Download Physiology of cerebral venous blood flow: from experimental data in

Brain Research Reviews 46 (2004) 243 – 260
www.elsevier.com/locate/brainresrev
Review
Physiology of cerebral venous blood flow: from experimental data in
animals to normal function in humans
B. Schaller*
Max-Planck-Institute for Neurological Research, Gleueler Strasse 50, D-50931 Cologne, Germany
Accepted 26 April 2004
Available online 13 November 2004
Abstract
In contrast to the cerebroarterial system, the cerebrovenous system is not well examined and only partly understood. The
cerebrovenous system represents a complex three-dimensional structure that is often asymmetric and considerably represent more variable
pattern than the arterial anatomy. Particular emphasis is devoted to the venous return to extracranial drainage routes. As the state-of-theart-imaging methods are playing a greater role in visualizing the intracranial venous system at present, its clinically pertinent anatomy and
physiology has gain increasing interest, even so only few data are available. For this reason, experimental research on specific biophysical
(fluid dynamic, rheologic factors) and hemodynamic (venous pressure, cerebral venous blood flow) parameters of the cerebral venous
system is more on the focus; especially as these parameters are different to the cerebral arterial system. Particular emphasis is devoted to
the venous return to extracranial drainage routes. From the present point of view, it seems that the cerebrovenous system may be one of
the most important factors that guarantee normal brain function. In the light of this increasing interest in the cerebral venous system, the
authors have summarized the current knowledge of the physiology of the cerebrovenous system and discuss it is in the light of its clinical
relevance.
D 2004 Published by Elsevier B.V.
Keywords: Cerebrovenous system; Physiology; Animal; Human; Anatomy; Brain function; Hemodynamic
Contents
1.
2.
3.
Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Anatomy of the venous system of the brain . . . . . . . . . . . . . . . .
2.1. Superficial cortical veins and their intracranial draining routes . . .
2.2. Anastomotic veins . . . . . . . . . . . . . . . . . . . . . . . . .
2.3. Deep (medullary and subependymal vein) and their draining routes
2.4. Extracranial draining pathways . . . . . . . . . . . . . . . . . . .
Venous drainage of the posterior fossa . . . . . . . . . . . . . . . . . . .
3.1. Brainstem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2. Cerebellar hemisphere. . . . . . . . . . . . . . . . . . . . . . . .
3.3. Bridging veins and posterior fossa venous anastomosis . . . . . .
3.4. Major dural sinuses of the posterior fossa . . . . . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
244
244
245
246
246
246
247
247
247
247
247
Abbreviations: BBB, blood–brain barrier; BOLD, blood oxygen level-dependent; CBF, cerebral blood flow; CBFV, cerebral blood flow velocity; CBV,
cerebral blood volume; CSF, cerebrospinal fluid; CT, computed tomography; CVS, cerebral venous system; ISS, inferior sagittal sinus; MR, magnetic
resonance; PET, positron emission tomography; pCO2, partial pressure of carbon dioxide; rSO2, regional cerebral oxygen saturation; SjO2, jugular bulb oxygen
saturation; SSS, superior sagittal sinus
* Tel.: +49 221 4726 0; fax: +49 221 4726 298.
E-mail address: [email protected].
0165-0173/$ - see front matter D 2004 Published by Elsevier B.V.
doi:10.1016/j.brainresrev.2004.04.005
244
B. Schaller / Brain Research Reviews 46 (2004) 243–260
4.
Collateral venous pathways . . . . . . . . . . . . . . . . . . . . . . . . .
4.1. Anastomoses of superficial cerebral veins . . . . . . . . . . . . . .
4.1.1. Classical description . . . . . . . . . . . . . . . . . . . . .
4.1.2. The superficial sylvian vein . . . . . . . . . . . . . . . . .
4.1.3. Regional anastomosis . . . . . . . . . . . . . . . . . . . .
4.2. Anastomoses of deep cerebral veins—transcerebral vein . . . . . . .
4.3. Anastomoses of intra- and extracranial veins . . . . . . . . . . . . .
4.4. Anastomoses of the posterior fossa . . . . . . . . . . . . . . . . . .
5. Elementary fluid dynamics as related to cerebral venous system . . . . . .
6. Rheologic factors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7. Physiological characteristics of the cerebral venous system . . . . . . . . .
7.1. Physiological factors influencing the cerebral venous drainage. . . .
7.2. Physiological parameters influencing the venous pressure . . . . . .
8. Changes of venous pressure . . . . . . . . . . . . . . . . . . . . . . . . .
9. Cerebral venous blood flow . . . . . . . . . . . . . . . . . . . . . . . . .
9.1. Biological background . . . . . . . . . . . . . . . . . . . . . . . .
9.2. Venous outflow as source of slow oscillation. . . . . . . . . . . . .
9.3. low ICP. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
9.4. CBV and CBF relationship . . . . . . . . . . . . . . . . . . . . . .
9.5. Cerebral venous oxygenation . . . . . . . . . . . . . . . . . . . . .
10. Correlation between superior sagittal sinus flow velocity and cerebral blood
11. Effect of age on cerebral venous circulation . . . . . . . . . . . . . . . . .
12. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
The cerebral vasculature plays a crucial role in
maintaining adequate brain perfusion to meet the
metabolic needs for normal cerebral function. In the
current literature, less space is devoted to physiological
studies of the cerebral venous system (CVS) than to that
of the cerebral arterial system until present times.
Therefore, a substantial gap still exists between the
results obtained at well-defined but singular time-points
in animal experiments, on one hand, and the findings
collected incidentally in patients at various time-points
after a CVS event, on the other hand [2,3,44,102]. In
addition, cerebral blood vessels have some structural
characteristics that are very different from those of blood
vessels in other parts of the human body [44,85]. The
lack of parallelism between arterial and venous circulations or the multiplicity of individual and hemispheric
variations in CVS organization explain why their
systemization remains difficult [97]. Anatomical descriptions—mainly based on embryological data—make a
clear, but distinct difference between superficial and
deep veins [68]. State-of-the-art imaging modalities have
failed to clearly visualize this topographical difference
until recently. However, technical advances in state-ofthe-art imaging methods such as magnetic resonance
(MR) imaging, computed tomography (CT) or positron
emission tomography (PET) facilitated CVS examination,
leading to an improved knowledge especially of physiology and biophysics of normal cerebral (venous)
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
. . .
flow
. . .
. . .
. . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
248
248
248
248
248
249
249
250
250
251
252
253
253
253
254
254
255
255
255
256
257
257
257
258
hemodynamics [97,96]. These physiological examinations
are important, so that transient pathophysiological
changes can be followed until the final state of damage
or recovery after pathological CVS events and can be
compared to normal function in different animal models
[95]. These different circumstances let to an increased
clinical interest to physiology and biophysics of CVS,
even so only few experimental data are available. For
this reason, we have summarized the current knowledge
of physiology and biophysics of CVS and discuss it in
the light of its clinical relevance.
2. Anatomy of the venous system of the brain
The CVS is mainly composed of dural sinuses and
cerebral veins [39,68,72]. The venous outflow from
cerebral hemispheres consists mainly of two different
vascular systems [1]: (i) the superficial (cortical) system
reaches dural sinuses by cortical veins and drains blood
mainly from cortex and subcortical white matter [7,68];
(ii) the deep (medullary and subependymal) system is
composed by subependymal veins, internal cerebral
veins, basal vein and great cerebral vein of Galen and
their tributaries, and drains the deep white and gray
matter surrounding the lateral and third ventricles or the
basal cistern [68,77]. A few superficial medullary veins
also contain blood from cortical regions [68]. However,
superficial cortical veins drain centrifugally and deep
veins course centripetally.
B. Schaller / Brain Research Reviews 46 (2004) 243–260
2.1. Superficial cortical veins and their intracranial draining routes
Superficial cortical veins are usually quite small in
diameter and highly variable in topography [1,7,68], so that
venous vascular territories demonstrate substantial differences in their extension (see Fig. 1). The superficial middle
cerebral vein runs along the sylvian cistern and drains the
anterior temporal lobe, parasylvian cortex and anterior–
inferior frontal lobes [88]. It subsequently empties into
cavernous sinus, sphenoparietal sinus or pterygoid plexus
[88]. It is formed by anastomosis of temporo-sylvian veins;
these veins are connected with midline bridging veins on
one side and juxta-basal temporal veins on the other [88]
and enter predominantly the cavernous sinus, either directly
or through the sphenoparietal sinus [88]. Many anatomical
variations are possible: (i) in size: when very thin or even
absent, neighboring veins become of greatest importance;
Fig. 1. Schematic drawing. (A) Cerebral venous system. (B) Cerebral
venous anastomosis. Legend: Cs, confluens sinuum; Ips, inferior petrosal
sinus; Iss, inferior sagital sinus; Sc, cavernous sinus; Os, occipital sinus; Ss,
sigmoid sinus; Sss, superior sagittal sinus; Ts, transverse sinus; Vai, V.
anastomotica inferior (Labbe); Vas, V. anastomotica superior (Troland); Vb,
V. basalis (Rosenthal); Vcm, V. cerebri magna (Galen); Vcms, V. cerebri
media superficialis; Vji, V. jugularis interna.
245
(ii) in termination: draining towards the pterygoid plexus or
the superior petrosal sinus [51,88]. The superficial sylvian
vein is dominant in 7.7–15% of the cases [4].
The superior sagittal sinus (SSS) starts at the foramen
coecum, just anterior to the crista galli [69]. It courses along
the gentle curvature of the inner table of the skull, within the
leaves of the dura mater, to reach the confluence of sinuses:
the torcular Herophili [6]. Along the way, the sinus receives
venous tributaries of the superficial venous system (i.e.
superficial cortical veins). Its vascular caliber increased
form anterior to posterior, but irregularly because of venous
lakes contained within the two layers of the dura mater
adjacent to the sinus and because of the penetration of
arachnoid villi inside its lumen [6]. The SSS is circulating in
a more or less laminal way, accentuated by the existence of
longitudinal septa, especially in midthird portion. The
lateral sinuses have an average diameter of 8–10 mm, but
with frequent difference in size between the two sides [88].
Lateral sinuses drain the SSS, equally on both sides in only
20% of cases and asymmetrically in more than 50%,
depending upon configuration of torcular Herophili [104].
In extreme, one lateral sinus may drain SSS in totality (most
often on right side) and the other one the straight sinus; this
accounts for 20% of the cases [104]. The transverse sinus
can be atretic or even totally absent on one side (17% of
cases) [104] so that the remaining sigmoid sinus drains the
inferior cerebral veins (i.e. the Labbé system). The sigmoid
sinus drains the posterior fossa [88] receiving the superior
and inferior petrosal sinuses and also (in constant) veins
coming from the lateral aspect of pons and medulla
oblongata [104]. Sigmoid sinus has frequent anastomosis
with cutaneous venous network through mastoid emissary
vein [104]. When the sigmoid segment of the lateral sinus is
atretic, the transverse sinus with its affluent drains toward
the opposite side [104]. The inferior sagittal sinus (ISS)
follows a similar curve within the free margin of the falx
cerebri [111]. Often, its anterior portion is deficient and the
sinus appears more linear than curvilinear. In contrast to its
superior counterpart, the ISS empties into straight sinus, at
or near its communicating with the vein of Galen [111]. The
straight sinus, therefore, drains the deep venous system
through the vein of Galen as well as much of superficial
venous system indirectly through the ISS and basal vein
[104]. As are all other sinuses, the straight sinus is situated
within dural leaves, in this case, of tentorium cerebelli and
falx cerebri [111]. Posteriorly, straight sinus empties into
torcular [111].
Another complex network of dural sinuses collects
blood along the brain’s ventral surface [6] including the
cavernous, superior and inferior petrosal, and sphenoparietal sinuses. Cavernous sinus is a trabeculated dural
venous packet along parasellar sphenoid bone (sphenoid
sinus) [20]. The sinus extends from superior orbital fissure
to petrous apex. Its venous inflow includes orbital venous
drainage (superior and middle ophthalmid veins), anterior
middle cranial fossa drainage (superior and inferior middle
246
B. Schaller / Brain Research Reviews 46 (2004) 243–260
cerebral veins) and sphenoorbital sinus. From cavernous
sinus, blood drains posterolaterally along superior petrosal
sinus to transverse sinus and inferior-laterally along
inferior petrosal sinus into jugular vein [104]. Deep sinuses
also interconnect by way of the basilar venous plexus
along the dorsal clivus and the intercavernous sinus among
the pituitary infundibulum. Occasionally, a prominent
venous plexus connects the cavernous sinuses along the
floor of the sella turcica.
2.2. Anastomotic veins
The vein of Trolard represents the largest anastomotic
cortical vein [1] and courses cephalad from the sylvian
fissure toward SSS [76]. Convexity veins often unite just
lateral to the midline, forming a common trunk, before
entering SSS [76]. Cortical veins typically enter SSS at an
angle perpendicular to the sinus and in its postcentral
region, but may, however, penetrate its central or
precentral portion [76]. This is particularly true in the
frontal region: The angle becomes increasingly more acute
towards posteriorly, however, especially in the occipital
region [76]. Often, cortical veins draining occipital lobes
proceed anteriorly before entering the sagittal sinus at an
acute angle, against the direction of blood flow in SSS
[76]. The vein of Trolard is predominantly in the minor
hemisphere (46–52% in the right and 18–24% in the left)
[4].
Inferior (juxta-basal) veins are cortical bridging veins
that channel into basal sinuses (or into the deep venous
system) [106]. The vein of Labbé, along with temporal
occipital veins, drains lateral temporo-occipital part of
cortex and empties into the transverse sinus [106]. The
vein of Labbé occasionally drains portions of inferiolateral
frontal lobes and in this case can be seen coursing across
sylvian fissure [61]. Typically, the vein of Labbé course
from sylvian fissure posteriolaterally toward anterior
portion of transverse sinus and creates an anastomosis
between superficial sylvian vein and the transverse sinus
before its junction to the sigmoid sinus. Numerous
variations exist, besides this classical topography. The
anterior inferiolateral vein usually demonstrates a course
that runs posterior and inferior toward the so-called
btransverse venous pointQ [106]. It occasionally reaches
the lateral and inferior temporal lobe margin and takes a
more medial course to run along the tentorial surface
towards the btransverse venous pointQ [106]. In about 20–
30% of the cases, this anterior inferiolateral vein can be
found to be the prominent draining vein of the posterior
temporal lobe region with an adjacent vein, which is located
in the expected anatomic site of the vein of Labbé, and that
plays a more minor role [106].
The veins of Trolard, Labbé and Sylvius are often
reciprocal constructed: when one is large, the others are
typically small, but is often not symmetric between the both
hemispheres [1].
2.3. Deep (medullary and subependymal vein) and their
draining routes
The subcortical and deep white matter are drained by
deep medullary veins [1] that originate 10–20 mm below the
cortex and course centrally to the subependymal veins that
surround the ventricles [33,49]. The subependymal veins
drain from the deeper subcortical structures, such as internal
and external capsule, the basal ganglia and the dorsal part of
the diencephalon, to the vein of Galen, which curves around
the posterior surface of the splenium of the corpus callosum
before terminating at the confluence of sinuses [49]. Except
from the anatomical variations of the basal veins, the system
of the inner cerebral veins remains relatively constant
compared to the superficial cortical venous system
[51,88]. Medullar veins can be subdivided into two different
subgroups: The superficial medullar veins drain 1–2 cm of
white matter and course through the gray matter [76]. They
are connected to the superficial cerebral veins. The deep
medullar veins begin within the white matter deeper than
superficial medullar veins and course toward lateral
ventricles, emptying into the subependymal veins of the
walls of the lateral ventricle [33]. A third group of medullar
veins (btranscerebral veinsQ) completely transverses the
hemisphere to reach subependymal veins [39,50]. All these
white matter veins run perpendicular to the long axis of the
lateral ventricle, creating a fem-shaped appearance [59].
Three subependymal veins are commonly seen on the
venous phase of a cerebral arteriogram [18,67]: (i)
thalamostriate vein, (ii) septal vein and (iii) internal cerebral
vein. The thalamostriate veins join the septal veins from the
internal cerebral veins [99,106]. The point at which the
anterior vein of the septum pellucidum joins the superior
thalamostriate vein is called the venous angle and is usually
located at the interventricular foramen [99]. The internal
cerebral veins are paired and run within the velum
interpositum posteriorly, above the roof of the third ventricle
[99]. These veins are joined by basal veins of Rosenthal
forming the vein of Galen [99]. The basal vein of Rosenthal
represents the confluence of veins draining basal and medial
parts of frontal lobe, temporal lobe, basal ganglia and insula
[99]. Occasionally, basal vein of Rosenthal can drain
aberrantly into a tentorial sinus or superior petrosal sinus
[99].
2.4. Extracranial draining pathways
Venous outflow from the SSS and deep cerebral veins is
usually directed via the confluens sinum toward the sigmoid
sinuses and jugular veins. Interconnections with other basal
venous structures permit additional drainage toward vertebral venous system [75]. This freely communicating,
valveless system is present throughout the entire spinal
column and may be divided into an internal intraspinal part,
the epidural veins and an extraspinal paravertebral part.
With increased intraabdominal and intrathoracic pressure,
B. Schaller / Brain Research Reviews 46 (2004) 243–260
blood is shunted through vertebral, prevertebral and epidural
venous networks. At the craniocervical level, anterior
sources of intraspinal system arise from basal plexus and
inferior petrosal sinus [22]. A posterior communicating
venous drainage exists with occipital sinus, which may be
relevant in cases of lateral sinus hypoplasia [92]. The
extraspinal system receives blood anteriorly from cavernous
sinus via pterygoid plexus [92]. A dorsal part is connected
to suboccipital venous plexus, which receives blood through
mastoid and condylar emissaries [15]. Although the jugular
veins were previously thought to be the predominant
draining pathway [23], anatomical recent study-findings
have demonstrated that this role is confined to the supine
position; redirection of venous flow to the vertebral veins
occurs in upright-position [92]. Rather than being a minor
plexus that surrounds vertebral artery, vertebral veins in the
cervical region represent large collecting vessels of the
vertebral venous system; they are readily and receive their
blood from condylar veins, from emissaries vein and
through segmental connections [92].
3. Venous drainage of the posterior fossa
Venous drainage of the posterior fossa is as complex as
that of the supratentorial compartment. In the posterior
fossa, venous blood exits through galenic and petrosal systems and, to a lesser extent, tentorial veins and transverse
sinuses [92]. Veins of the upper brainstem, dorsal cerebellum and vermis may drain through their various tributaries
into the vein of Galen [22]. Included in this subgroup may
be the precentral vein, a midline structured vessel that drains
ventral and superior vermis [15] and initially parallels the
anterior medullary velum only to turn posteriorly toward the
quadrigeminal cistern at the colliculocentral point [92]. In
the superior cerebellar cistern, this vein merges with the
superior vermian veins as well as smaller midline and lateral
tributaries, to reach vein of Galen [15]. The anterior pontomesencephalic vein, which lies ventral to brainstem, may
drain rostrally to basal vein of Rosenthal (and, therefore, the
vein of Galen) or petrosal venous system [15]. Posterior
fossa veins are divided into four groups: (i) superficial, (ii)
deep, (iii) brainstem and (iv) bridging veins. However, the
veins of the posterior fossa terminate as bridging veins [1].
3.1. Brainstem
Generally, brainstem veins are named on the basis of
whether they drain midbrain, pons or medulla and course
transversely or horizontally [1,40]. The superior collector
corresponds to the superior petrosal vein(s)—so-called
Dandy vein(s)—which flow(s) to the superior petrosal sinus
[1]. Its affluents consist of the vein of the lateral recess of the
fourth ventricle, the lateral mesencephalic vein and the
pontine vein. Superior petrosal veins also receive vein(s) of
the superior aspect of cerebellar hemisphere. The inferior
247
collector is much less important and corresponds to the
inferior petrosal vein and its main affluents: the vein of the
horizontal fissure, which drains the anterior part of cerebellar
hemisphere [73]. The inferior petrosal veins often anastomoses with the vein of the lateral recess of the fourth
ventricle. Venous drainage is toward the inferior petrosal
sinus.
3.2. Cerebellar hemisphere
The superficial veins drain cortical surface of cerebellum
and are divided on the basis of whether they drain tentorial,
petrosal or suboccipital surface and whether they drain
hemisphere or vermis [90]: (i) veins of the posterior territory
which drains toward torcular and median portion of transverse sinus directly or through medial intratentorial (small)
sinuses; (ii) vein of superior territory, toward superior
petrosal sinus; (iii) vein of anterior territory, toward inferior
petrosal sinus [90]; (iv) veins of the superior aspect which
drain to vein of Galen; (v) veins of inferior vermis, to torcular
and/or medial portion of transverse sinuses. Constant
precentral vermian vein runs anteriorly to culmen, up to
the vein of Galen.
3.3. Bridging veins and posterior fossa venous anastomosis
The terminal ends of veins draining brainstem and
cerebellum form bridging veins that cross subarachnoid and
subdural spaces to reach venous sinuses in the dura [105].
These bridging veins collect into three subgroups [105]: (i) a
superior or galenic group that drains into the vein of Galen,
(ii) an anterior or petrosal group that drains into petrosal
sinuses and (iii) a posterior or tentorial group that drains into
sinuses converging on the torcula. In the posterior fossa,
venous anastomosis can be found longitudinally with upper
cervical and foramen magnum veins (inferiorly) and the
system of Galen (superiorly), as well as transversally between
both sides across the ventral aspect of medulla, pons and
mesencephalon [22]. Petrosal venous system drains the
inferior, anterolateral portion of posterior fossa [22]. Specifically, anterior medullary vein (along the ventral medulla),
anterior pontomesencephalic venous complex (including the
transverse pontine veins), longitudinal lateral pontomesencephalic veins, anterolateral superior and inferior cerebellar
hemispheric veins and the vein of the lateral recess of fourth
ventricle, all reach the petrosal venous complex [105].
Finally, tentorium receives direct venous drainage from
medial superior and inferior cerebellar hemispheres, and
inferior vermian veins drains around vermis and ascends to
straight sinus [105]. Posterior inferior cerebellar hemispheres
may drain directly into the transverse sinus [105].
3.4. Major dural sinuses of the posterior fossa
Perioccipital sinus constitutes a venous intradural ring
around foramen magnum [52]. Superior petrosal sinus
248
B. Schaller / Brain Research Reviews 46 (2004) 243–260
courses along petrous ridges from the cavernous sinus to
the transverse sinus [52]. The inferior petrosal sinus
courses along the petro-clival suture; it drains retroclival
sinus and cavernous sinus toward jugular foramen [52].
Retroclival sinus anastomoses both sinuses posteriorly to
clivus, and dorsum sellae, it is connected with numerous
and often voluminous extradural venous plexuses [52].
Small venous lakes can be more or less developed
inside the tentorium. Part of these intratentorial sinuses
have a median topography along the straight sinus; they
drain cerebellar vemian afferent veins [52] draining
cerebellar hemispheric veins and also occipital temporal
veins (with sometimes the Labbe’ vein) toward transverse sinus.
4. Collateral venous pathways
In addition to major anastomotic vascular venous
channels that connect them both to meningeal veins and
to intra- and extracranial veins, superficial cerebral veins
widely anastomized with each other and build a fine
network of venous vessels. This cortical drainage has a
surprisingly regular organization [66]. Within grey matter,
capillaries of 5 cm diameter (just wide enough to admit red
cells) and mean length 200 Am drain into venules of 10–20
Am diameter. These combine, at angles close to 908, to form
larger venules. When a diameter of about 50–100 cm is
reached, the venule is termed a principal intracortical vein
and typically leads directly to the cortical surface, at right
angles to it. These veins often extend the full depth (about 3
mm) of the cortex, increasing in diameters as they approach
the surface, swelled by incoming venules. Once the
principal intracortical vein, spaced about 300–500 cm apart,
reach the surface they combine to form pial veins in a twodimensional drainage network on cortical surface [83]. Like
intracortical venules, pial veins join nearly at right angles
(Table 1).
Table 1
Changes of cerebrovascular and cerebrometabolic parameters
Primary reduction
CMRO2
CPP (autoregulation intact)
CPP (autoregulation defective)
Blood viscosity
(autoregulation intact)
Blood viscosity
(autoregulation defective)
PaCO2
Conductive vessel diameter
(vasospasm above
ischemic threshold)
CBF
CBV(ICP)
=
+
=
+
AVDO2
=
=
+
=
=
+
+
+
CBF, cerebral blood flow; CBV, cerebral blood volume; ICP, intracranial
pressure; AVDO2, arteriovenous O2 difference; CMRO2, cerebral metabolic
rate of oxygen; CPP, cerebral perfusion pressure; PaCO2, arterial CO2
tension.
4.1. Anastomoses of superficial cerebral veins
4.1.1. Classical description
On the lateral surface of each cerebral hemisphere two
main anastomotic vascular-venous channels have been
described [1]: (i) Labbe’s vein and (ii) Trolard’s vein. Both
venous to venous anastomoses build a vascular connection
between SSS and basal transverse sinus. Trolard’s vein
(vena anastomotica superior) links veins of the lateral sulcus
to SSS. It runs along the surface of frontal and parietal lobe,
at the level with the central region. According to Oka et al.
[75], it usually corresponds to a postcentral vein. However,
it is thought to be more frequent on non-dominant hemisphere [25]. Labbe’s vein (vena anastomotica inferior)
interconnects the veins of lateral sulcus and the transverse
sinus. Oka et al. [75] demonstrated that this vein usually
corresponds to a middle temporal vein and, less frequently,
to a posterior temporal vein. It is thought to be more
frequent on dominant hemisphere [25]. This is in accordance with an anatomical study of 175 brains, in which
Delmas et al. [24] could show that Labbe’s vein was more
frequent located on the left side (42%) than on the right side
(21%), whereas Trolard’s vein was more frequently found
on the right than on the left side.
4.1.2. The superficial sylvian vein
In the embryo, the middle cerebral vein system is
ramified [24]. Their tributary veins are arranged around
middle cerebral veins at three branches [24]. As the opercula
begins to develop, the veins of the hemispheric convexity
get closer to each other [10] and eventually fuse to form
superficial sylvian vein. This usually single vein runs along
the whole length of sylvian fissure along lateral sulcus and
receives fronto-sylvian, parieto-sylvian and temporo-sylvian
veins. At the anterior end of the lateral sulcus, the superficial
slyvian vein crosses subarachnoidal spaces to join cavernous sinus either directly or through spheno-parietal sinus
[107]. Other modes of ending, described as para-cavernous
sinus, are possible [2,107]; they run towards pterygoidal
veins (spheno-basal sinus) or superior petrosal sinus
(sphenopetrosal sinus). Among all the veins of the lateral
brain surface, superficial slyvian vein is the most variable in
both size and extend of venous anastomosis, which accounts
for the great facilities of venous drainage of lateral sulcus
and cavernous sinus.
4.1.3. Regional anastomosis
Classical venous vascular arrangement does not account,
by itself, for importance of fine and wide-spread anastomoses established by veins of the lateral surface of the
hemisphere [1,35]. For this reason, Petit-Dutaillis et al. [82]
described two types of cortical veins according to their
mode of ending: (i) bipolar and (ii) unipolar. Bipolar veins
have a central end in the superficial sylvian vein and a
peripheral end in a venous sinus [82]. Unipolar veins only
have a peripheral end. These types of ending veins are
B. Schaller / Brain Research Reviews 46 (2004) 243–260
already found during fetal life [82]. In the 3-month-old
fetus, there can be already found such a dual cortical venous
system: the first one is central and joins the vein of lateral
sulcus, whereas the second one is peripheral and joins dural
sinuses [82]. In older fetus, both systems are anastomized
[82]. In adults, the two-end arrangement is found only in
certain topographical brain regions [82]. In other brain
areas, veins revert to their bprimitiveQ character. Depending
on frequency of anastomoses with the sylvian system, PetitDutaillis et al. [82] have defined three venous brain areas,
which lean against the above described unipolar–bipolar
venous system: (i) an bunipolar circulation areaQ, where the
regional veins are found to be little or not anastomized with
the sylvian veins, this is the case in the occipital and parietal
regions; (ii) a bbipolar circulation areaQ, where anastomoses
are constantly found as is the case in the rolandic and
sylvian regions; and (iii) a blow circulation areaQ, where the
venous networks vary considerable in number, caliber and
anastomoses, as in the frontal and anterior temporal regions.
4.2. Anastomoses of deep cerebral veins—transcerebral
vein
Multiple venous anastomoses interconnecting deep cervical veins and other venous systems [107] are summarized
in Table 2 borrowed from Mikhailov and Kagan [70].
Among these anastomoses, transcerebral veins have been
described by Duret [27] and have given rise to important
anatomical studies [35,70]. Their role has been considered
in different studies [11,38,98] in that have been described
two anastomotic systems that open after ligation of medial
cerebral veins: (i) veins which cross hemispheric white
Table 2
Anastomoses of deep cerebral veins (after Mikhailov and Kagan [70])
I. Deep cerebral veins—superficial cerebral veins
A. Extracerebral anastomoses
1. Medial Vs of hemisphere (Vs of corpus callosum—SSS)
2. Inferior frontal Vs (RBV-SSS)
3. Inferior temporal Vs (RBV-LS)
4. V. of lateral sulcus (DSV-SSV)
5. Infero-medial occipital Vs (Vs of corpus callosum—SSS+LS)
B. Transcerebral anastomoses
II. Deep cerebral anastomoses
1. Ventral Vs of pons
2. Superior cererbral Vs
III. Deep cerebral veins—dura mater sinuses
1. Spheno-parietal sinus
2. Cavernous sinus
3. Superior petrosal sinus
IV. Deep cerebral veins with each other
A. Extracerebral anastomoses
1. Plexus of lateral ventricle
2. Rosenthal’s basal Vs
V. Intracerebral anastomoses
1. Vs of corpus callosum
2. Lenticular Vs
DSV: Deep sylvian vein, LS: lateral sinus, RBV: Rosenthal’s basal vein,
SSV: superficial sylvian vein, SSS: superior sagittal sinus, Vs: veins.
249
matter and connect caudate longitudinal vein to cortical
veins; (ii) veins which cross basal ganglia and connect
subependymal veins of lateral ventricle to Rosenthal’s basal
vein; they are called external and internal lenticular veins.
Similar to cisternal basal arteries, inner cerebral veins
form a venous circuit. The basal vein of Rosenthal is the
most important common final passage and represent the
most prominent basal venous vessel, which can be separated
into three segments: (i) anterior, (ii) middle and (iii)
posterior [106]. Hypoplasia seldom occurs. Variations are
restricted to anterior and posterior segments, whereas the
middle segment of basal vein of Rosenthal is almost always
standard in location and size, with a diameter of 2–3 mm.
The deep middle cerebral vein is the second most important
vein. It passes through the anterior perforated substance,
where it joins anterior cerebral vein to form the anterior
segment of the basal vein of Rosenthal [106].
On the basis of a microradiographic study performed
after opafication, Hassler [39] considers that there is a brain
area of habitual drainage of deep venous system complementing to some extent the superficial system. Moreover,
this author has shown that injecting a radio-opaque
substance into great cerebral vein of Galen promptly
opacifies SSS and transverse sinuses [22] confirming the
existence of transcerebral veins, the number of which is
estimated at 2–4000 in each hemisphere [22]. Their usual
caliber ranges from 0.25 to 0.35 mm, but wider veins have
been rarely described [22]. They are sometimes located on
the same sites as the white matter fibers [39,70] and seem to
be influenced by locations of wide superficial veins.
Goetzen [35] studied 100 injected hemispheres and
concluded that deep veins of the brain tissue participate in
the drainage of the cerebral cortex and, conversely, that the
lateral superficial veins can drain lateral ventricle wall. For
this reason, there are bvenous channelsQ in hemispheric
white matter, corresponding to centro-peripheral anastomoses [35]. These elements are characteristic of transcerebral
anastomoses, as they demonstrate larger anastomotic network of cerebral veins compared to arteries [35]. Goetzen
[35] observed centro-peripheral veins in 62% as against 3%
for arterial centro-peripheral anastomoses.
4.3. Anastomoses of intra- and extracranial veins
Batson [9] described vessel-connections between intraand extracranial veins at cranial base as a single large
venous plexus, and this appears to be the most practical
view: (i) The suboccipital venous plexus represents the
cranial beginning of the posterior external vertebral plexus
between the dorsal muscles; it is connected to the sigmoid
sinuses via mastoid and condylar emissaries [80]. (ii) The
posterior internal vertebral plexus receives blood from
occipital sinus and thus from confluens sinuum (torcular)
[80]. The torcular is often plexiform and asymmetrical, and
when one lateral sinus is narrow or absent, occipital sinus is
larger than usual; and in neonates the occipital sinus is very
250
B. Schaller / Brain Research Reviews 46 (2004) 243–260
large [9,80]. (iii) The anterior internal vertebral plexus is a
continuation of basal plexus, which lies on clivus and
connects inferior petrosal sinuses and both cavernous
sinuses [80]. (iv) The anterior external vertebral plexus is
a continuation of large pterygoid plexus, which receive
blood from cavernous sinuses and, via middle meningeal
veins, from superior longitudinal sinus [9,80]. The pharyngeal venous plexuses may play a role in the anterior
region that should not be ignored.
Besides these affluent pathways, the outflow channels of
vertebral plexuses can also be summarized [9]: (i) In the
thoracolumbar area, outflow from vertebral plexuses takes
place via the lumbo-azygos system, which also forms a
collateral channel between inferior and superior vena cava.
Valves in the azygos system are superior rudimentary and
nonfunctioning. Obstruction of the superior vena cava
cranially from the azygos vein, and is tolerated well, but
obstruction involving connection of termination of azygos
vein to heart leaves collateral flow only toward inferior vena
cava, which results in insufficient cranial venous outflow
[47]. (ii) In vertebral plexuses of cervical area, longitudinal
collecting channels besides internal jugular vein on either
side are deep cervical vein posteriorly between muscles,
vertebral vein (through the transverse process of the cervical
vertebrae) and, subcutaneously, external jugular vein [9].
These veins join subclavian and internal jugular veins in
forming brachiocephalic vein [9].
4.4. Anastomoses of the posterior fossa
Deep venous system is not primarily vulnerable at the
great vein of Galen, because channels towards basal vein
can afford sufficient collateral flow [22]. The most
vulnerable area is around the junction of internal cerebral
and superior choroidal veins, because at this point principal
flow and collateral flow can even be hindered at a distance,
when obstruction of superior vena cava includes collateral
outflow through azygos vein [80].
Anatomy of collateral venous pathways indicates location of vascular areas, where principal and collateral flow
can be impaired simultaneously [80]. The most obvious
example is the posterior cranial fossa, where flow both
through compressible sigmoid sinus and towards vertebral
plexuses can be impeded by a space-occupying lesion or a
hypoplasia of chondrocranium [9] causing increased blood
flow through cavernous sinus that has become connected to
cerebral veins [52]. In most infants and some adults this is
not case, so that vulnerability is increased. On the other
hand, other routes from venous outflow from superficial
veins may exist in infant, namely via occipital sinus, which
is still large, and through open cranial sutures via scalp
veins, although open cranial sutures via scalp veins, and
these will always be insufficient [15].
Cerebrospinal fluid (CSF) pressure depends on a hydrostatic-osmotic pressure equilibrium with choroidal capillaries and veins [101]. Cranial enlargement will occur when
cerebrospinal fluid pressure greatly exceeds atmospheric
pressure, while cranial sutures are still open [101]. Cerebral
surface retains its relationship to enlarging cranium and size
of lateral ventricles increases [101]. But insufficient deep
venous flow also causes periventricular atrophy, manifest as
ventricular dilatation, when cranial vault is not enlarged
[101].
5. Elementary fluid dynamics as related to cerebral
venous system
Cerebral veins were collapsible because of their specific
cytoarchitectionial construction. Collapsible blood vessels
or tubes are characterized by marked changes in their crosssectional configuration when transmural pressure is slightly
positive or negative. Transmural pressure can drop either by
lowering intraluminal pressure or by increasing external
pressure or both. Internal pressure can change by variables
in Bernoulli-Poiseuille equation (e.g. upstream or downstream resistance to flow, flow rate, acceleration or
deceleration, negative gravitational pressure). It should be
emphasized that changes in external forces, meaning
increased compartment pressures, can affect blood flow
simply by altering the bgeometryQ of collapsible tubes,
which affects variables in Bernoulli-Poisuille equation, such
as viscous resistance, acceleration–deceleration [108].
When transmural pressure is slightly positive, the vessel is
circular and distends with increasing transmural pressure.
However, slightly negativity of transmural pressure causes
very marked collapse of the vessel and a reduction in its
cross-sectional area or possibly complete closure [108]
implying a great increase in viscous resistance to flow. The
mathematical equations for resistance to flow of collapsible
vessels that are flat, biconcave or dumbbell-shaped in crosssection have not been worked out to knowledge [108].
Such studies are pertinent to our discussion since blood
flow in collapsible vessels, like veins, has flow characteristics somewhat similar to that of collapsible tubes [108].
The earliest study was carried out by Holt in 1941 using
latex penrose drain tube placed horizontally in an enclosed
jacket with flow derived from a Mariotte bottle which keeps
energy head constant as liquid flows through tube system
[48]. Energy gradient could be altered by elevating or
lowering the temperature of a thick-walled outflow rubber
tube. The pressure immediately upstream and downstream
of the jacket and the jacket pressure were recorded with
water manometers. Such studies were extended by Permutt
et al. [81] in models in which external pressure compressing
collapsible tube (called Starling resistor) was either below or
above downstream pressure. Analysis of these experimental
models led to the following conclusions: (i) when downstream pressure adjacent to collapsible tube is greater than
external pressure on the tube, flow is proportional to the
difference between upstream and downstream pressure and
changes in external pressure on the collapsible tube have no
B. Schaller / Brain Research Reviews 46 (2004) 243–260
influence on flow; (ii) when external pressure on collapsible
tube is greater than downstream pressure, flow is proportional to the difference between upstream pressure and
external pressure on the tube and changes in downstream
pressure have no influence on flow [108]. The latter
relationship was considered to be similar to a bwaterfallQ.
These concepts were applied to pulmonary circulation
shown in constant, while pulmonary venous pressure is
reduced to and below the alveolar pressure. If down-stream
pressure is kept constant and up-stream pressure is
increased, the pressure-flow curve is quite different and
does not demonstrate flat portion, which is the basis of the
bwaterfallQ concept [46,81].
Subsequent experimental studies on collapsible tubes
(penrose drain) were carried out by Katz et al. [57] using
measurements of pressured gradients and flow together with
photographs of tube contour at different perfusion pressures.
Pressure gradients along the length of the tube were altered
by varying constriction of orifices upstream or downstream
to the tube [57]. This experimental approach is significantly
different from the model of Permutt et al. [81] in which
upstream pressure is held constant and downstream pressure
is reduced, thereby increasing in pressure gradient. According to Katz et al. [57] these results on flow and on
configuration of distensible tube vary depending on which
pressure is primarily altered: upstream or downstream.
When the penrose drain is fully open, flow increases with
increase in pressure gradient between up-stream and downstream pressure. However, once the tube begins to collapse,
flow diminishes progressively as perfusion pressure
increases (called bnegative slopeQ by these authors) until a
maximum pressure gradient is reached, beyond which
collapse is so severe that all flow stops. In some experiments, there was flutter in the partially collapsed tube in the
region of negative slope [57].
Further studies on pressure-flow-through penrose tubing
(Starling resistor) were conducted by Lyon et al. using
different viscosities of liquids to vary Reynolds’number
[65,64] and demonstrated that the waterfall model proved
adequate to describe flow in the Starling resistor only at very
low Reynold’s number (Reynold’s numberb1) [65]. Since
such low Reynold’s number occur only in microvessels,
they concluded that it is inappropriate to apply the waterfall
model to flow through large collapsible veins [65,64]. In our
opinion, data on penrose drain tubes cannot be applied
without some reservation to vascular beds in vivo.
6. Rheologic factors
Mean blood velocity amount accounts ~0.05 cm/s in
microvessels of cerebral venous drainage [100] and does not
exceed 10 cm/s of the vein’s vessel of capacity [100]. At the
present time, exact blood velocity in veins (variation
between 30 and 50 cm/s in internal jugular vein) is
unknown, so that it can be only said that blood velocity
251
may be rapid in the sinus [100]. Physiology of venous
pressure is better understood. It varies in capacity of venous
vessels dependent on the patient’s position, revealing the
important role of position in CVS. In cerebral sinus, venous
pressure may be about +1 mm Hg in the lying position and
3 mm Hg in the up-right position [42]. It is suggested that,
in up-right position, there may be assumed a venous flow of
600–700 ml/min corresponding to a displacement of
approximately 80 ml [42].
In the main CVS (e.g. straight sinus, vein of Galen and
basilar veins) the markedly cyclic changes are synchronous
with arterial pulsations. The position of systolic arterial
velocity pulse at the ascending part of venous waveform
suggest that arterial systolic volume pulse might compress
venous channels and thus increase velocity. This argument
is, however, only valid, when venous volume flow is
assumed to remain constant. Several factors might lead to a
pulsatile venous pattern [19]: (i) increased systolic volume
pulse due to increased cerebral blood flow (CBF); (ii) a
large difference in systolic–diastolic pressure, particularly
with impaired autoregulation; (iii) increased stiffness of
brain parenchyma due to edema or increased intracranial
pressure (ICP); (iv) modulation of flow velocity by changes
in intrathoracic pressure.
With the exception of increased partial pressure of carbon
dioxide ( pCO2), two factors were of major importance for
venous flow velocity [53]: (i) diastolic arterial blood
pressure and (ii) peak ventilation pressure. Stepwise
discriminating analysis indicates that resistance index of
pericallosal artery is closely related to diastolic blood
pressure, whereas venous flow velocities and pulsatile
factors were markedly below any level of significance
[53]. A high resistance index of, for example, 1.00 or more,
any thus merely indicated low diastolic blood pressure
(below 25 mm Hg) and is of little or no additional value in
such a case [53]. An increased peak ventilation pressure is
significantly associated with a relative period of no recorded
flow velocity in the basilar veins [34,86]. The other two
factors as selected by discrimination analysis were time
average velocity in pericallosal artery and straight sinus, but
these F-values are not significant [34]. High ventilation
pressure could thus impair cerebral venous drainage
intermittently and not solely act through an increased ICP
[19], possibly explaining a slight fall of time average arterial
velocity with high ventilation pressure [19]. Transduceinduced pressure is another major factor influencing arterial
and venous flow velocity in small premature, ventilated
infants: diastolic arterial flow velocity decreases, as does
systolic to a lesser degree, whereas flow velocity in the
straight sinus rises [100], indicating that the straight sinus
might be compressible [100].
One can assume that CVS has some kind of pulsation,
which means that there can be demonstrated a hydraulic
translation that can be observed at the exit of the sinus
(named bsinus pulseQ). In view of the frequency of the
pulsation, the origin seems to be a residual arterial pressure.
252
B. Schaller / Brain Research Reviews 46 (2004) 243–260
But the respiration, which means the thoraco-abdominal
pump, lead to changes of the amplitude of these pulsations
[16]. Among dural sinuses, the vein of Galen has lower
amplitude pulsations than other dural sinuses suggesting
that amplitude of intracranial venous pulsations might
increase as flow runs from periphery toward proximal
portion [100]. Physiologically, intracranial venous pulsation
can be explained as passive pulsations transmitted from the
heart or brain. The fact that brain pulsation exist is known
and a pulsatile brain can be seen after craniotomy. Brain
pulsations associates with cardiac cycles were proved by
studying epidural pulse waves, CSF pulse waveforms and
anterior frontal pulsations. Hirai et al. [45] investigated the
origin of epidural-pressure pulse waveforms measuring
epidural-pulse and pressure waveforms of cortical artery
or vein simultaneously and found that pulsatile arterial
blood flow into the brain can generate brain pulsations and
that cortical venous pulse can be affected passively by brain
pulsations [45]. CVS can also have a passive pulsation
directly transmitted from the heart [45]. Whether cerebral
venous flow is influenced by brain pulsation or heartbeat
remains unclear, but it is reasonable to suggest that the
amplitude of venous pulsations increases from distal to
proximal portion of CVS.
The veins, which have thin walls, are easily affected by
the tissue-pressure outside of CVS. Intracranial dural
sinuses (e.g. SSS) are outside the convexity between
hemispheres; therefore, venous circulation can be subjected
to a larger effect than arterial circulation because of the
increased tissue-pressure around it [86]. However, SSS is
within the dura mater that covers the buffer zone, which
absorbs pressure transmitted to it by moderately increased
ICP. When that pressure increases, it progressively obliterates this buffer zone; thus the pressure stretches the dura
mater or sinus so that brain pulsations are not transmitted to
them. That physical explanation might account for the
flattered venous waveforms in cerebral sinus. ICP waveforms are influenced by intracranial constituents and
compliance of the container [94], so disappearance of
venous pulsations might indicate high ICP [37].
MR spectroscopy of venous signal (for detail description
of the method, see Ref. [28]) demonstrates a considerably
smaller proportion of heart rate-and respiration related
oscillation, but a considerably higher proportion of low
and very low frequencies, compared with all the other
parameters [74]. The fixed diameter of the incompressible
venous sinus may be one reason for this minor influence of
heart action; also, the capillary system and venules cause a
deceleration of the pulse wave before it reaches large
cerebral veins. Respiratory effects on venous outflow via
central venous pressure also seem to be of minor effect on
oscillations in the venous sinus [103]. The higher proportion
of low and very low frequencies may reflect a venous
autoregulatory mechanism [103]. Apart from the description
of low pulsatility, no comparable data for the venous CBF
exists in the literature.
7. Physiological characteristics of the cerebral venous
system
CVS is maintained by non-contractile veins with some
hinds of pulsative waves, which were consequently influenced among other things by pulsation of concomitant
arteries. In effect, blood arrives at the exit of the capillaries
with a certain pressure, as pressure and pulsability of
cerebral arteries are key-source of cerebrovenous flow.
Physiologically, CVS is mainly passive and influenced by
different extravascular factors. Venous reflow of the brain is
supported by an estimated pressure of 20F5 mm Hg in the
subarachnoidal veins [31] and is maintained by the residual
capillary pressure (vis a tergo), by the transmission-pressure
of the ICP (vis a latere) or by the niveau of pressure in the
venous sinus (vis a fronte) itself [31]. From this mathematical point of view, a venous reflow exist physiologically in
the case that the arterial pressure is superior to the
subarachnoidal pressure [31].
Based on principles of physics to intracranial contents, it
can be hypothesized according to the Monro-Kellie hypothesis, that going out from an intact skull, the sum of brain
volume plus CSF, plus cerebral blood volume (CBV)
always remains constant [19]. Therefore, an increase in
one of these parameters should cause a reduction in one or
both of the remaining two. As the intracranial content is
incompressible under physiological conditions, the blood
circulating in the cranium is therefore of a constant volume
at all times [19]. Arterial vasodilatation can only be
produced by a volume reduction of the intracranial veins
that, as far as it is concerned, can be achieved by lowering
the venous pressure [109]. The subsequent volume compensation by blood can be achieved by variations of the
cerebral fluid volume extra- and intracellularly [109]. For
this reason, every increase of the volume of a part of the
intracranial content would require volume compensation.
CVS is primarily affected, as it maintains a pressure that is
normally not largely different from that of CSF [98]. On the
other hand, circulating arterial blood is not reduced as
venous pressure is not as high as that of arteries [109].
Changes also take place at the spinal level. The vertebral
canal is encased by bony and fibrous components that are
though and only slightly elastic. While in the cranial cavity,
the dura mater is closely applied to the inner surface of
cranial bone; in the spinal canal, there is an epidural space
between the dura mater and the fibroosteal canal, which is
filled with fatty areolar tissue and epidural venous plexus.
The capacity of the spinal venous system is not totally
known because the numerous anastomoses, but varies
between 200 and 1000 ml [112].
The biological significance of the tendency that small
arteries pass superficial to veins more frequently than large
arteries remains yet unclear. But it is easily understood that
compression of veins by arteries is reduced, thus inducing
less stasis of venous flow at locations where veins are
crossed over by smaller arteries, as compared to locations
B. Schaller / Brain Research Reviews 46 (2004) 243–260
where veins are crossed over by larger arteries. It has been
proposed that a major route for drainage of interstitial fluid
from the cortical gray matter in the periarterial space along
the cerebral arteries and that this route plays an important
role in protecting the cortex from edema in different cerebral
diseases [110]. However, it seems more likely that the
cortex, the most superficially situated tissue of the brain, is
protected from excessive retention of interstitial fluid
primarily by unhindered venous flow from the surface of
the brain tissue to the dural venous sinuses.
7.1. Physiological factors influencing the cerebral venous
drainage
CVS is additionally influenced by the thoracic aspiration
(subathmosphere pressure). At the time of expiration, the
intrathoracal or pleural pressure is negative, approximately
5 cm H2O. The inspiration is the source of the respiratory
muscular action which can generate an intrathoracal
pressure still more negative ( 8 cm H2O). This intrapleural
pressure decrease contains the pressure changes of intrathoracal veins being constantly dilatated and favors the
venous return to the right heart [17].
The transmural venous pressure of the spinal venous
system is determinated by the CSF pressure [56]. The
intracranial and spinal liquor system communicate freely by
the foramen magnum. For this reason, the pressure gradient
between CSF and veins is the forcing power of spinal
venous blood flow [56]. Under physiological conditions,
there can be found in the horizontal position a pressure of 11
mm Hg at the level of craniocervical junction [1]. In the upright position, CSF pressure at occipital niveau is subathmospheric ( 5 cm H2O) and, at lower spinal level, it can be
reached a pressure of 40–45 cm H2O. From a physiological
point of view, one should also consider that same postural
influences affecting cerebral venous drainage might redirect
the circulation of the internal and external vertebral venous
system.
Two different ways of cerebral venous reflow related to
the posture is known in primates and in humans. In up-right
positions, venous drainage is preferentially via the spinal
venous system, while it is the anterior jugular system in the
lying position [89]. The spinal venous system represents a
main venous drainage system in humans, even in the sitting
or lying position [89].
7.2. Physiological parameters influencing the venous
pressure
Regarding the brain tissue, the cerebrospinal canal may
also represent a column of fluid outside the true blood
vessels, which could compensate automatically for the
transmural pressure variations during shifts for recumbent
to erect positions and vice versa. If so, transmural vascular
venous pressure will be independent on the height of the
organ above the heart and no venous collapse or trans-
253
capillary absorption will occur [56]. However, these
physiological explanations are unlikely as the tissue
pressure is shown to be roughly constant in, for example,
the epidural space, independent of the position of the body.
The interstitial and epidural pressure are close to the
atmospheric pressure or even slightly negative. Furthermore, the cerebrospinal space is a closed and quite rigid
cavity, and therefore the intracranial ventricular pressure
will not decrease in relation to the elevation of the head.
It is a well known fact that autoregulatory mechanisms
protect organs such as the brain from variations in CBF and
hydrostatic capillary pressure during alterations in arterial
pressure. The results of Asgeirsson et al. demonstrate that
organs positioned above the heart are protected from the
venous side, during elevation, via variations in the outflow
resistance [5]. Provided these results can be transferred to
the damaged brain with impaired autoregulation and
disrupted blood–brain barrier (BBB), head elevation will
not reduce intracranial hypertension through increase in
venous drainage as previously suggested, but ICP may
instead be reduced from the arterial side through transcapillary absorption [12]. However, a decrease in interstitial
pressure causing transcapillary filtration may occur during
head elevation due to the existence of the semi-rigid spinal
canal [5]. The upright position evokes a venous resistance at
the outlet of CVS and the size of this resistance is directly
related to the height of the elevation [12]. The resistance
starts to develop as soon as the elevation exceeds venous
pressure level. This variable outflow resistance effectively
isolates the organ from any hemodynamic influence of the
decrease in venous hydrostatic pressure, except for the small
volume changes inherent in variation in the venous outflow
resistance per se [12].
8. Changes of venous pressure
With the assumption that the entire increase in right
arterial pressure is transmitted through the jugular venous
channel, the subsequent collapse of jugular veins, when the
head is elevated, may be the main vascular resistance to
pressure transmission upward [63]. One mechanisms by
which the surrounding pressure of a vascular system can
affect CBF is based on vascular waterfall model of the
pulmonary circulation [63]. This model suggests that, if
extravascular pressure exceeds intravascular pressure within
a collapsible segment, there must be a certain point at which
the surrounding pressure will exactly be equal to the
intrasvascular pressure. Under these conditions, CBF
through vascular segment proximal to that point will be
proportional to arterial inflow pressure minus surrounding
pressure. As long as outflow pressure remains less than
surrounding pressure, outflow pressure will have no effect
on altering CBF through vascular segment. However, when
outflow pressure is equal to or higher than surrounding
pressure, it becomes the bach pressure for CBF. Similarly, it
254
B. Schaller / Brain Research Reviews 46 (2004) 243–260
has been demonstrated that cerebral vein collapses when it
is elevated above the heart because surrounding pressure is
greater than pressure inside the vein, thus creating a Starling
resistor effect [65]. In a Starling resistor, defined as an easily
collapsible vascular segment submitted to external pressure,
CBF will start when upstream pressure is large enough to
cause pressure inside the collapsed segment (intravascular
pressure) to exceed external pressure (extravascular pressure) and thus open the vessels [65]. Starling resistor
upstream pressure at which vessels collapse is often referred
to as the closing pressure [65]. With relatively constant
CBF, such as in a living subject, the upstream pressure
remains almost constant at this level, despite small changes
in downstream pressure [65]. Holt [48] demonstrated in
dogs that, when a vein was held above heart level, arterial
pressure had to be increased by several centimeters of water
before there was any rise in peripheral venous pressure.
Humans in the sitting position, the elevated cephalic vein
partially collapsed at the point at which it entered the upper
end of the thorax, and the venous pressure was not a
function of right arterial pressure [48].
In the sitting or head-elevated position, cerebral venous
blood exists through the internal jugular veins, emissary
veins and vertebral venous plexus in humans. Epstein et al.
[32] demonstrated in monkeys with erect position that
cerebral venous blood drains primarily from the vertebral
venous system with little from the jugular veins and that the
proportion of outflow depended on the airway pressure.
Eckenhoff [30] explained the cerebral venous outflow as a
dynamic state: during expiration, high-intrathoracic pressure
causes a major proportion of blood to drain via the vertebral
plexus; during inspiration, low-intrathoracic pressure causes
blood to drain freely from both the jugular veins and
vertebral plexus. During forced expiration, high-intrathoracic pressure stops the return of blood via jugular veins [79],
so that all cerebral venous blood flows into vertebral plexus
or out into other venous beds [79]. The vertebral venous
plexus has been described as an enormous, valveless, thinwalled vascular bed contained within the spinal canal that
courses between and parallel to vertebral bodies [8]. Blood
is free to flow in and out of these venous plexus and do not
directly connect to the superior vena cava, so that it is not
subjected to immediated intrathoracic pressure variations
[65]. These two unique characteristics, its large capacitance
and its indirect connection with the superior vena cava, may
also partially explain why pressure transmission is less
effective in the head-elevated position [65].
Confluens sinuum pressure is elevated by retroflexion
and lowered by anteflexion of the neck [55]. Right
rotatation of the neck causes slight elevation of confluens
sinuum pressure while left rotation causes no marked
change. The cause of this difference is not obvious [55].
Of extraordinary importance is the fact that confluens
sinuum pressure is elevated without exception by jugular
compression, especially when applied bilaterally [55]. In
patients in supine position, confluens sinuum pressure is
raised from 6.6F2 to 19.6F3.6 mm Hg by bilateral
compression [55]. In the patients in the sitting position,
bilateral jugular compression elevated confluens sinuum
pressure from 5.5F1.3 to +6.7F4.2 mm Hg [55].
9. Cerebral venous blood flow
9.1. Biological background
Starling resistor formula has been used to represent
cerebral venous outflow, wherein flow is independent of
extracranial venous pressure and depends only on the
upstream transmural pressure [65,93]. However, cerebral
perfusion pressure, which corresponds to the upstream
pressure for the whole brain, does not convincingly fit the
waterfall model and completed cessation of CBF, when ICP
increases to blood pressure levels, is difficult to imagine
because of presence of a significant arteriovenous pressure
difference along an open vascular system [71]. This
discrepancy also was demonstrated experimentally by use
of two collapsible tubes perfused in an enclosed chamber to
simulate arterial and venous intracranial beds. Equalizing
the chamber and inflow pressures produced on 80% CBF
drop, but no complete cessation as would be predicted from
the Starling model [71]. Unfortunately, this pathophysiological discrepancy is left unexplained.
There is a close coupling relationship between ICP and
cortical venous pressure, with cortical venous pressure ~2–5
mm Hg higher than ICP. This offset is not dependent on
even large changes in ICP that might affect CBF and does
not agree with the Starling resistor principle, in which flow
is directly proportional to upstream transmural pressure,
namely venous pressure minus ICP. The laboratory model
indicated that this apparent contradiction is related to the
place at which upstream pressure is measured. Provided an
adequate level of CBF is maintained, the pressure just at the
entrance to the collapsible part is changing in parallel with
ICP after a sharp exponentional relationship between flow
and pressures at this levels. Under the same conditions, the
pressures separated from the collapsible segment by an
additional resistance, followed the Starling formula.
Pressure and flow in the bridging veins are related each
other through the same exponential curve. Consequently, in
humans, the change from severe hyperemia (total CBF,
1000 ml/min) to serve ischemia (CBF, 300 ml/min) produce
only 1.5 mm Hg change in difference between ICP and
pressure in the bridging veins. Unless specifically thought,
such as small differences would go unnoticed in any clinical
or experimental study, and pressures would be assumed to
change bin parallelQ. In contrast, the model predicts that at
the level of small pial veins, effects of distal venous
resistance would prevail and flow would obey the laws of a
Starling resistor [65]. For flow changes from hyperemia to
ischemia, pressure will change by up to 37 mm Hg,
proportionally to CBF [65]. For a large CBF decrease,
B. Schaller / Brain Research Reviews 46 (2004) 243–260
nonlinear logarithmic term becomes significant, and pressure coupling downstream and flow-pressure proportionally
upstream cease [65]. Specifically, there will be non-zero
flow for ICP as high as inflow pressure.
9.2. Venous outflow as source of slow oscillation
Normal CVS exhibit natural slow variations in pressure
and flow values. It is accepted that increased intracranial
slow wave activity denotes an abnormality, although exact
mechanism of this phenomenon is still disputed. An
interesting features of the proposed flow-pressure model is
that it is not continuous when ICP crosses outflow pressure
(equivalent to SSS pressure). The amplitude of the fluctuations increased visibly with increased amplitude of pulsation
transmitted downstream to inflow pressure (simulating
cerebral intraparenchymal venous pressure) when proximal
resistance is removed noncontinuous flow-pressure characteristics of the collapsible tube have been noted previously
[43]. The measurement of these characteristics is difficult
owing to possible hysteresis in collapsible tube behavior
[13] and resulting self-generated flow [80]. In the formula
suggested earlier, transition between linear and logarithmic
models is immediate. Under physiological conditions, the
influence of rapid change of behavior of venous outflow is
likely to be small, because of provision of a pressure head
for flow. The upstream system displays strong flowregulating properties. Therefore, transition between stable
states will occur without much changes of flow and
moderate change in transmural pressure. However, in
systems in which the up-stream regulation of flow is
disturbed, steep change in properties for venous outflow
may add substantially to generation and transmission of
pressure and flow waves.
9.3. low ICP
Piechnik et al. [84] investigated low CBF behavior for
negative downstream transmural pressures (ICPbSSS).
Although such pressure distribution is not physiological
during longer time periods, it may attain clinical importance
by shunting for hydrocephalus with intracranial hypotension, as a result of overdrainage related to vertical body
position, increased ICP wave activity or CSF leaks [21].
Under such experimental conditions, venous pressure in
bridging veins and ICP become nonphysiologically dissociated [21]. An additional stress is placed on the walls of
bridging veins that may be relevant to our understanding of
postshunting complications in hydrocephalus: it is thought
that artificially CSF overdrainage from cerebral ventricles
produces their passive collapse [87]. These results in
stretching of venous vessels in subarachnoid space, which
increases the chance of their rupture and subsequently
hemorrhage [91]. From our model, a complementary
scenario may be proposed in which pial veins engorge
because of unphysiologically large transmural pressures
255
[84]. These changes in subarachnoid space and parenchyma
may contribute to postshunting ventricular collapse. In
addition, repeated stretching and relaxing of veins in the
subarachnoid space from pressure fluctuations may produce
an additional bwear-and-tearQ effect, which could be
significant in producing venous rupture in addition to
increasing the stretch from collapsing brain [84].
9.4. CBV and CBF relationship
Venous regional cerebral blood volume (rCBV) changes
are much less than arterial rCBV changes (see Fig. 2). The
ratio of arterial and venous rCBV changes measured by
nuclear magnetic resonance (NMR) is consistent with that
determined by vessels diameter measurements [41]. It is
well-known that hypercapnia similarly induces vascular
vessel diameter changes in cerebrum and cerebellum.
Furthermore, although differences in anesthesia—under
experimental or clinical conditions—may affect vascular
responses to hypercapnia, it is likely that the ratio between
the diameter changes of arteries and veins will be preserved
[41]. Translation of the vessel diameter data into accurate
rCBV changes should take into account the fractional
diameter changes represent by all size and distribution of
vessels [41]. Thus, it is difficult to directly compare
diameter changes obtained by videomicroscopy and with
rCBV measured a diffusion-weighted by 19F NMR method
(diffusion-weighted NMR signals show two distinct pseudodiffusion (D*) components: the larger D* component
predominantly reflects more oxygenated arterial blood, the
smaller D* component represent (less) oxygenated venous
blood [28]). However, the ratio of arterial and venous rCBV
changes in the entire brain measured by 19F NMR can be
compared with the ratio of an arterial and venous diameter
changes in small-size vessels measure by videomicroscopy,
assuming larger arterial and venous blood vessels behave
similarly and also assuming that the ratio of blood volume
fractions in small and large vessels are similar in the arterial
and venous trees [41].
Fig. 2. Schematic plot. Venous and arterial rCBV vs. rCBF in the brain.
Legend: CBV, cerebral blood volume; CBF, cerebral blood flow.
256
B. Schaller / Brain Research Reviews 46 (2004) 243–260
CBV through vessels, which can be determined by the
product of the cross section of the blood vessel (A) and the
linear velocity (V), should be conserved at various sections
of blood vessels. Thus, CBF can be changed by the
modulation of A and/or V. Since the changes of A is directly
related to CBV, CBF and CBV changes are interrelated as
CBF stim /CBF cont =(A stim /A cont ) (V stim /V cont )=(CBV stim /
CBVcont)(V stim/V cont), where subscripts bstimQ and bcontQ
indicated bstimulatedQ and bcontrolQ conditions, respectively. According to CBV and CBF observations during
hypercapnia, it is expected that in case of venous blood
velocity is much more than that of arterial blood velocity
considering that the rCBV change in venous blood is much
less than that of arterial blood. An increase in blood velocity
is much less than that of arterial blood. An increase in blood
velocity, especially in the venous blood pool, increases the
dephasing of diffusion-weighted NMR signals, resulting in
increased D* during hypercapnia. D*1 (fast-moving components) and D*2 (slow-moving components) are linearly
correlated with pCO2 level, which is closely related to CBF
[60]. In the study of Lee et al. [60], the D* values of arterial
and venous blood did not show significant correlation with
CBF due to a large variability between animals and trials.
This needs to be further investigated. However, it is
generally accepted that cerebral blood flow velocity (CBFV)
functioned as an indicator of the cerebral blood volume,
since the CBFV is proportional to the cerebral blood volume
and corresponding changes.
Until now, it has been assumed that relative total CBV
change, which was answered by contrast agent-based
methods or estimated from relative CBF changes using
Grubb’s equitation of CBF-total CBV relationship. Based on
Grubb’s equation and the findings of Lee et al., a 100%
increase in CBF induces 31% total CBV increase [61].
However, venous rCBV change (e.g. 15%) is about half of
the total venous rCBV change (e.g. 31%) [61]. An increase
in venous blood volume decreases the blood oxygen leveldependent (BOLD) MR imaging signal (for detailed
description of the method, see Ref. [36]), while an increase
in venous oxygenation level increases the BOLD signal
[61]. For a given BOLD signal changes, less blood
oxygenation level change. Therefore, the venous oxygenation level change calculated from BOLD and total rCBV
changes (instead of the venous CBV change) would be
overestimated [61]. The overestimation of venous oxygenation level by using total rCBV during neural stimulation
results in an underestimation of oxygen consumption
changes determined from BOLD and CBF/CBV data [61].
These problems can be alleviated by replacing the total
rCBV change with the venous rCBV change, i.e. approximately 50% of total rCBV change [61].
9.5. Cerebral venous oxygenation
Oxygen in the cerebral blood must cross the BBB to
reach into the interstitial space and subsequently into the
intracellular space to be utilized predominantly in the
mitochondria. It has been proposed that the dissolved
oxygen does not diffuse freely from the blood pool into
the interstitial space because the BBB acts as a barrier to the
passage of oxygen [12]. If this is the case, a large gradient of
O2-concentration across the vascular-interstitial compartment would be theoretically expected. Venous hemoglobin
saturation of oxygen is an important physiological parameter for assessment of tissue oxygenation [61]. The dynamic
changes of blood oxygenation provide a passage of functional information, and this physiological variable could be
used to assess the strength of brain activation directly. Nearinfrared spectroscopy is a tool that has the potential to
provide similar but continuous, noninvasive and safe
information about cerebral oxygenation status. Although
estimates of regional cerebral oxygen saturation (rSO2)
include arterial and capillary components, the largest
contribution is considered to be venous, which has been
estimated to represent 75% of the CBV [62]. Thus, changes
in jugular bulb oxygen saturation (SjO2) should be
paralleled by changes in rSO2, although close agreement
between the two parameters would not necessarily be
expected as different entities are being measured [62]. The
relationship between the two variables (as defined by linear
regression analysis) varies considerably between patients
[62] suggesting that it may not be possible to predict
absolute SjO2 for any given patient based solely on rSO2
measurements [62].
It should also be noted that magnitude and direction of
the difference between rSO2 and SjO2 varied with the
absolute value of SjO2. This means in practical terms, for
high values of SjO2, rSO2 runs low, whereas at low values it
runs high. Thus, severe desaturation of jugular venous
return might not always be recognized [62]. Conversely, it
may be hard to be sure when cerebral metabolism has nearly
ceased during profound hypothermia as rSO2 values rarely
rose to more than 90%. In addition, it should be noted that
intravascular oxygenation may not always accurately reflect
intracellular oxygen availability. du Plessis et al. [26]
recently described a dissociation of cerebral intravascular
and mitochondrial oxygenation by comparing changes in
hemoglobin O2 saturation to changes in oxidized cytochrome aa3. Thus, measurement of cerebral intravascular
oxygenation alone may be an inadequate method for
assessing adequacy of cerebral protection during periods
of decreased CBF [26]. The reasons for the variable
relationship between rSO2 and SjO2 between patients
(despite the excellent correlation in individual patients) are
not entirely clear.
Some laboratories have reported the mean tissue pO2
(weighted average of all tissue compartments) to be close to,
or below, venous pO2 [26], while other reported the mean
tissue pO2 to fall in between arterial and venous pO2 [26].
In addition, little is known regarding how interstitial or
tissue oxygen tension is modulated in response to changes
in arterial oxygen tension and/or CBF [26]. Thus, the ability
B. Schaller / Brain Research Reviews 46 (2004) 243–260
to measure compartment-specific interstitial, arterial and
venous oxygen tension in the brain could potentially shed
light on the underlying mechanism by which oxygen passes
from capillary across BBB and into the brain tissue. In the
study of Duong et al. [29], the relationship between piO2
and CBF was roughly linear for the CBF values of 1–2 ml/g/
min. At this range, a 100% increase in CBF resulted in 50%
increase in oxygen delivery to the interstitial space,
suggesting that the decreased transit time resulting from
increased CBF had a significant effect on the oxygen
passage across BBB [29]. The degree of coupling between
neural activity and oxidative metabolism associated with
increased neuronal activity, however, remains controversial
[29].
When oxygen delivery increases via an augmentation in
CBF with no change in oxygen demand, HbO2 and a
reciprocal decrease in deoxy-Hb means that flow velocity
increased without accompanying either vasodilatation or
recruitment, which resulted in increases in venous oxygenation. This same pattern of changes in hemoglobulin
oxygenation has also been observed in the activated area
in near infrared spectroscopy studies [26], although the
dilatative response of pial arterioles to neuronal activation
has been determined videomicroscopically in several studies
[26]. Kleinschmidt et al. [58] proposed two explanations for
this absence of the tHb response during activation: changes
in local cerebral hematocrit associated with flow velocity
changes, or a short interval between task performance,
which does not allow for recovery of vasomotor tone.
However, the mechanism of dilatation of pial arterioles are
still controversial. There is no valid evidence to deny the
possibility that, when increases in CBF are very small, the
degree of dilatation of arterioles is too small to detect [58].
This possibility is supported by observation in microspectroscopy measurements through a cranial window and
a thinned skull in rats pial arterioles did not show detectable
dilatation, whereas optical and electrocortical signal changes
were observed in capillary areas [58]. In general, activitydependent changes in rCBF for subtle cognitive tasks are
small (b10%) [58]. Thus, an increase in flow velocity
without detectable vasodilatation might account for the
absence of an increase in tHb during activation.
10. Correlation between superior sagittal sinus flow
velocity and cerebral blood flow
A significant linear correlation between peak velocity of
SSS flow and both cortical and hemispheric blood flow is
identified [54]. It has also been analyzed the correlation
between the mean velocity of SSS flow by averaging the
velocities obtained in each cardiac phase, and both cortical
and hemispheric blood flow [54]. As indicated in the
relation to the peak velocity, the mean velocity of SSS flow
is a good indicative for CBF. It has been shown that the
cross-sectional area of SSS does not change significantly
257
during hyperventilation of hypercapnea, suggesting that SSS
flow velocity (cm s 1) reflects SSS blood flow (ml s 1)
[66].
Previous studies utilizing the arterial in-flow method
involved prediction of CBF by carotid velocity measurements, and these studies have yielded a good correlation
between actual CBF measured by the 133Xe clearance
method and carotid flow velocity assessed by the Doppler
technique. The venous outflow method, performed in
experimental animals, was also found to provide accurate
estimates of CBF. However, in human measurements, the
use of SSS flow velocity as an index of CBF may result in a
relatively low estimate because of the influence of other
venous drainage systems that were eliminated in the animal
experiments. There have been a few studies using transcranial Doppler measurements of SSS using transcranial
fants [19]. Bezinque et al. [14] showed that SSS flow
velocity measured by Doppler technique at the anterior
fontanel was about 15 cm s 1, which was near the lowest
value for adult patients in our series, but they failed to
obtain significant correlation between SSS flow velocity and
clinical parameters, possibly because of the large fluctuations in both flow velocity and pressure in SSS of infants
[14].
11. Effect of age on cerebral venous circulation
Documented morphological changes in the cerebral
vasculature of the aging brain include, among other things,
thinning of the endothelium, reduction in capillary lumen
diameter and decreasing number of capillary endothelial
cells. These structural and blood coagulative changes (such
as reduced blood filterability associated with advancing age)
might results in a shift of the thrombogenic/thrombolytic
equilibrium. The different behavior of CVS in advanced age
compared to young brain is not already understood [78].
There is a need of further physiological and biophysical
studies to shed more light into this aspect, especially on its
impact on the clinical routine [78]. In addition, these
existing differences between different age stages in CVS
may be also an important reason, whether experimental data
on CVS can not be easily transferred to clinical condition
[78]. This may be underlined by the fact, that for
experimental research, there were used, in most of the
cases, young animals, but the affected patients are almost in
advanced aged [98].
12. Conclusion
The CVS represents an important to control not only in
the physiological hemodynamic and metabolic course, but
has also an impact on the pathophysiological changes, such
as increased ICP. The cerebrovenous system seems to be
more complex than the arterial one, even so only little of its
258
B. Schaller / Brain Research Reviews 46 (2004) 243–260
physiological and biophysical behaviour is yet understood.
The importance of the cerebrovenous system on the different physiological parameter of normal brain function can
not be estimated, but it seems that it may be greater than
previously assumed. Possibly, the CVS may be one of the
most important factors to guarantee normal cerebral
function. We could demonstrate the importance and the
need of further experimental work on this subject, especially
to better understand the relationship of different physiological factors on the CVS. In the future, different state-ofthe-art-imaging methods may play an important role in
further understanding the complexity of the CVS.
References
[1] J. Anderweg, Intracranial venous pressure, hydrocephalus and
effects of cerebrospinal fluid shunts, Child’s. Nerv. Syst. 5 (1989)
318 – 323.
[2] R. Anxionnat, Anatomie et radio-anatomie du lobe temporal (MD
thesis). Nancy, 1989.
[3] M.L.J. Apuzzo, O.K. Chikovani, P.S. Gott, et al., Transcallocal,
interfornical approaches for lesions affecting the third ventricle.
Surgical considerations and consequences, Neurosurgery 10 (1982)
547 – 554.
[4] J. Auque, Th. Civit, Les veines superficielles, in: J. Auque (Ed.), Le
Sacrifice Veineux, Neurochirurgie (Suppl.), vol. 1, 1996, pp. 88 – 108.
[5] B. Asgeirsson, P.C. Grande, Local vascular response to elevation of
an organ above the heart, Acta Physiol. Scand. 156 (1996) 9 – 18.
[6] R.H. Ayanzu, C.R. Bird, P.J. Keller, et al., Cerebral MR venography:
normal anatomy and potential diagnostic pitfalls, AJNR 21 (2000)
74 – 78.
[7] I.H. Aydin, Y. Tuzun, E. Takci, et al., The anatomical variations of
sylvian veinsand cisterns, Minim. Invasive Neurosurg. 40 (1997)
68 – 73.
[8] O.V. Batson, The vertebral vein system—Caldwell lecture 1956, Am.
J. Roentgenol. 78 (1957) 195 – 212.
[9] O.V. Batson, The vertebral system of veins as a menas for cancer
dissemination, Prog. Clin. Cancer 3 (1967) 1 – 18.
[10] A. Beau, P. Rabischong, Les veines internes du cerveau, C. r. Assoc.
Anat. 102 (1959) 175 – 181.
[11] T.H.B. Bedford, The venous system of the velum interposition of the
Rhesus monkey and the effect of experimental occlusion of the great
vein of Galen, Brain 57 (1934) 225 – 265.
[12] M. Bergsneider, A.A. Alwan, L. Falkson, et al., The relationship of
pulsatile cerebrospinal fluid to cerebral blood flow and intracranial
pressure: a new theoretical model, Acta Neurochir., Suppl. (Wien) 71
(1998) 266 – 268.
[13] C.D. Bertram, Unstable equilibrium behavior in collapsible tubes,
J. Biochem. 19 (1986) 61 – 69.
[14] S.L. Bezinque, T.L. Slovis, A.S. Touchette, et al., Characterization of
superior sagittal sinus blood flow velocity using color Doppler in
neonates and infants, Pediatr. Radiol. 25 (1995) 175 – 179.
[15] S. Brew, Normal galenic drainage of the deep cerebral venous
system, Child’s Nerv. Syst. 20 (2004) 98 – 99.
[16] R.H. Britt, G.T. Rossi, Quantitative analysis of methods for
reducing physiological brain pulsations, J. Neurosci. Methods 6
(1982) 219 – 229.
[17] P.E. Burrows, O. Konez, A. Birdorff, Venous variations of the brain
and cranial vault, Neuroimaging Clin. N. Am. 13 (2003) 13 – 26.
[18] N.F. Capra, K.V. Anderson, Anatomy of the cerebral venous system,
in: J.P. Kapp, H.H. Schmidek (Eds.), The Cerebral Venous System
and its Disorders, Grune and Stratton, Philadelphia, 1984, pp. 1 – 36.
[19] A. Carmelo, A. Ficola, M.L. Fravolini, et al., ICP and CBF
regulation: a new hypothesis to explain the bwindkesselQ phenomenon, Acta Neurochir., Suppl. 81 (2002) 112 – 116.
[20] A. Chanda, A. Nanda, Anatomical study of the orbitozygomatic
transsellar-transcavernous-transclinoidal approach to the basilar
artery bifurcation, J. Neurosurg. 97 (2002) 151 – 160.
[21] P.H. Chapman, E.R. Cosman, M.A. Arnold, The relationship
between ventricular fluid pressure and body position in normal
subjects and subjects with shunts. A telemetric study, Neurosurgery
26 (1990) 181 – 186.
[22] P. Chaynes, Microsurgical anatomy of the great cerebral vein of
Galen and its tributaries, J. Neurosurg. 99 (2003) 1028 – 1038.
[23] F. Cowan, M. Thorensen, Ultrasound study of the cranial venous
system in the human new-born infant and the adult, Acta Physiol.
Scand. 117 (1983) 131 – 137.
[24] A. Delmas, B. Pertuiset, G. Bertrand, Les veines du lobe temporal,
Rev. Oto-Neuro-Ophtalmol. 23 (1951) 224 – 230.
[25] G. DiChiro, Angiographic patterns of cerebral convexity veins and
superficial dural sinuses, AJR 87 (1962) 308 – 321.
[26] A.J. du Plessis, Near-infrared spectroscopy for the in vivo study of
cerebral hemodynamics and oxygenation, Curr. Opin. Pediatr. 7
(1995) 632 – 639.
[27] H. Duret, Recherches anatomiques sur la circulation veineuse de
l’encephale, Arch. Physiol. Norm. Pathol. 1 (1874) 316 – 356.
[28] T.Q. Duong, S.-G. Kim, In vivo MR measurements of regional
arterial and venous blood volume fractions in intract rat brain, Magn.
Reson. Med. 43 (2000) 393 – 402.
[29] T.Q. Duong, E. Yacoub, G. Ariany, et al., High-resolution spin-echo
BOLD, and CBF fMRI at 4 and 7 T, Magn. Reson. Med. 48 (2002)
589 – 593.
[30] J.E. Eckenhoff, The physiologic significance of the vertebral venous
plexus, Surg. Gynecol. Obstet. 131 (1970) 72 – 78.
[31] J. Ekstedt, CSF hydrodynamic studies in man: 2. Normal hydrodynamic variables related to CSF pressure and flow, J. Neurol.
Neurosurg. Psychiatry 41 (1978) 345 – 353.
[32] H.M. Epstein, H.W. Linde, A.R. Crampton, et al., The vertebral
venous plexus as a major cerebral venous outflow tract, Anesthesiology 32 (1970) 332 – 338.
[33] D.P. Friedman, Abnormalities of the deep medullary white matter
veins: MR imaging findings, Am. J. Roentgenol. 168 (1997)
1103 – 1108.
[34] D. Georgiadis, S. Schwarz, R. Kollmar, et al., Influence of
inspiration: expiration ratio on intracraial and cerebral perfusion
pressure in acute stroke patients, Intensive Care Med. 28 (2002)
1089 – 1093.
[35] B. Goetzen, Veines internes du cerveau humain. Morphologie et
topographie des anastomoses veineuses centrol-peripheriques, Arch.
Anat. Pathol. 12 (1964) 122 – 133.
[36] D.A. Hall, M.S. Goncalves, Smiths, et al., A method for determining
venous contribution to BOLD contrast sensory activation, Magn.
Reson. Imaging 20 (2002) 695 – 706.
[37] J. Hamer, E. Alberti, S. Hoyer, et al., Influence of systemic and
cerebral vascular factors on the cerebrospinal fluid pulse waves,
J. Neurosurg. 46 (1977) 36 – 45.
[38] M.K. Hammock, T.H. Milhorat, K. Earle, et al., Vein of Galen
ligation in the primate, J. Neurosurg. 34 (1971) 77 – 83.
[39] O. Hassler, Deep cerebral venous system in man: a microangiographic study on its areas of drainage and its anastomoses with
superficial cerebral veins, Neurology 16 (1966) 505 – 511.
[40] O. Hassler, Venous anatomy of human hindbrain. A stereomicroangiographic study of the venous angio-architecture and the venous
areas of drainage, Arch. Neurol. 16 (1967) 404 – 409.
[41] G.M. Hathout, S.S. Gambhir, R.K. Gaopi, et al., A quantitative
physiologic model of blood oxygenation for functional magnetic
resonance imaging, Invest. Radiol. 30 (1995) 669 – 682.
[42] P. Haure, G.E. Cold, T.M. Hansen, et al., The ICP-lowering effect of
10 degrees reverse Trendelenburg position during craniotomy is
B. Schaller / Brain Research Reviews 46 (2004) 243–260
[43]
[44]
[45]
[46]
[47]
[48]
[49]
[50]
[51]
[52]
[53]
[54]
[55]
[56]
[57]
[58]
[59]
[60]
[61]
[62]
[63]
[64]
stable during a 10-minute period, J. Neurosurg. Anesthesiol. 15
(2003) 297 – 301.
M. Heil, T.J. Pedley, Stokes flow in collapsible tubes: computation
and experiment, J. Fluid Mech. 353 (1997) 285 – 312.
W.D. Heiss, R. Graf, K. Wienhard, Relevance of experimental
ischemia in cats for stroke management: a comparative reevaluation,
Cerebrovasc. Dis. 11 (2001) 73 – 81.
O. Hirai, H. Honda, M. Ishikawa, et al., Epidural pulse waveform as
an indicator of intracranial pressure dynamics, Surg. Neurol. 21
(1984) 67 – 74.
J. Hlinka, S. Kamba, J. Petzelt, et al., Origin of the bwaterfallQ effect
in phonon dispersion of relaxar perovsites, Phys. Rev. Lett. 91
(2003) 107602.
O. Hoffmann, R. Klingelbiel, J.S. Braun, et al., Diagnostic pitfall:
atypical cerebrovenous drainage via the vertebral venous system,
AJNR 23 (2002) 408 – 411.
J.P. Holt, The collapse factor in the measurement of venous pressure,
Am. J. Physiol. 134 (1941) 292 – 299.
I. Hooshmand, A.E. Rosenbaum, R.L. Stein, Radiographic anatomy of
normal cerebral deep medullary veins. Critical for distinguishing them
from their abnormal counterparts, Neuroradiology 7 (1974) 75 – 84.
Y.P. Huang, B.S. Wolf, Veins of the white matter of the cerebral
hemispheres (the medullary veins), AJR 92 (1964) 739 – 755.
G. Huther, J. Dorth, H. Van der Loos, et al., Microanatomic and
vascular aspects of the temporomesial region, Neurosurgery 43
(1998) 1118 – 1136.
G. Iaconetta, M. Fusco, M. Samii, The sphenopetroclival venous
gulf: a microanatomical study, J. Neurosurg. 99 (2003) 366 – 375.
K. Ide, N.H. Secher, Cerebral blood flow and metabolism during
exercise, Prog. Neurobiol. 61 (2000) 397 – 414.
S. Inao, H. Kuchiwaki, J. Yoshida, et al., Magnetic resonace imaging
quatification of superior sagittal sinus flow. Correlation to cerebral
blood flow measured by xenon-enhanced computed tomography,
Neurol. Res. 19 (1997) 35 – 40.
T. Iwabuchi, E. Sobata, K. Ebina, et al., Dural sinus pressure: various
aspects in human brain surgery in children and adults, Am. J.
Physiol. 250 (1986) H389 – H396.
Y. Kate, M. Mokay, R. Pucher, et al., Cerebrovascular response to
change of cerebral venous pressure and cerebrospinal fluid pressure,
Acta Neurochir. (Wien) 109 (1991) 52 – 56.
M.G. Katz, V. Khazia, A. Steinmetz, et al., Distribution of cerebral
flow using retrograde versus antegrade cerebral perfusion, Ann.
Thorac. Surg. 67 (1999) 1065 – 1069.
A. Kleinschmidt, A. Obrig, M. Requardt, et al., Simultaneous
recording of cerebral blood oxygenation changes during human brain
activation by magnetic resonance imaging and near-infrared spectroscopy, J. Cereb. Blood Flow Metab. 16 (1996) 817 – 826.
C. Lee, M.A. Pennington, C.M. Kenney, MR evaluation of
developmental venous anomalies: medullary venous anatomy of
venous angiomas, AJNR 17 (1996) 61 – 70.
S.P. Lee, T.Q. Duong, G. Yang, et al., Relative changes of cerebral
arterial and venous blood volumes during increased cerebral blood
flow: implications for BOLD FMRI, Magn. Reson. Med. 45 (2001)
791 – 800.
M. Lemay, Left–right dissymmetry, handedness, AJNR 13 (1992)
493 – 504.
W. Lin, A. Celik, R.P. Paczynski, et al., Quantitative magnetic
resonance imaging in experimental hypercapnia: improvement in the
relation between changes in bran R2 and the oxygen saturation of
venous blood after correction for changes in cerebral blood volume,
J. Cereb. Blood Flow Metab. 19 (1999) 853 – 862.
R. Lopez-Muniz, N.L. Stephens, B. Bromberger-Barnea, et al.,
Critical closure of pulmonary vessels analyzed in terms of Starling
resistor models, J. Appl. Physiol. 24 (1968) 625 – 635.
C.K. Lyon, J.B. Scott, C.Y. Wang, Flow through collapsible tubes at
low Reynolds numbers. Applicability of the waterfall model, Circ.
Res. 47 (1980) 68 – 73.
259
[65] C.K. Lyon, J.B. Scott, D.K. Anderson, et al., Flow through collapsible
tubes at high Reynolds numbers, Circ. Res. 49 (1981) 988 – 996.
[66] H.P. Mattle, R.R. Edelman, M.A. Reis, et al., Flow quantification in
the superior sagittal sinus using magnetic resonance, Neurology 40
(1990) 813 – 815.
[67] H.P. Mattle, K.U. Wentz, R.R. Edelman, et al., Cerebral venography
with MR, Radiology 178 (1991) 453 – 458.
[68] J.F. Meder, J. Chiras, J. Roland, et al., Venous territories of the brain,
J. Neuroradiol. 21 (1994) 118 – 133.
[69] N.R. Mehta, L. Jones, M.A. Kraut, et al., Physiologic variations in
dural venous sinus flow on phase-contrast MR imaging, Am. J.
Roentgenol. 175 (2000) 221 – 225.
[70] S.S. Mikhailov, I.I. Kagan, The anastomoses of the venous system of
the brain and their role in the collateral circulation, Folia Morphol.
16 (1968) 10 – 18.
[71] J.D. Miller, A.E. Stanek, T.W. Langfitt, Cerebral blood flow
regulation during experimental brain compression, J. Neurosurg.
39 (1973) 186 – 196.
[72] J.P. Muizelaar, Cerebral blood flow, cerebral blood volume, and
cerebral metabolism after severe head injury, in: D.P. Becker, S.K.
Gudeman (Eds.), Textbook of Head Injury, WB Saunders, Philadelphia, PA, 1989, pp. 221 – 240.
[73] N. Muthukumar, P. Palaniappan, Tentorial venous sinuses: an
anatomic study, Neurosurgery 42 (1998) 363 – 371.
[74] N. Nagdyman, T. Fleck, S. Barth, et al., Relation of cerebral tissue
oxygenation index to central venous oxygen saturation in children,
Intensive Care Med. 30 (2004) 468 – 471.
[75] K. Oka, A.L. Rhoton, M. Barry, et al., Microsurgical anatomy of the
deep venous system of the brain, Neurosurgery 15 (1984) 621 – 657.
[76] T. Okudera, T. Ohta, Y.P. Huang, et al., Developmental and
radiological anatomy of the superficial cerebral convexity vessels
in the human fetus, J. Neuroradiol. 15 (1988) 205 – 224.
[77] M. Ono, A.L. Rhoton, D. Peace, et al., Microsurgical anatomy of the
deep venous system of the brain, Neurosurgery 15 (1984) 621 – 657.
[78] H. Otsuka, H. Nakase, K. Nagata, et al., Effect of age on cerebral
venous circulation disturbances in the rat, J. Neurosurg. 93 (2000)
298 – 304.
[79] J.L. Parker, C.J. Flucker, N. Harvey, et al., Comparison of external
jugular and central venous pressures in mechanically ventilated
patient, Anesthesia 57 (2002) 596 – 600.
[80] T.J. Pedley, X.Y. Luo, Modeling flow and oscillations in collapsible
tubes, Theor. Comput. Fluid Dyn. 10 (1998) 277 – 294.
[81] S. Permutt, B. Bromberger-Barnea, H.N. Bane, Alveolar pressure,
pulmonary venous pressure, and the vascular waterfall, Med. Thorac.
19 (1962) 239 – 260.
[82] D. Petit-Dutaillis, A. Delmas, B. Pertuiset, Le reseau veineux du
cortex cerebral, Sem. Hop. Paris 26 (1950) 543 – 552.
[83] J.H. Piatt, J.X. Kellogg, A hazard of combining the infratentorial
supracerebellar and the cerebellomedullary fissure approaches:
cerebellar venous insufficiency, Pediatr. Neurosurg. 33 (2000)
243 – 248.
[84] S.K. Piechnik, M. Czosnyka, H.K. Richards, et al., Cerebral venous
blood outflow: a theoretical model based on laboratory simulation,
Neurosurgery 49 (2001) 1214 – 1223.
[85] K. Plaschke, C. Sommer, A. Fahrner, et al., Pronounced arterial
collateralization was induced after permanent rat cerebral four-vessel
occlusion. Relation to neuropathology and capillary ultrastructure,
J. Neural Transm. 110 (2003) 719 – 732.
[86] T. Przybylowski, M.F. Bangash, K. Reichmuth, et al., Mechanisms
of the cerebrovascular response to apnoea in humans, J. Physiol. 548
(2003) 323 – 332.
[87] R.H. Pudenz, E.L. Foltz, Hydrocephalus: overdrainage by ventricular
shunts—a review and recommendations, Surg. Neurol. 35 (1991)
200 – 212.
[88] R. Reisch, L. Vutskits, R. Filippi, et al., Topographic microsurgical
anatomy of the parclinoid cartotid artery, Neurosurg. Rev. 25 (2002)
177 – 183.
260
B. Schaller / Brain Research Reviews 46 (2004) 243–260
[89] D.S.M. Ruit, P. Gailloud, D.A. Ruefenacht, et al., The craniocervical
venous system in relation to cerebral venous drainage, AJNR 23
(2002) 1500 – 1508.
[90] K. Sakata, O. Al-Mefty, I. Yamamoto, Venous consideration in
petrosal approach: microsurgical anatomy of the temporal bridging
vein, Neurosurgery 47 (2000) 153 – 160.
[91] S. Samuelson, D.M. Long, S.N. Chou, Subdural hematoma as a
complication of shunting procedures for normal pressure hydrocephalus, J. Neurosurg. 37 (1972) 548 – 551.
[92] D. San Millan Ruiz, P. Gailloud, D.A. Rufenacht, et al., The
craniocervical venous system in relation to cerebral venous drainage,
AJNR 23 (2002) 1500 – 1508.
[93] B. Schaller, R. Graf, Cerebral ischemia and reperfusion: the
pathophysiological concept as basis of clinical therapy? J. Cereb.
Blood Flow Metab. 24 (2004) 351 – 371.
[94] B. Schaller, R. Graf, Cerebral venous infarction: the pathophysiological concept, Cerebrovasc. Dis. 18 (2004) 179 – 188.
[95] B. Schaller, R. Graf, Y. Sanada, et al., Hemodynamic changes after
occlusion of the posterior superior sagittal sinus. An experimental
PET-study in cats, AJNR 24 (2003) 1876 – 1880.
[96] B. Schaller, R. Graf, A.H. Jacobs, Invited commentary: ischemic
tolerance: a window to endogenous neuroprotection? Lancet 362
(2003) 1007 – 1008.
[97] B. Schaller, A.H. Jacobs, R. Graf, Hemispheric dominance for the
cortical control of swallowing in humans: a contribution to better
understand cortical organization?, Eur. J. Radiol. 51 (2004) 290 – 291.
[98] B. Schlesinger, The venous system of the brain with special reference
of the Galenic system, Brain 62 (1939) 274 – 291.
[99] J.N. Scott, R.I. Farb, Imaging and anatomy of the normal intracranial
venous system, Neuroimaging Clin. N. Am. 13 (2003) 1 – 12.
[100] A.R. Shakhnovich, V.A. Shakhnovich, A.A. Glashkina, Noninvasive assessment of the elastance and reserve capacity of the
craniovertebral contents via flow velocity measurements in the
straight sinus by TCD during body tilting test, J. Neuroimaging 9
(1999) 141 – 149.
[101] K. Shapira, A. Fried, F. Takei, et al., Effect of the skull and dura on
neural axis pressure–volume relationships and CSF hydrodynamics,
J. Neurosurg. 63 (1985) 76 – 81.
[102] M. Sindou, F. Alaywan, P. Hallacq, Chirurgie des grands sinus
veineux duraux intracraniens, in: J. Auque (Ed.), Le Sacrifice
Veineux en Neurochirurgie, Neurochirurgia (Suppl.), vol. 1, 1996,
pp. 45 – 87.
[103] C. Strik, U. Koose, C. Kiefer, et al., Slow rhythmic oscillations in
intracranial CSF and blood flow: registered by MRI, Acta Neurochir., Suppl. 81 (2002) 139 – 142.
[104] Y. Suzuki, H. Ikeda, M. Shimada, et al., Variations of the basal vein:
identification using three-dimensional CT angiography, AJNR 22
(2001) 670 – 676.
[105] S. Takahashi, K. Kato, N. Tomura, et al., Dural arteriovenous fistula
of the cavernous sinus with cortical venous reflux of the posterior
fossa via a bridging vein, Radiat. Med. 19 (2001) 219 – 222.
[106] M. Teksum, S. Casey, A. McKinney, et al., Anatomy and frequency
of large pontomesencephalic veins on 3D CT angiograms of the
circle of Willis, AJNR 24 (2003) 1598 – 1601.
[107] J. Theron, Les affluents du sinus caverneux, Neurochirurgie 18
(1972) 623 – 638.
[108] M. Ursino, C.A. Lodi, A simple mathematical model of the
interaction between intracranial pressure and cerebral hemodynamic,
J. Appl. Physiol. 82 (1997) 1256 – 1269.
[109] E.P. Wei, H.A. Kontos, Responses of cerebral arterioles to increased
venous pressure, Am. J. Physiol. 243 (1982) H442 – H447.
[110] R.O. Weller, Pathology of cerebrospinal fluid and interstitial fluid of
the CNS: significance for Alzheimer disease, J. Neuropathol. Exp.
Neurol. 57 (1998) 885 – 894.
[111] S.G. Wetzel, E. Kirsch, K.W. Stock, et al., Cerebral veins:
comparative study of CT venography with intraarterial digital
subtraction angiography, AJNR 20 (1999) 249 – 255.
[112] A. Zahkarov, C. Papaiconomon, L. Koh, et al., Intergrating the roles
of extracranial lymphaties and intracranial veins in cerebrospinal
fluid absorption in sheep, Micriovasc. Res. 67 (2004) 96 – 104.