals

without the high-risk features of AVMs. In such patients, anticonvulsants


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(phenytoin, carbamazepine) and appropriate analgesia (either non-specific or

migraine-specific) may be sufficient.

REFERENCE

1. Parsa AT, Solomon RA. Vascular Malformations Affecting the Nervous System.

In: Rengarchary SS, Ellenbogen RG. Principles of Neurosurgery. Second Edition.

Elsevier Mosby 2008; 14: 241-258


Hemoragice. Editura Medicală Universitară „Iuliu Hațieganu” Cluj-Napoca

2007; 2.1: 331-346

3. Hashimoto N, Nozaki K, Tagagi Y, Kikuta K, Mikuni N. Surgery of Cerebral

Arteriovenous Malformations. In: Apuzzo MLJ. Surgery of the Human Cerebrum.

Neurosurgery 2009; 375-389

4. Wurm G, Schnizer M, Fellner FA. Cerebral Cavernous Malformations Associated

with Venous Anomalies: Surgical Considerations. In: Apuzzo MLJ. Surgery of

the Human Cerebrum. Neurosurgery 2009; 390-406

5. Sen S, Lutsep HL. Arteriovenous Malformations. Medscape Reference. Cited 8

Jan 2014

CHAPTER 11 ARTERIOVENOUS MALFORMATIONS – CLASSIFICATION

SYSTEMS, DECISION MAKING AND CLINICAL ORIENTATION

VICTOR VOLOVICI

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Even though one would find in the old surgical/neurosurgical books references to

various attempts to handle this lesion sugically, true veritable surgery only took

place since 1960, with the most eloquent series up to this date being that of

Yasargil[1]. Around the same time, Luessenhop and Spence describe the first

embolization procedure[2]. It was only in 1980 with the appearance of the first

radiosurgical procedures that a three pylon treatment was established for

intracranial AVMs.

The same Luessenhop proposed in 1977 together with Gennarelli a

classification taking into consideration aspects of the arterial pedicles belonging

to the AVM[3], which din not take into account localization, size, age of the

patient or other criteria. In 1984 Luessenhop published another attempt at

classifying the AVMs based on their size[4,5]. In 1986, two complex classification

systems would be published, and one would be up to this date regarded as the

definitive one, even though new attempts are published every year. The first

system had 7 grades and was proposed by Shi and Chen in 1986, however it was

difficult to remember and had thus low applicability for the busy surgeon who had

to resort to sometimes rapid decisions when facing a patient[5]. The other

classification system which would remain is the one proposed by Spetzler and

Martin in the same year and published in Journal of Neurosurgery[4]. Its

unanimous acceptance is proof of its feasibility, easy application and relevance up

to this date. However, the Spetzler-Martin grade III poses a unique problem: it is

a very heterogenous group of lesions, which can range from a medium-sized

lesion in the brainstem to a small lesion in Broca with deep venous drainage, and


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all possible combinations inbetween. There is obviously a very big difference in

prognosis and treatment between these 2 lesions, which obviously with itself the

need to further develop the classification system in order to better classify the

grade III AVMs. This will then be known as the Lawton modified scale[6], who

in a study published in 2003 solves the dillemma in the following manner:

- Grade III- AVMs (S1V1E1) have a surgical risk similar to that of low-grade

AVMs and can be safely treated with microsurgical resection;

- Grade III+ AVMs (S2V0E1) have a surgical risk similar to that of high-grade

AVMs and were to be best managed conservatively;

- Grade III AVMs (S2V1E0) have intermediate surgical risks and require

judicious selection for surgery;

- Grade III* AVMs (S3V0E0) are either exceedingly rare, with a surgical risk

that is unclear, or theoretical lesions with no clinical relevance.

For the Grade III lesion described above of great relevance is the study by

Hernesniemi describing the natural history of the lesion and the bleeding chance

per year, whereby younger people would be much earlier and more aggresively

treated as opposed to older people[7].

In 1979 Drake published a paper about the management of AVMs whose

prerogatives hold true to this day[8]. These imply that a neurosurgeon has 5

options at hand when dealing with these lesions:

Expectant behavior (nothing except symptomatic treatment)

Surgery

Endovascular therapy

Radiosurgery

Combination of the aforementioned options


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With respect to decision-making, there are a series of studies published

providing guidelines for each Spetzler-Martin grade in particular (Vasquez and

Larrea in 2000, Ogilvy et al 2001 and Starke et al, 2009)[9,10,11]. They do not

differ much in their reccomendations, and these, resumed, would be as

following[12]:

Grade I and II: Must always be treated. They should not pose any

difficulty to the surgeon and have a curative rate of 100%. They can also be treated

endovascularily or radiosurgically, but radiosurgery in the case of grade I lesions

implies a period of about 2 years during which the malformation can bleed before

it disappears. Moreover, for grade II lesions of higher volume the nidus may not be

fully irradiated, leading to a recurrence with perhaps more risk of a bleeding

event. Endovascular options may show angiographical complete disappearance of

the lesion, but surgeons often see when operating on AVMs with complete

angiographical closure that there are often several arterial pedicles which are not

visible angiographically and which are at risk of bleeding.

Grade III: Must always be treated, as their heteorgenity predisposes

them to become problematic and symptomatic with time. Herein a

multidisciplinary team may be set up to preembolize the lesion (which would

intraoperatively bleed less) and it may also be combined ith radiosurgery. When

the lesions are treated they have a cure rate very close to 100%, but morbidity

reaches 25% even in the best series, especially with lesions in eloquent areas.

Grade IV: If the lesion has not bled and has no complications such as

flow-related aneurysms then it is amenable to wait-and-scan treatment. If it does

bleed then treatament should always be preeceded by endovascular treatment,

save for the most experienced surgical hands. There is high morbidity risk

associated with this entity.

Grade V: In principle, these should not be treated. When they are

treated, they have a very high morbidity and mortality rates and thus treatment is

for most surgeons of a palliative nature, to try to prevent bleeding. There are


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studies which suggest that operation without total excision involves a greater risk

of bleeding ultimately[12]. In principle, the lesion should be first embolized and

then operated on, keeping in mind the very high risk of postoperative sequelae.

In conclusion, AVMs are lesions which pose a number of risks even in

the most experienced hands and must thus only be treated by a handful of people

with the knowledge, experience and character, able to take on such a lesion, as

unforgiving as satisfactory as its obliteration can be.

REFERENCE

1. M.G. Yasargil: `Microneurosurgery, vol. III B: AVM of the Brain.1998 Georg

Thieme Verlag Stuttgart 25-53

2. A.J. Luessenhop, W.T. Spence: Artificial embolization of brain arteries: report of

use in a case of arteriovenous malformation. JAMA.172:1153-1155 1960

3. E. Spagnuolo, L. Lemme-Plaghos, F. Revilla, et al.:Recomendaciones para el

manejo de las malformaciones arteriovenosas cerebrales. Neurocirugía-Rev.

Española de Neurociencias. 20:5-14 2009

4. R.F. Spetzler, N.A. Martin, L.P. Carter, et al.: Surgical management of large

AVMs by staged embolization and operative excision. J Neurosurg. 67:17-28 1987

5. E. Spagnuolo: Deep arteriovenous

malformations. A.Pedroza L. Quintana T. Perilla Latinamerican Treaty of

Neurosurgery. 2008 FLANC Bogotá 425-436 Chap: 30

6. M.T. Lawton: Spetzler-Martin grade III AVMs: surgical results and a modification

of the grading scale. Neurosurgery. 52:740-749 2003

7. A. Hernesniemi, R. Dashti, S. Juvela, et al.: Natural history of brain arteriovenous

malformations: a long-term follow-up study of risk of hemorrhage in 238

patients. Neurosurgery. 63 (5):823-831 2008

8. C. Drake: Brain arteriovenous malformations: considerations for and experience with

surgical treatment in 166 cases. Clin Neurosurg.26:145-208 1979

9. Vazquez F, Larrea, J: Guides of treatment of AVMs. Guides of endovascular

emoblization. In: GENI: Grupo español de neurorradiología intervencionista


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10. C.L. Ogilvy, I. Awad, R. Brown, et al.: Recommendations for the management of

intracranial arteriovenous malformations: a statement for healthcare professionals

from a special writing group of Stroke Council, American Stroke

Association. Stroke. 32:1458-1471 2001

11. R. Starke, R. Komotor, B. Hwang: Treatment guidelines for arteriovenous

malformations microsurgery. BJNS. 23:376-385 2009

12. A. Quinones-Hinojosa, et al.: Schmidek and Sweet Operative Neurosurgical

Techniques, chap. 83, Elsevier Saunders 2012

CHAPTER 12 SURGICAL MANAGEMENT OF ARTERVIOVENOUS MALFORMATIONS

IOAN-ȘTEFAN FLORIAN, CRISTIAN PÂRJOL, IOAN-ALEXANDRU FLORIAN

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INTRODUCTION

Quite a few treatment methods for AVMs have been inducted and applied into the

neurosurgical practice. All of them have one common element, which is the risk of

inflicting additional cerebral lesions and deficits. This calls for measuring both

the emergency of treatment initiation and the risk it implies along with

conservative attitude, as well as the risks of nonsurgical therapy. AVM

pathology counts among the few cases in which deciding if and how to treat a

lesion may prove difficult. In these scenarios especially, Hippocrates' dictum

"primum non nocere" truly finds its applicability.

As methods of treatment, microsurgical excision of AVMs has been the

standard option for the last 25 years. It has the advantage of permanently

eliminating the nidus and closing the arterial feeders. Also, treatment of AVM-

associated aneurysms and hemorrhage control are practiced. It has been proven

that surgical resection grants an adequate control over AVM-induced strokes.

Currently, electing the treatment and adjuvant methods, as well as time of

surgery, are challenging decisions, being individualized for each and every case.

This depends on a series of risk factors tied to the features of the lesion, state of

the patient, and the patient's options. The aim is to avoid causing a worsening of

the deficit.

The indication of surgery is based upon significant symptomatology:

Hemorrhage with progressive clinical deterioration;

Gradual neurologic deficit;


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Severe, repeating, and incapacitating strokes that cannot be medically-

managed;

Recurrent hemorrhage;

Mental status deterioration;

Persistent and medically unresponsive headache.

Radical surgical approach is also encouraged in the case of small

cortical, or subcortical AVMs, especially located in non-eloquent regions of

the brain.

SURGICAL TIMING

Surgical treatment of AVMs has had a long history. Along the course of time, a

few principles of application have been implemented.

Surgical resection must be done selectively, not as emergency

treatment. Exceptions to this are when surgery is mandatory, the life of the patient

hanging in the balance due to the mass effect produced by the hematoma

following AVM hemorrhage.

In case it is feasible, conservatory treatment for about 3-4 weeks is

preferred. This leads to amelioration of the patient’s clinical condition and may

stabilize neurologic deficits. During this period, the hematoma caused by AVM

rupture liquefies, allowing for an easier removal. After this interval, angiographic

reevaluation is made (even if this is the initial angiographic examination), since

the rapports between the lesion and adjacent vessels may change following edema

resorption and hematoma organization. This allows for a simpler and facile

surgical approach of the AVM, as the brain is relaxed and the hematoma is

liquefied.

In the case of emergency surgical intervention, determined by progressive

neurologic worsening of the patient and life-threatening AVM hemorrhage, some


CHAPTER 12: SURGICAL MANAGEMENT OF ARTERIOVENOUS MALFORMATIONS

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authors recommend a more conservative attitude. They imply dividing surgery into

two separate times: initially, removal of the hematoma and avoiding tributary

vessels of the lesion; afterwards, once the patient is stabilized and the cerebral

edema has been resorbed, reintervention with radical excision of the AVM is

recommended. This algorithm offers operative comfort and alleviates surgical

dissection by reducing the acute effects of hemorrhage and assuring brain

relaxation at an interval from the moment of bleeding.

In patients harboring an aneurysm of the feeding artery of the nidus, if

this has ruptured, it is recommended to urgently clip the aneurysm, after which the

AVM can be approached. If the source of hemorrhage cannot be identified,

surgical treatment will also target the aneurysm first, and only then the AVM. It

should be mentioned that these patients present with a higher risk of bleed (7% per

year) than patients without AVM-associated aneurysms (4% per year). This is a

reason for early surgery. Aside from this, 50% of these patients carry multiple

aneurysms, 85% of which are situated on the feeding arteries or the major arteries

from which the feeders derive. This too encourages mainly surgery in favor of

other treatment options.

It must be emphasized that, form a clinical standpoint, hemorrhage arising

from AVMs are less severe than spontaneous bleed or aneurysmal rupture. As a

rule, after a rather dramatic start, progressive neurologic amelioration ensues,

permitting a delay of the surgical intervention. Even though neurological status

does not permit a postponement of more than 3-4 weeks, 4-5 days may seem

reasonable from the outlook of cerebral edema resorption and local

“appeasement”.

PREPARATIONS FOR SURGERY

As previously mentioned, preparatory steps must first include an angiographic

reevaluation. During this interval, selected cases would undergo main feeder


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vessel embolization, so as to reduce the risk of intraoperative bleeding. Also

during this period of time, the blood of the patient is collected for autotransfusion

(available for centers where this is performed as a routine), rheological values are

reassessed, and presumed hydric and electrolytic imbalances are adjusted.

If the patient is conscious and oriented, a series of neuropsychological

tests must be taken. All neurologic status elements must be well documented for a

more accurate comparison between preoperative and postoperative states.

POSITIONING OF THE PATIENT

The position of the patient on the operating table must be adjusted to a series of

principles. It should:

Be adapted to the location of the lesion;

Assure greater access of the lesion, offering the greatest amount of visibility

with the minimum degree of microscopic mobility;

Assure the greatest amount of brain relaxation, so as to avoid excessive

traction of the brain;

Not impede venous flow, even if this implies a slight intraoperative

repositioning of the patient’s head;

Guarantee a thoracic respiratory cycle as close to normal as possible.

Concerning supratentorial lesions, especially deep ones, we prefer dorsal

decubitus with turning the head sideways and eventually lifting the shoulder

(which allows lateral turning of the head without compromising venous flow in the

contralateral jugular vein). Lateral decubitus, especially for overweight patients,

cannot assure any degree of freedom of thoracic respiratory cycle, and may

sometimes at least encumber venous flow in the contralateral jugular vein.

Regarding posterior fossa AVMs, our opinion is that the sitting position

corresponds (Figure 12.1) in the highest degree to the principles presented earlier.



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Venous flow is greatly preserved, which is why we recommend this position,

along with all the measures of preventing air embolism.

Figure 12.1 - Median suboccipital craniotomy with the resection of the

superior ½ of the posterior C1 arch, which grants an additional 2-3mm

enlargement of the surgical field without compromising vertebral

stability.

We considered highlighting these aspects of AVM surgery and patient

positioning as necessary, since personal experience revealed the dramatic shifts in

operative aspect and conduct just through alleviating venous flow. Therefore,

whenever we notice an increase of AVM pressure and volume during surgery

(without this being tied to a lesion of nidus drainage veins), we ask the anesthetic

personnel to establish whether the head had turned slightly, compressing the

jugular veins.


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CRANIOTOMY

It is obvious that the bone flap must be centered on the AVM. What is particular

in these certain cases is the size of the flap, which more often must be wide enough

to permit:

Direct access toward the nidus feeder vessels (which may have a distant

origin from the lesion itself), as well as toward the nidus and its drainage

vessels;

A multidirectional approach of the AVM, without exerting traction or

excessive compression of the brain;

Differentiating between the normal drainage vessels, which should be

preserved, and the pathological ones, which must be excised;

Postoperative decompression of the brain, when cerebral edema, normal

perfusion pressure breakthrough phenomenon, or eventually rebleeding

(though an insufficiently obliterated feeder artery or AVM remnant) might

occur.

For posterior fossa lesions, a large suboccipital craniotomy is

performed, eventually partially removing the posterior arch of the C1. This latter

element is implemented when MRI reveals descended cerebellar tonsils.

SURGICAL EXCISION OF AVMs

The basic aim of surgery is complete resection of the AVM, abolishing the risk of

ulterior hemorrhage. This is also the essential treatment of AVM-induced strokes.

Incomplete resection does not reduce the risk of either recurrent hemorrhage, or

further stroke episodes.

The AVM excision technique includes several well-established

objectives. These may be separated into five steps: identifying and eliminating



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feeder vessels, circumferential nidus dissection, apex dissection, venous pedicle

removal, and definitive hemostasis.

Identifying and eliminating the feeder vessels is the first step. This

implies dissecting AVM tributary arteries up to the level of the nidus, verifying

their role in AVM supply through temporary occlusion (with a temporary clip),

and removing them via coagulation or permanent clips. Also during this steps,

presumed “en passage” arteries are evaluated, which although traverse the nidus

have no connection to it whatsoever and must be preserved at all costs. These

supply the adjacent cerebral parenchyma.

In theory, this is a relatively easy step. In truth, this is a lot more

challenging due to the sinuous pathway of the arteries, their duplication, or

triplication sometimes further from the nidus. In this case, comparing

intraoperative aspects with angiographic imagery may offer valuable

indications, although these two facets may not always match perfectly. In many

cases, intraoperative observation shows the transformation of a normal artery into

a secondary feeder vessel, or numerous feeder arteries that provide perforators for

the normal brain. On the other hand, distal dissection of the nutrient vessels is not

without its risks of damaging the brain, even superficially, during opening the

sulci. An approach that is as close to the nidus as possible may increase the

difficulty of identifying these vessels and thus complicate surgery. Removal of the

nidus without proximal control on at least one major feeder vessel is also a delicate

procedure. This is the reason why there is no universally available technique for

AVM management (Figure 12.4).

In the case of superficial malformations, once the feeder artery has been

identified, it is dissected along its entire path adjacent to the AVM itself. This is

performed with great regard towards recognizing and maintaining the arteries as

well as the veins that serve the normal cortex (Figures 12.2 and 12.3).


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Figures 12.2 and 12.3 - In superficial malformations, identification of

the feeder artery and the nidus is easy. Placing a temporary clip

enables malformation collapse.



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Figure 12.4: Feeder artery dissection within the intergyral sulcus is

performed with the preservation of the normal draining veins, as well

as the normal arteries that supply the surface of the brain.

In the case of deep malformations, especially insular or medial temporal,

dissection must start from the main cerebral arteries: ICA and MCA. From these

on, dissection would progress until the nidus feeder has been identified, followed

by the malformation.

For medial line supratentorial AVMs, interemispheric approach may

appear as the most logical. Craniotomy should therefore be performed so as to

offer access of the A2 segment as proximally as possible. It should also allow

access of the drainage veins that usually flow into the sagittal sinus (frequently

posterior to the anteriormost third of said sinus). Interemispheric access must be

performed with the utmost care, so as to not generate compression or lesion of the

AVM drainage vein proximal to the malformation. The pericallosal artery must


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also be correctly distinguished and preserved. From this on, the feeder vessels

would be identified, coagulated and sectioned.

Paraventricular AVMs present a serious challenge: their feeder arteries

may have multiple origins (MCA, ACA as well as PCA). Clearly, there is no

craniotomy technique that allows dissection of all feeder arteries. Therefore, the

approach is made through the wide opening of the gyral sulcus that may lead

closest to the lesion. Angiographic data helps in pinpointing the superficial feeder

arteries, which will be dissected, later followed by the nidus itself.

For posterior fossa AVMs, finding the nutrient vessel may be difficult.

Our advice is to dissect the vertebral artery ipsilateral to the AVM, followed by

identifying the origin of the PICA, which most frequently generate the feeder

arteries. Dissection of the PICA and the nutrient arteries offers the possibility of

proximal control of the AVM, and by placing a temporary clip, nidus dissection

may ensue.

The most efficient method of occluding feeder arteries, which usually

have thin vascular walls, is bipolar coagulation, followed by microsurgical

sectioning. Few are the cases in which two vascular clips must be placed with the

arterial section made between them. Even arteries of remarkable diameters can be

coagulated, sometimes gradually, as to reduce its caliber until it no longer presents

a problem for ulterior coagulation and sectioning. The intensity of coagulation,

however, must receive great care. If this is too high, it may lead to hemorrhage of

remarkable proportions, complicating surgery from the very start (Figures 12.5 and

12.6).



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Figures 12.5 & 12.6 - Through progressive coagulation, even large

vessels can diminish their diameter, facilitating sectioning.


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Circumferential dissection of the nidus would be performed only after

the nutrient arteries have been individualized and eliminated. This step should be

taken as close to the margins of the lesion as possible, to avoid damaging adjacent

cerebral tissue (especially in the eloquent cerebral areas). Although some surgeons

prefer dissection in the glial plane surrounding the nidus, our experience revealed

that, in most cases, this plane does not exist to begin with, the monstrous nidus

being bordered by apparently normal cerebral tissue. Through coagulation of the

nidus walls, a progressively increasing dissection plane can be obtained. This is

performed circumferentially, while protecting the adjacent cortex with serum

soaked tampons. Gradual nidus coagulation leads to a decrease of its volume and

creating new dissection planes. As this increases in depth, newer feeder arteries

may be discovered, some of them small in size, which would also be coagulated

and dissected (Figure 12.7).

Figure 12.7 - Circumferential dissection of a deep malformation is

practically impossible. In cases such as this, the AVM is gradually

coagulated.



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Figure 12.8 - Circumferential dissection of a superficial AVM.

Accidental lesion of a nidus vessel represents a possible scenario with

impressive bleeding, which can be resolved with aspiration to pinpoint the origin

of hemorrhage and progressive coagulation along the entire path of the affected

vessel. Applying a small tampon and aspirating through it offers a neat cleansing

of the surgical field and the possibility of adequate reevaluation of the situation.

This event may seem a trial to the inexperienced neurosurgeon. The loss

of a relatively high amount of blood in short time, decrease of arterial pressure, the

pressure exerted by the event itself and possibly by the anesthetist team may lead

to a state of panic. From this moment on, precipitated gestures, tempestuous

maneuvers, and random coagulation of nidus vessels can lead to a cataclysmic

conclusion. That is precisely why we consider this type of surgery only available

to the high-experienced neurosurgeons. In our experience, we have not met with a


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single intraoperative AVM hemorrhage that we could not contain in the proper

amount of time, although this type of hemorrhage was not seldom encountered.

In the most frequent cases in which the AVM became apparent through

bleeding, the hematoma represents a pathway to the nidus simply by aspirating

the liquefied clot. If surgery is performed as an emergency to save the patient (due

to the increased volume of the hematoma), the aspired clots generally lead to a

bleeding nidus. Therefore, it is preferable to partially drain the hematoma at a

slight distance from the AVM, with the purpose of cerebral decompression,

followed by identifying the nutrient vessels and excluding them and only

afterwards returning to the nidus and removing it.

Apex dissection continues the previous step and represents the hardest

part of AVM surgery. The last nutrient vessels to be removed from circulation are

found at the AVM apex. Usually, vascular dissection, coagulation, and

hemostasis are challenging at this point, considering the depth of the field.

Dissection is also made difficult by the numerous small vessels that perforate the

white matter to reach the nidus. Isolating and coagulating them must be preformed

gently so as not to section them. Otherwise, coagulation within cerebral

parenchyma may determine further brain damage.

Venous pedicle removal and AVM excision are performed in this

relatively simplistic step, after circumferential and apex dissections. Great care

must especially be attributed to the small remaining feeder vessels that may be

situated underneath and masked by the venous pedicles. By any and all means,

normal veins must be carefully preserved (Figures 12.9 and 12.10).



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Figure 12.9 - Isolation and coagulation of the draining vein.

Figure 12.10 - Dissection of the draining vein.


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Figure 12.11 - Resection of a temporal malformation situated on both

sides of the vein of Labbe, with anatomical and functional preservation

of aforementioned vein.

Definitive hemostasis is the final step of AVM resection. It is achieved

through electrocoagulation or hemostatic materials. Any residual damage at the

border of the cavity must be identified. Hemostasis confirmation is made by

soliciting the anesthetist team to progressively increase arterial blood pressure

up to values of 150-160 mmHg. Venous return, on the other hand, is verified by

moderate jugular compression. In the case of residual lesions, these may bleed

upon either blood pressure increase, or jugular compression test. These lesions

must be subsequently removed. After complete hemostasis is attained, hemostatic

material (Surgicel) is placed in the surgical field.

Regarding the cases involved in our study, all patients received surgical

treatment, without preoperative intravascular embolization or radiosurgery. The

majority of cases included presented a profoundly altered neurologic status upon

admission. Therefore, the most important decision regarding treatment concerned

the optimal time for surgery.



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In the case of patients with severe neurologic status upon admission

(GCS=6 or less), presenting considerable cerebral hematomas, surgery was

performed in emergency as primary intention. It implied hematoma evacuation

with cerebral decompression, followed by complete removal of the AVM. This

goal, however, was not achieved in every case, rebleeding being present in 6 out of

the 48 cases included in the study. If the neurologic status of the patient does not

improve, or even deteriorates, a second intervention is necessary in the shortest

amount of time possible. For an increase in surgical ease and if the patient’s

neurological status allows it, it is preferred to postpone the second intervention for

a few days to permit a decrease of the cerebral edema.

For patients who presented with a GCS=7 or above, recommended

attitude was delaying the surgical intervention (for as long as the neurologic status

allowed it), until a significant remission of the cerebral edema was achieved,

leading to an increase of surgical comfort for both surgeon and patient.

Neurological follow-up presented the most important aspect of this strategy. Any

deterioration of the neurological status called for surgical intervention.

Translated by Ioan-Alexandru Florian from: Florian IS, Perju-Dumbravă L.

Opțiuni Terapeutice în Accidentele Vasculare Hemoragice. Editura Medicală

Universitară „Iuliu Hațieganu” Cluj-Napoca 2007

an introduction to vascular neurosurgery

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