Vascular Supply of the Brain and Spinal Cord

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Chapter 6 Vascular Supply of the Brain and Spinal Cord

The brain is a highly vascular organ and its profuse blood supply is characterized by a densely branching arterial network (Fig. 6.1). It has high metabolic activity due in part to the energy requirements of constant neural activity. It demands about 15% of the cardiac output and uses 25% of the total oxygen consumed by the body. The brain is supplied by two internal carotid arteries and two vertebral arteries that form a complex anastomosis (circulus arteriosus, or the circle of Willis) on the base of the brain. Vessels diverge from this anastomosis to supply the various cerebral regions. In general, the internal carotid arteries and the vessels arising from them supply the forebrain, with the exception of the occipital lobe of the cerebral hemisphere; the vertebral arteries and their branches supply the occipital lobe, the brain stem and the cerebellum. Venous blood from the brain drains into sinuses within the dura mater. Acute interruption of the blood supply to the brain for more than a few minutes causes permanent neurological damage. Such ischaemic strokes along with intracranial haemorrhages are major sources of morbidity and mortality.

Fig. 6.1 Resin cast of the arterial supply of the brain.

(Photograph by Sarah-Jane Smith.)

Arterial Supply of the Brain

The arterial supply of the brain is derived from the internal carotid and vertebral arteries, which lie, together with their proximal branches, within the subarachnoid space at the base of the brain.

Internal Carotid Artery

The internal carotid arteries and their major branches (sometimes referred to as the internal carotid system) essentially supply blood to the forebrain, with the exception of the occipital lobe.

The internal carotid artery (Figs 6.2, 6.3) arises from the bifurcation of the common carotid artery, ascends in the neck and enters the carotid canal of the temporal bone. Its subsequent course is said to have petrous, cavernous and cranial parts.

Fig. 6.2 Internal carotid arteriogram. This image is a lateral projection obtained by intra-arterial digital subtraction angiography.

(Courtesy of Professor P. D. Griffiths, Academic Unit of Radiology, University of Sheffield.)

Fig. 6.3 Internal carotid arteriogram. This image is a Towne’s projection obtained by intra-arterial digital subtraction angiography.

(Courtesy of Professor P. D. Griffiths, Academic Unit of Radiology, University of Sheffield.)

Several preterminal vessels leave the cerebral portion of the internal carotid. The ophthalmic artery arises from the internal carotid as it leaves the cavernous sinus, often at the point of piercing the dura, and enters the orbit through the optic canal. The posterior communicating artery (Figs 6.4–6.6) runs back from the internal carotid above the oculomotor nerve and anastomoses with the posterior cerebral artery (which is a terminal branch of the basilar artery), thereby contributing to the circulus arteriosus around the interpeduncular fossa. The posterior communicating artery is usually very small. Sometimes, however, it is so large that the posterior cerebral artery is supplied via the posterior communicating artery rather than the basilar artery (‘fetal posterior communicating artery’). It is often larger on one side. Small branches from its posterior half pierce the posterior perforated substance, together with branches from the posterior cerebral artery. Collectively, they supply the medial thalamic surface and walls of the third ventricle. The anterior choroidal artery leaves the internal carotid near its posterior communicating branch and passes back above the medial part of the uncus. It crosses the optic tract to reach and supply the crus cerebri of the midbrain; it then turns laterally, recrosses the optic tract and gains the lateral side of the lateral geniculate body, which it supplies with several branches. It finally enters the inferior horn of the lateral ventricle via the choroid fissure and ends in the choroid plexus. This small but important vessel also contributes to the blood supply of the globus pallidus, caudate nucleus, amygdala, hypothalamus, tuber cinereum, red nucleus, substantia nigra, posterior limb of the internal capsule, optic radiation, optic tract, hippocampus and fimbria of the fornix.

Fig. 6.4 Arteries at the base of the brain. The anterior part of the right temporal lobe has been removed to display the initial course of the middle cerebral artery within the lateral fissure.

Fig. 6.5 Arteries on the base of the brain injected with resin.

(By permission from Crossman, A.R., Neary, D. 2000. Neuroanatomy, 2nd ed. Edinburgh, Churchill Livingstone.)

Fig. 6.6 Circulus arteriosus at the base of the brain showing the distribution of central (perforating or ganglionic) branches. The anteromedial, posteromedial, posterolateral and anterolateral (lateral striate) vessels are shown. The medial striate and anterior choroidal arteries are also shown.

Anterior Cerebral Artery

The anterior cerebral artery is the smaller of the two terminal branches of the internal carotid artery (see Figs 6.5, 6.6).

The surgical nomenclature divides the vessel into three parts: A1, from the termination of the internal carotid artery to the junction with the anterior communicating artery; A2, from the junction with the anterior communicating artery to the origin of the callosomarginal artery; A3, distal to the origin of the callosomarginal artery. This segment is also known as the pericallosal artery.

The anterior cerebral artery starts at the medial end of the stem of the lateral cerebral fissure and passes anteromedially above the optic nerve to the great longitudinal fissure, where it connects with its fellow by a short transverse anterior communicating artery. The anterior communicating artery is approximately 4 mm long and may be double. It gives off numerous anteromedial central branches that supply the optic chiasma, lamina terminalis, hypothalamus, para-olfactory areas, anterior columns of the fornix and cingulate gyrus.

The two anterior cerebral arteries travel together in the great longitudinal fissure. They pass around the curve of the genu of the corpus callosum (Fig. 6.7) and then along its upper surface to its posterior end, where they anastomose with posterior cerebral arteries. They give off cortical and central branches.

Fig. 6.7 Major arteries of the brain. A, Medial aspect. B, Lateral aspect.

The cortical branches of the anterior cerebral artery are named by distribution. Two or three orbital branches ramify on the orbital surface of the frontal lobe and supply the olfactory cortex, gyrus rectus and medial orbital gyrus. Frontal branches supply the corpus callosum, cingulate gyrus, medial frontal gyrus and paracentral lobule. Parietal branches supply the precuneus, and the frontal and parietal branches both send twigs over the superomedial border of the hemisphere to supply a strip of territory on the superolateral surface (Fig. 6.8). Cortical branches of the anterior cerebral artery, therefore, supply the areas of the motor and somatosensory cortices that represent the lower limb.

Fig. 6.8 A, Lateral surface of the left cerebral hemisphere, showing the areas supplied by the cerebral arteries. B, Medial surface of the left cerebral hemisphere, showing the areas supplied by the cerebral arteries. In these figures, the area supplied by the anterior cerebral artery is coloured blue, that by the middle cerebral artery is pink and that by the posterior cerebral artery is yellow.

Central branches of the anterior cerebral artery arise from its proximal portion and enter the anterior perforated substance (see Fig. 6.6) and lamina terminalis. Collectively, they supply the rostrum of the corpus callosum, the septum pellucidum, the anterior part of the putamen, the head of the caudate nucleus and adjacent parts of the internal capsule. Immediately proximal or distal to its junction with the anterior communicating artery, the anterior cerebral artery gives rise to the medial striate artery, which supplies the anterior part of the head of the caudate nucleus and adjacent regions of the putamen and internal capsule.

Middle Cerebral Artery

The middle cerebral artery is the larger terminal branch of the internal carotid.

The surgical nomenclature identifies four subdivisions: M1, from the termination of the internal carotid artery to the bi- or trifurcation (also known as the sphenoidal segment); M2, the segment running in the lateral (Sylvian) fissure (also known as the insular segment); M3, coming out of the lateral fissure (also known as the operator segment); and M4, the cortical portions.

The middle cerebral artery runs first in the lateral cerebral fissure, then posterosuperiorly on the insula; it divides into branches distributed to this and the adjacent lateral cerebral surface (see Figs 6.5, 6.6, 6.8). Like the anterior cerebral artery, it has cortical and central branches.

Cortical branches send orbital vessels to the inferior frontal gyrus and the lateral orbital surface of the frontal lobe. Frontal branches supply the precentral, middle and inferior frontal gyri. Two parietal branches are distributed to the postcentral gyrus, the lower part of the superior parietal lobule and the whole inferior parietal lobule. Two or three temporal branches supply the lateral surface of the temporal lobe. Cortical branches of the middle cerebral artery, therefore, supply the motor and somatosensory cortices representing the whole body, with the exception of the lower limb, the auditory area and the insula.

Small central branches of the middle cerebral artery—the lateral striate or lenticulostriate arteries—arise at its commencement and enter the anterior perforated substance together with the medial striate artery. Lateral striate arteries ascend in the external capsule over the lower lateral aspect of the lentiform complex; they then turn medially, traverse the lentiform complex and the internal capsule and extend as far as the caudate nucleus.

Vertebral Artery

The vertebral arteries and their major branches (sometimes referred to as the vertebrobasilar system) essentially supply blood to the upper spinal cord, brain stem, cerebellum and occipital lobe of the cerebrum (Figs 6.9, 6.10). In addition, other branches have a wider distribution.

Fig. 6.9 Vertebral arteriogram. This image is a lateral projection obtained by intra-arterial digital subtraction angiography.

(Courtesy of Professor P. D. Griffiths, Academic Unit of Radiology, University of Sheffield.)

Fig. 6.10 Vertebral arteriogram. This image is a Towne’s projection obtained by intra-arterial digital subtraction angiography.

(Courtesy of Professor P. D. Griffiths, Academic Unit of Radiology, University of Sheffield.)

The vertebral arteries are derived from the subclavian arteries. They ascend through the neck in the foramina transversaria of the upper six cervical vertebrae and enter the cranial cavity through the foramen magnum, close to the anterolateral aspect of the medulla (see Fig. 6.5). They converge medially as they ascend the medulla and unite to form the midline basilar artery at approximately the level of the junction between the medulla and the pons.

One or two meningeal branches arise from the vertebral artery near the foramen magnum. These ramify between the bone and dura mater in the posterior cranial fossa and supply bone, diploë and the falx cerebelli.

A small anterior spinal artery arises near the end of the vertebral artery and descends anterior to the medulla oblongata to unite with its fellow from the opposite side at the mid-medullary level. The single trunk then descends on the ventral midline of the spinal cord and is reinforced sequentially by small spinal rami from the vertebral, ascending cervical, posterior intercostal and first lumbar arteries, which all enter the vertebral canal via intervertebral foramina. Branches from the anterior spinal arteries and the beginning of their common trunk are distributed to the medulla oblongata.

The largest branch of the vertebral artery is the posterior inferior cerebellar artery. It arises near the lower end of the olive, which it curves back around, and then ascends behind the roots of the glossopharyngeal and vagus nerves to reach the inferior border of the pons. There it curves and descends along the inferolateral border of the fourth ventricle before it turns laterally into the cerebellar vallecula between the hemispheres and divides into medial and lateral branches. The medial branch runs back between the cerebellar hemisphere and inferior vermis and supplies both. The lateral branch supplies the inferior cerebellar surface as far as its lateral border and anastomoses with the anterior inferior and superior cerebellar arteries (from the basilar artery). The trunk of the posterior inferior cerebellar artery supplies the medulla oblongata dorsal to the olivary nucleus and lateral to the hypoglossal nucleus and its emerging nerve roots. It also supplies the choroid plexus of the fourth ventricle and sends a branch lateral to the cerebellar tonsil to supply the dentate nucleus. The posterior inferior cerebellar artery is sometimes absent.

A posterior spinal artery usually arises from the posterior inferior cerebellar artery, but it may come directly from the vertebral artery near the medulla oblongata. It passes posteriorly and descends as two branches that lie anterior and posterior to the dorsal roots of the spinal nerves. These are reinforced by spinal twigs from the vertebral, ascending cervical, posterior intercostal and first lumbar arteries, all of which reach the vertebral canal by the intervertebral foramina, thereby sustaining the posterior spinal arteries to the lower spinal levels.

Minute medullary arteries arise from the vertebral artery and its branches and are distributed widely to the medulla oblongata.

Basilar Artery

This large median vessel is formed by the union of the vertebral arteries at the mid-medullary level and extends to the upper border of the pons (see Figs 6.5, 6.6). It lies in the pontine cistern and follows a shallow median groove on the ventral pontine surface. The basilar artery terminates by dividing into two posterior cerebral arteries at a variable level, but most frequently in the interpeduncular cistern, behind the dorsum sellae.

Numerous small pontine branches arise from the front and sides of the basilar artery along its course and supply the pons. The long and slender labyrinthine (internal auditory) artery has a variable origin. It usually arises from the anterior inferior cerebellar artery, but it may originate from the lower part of the basilar artery, the superior cerebellar artery or, occasionally, the posterior inferior cerebellar artery. The labyrinthine artery accompanies the facial and vestibulocochlear nerves into the internal acoustic meatus and is distributed to the internal ear.

The anterior inferior cerebellar artery (see Fig. 6.6) is given off from the lower part of the basilar artery and runs posterolaterally, usually ventral to the abducens, facial and vestibulocochlear nerves. It commonly exhibits a loop into the internal acoustic meatus below the nerves, and when this occurs, the labyrinthine artery may arise from the loop. The anterior inferior cerebellar artery supplies the inferior cerebellar surface anterolaterally and anastomoses with the posterior inferior cerebellar branch of the vertebral artery. A few branches supply the inferolateral parts of the pons and occasionally also supply the upper medulla oblongata.

The superior cerebellar artery (see Fig. 6.6) arises near the distal portion of the basilar artery, immediately before the formation of the posterior cerebral arteries. It passes laterally below the oculomotor nerve, which separates it from the posterior cerebral artery, and curves around the cerebral peduncle below the trochlear nerve to gain the superior cerebellar surface. There it divides into branches that ramify in the pia mater and supply this aspect of the cerebellum and also anastomose with branches of the inferior cerebellar arteries. The superior cerebellar artery supplies the pons, pineal body, superior medullary velum and tela choroidea of the third ventricle.

Posterior Cerebral Artery

The posterior cerebral artery (see Figs 6.5, 6.6) is a terminal branch of the basilar artery.

The surgical nomenclature identifies three segments: P1, from the basilar bifurcation to the junction with the posterior communicating artery; P2, from the junction with the posterior communicating artery to the portion in the perimesencephalic cistern; and P3, the portion running in the calcarine fissure.

The posterior cerebral artery is larger than the superior cerebellar artery, from which it is separated near its origin by the oculomotor nerve and, lateral to the midbrain, by the trochlear nerve. It passes laterally, parallel with the superior cerebellar artery, and receives the posterior communicating artery. It then winds around the cerebral peduncle and reaches the tentorial cerebral surface, where it supplies the temporal and occipital lobes. Like the anterior and middle cerebral arteries, the posterior cerebral artery has cortical and central branches.

The cortical branches of the posterior cerebral artery are named by distribution. Temporal branches, usually two, are distributed to the uncus and the parahippocampal, medial and lateral occipitotemporal gyri. Occipital branches supply the cuneus, lingual gyrus and posterolateral surface of the occipital lobe. Parieto-occipital branches supply the cuneus and precuneus. The posterior cerebral artery supplies the visual areas of the cerebral cortex and other structures in the visual pathway.

The central branches supply subcortical structures. Several small posteromedial central branches arise from the beginning of the posterior cerebral artery (see Fig. 6.6) and, together with similar branches from the posterior communicating artery, pierce the posterior perforated substance and supply the anterior thalamus, subthalamus, lateral wall of the third ventricle and globus pallidus. One or more posterior choroidal branches pass over the lateral geniculate body and supply it before entering the posterior part of the inferior horn of the lateral ventricle via the lower part of the choroid fissure. Branches also curl around the posterior end of the thalamus and pass through the transverse fissure, go to the choroid plexus of the third ventricle or traverse the upper choroid fissure. Collectively, these supply the choroid plexuses of the third and lateral ventricles and the fornix. Small posterolateral central branches arise from the posterior cerebral artery beyond the cerebral peduncle and supply the peduncle and the posterior thalamus, superior and inferior colliculi, pineal gland and medial geniculate body.

Circulus Arteriosus

The circulus arteriosus (circle of Willis) is a large arterial anastomosis that unites the internal carotid and vertebrobasilar systems (see Figs 6.5, 6.6). It lies in the subarachnoid space within the deep interpeduncular cistern and surrounds the optic chiasma, the infundibulum and other structures of the interpeduncular fossa. Anteriorly, the anterior cerebral arteries, which are derived from the internal carotid arteries, are joined by the small anterior communicating artery. Posteriorly, the two posterior cerebral arteries, which are formed by the division of the basilar artery, are joined to the ipsilateral internal carotid artery by a posterior communicating artery. In the majority of cases, the posterior communicating arteries are very small; however, a limited flow is possible between the anterior and posterior circulations. This is important because the primary purpose of the vascular circle is to provide anastomotic channels if one vessel is occluded. The normal-sized posterior communicating artery usually cannot fulfill this role.

There are considerable individual variations in the pattern and calibre of vessels that make up the circulus arteriosus. Although a complete circular channel almost always exists, one vessel is usually sufficiently narrowed to reduce its role as a collateral route. Cerebral and communicating arteries may be absent, variably hypoplastic, double or even triple. The circle is rarely functionally complete.

The haemodynamics of the circle is influenced by variations in the calibre of communicating arteries and in the segments of the anterior and posterior cerebral arteries that lie between their origins and their junctions with the corresponding communicating arteries. The greatest individual variation in calibre occurs in the posterior communicating artery. Commonly, the diameter of the precommunicating part of the posterior cerebral artery is larger than that of the posterior communicating artery, in which case the blood supply to the occipital lobes is mainly from the vertebrobasilar system. Sometimes, however, the diameter of the precommunicating part of the posterior cerebral artery is smaller than that of the posterior communicating artery, in which case the blood supply to the occipital lobes is mainly from the internal carotids via the posterior communicating arteries. Agenesis or hypoplasia of the initial segment of the anterior cerebral artery is more frequent than anomalies in the anterior communicating artery and contributes to defective circulation in about one third of individuals.

CASE 1 Subarachnoid Haemorrhage

A 42-year-old woman develops neck pain followed by a severe headache after lifting a laundry basket. She has a history of poorly controlled hypertension and smokes a pack of cigarettes daily. She is initially awake and alert, but within an hour she becomes somnolent. On examination, she can be aroused briefly, can answer simple questions and can follow one-step commands. She has no weakness. A head computed tomography (CT) scan shows diffuse subarachnoid blood with hydrocephalus (Fig. 6.11). Emergent angiography demonstrates a left middle cerebral artery aneurysm, which is treated by endovascular coiling.

Fig. 6.11 CT scan demonstrates diffuse subarachnoid haemorrhage (arrows) secondary to rupture of a middle cerebral artery aneurysm.

Discussion: Bleeding into the subarachnoid space is frequently caused by a ruptured cerebral aneurysm (Fig. 6.12). The circle of Willis and cerebral arteries lie within the subarachnoid space. It also contains CSF. Blood in the subarachnoid space disrupts the circulation of CSF and frequently leads to hydrocephalus.

Fig. 6.12 Ruptured anterior communicating artery aneurysm (arrow).

The clinical presentation of subarachnoid haemorrhage (SAH) can range from a mild headache to lethargy, hemiparesis, coma or even sudden death. Patients frequently complain of having the worst headache of their life. Risk factors for developing a cerebral aneurysm include hypertension, smoking and a family history of aneurysm.

Other causes of SAH include head trauma, cerebrovascular malformations and vasculopathies. Diagnosis of SAH is made by CT scan, but an arteriogram is usually required to identify its cause. A lumbar puncture demonstrates a large number of red blood cells in the CSF. Cerebral aneurysm may be treated surgically by craniotomy and clipping of the aneurysm or, in certain cases, by placing coils in the aneurysm via an endovascular approach. Hydrocephalus may require placement of a ventriculostomy to externally drain CSF to control intracranial pressure.

Central or Perforating Arteries

Numerous small central (perforating or ganglionic) arteries arise from the circulus arteriosus or from vessels near it (see Fig. 6.6). Many of these enter the brain through the anterior and posterior perforated substances (see Fig. 15.9). Central branches supply nearby structures on or near the base of the brain, along with the interior of the cerebral hemisphere, including the internal capsule, basal ganglia and thalamus. They form four principal groups. The anteromedial group arises from the anterior cerebral and anterior communicating arteries and passes through the medial part of the anterior perforated substance. These arteries supply the optic chiasma; lamina terminalis; anterior, preoptic and supraoptic areas of the hypothalamus; septum pellucidum; paraolfactory areas; anterior columns of the fornix; cingulate gyrus; rostrum of the corpus callosum; anterior part of the putamen and head of the caudate nucleus. The posteromedial group comes from the entire length of the posterior communicating artery and from the proximal portion of the posterior cerebral artery. Anteriorly, these arteries supply the hypothalamus and pituitary and the anterior and medial parts of the thalamus via thalamo-perforating arteries. Caudally, branches of the posteromedial group supply the mammillary bodies, subthalamus, lateral wall of the third ventricle, including the medial thalamus, and globus pallidus. The anterolateral group comprises mostly branches from the proximal part of the middle cerebral artery; they are also known as striate, lateral striate or lenticulostriate arteries. They enter the brain through the anterior perforated substance and supply the posterior striatum, lateral globus pallidus and anterior limb, genu and posterior limb of the internal capsule. The medial striate artery, which is derived from the middle or anterior cerebral arteries, supplies the rostral part of the caudate nucleus and putamen and the anterior limb and genu of the internal capsule. The posterolateral group is derived from the posterior cerebral artery distal to its junction with the posterior communicating artery and supplies the cerebral peduncle, colliculi, pineal gland and, via thalamogeniculate branches, posterior thalamus and medial geniculate body.

Regional Arterial Supply of the Brain

Brain Stem

The medulla oblongata is supplied by the branches of the vertebral, anterior and posterior spinal arteries, posterior inferior cerebellar arteries and basilar arteries, which enter along the anterior median fissure and the posterior median sulcus. Vessels that supply the central substance enter along the rootlets of the glossopharyngeal, vagus, accessory and hypoglossal nerves. There is an additional supply via a pial plexus from the same main arteries.

The pons is supplied by the basilar artery and the anterior inferior and superior cerebellar arteries. Direct branches from the basilar artery enter the pons along the ventral medial groove (basilar sulcus). Other vessels enter along the trigeminal, abducens, facial and vestibulocochlear nerves and from the pial plexus.

The midbrain is supplied by the posterior cerebral, superior cerebellar and basilar arteries. The crura cerebri are supplied by vessels entering on their medial and lateral sides. The medial vessels enter the medial side of the crus and also supply the superomedial part of the tegmentum, including the oculomotor nucleus; lateral vessels supply the lateral part of the crus and the tegmentum. The colliculi are supplied by three vessels on each side from the posterior cerebral and superior cerebellar arteries. An additional supply to the crura and the colliculi and their penduncles comes from the posterolateral group of central branches of the posterior cerebral artery.

Cerebellum

The cerebellum is supplied by the posterior inferior, anterior inferior and superior cerebellar arteries. The cerebellar arteries form superficial anastomoses on the cortical surface. Anastomoses between deeper, subcortical branches have been postulated.

The choroid plexus of the fourth ventricle is supplied by the posterior inferior cerebellar arteries.

Optic Chiasma, Tract and Radiation

The blood supplies of the optic chiasma, tract and radiation are of considerable clinical importance. The chiasma is supplied in part by the anterior cerebral arteries, but its median zone depends on rami from the internal carotid arteries reaching it via the stalk of the hypophysis. The anterior choroidal and posterior communicating arteries supply the optic tract, and the optic radiation receives blood through deep branches of the middle and posterior cerebral arteries.

Diencephalon

The thalamus is supplied chiefly by branches of the posterior communicating, posterior cerebral and basilar arteries. A contribution from the anterior choroidal artery is often noted, but this has been disputed. The medial branch of the posterior choroidal artery supplies the posterior commissure, habenular region, pineal gland and medial parts of the thalamus, including the pulvinar. Small central branches, which arise from the circulus arteriosus and its associated vessels, supply the hypothalamus. The pituitary gland is supplied by hypophysial arteries derived from the internal carotid artery, and the anterior cerebral and anterior communicating arteries supply the lamina terminalis.

The choroid plexuses of the third and lateral ventricles are supplied by branches of the internal carotid and posterior cerebral arteries.

Basal Ganglia

The majority of the arterial supply to the basal ganglia comes from the striate arteries, which are branches from the roots of the anterior and middle cerebral arteries (Fig. 6.13). They enter the brain through the anterior perforated substance and also supply the internal capsule. The caudate nucleus receives blood additionally from the anterior and posterior choroidal arteries. The posteroinferior part of the lentiform complex is supplied by the thalamostriate branches of the posterior cerebral artery. The anterior choroidal artery, a preterminal branch of the internal carotid artery, contributes to the blood supply of both segments of the globus pallidus and the caudate nucleus. In a well known case, ligation of this vessel during a neurosurgical procedure on a patient suffering from Parkinson’s disease led to the alleviation of Parkinsonian symptoms, presumably as a consequence of infarction of the globus pallidus. This chance observation led to the initiation of pallidal surgery (pallidotomy) for this condition.

Fig. 6.13 Arterial supply to the internal capsule and parts of the basal ganglia of the left cerebral hemisphere. The outer layers of the hemisphere have been removed to reveal these structures. The putamen and globus pallidus are displaced downward to display the internal capsule. Territory supplied by branches of the anterior and middle cerebral arteries is shown in red. Territory supplied by the anterior choroidal artery is shown in green.

Internal Capsule

The internal capsule is supplied by central, or perforating, arteries that arise from the circulus arteriosus and its associated vessels (see Fig. 6.13). These include the lateral and medial striate arteries, which come from the middle and anterior cerebral arteries and also supply the basal ganglia. The lateral striate arteries supply the anterior limb, genu and much of the posterior limb of the internal capsule and are commonly involved in ischaemic and haemorrhagic strokes. One of the larger striate branches of the middle cerebral artery is known as Charcot’s artery of cerebral haemorrhage.

The medial striate artery, a branch of the proximal part of the middle or anterior cerebral, supplies the anterior limb and genu of the internal capsule and the basal ganglia. The anterior choroidal artery also contributes to the supply of the ventral part of the posterior limb and the retrolenticular (retrolentiform) part of the internal capsule.

Cerebral Cortex

The entire blood supply of the cerebral cortex comes from cortical branches of the anterior, middle and posterior cerebral arteries. In general, long branches traverse the cortex and penetrate the subjacent white matter for 3 or 4 cm without communicating. Short branches are confined to the cerebral cortex and form a compact network in the middle zone of the grey matter, whereas the outer and inner zones are sparingly supplied. Although adjacent vessels anastomose on the surface of the brain, they become end-arteries as soon as they enter it. In general, superficial anastomoses occur only between microscopic branches of the cerebral arteries, and there is little evidence that they can provide an effective alternative circulation after the occlusion of larger vessels.

The lateral surface of the hemisphere is supplied mainly by the middle cerebral artery (see Fig. 6.8). This includes the territories of the motor and somatosensory cortices, which represent the whole body except for the lower limb and also the auditory cortex and language areas. The anterior cerebral artery supplies a strip next to the superomedial border of the hemisphere, as far back as the parieto-occipital sulcus. The occipital lobe and most of the inferior temporal gyrus (excluding the temporal pole) are supplied by the posterior cerebral artery.

Medial and inferior surfaces of the hemisphere are supplied by the anterior, middle and posterior cerebral arteries. The area supplied by the anterior cerebral artery is the largest; it extends almost to the parieto-occipital sulcus and includes the medial part of the orbital surface. The rest of the orbital surface and the temporal pole are supplied by the middle cerebral artery, and the remaining medial and inferior surfaces are supplied by the posterior cerebral artery.

Near the occipital pole, the junctional zone between the territories of the middle and posterior cerebral arteries corresponds to the visual (striate) cortex, which receives information from the macula. When the posterior cerebral artery is occluded, a phenomenon known as macular sparing may occur, in which vision involving the central part of the retina is preserved. Collateral circulation of blood from branches of the middle cerebral artery into those of the posterior cerebral artery may account for this phenomenon. Indeed, in some individuals, the middle cerebral artery may itself supply the macular area.

CASE 2 Cerebrovascular Disease

A 68-year-old man with hypertension, diabetes mellitus, and a long history of cigarette smoking suddenly collapses at work. He is unable to speak or move his right side. He is taken to the local emergency department, where he is found to be lethargic and to have a dense right hemiparesis, left gaze preference and global aphasia. His head CT scan is unremarkable. He is diagnosed with an acute ischaemic stroke; intravenous recombinant tissue plasminogen activator (rtPA) is administered. The following day his magnetic resonance imaging (MRI) scan reveals extensive infarction of the left middle cerebral artery territory. Three months later, he is awake, has dysarthric speech but no aphasia and is able to walk with the assistance of a cane.

Discussion: Cerebrovascular disease may be broadly categorized as ischaemic or haemorrhagic. Ischaemic cerebrovascular disease, or stroke, occurs when there is a lack of bloodflow to a region of the brain. The symptoms of stroke are variable and are determined by the blood vessels and area of the brain affected. Patients with anterior cerebral artery strokes may present with contralateral leg weakness greater than arm weakness. Middle cerebral artery strokes are usually associated with a dense contralateral hemiparesis, whereas posterior cerebral artery strokes may cause homonymous visual field loss. Strokes affecting the dominant hemisphere often result in an aphasia; non-dominant hemisphere strokes can cause neglect syndromes such as anosognosia (patient’s lack of recognition of any deficits).

Ischaemic strokes are frequently defined by their cause. They may be cardioembolic, such as from atrial fibrillation or intracardiac pathology, or the cause may be artery-to-artery emboli, such as from carotid artery disease, or thrombosis of small perforating arteries, called lacunar strokes. Acute strokes are frequently not seen on initial CT scanning. Treatment in the first several hours after a stroke occurs may include intravenous rtPA or endovascular procedures to remove the arterial blockage.

Haemorrhagic stroke occurs when a cerebral blood vessel ruptures. Depending on the location of the vessel, bleeding may be epidural, subdural, intraparenchymal, intraventricular or subarachnoid (Fig. 6.14). The most common cause of intracerebral haemorrhage is hypertension; other causes include cerebral aneurysms, vascular malformations and amyloid angiopathy. Treatment options for intracerebral haemorrhage are limited and are largely directed toward preventing secondary damage from the haemorrhage mass.

Fig. 6.14 Massive acute hypertensive intracerebral haemorrhage.

Cerebral Bloodflow

The brain is devoid of either glucose stores or a means of storing oxygen and is therefore dependent, minute by minute, on an adequate blood supply. It has a high metabolic rate in comparison with other organs, which reflects the metabolic demands of constant neural activity. The blood supply of grey matter is more copious than that of white matter.

Cerebral bloodflow in the human brain is approximately 50 ml/g/min. Global cerebral bloodflow is autoregulated—that is, it remains constant in normal individuals despite variations in mean arterial blood pressure over a range of approximately 8.7 to 18.7 kPa (65 to 140 mm Hg). If the blood pressure falls below this range, cerebral bloodflow decreases. Alternatively, if the pressure rises above this range, cerebral bloodflow may increase. Arterial and arteriolar intraluminal pressures directly control the contraction of intramural muscle, so an increase in arterial pressure, for example, causes arterial constriction, and bloodflow remains constant.

Although autoregulation normally ensures that global cerebral bloodflow remains constant, regional bloodflow varies in response to the level of neural activity and, thus, to local metabolic demand. This has been demonstrated in many brain areas, including the motor and sensory cortical regions, areas involved in convulsive activity and even cortical areas involved in complex thought processes. The principal local factors affecting regional bloodflow are the local hydrogen ion (H⁺) or carbon dioxide concentration, which causes arterial dilatation.

Not all substances circulating in arterial blood have access to the brain parenchyma. Particulate matter, such as bacteria, is excluded. In general, lipophilic molecules and small molecules, such as oxygen and carbon dioxide, can cross the blood–brain barrier, but hydrophilic ones (excluding glucose) cannot. The cellular basis for the blood–brain barrier is discussed in Chapter 2.

Venous Drainage of the Brain

The venous drainage of the brain occurs through a complex system of deep and superficial veins. These veins possess no valves and have thin walls devoid of muscular tissue. They pierce the arachnoid mater and the inner layer of the dura mater to open into the dural venous sinuses.

Veins of the Brain Stem

The veins of the brain stem form a superficial venous plexus deep to the arteries.

Veins of the medulla oblongata drain into the veins of the spinal cord or the adjacent dural venous sinuses or into variable radicular veins that accompany the last four cranial nerves either to the inferior petrosal or occipital sinuses or to the superior bulb of the jugular vein. Anterior and posterior median medullary veins may run along the anterior median fissure and posterior median sulcus to become continuous with the spinal veins in corresponding positions. Pontine veins, which may include a median vein and a lateral vein on each side, drain into the basal vein, cerebellar veins, petrosal sinuses, transverse sinus or venous plexus of the foramen ovale. Veins of the midbrain join the great cerebral vein or basal vein.

Veins of the Cerebellum

The veins of the cerebellum drain mainly into sinuses adjacent to them or, from the superior surface, into the great cerebral vein. The cerebellar veins course on the cerebellar surface and constitute superior and inferior groups. Superior cerebellar veins either run anteromedially across the superior vermis to the straight sinus or great cerebral vein or run laterally to the transverse and superior petrosal sinuses. Inferior cerebellar veins include a small median vessel running backward on the inferior vermis to enter the straight or sigmoid sinus. Laterally coursing vessels join the inferior petrosal and occipital sinuses.

Veins of the Cerebral Hemisphere

External and internal cerebral veins (Figs 6.15–6.19) drain the surfaces and the interior of the cerebral hemisphere. External cerebral veins may be divided into three groups: superior, middle and inferior.

Fig. 6.15 Cerebral venous system (viewed from the left side) showing the principal superficial and deep veins of the brain and their relationship to the dural venous sinuses. The more deeply placed veins are shown in blue and those inside the brain are shown in interrupted blue.

Fig. 6.16 External (superficial) cerebral veins of the left hemisphere and their relationship to the dural venous sinuses.

Fig. 6.17 Internal (deep) cerebral veins, viewed from above after removal of the central portion of the corpus callosum.

Fig. 6.18 Lateral projection from a magnetic resonance venogram using time-of-flight methods.

(Courtesy of Professor P. D. Griffiths, Academic Unit of Radiology, University of Sheffield.)

Fig. 6.19 Frontal projection from a magnetic resonance venogram using time-of-flight methods.

(Courtesy of Professor P. D. Griffiths, Academic Unit of Radiology, University of Sheffield.)

Eight to 12 superior cerebral veins drain the superolateral and medial surfaces of each hemisphere. They mainly follow the sulci, although some do pass across gyri. They ascend to the superomedial border of the hemisphere, where they receive small veins from the medial surface, and then open into the superior sagittal sinus. Superior cerebral veins in the anterior part of the hemisphere join the sinus almost at right angles. The larger posterior veins are directed obliquely forward, against the direction of flow in the sinus, an arrangement that may resist their collapse when intracranial pressure is raised.

The superficial middle cerebral vein drains most of the lateral surface of the hemisphere and follows the lateral fissure to end in the cavernous sinus. A superior anastomotic vein runs posterosuperiorly between the superficial middle cerebral vein and the superior sagittal sinus, thus connecting the superior sagittal and cavernous sinuses. An inferior anastomotic vein courses over the temporal lobe and connects the superficial middle cerebral vein to the transverse sinus. The deep middle cerebral vein drains the insular region and joins the anterior cerebral and striate veins to form a basal vein. Regions drained by the anterior cerebral and striate veins correspond approximately to those supplied by the anterior cerebral artery and the central branches that enter the anterior perforated substance. The basal veins pass back alongside the interpeduncular fossa and midbrain, receive tributaries from this vicinity and join the great cerebral vein.

Inferior cerebral veins on the orbital surface of the frontal lobe join the superior cerebral veins and thus drain to the superior sagittal sinus. Those on the temporal lobe anastomose with basal veins and middle cerebral veins and drain to the cavernous, superior petrosal and transverse sinuses.

The basal vein begins at the anterior perforated substance by the union of a small anterior cerebral vein, which accompanies the anterior cerebral artery; a deep middle cerebral vein, which receives tributaries from the insula and neighbouring gyri and runs in the lateral cerebral fissure; and striate veins, which emerge from the anterior perforated substance. The basal vein passes back around the cerebral peduncle to the great cerebral vein (see Fig. 6.15) and receives tributaries from the interpeduncular fossa, inferior horn of the lateral ventricle, parahippocampal gyrus and midbrain.

The internal cerebral vein drains the deep parts of the hemisphere and the choroid plexuses of the third and lateral ventricles. It is formed near the interventricular foramen, behind the column of the fornix, primarily by union of the thalamostriate and choroidal veins, although numerous smaller veins from surrounding structures also converge there. The thalamostriate vein runs anteriorly, between the caudate nucleus and thalamus, and receives many tributaries from both. The choroidal vein runs a convoluted course along the whole choroid plexus and receives veins from the hippocampus, fornix, corpus callosum and adjacent structures. After their formation, the two internal cerebral veins travel back parallel to each other, beneath the splenium of the corpus callosum, where they unite to form the great cerebral vein. The great cerebral vein is a short median vessel that curves sharply up around the splenium of the corpus callosum and opens into the anterior end of the straight sinus after receiving the right and left basal veins.

CASE 3 Carotid Cavernous Fistula

A 45-year-old man sustains a minor head injury with fleeting loss of consciousness but no immediate sequelae. Several days later he notes increasing pain in and around the left eye, along with double vision, lid ptosis and protrusion of the affected eye. On examination, he demonstrates unilateral exophthalmos, ptosis, ophthalmoparesis, orbital oedema and papilloedema with retinal haemorrhages. A loud bruit is audible over the left eye. The exophthalmos is pulsatile in character.

Discussion: This man has developed a carotid cavernous fistula secondary to head trauma, with laceration of the carotid artery within the cavernous sinus (Fig. 6.20). In a small proportion of cases the lesion is spontaneous, secondary to rupture of a previously unrecognized carotid aneurysm. Several structures within the cavernous sinus are variously affected, along with the pulsatile exophthalmos, orbital congestion and oedema secondary to involvement of the carotid artery within the sinus itself. The differential diagnosis includes, most importantly, cavernous sinus thrombosis secondary to spread of sepsis from infection in the sinuses or the upper face. Under these circumstances, the patient is generally febrile and acutely ill; physical findings are otherwise much the same as in a traumatic carotid cavernous fistula, as observed in this patient.

Fig. 6.20 Magnetic resonance imaging of a carotid cavernous fistula, demonstrating blood in the cavernous sinus (solid arrow) and dilatation of the ipsilateral superior ophthalmic vein (dashed arrow).

Vascular Supply of the Spine (see also Crock 1996)

Arteries

The vertebral column, its contents and its associated soft tissues all receive their arterial supply from derivatives of dorsal branches of the embryonic intersegmental somatic arteries (Fig. 6.21). The relevant named artery depends on the level of the column. These intersegmental vessels persist in the thoracic and lumbar regions as the posterior intercostal and lumbar arteries. In the cervical and sacral regions, longitudinal anastomoses between the intersegmental vessels persist as longitudinal vessels, which themselves give spinal branches to the vertebral column. In the neck, the postcostal anastomosis becomes most of the vertebral artery, whereas the post-transverse anastomosis forms most of the deep cervical artery. The ascending cervical artery and the lateral sacral artery are persistent parts of the precostal anastomosis.

Fig. 6.21 Arterial supply to the vertebrae and contents of the vertebral canal. A, Branching pattern of lumbar segmental arteries. B, Arterial anastomoses between postcentral branches of spinal arteries within the vertebral canal.

In the thorax and abdomen, the primitive arterial pattern is retained by the paired branches of the descending aorta, which supply the vertebral column (see Fig. 6.21A). On each side, the main trunk of the artery (posterior intercostal or lumbar) passes around the vertebral body, giving off primary periosteal and equatorial branches to the body and then a major dorsal branch. The dorsal branch gives off a spinal branch, which enters the intervertebral foramen before supplying the facet joints, posterior surfaces of the laminae and overlying muscles and skin. There is free anastomosis between these dorsal articular and soft tissue branches, extending over several segments (Crock and Yoshizawa 1976; Boelderl et al 2002). At cervical and sacral levels, the longitudinally running arteries described earlier have direct spinal branches. The spinal branches are the main arteries of supply to all bony elements of the vertebrae and to the dura and epidural tissues; they also contribute to the supply of the spinal cord and nerve roots via radicular branches (see later). As they enter the vertebral canal, the spinal arteries divide into postcentral, prelaminar and radicular branches. The postcentral branches, which are the main nutrient arteries to the vertebral bodies and to the periphery of the intervertebral discs, anastomose beneath the posterior longitudinal ligament with their fellows above and below, as well as across the midline (see Fig. 6.21). This anastomosis also supplies the anterior epidural tissues and dura. The majority of the vertebral arch, the posterior epidural tissues and dura and the ligamentum flavum are supplied by the prelaminar branches and their anastomotic plexus on the posterior wall of the vertebral canal.

Veins

Veins of the vertebral column form intricate plexuses along the entire column, external and internal to the vertebral canal (Fig. 6.22). Both groups are devoid of valves, anastomose freely with each other and join the intervertebral veins. Interconnections are widely established between these plexuses and longitudinal veins early in fetal life. When development is complete, the plexuses drain into the caval and azygos ascending lumbar systems via named veins that accompany the arteries described earlier.

Fig. 6.22 A and B, Venous drainage of the vertebral column.

The veins also communicate with cranial dural venous sinuses and with the deep veins of the neck and pelvis. The venous complexes associated with the vertebral column can dilate considerably and can form alternative routes of venous return in patients with major venous obstruction in the neck, chest or abdomen. The absence of valves allows pathways for the wide and sometimes paradoxical spread of malignant disease and sepsis. Pressure changes in the body cavities are transmitted to these venous plexuses and thus to the CSF, although the cord itself may be protected from such congestion by valves in the small veins that drain from the cord into the internal vertebral plexus.

External Vertebral Venous Plexuses

The external vertebral venous plexuses are anterior and posterior. They anastomose freely and are most developed in the cervical region. Anterior external plexuses are anterior to the vertebral bodies, communicate with basivertebral and intervertebral veins and receive tributaries from vertebral bodies. Posterior external plexuses lie posterior to the vertebral laminae and around spinous, transverse and articular processes. They anastomose with the internal plexuses and join the vertebral, posterior intercostal and lumbar veins.

Internal Vertebral Venous Plexuses

The internal vertebral venous plexuses occur between the dura mater and vertebrae and receive tributaries from the bones, red bone marrow and spinal cord. They form a denser network than the external plexuses and are arranged vertically as four interconnecting longitudinal vessels, two anterior and two posterior.

The anterior internal plexuses are large plexiform veins on the posterior surfaces of the vertebral bodies and intervertebral discs. They flank the posterior longitudinal ligament, beneath which they are connected by transverse branches into which the large basivertebral veins open. The posterior internal plexuses, on each side in front of the vertebral arches and ligamenta flava, anastomose with the posterior external plexuses via veins that pass through and between the ligaments. The internal plexuses interconnect by venous rings near each vertebra. Around the foramen magnum they form a dense network connecting with vertebral veins, occipital and sigmoid sinuses, the basilar plexus, the venous plexus of the hypoglossal canal and the condylar emissary veins.

Basivertebral Veins

The basivertebral veins emerge from the posterior foramina of the vertebral bodies. They are large and tortuous channels in bone, like those in the cranial diploë. The basivertebral veins also drain into the anterior external vertebral plexuses through small openings in the vertebral bodies. Posteriorly, they form one or two short trunks that open into the transverse branches and unite the anterior internal vertebral plexuses. They enlarge in advanced age.

Intervertebral Veins

The intervertebral veins accompany the spinal nerves through intervertebral foramina, draining the spinal cord and internal and external vertebral plexuses and ending in the vertebral, posterior intercostal, lumbar and lateral sacral veins. Upper posterior intercostal veins may drain into the caval system via brachiocephalic veins, whereas the lower intercostals drain into the azygos system. Lumbar veins are joined longitudinally in front of the transverse processes by the ascending lumbar veins, in which they may terminate. Alternatively, they may proceed around the vertebral bodies to drain into the inferior vena cava. Whether the basivertebral or intervertebral veins contain effective valves is uncertain, but experimental evidence strongly suggests that their bloodflow can be reversed (Batson 1957). This may explain how pelvic neoplasms (e.g. prostate carcinoma) may metastasize in vertebral bodies: the cells spread into the internal vertebral plexuses via their connections with the pelvic veins when bloodflow is temporarily reversed by raised intra-abdominal pressure or postural alterations.

Vascular Supply of Spinal Cord, Roots and Nerves

Arteries

The spinal cord, its roots and nerves are supplied with blood by both longitudinal and segmental vessels. Three major longitudinal vessels—a single anterior and two posterior spinal arteries (each of which is sometimes doubled to pass on either side of the dorsal rootlets)—originate intracranially from the vertebral artery and terminate in a plexus around the conus medullaris (Fig. 6.23). The anterior spinal artery forms from the fused anterior spinal branches of the vertebral artery and descends in the anterior median fissure of the cord. Each posterior spinal artery originates either directly from the ipsilateral vertebral artery or from its posterior inferior cerebellar branch and descends in a posterolateral sulcus of the cord. The segmental arteries are derived in craniocaudal sequence from spinal branches of the vertebral, deep cervical, intercostal and lumbar arteries. These vessels enter the vertebral canal through the intervertebral foramina and anastomose with branches of the longitudinal vessels to form a pial plexus on the surface of the cord. The segmental spinal arteries send anterior and posterior radicular branches to the spinal cord along the ventral and dorsal roots. Most anterior radicular arteries are small and end in the ventral nerve roots or in the pial plexus of the cord. The small posterior radicular arteries also supply the dorsal root ganglia; branches enter at both ganglionic poles to be distributed around ganglion cells and nerve fibres.

Fig. 6.23 Arteries of the spinal cord.

Segmental Medullary Feeder Arteries

Some radicular arteries, mainly situated in the lower cervical, lower thoracic and upper lumbar regions, are large enough to reach the anterior median sulcus, where they divide into slender ascending and large descending branches. These are the anterior medullary feeder arteries (Dommisse 1975). They anastomose with the anterior spinal arteries to form a single or partly double longitudinal vessel of uneven calibre along the anterior median sulcus. The largest anterior medullary feeder, the great anterior segmental medullary artery of Adamkiewicz, varies in level, arising from a spinal branch of one of the lower posterior intercostal arteries (T9–11) or subcostal artery (T12) or, less frequently, a spinal branch of the upper lumbar arteries (L1 and L2). It most often arises on the left side (Carmichael and Gloviczki 1999). Reaching the spinal cord, it sends a branch to the anterior spinal artery below and another to anastomose with the ramus of the posterior spinal artery, which lies anterior to the dorsal roots. It may be the main supply to the lower two-thirds of the cord. Central branches of the anterior spinal artery enter the anterior median fissure and then turn right or left to supply the ventral grey column, the base of the dorsal grey column, including the dorsal nucleus, and the adjacent white matter (Fig. 6.24).

Fig. 6.24 Arterial disposition within the spinal cord.

Each posterior spinal artery contributes to a pair of longitudinal anastomotic channels, anterior and posterior to the dorsal spinal roots. These are reinforced by posterior medullary feeders from the posterior radicular arteries. The latter are variable in number and size but are smaller, more numerous and more evenly distributed than the anterior medullary feeders. The anterior channel is joined by a ramus from the descending branch of the great anterior segmental medullary artery of Adamkiewicz. In all longitudinal spinal arteries, the width of the lumen is uneven, and complete interruptions may occur. At the conus medullaris, they communicate by anastomotic loops. Anastomoses other than those between the pial or peripheral spinal arterial branches may be important, such as a posterior spinal series of anastomoses between rami of the dorsal divisions of segmental arteries near the spinous processes.

Intramedullary Arteries

The central branches of the anterior spinal artery supply about two-thirds of the cross-sectional area of the cord. The rest of the dorsal grey and white columns and peripheral parts of the lateral and ventral white columns are supplied by numerous small radial vessels that branch from posterior spinal arteries and the pial plexus. In a microangiographic study of the human cervical spinal cord, up to six anterior and eight posterior radicular spinal arteries were described, and up to eight central branches arose from each centimetre of the anterior spinal artery (Turnbull, Brieg and Hassler 1966).

Spinal Cord Ischaemia

The spinal cord cannot rely entirely on the longitudinal arteries for either its transverse or its longitudinal blood supply. The anterior longitudinal artery and the intramedullary arteries are functional end-arteries, although overlapping territories of supply have been described. Damage to the anterior longitudinal artery can result in loss of function of the anterior two-thirds of the cord. The longitudinal arteries cannot supply the whole length of the cord, and the input of the segmental medullary feeder vessels is essential. This is especially true of the artery of Adamkiewicz (great anterior segmental medullary artery), which may effectively carry the major supply for the lower cord. The midthoracic cord, distant from the main anterior medullary feeders, is particularly liable to become ischaemic after periods of hypotension.

Veins

The venous drainage of the spinal cord (Fig. 6.25) follows a similar pattern to that of its arterial supply (Gillilan 1970). Intramedullary veins within the substance of the cord drain into a plexus of surface veins, the coronal plexus. There are six tortuous longitudinal channels within this plexus—one in each of the anterior and posterior median fissures, and four others that run on either side of the ventral and dorsal nerve roots. Only the anterior median vein, which drains the central grey matter, is consistently complete. These vessels connect freely. They drain superiorly into the cerebellar veins and cranial sinuses and segmentally into mainly the medullary veins. These segmental veins drain into the intervertebral veins and then into the external vertebral venous plexuses, the caval and azygos systems.