10 406 · 10 Coverings of the Brain and Spinal Cord; Cerebrospinal Fluid and Ventricular System

Pia Mater

The pia mater consists of thin layers of mesodermal cells resembling endothelium. Unlike the arachnoid, it covers not just the entire externally visible surface of the brain and spinal cord but also all of the hidden surfaces in the depths of the sulci (Figs. 10.1 and 10.2). It is fixed to the central nervous tissue beneath it by an ectodermal membrane consisting of marginal astrocytes (pialglial membrane). Blood vessels that enter or leave the brain and spinal cord by way of the subarachnoid space are surrounded by a funnel-like sheath of pia mater. The space between a blood vessel and the pia mater around it is called the Virchow­Robin space.

The sensory nerves of the pia mater, unlike those of the dura mater, do not respond to mechanical or thermal stimuli, but they are thought to respond to vascular stretch and changes in vascular wall tone.

Cerebrospinal Fluid and Ventricular System

Structure of the Ventricular System

The ventricular system (Fig. 10.3) consists of the two lateral ventricles (each of which has a frontal horn, central portion = cella media, posterior horn, and inferior horn); the narrow third ventricle, which lies between the two halves of the diencephalon; and the fourth ventricle, which extends from pontine to medullary levels. The lateral ventricles communicate with the third ventricle through the interventricular foramina (of Monro); the third ventricle, in turn, communicates with the fourth ventricle through the cerebral aqueduct. The fourth ventricle empties into the subarachnoid space through three openings: the single median aperture (foramen of Magendie) and the paired lateral apertures (foramina of Luschka).

Cerebrospinal Fluid Circulation and Resorption

Properties of the cerebrospinal fluid. Thenormalcerebrospinalfluidisclearand colorless, containing only a few cells (up to 4/μl) and relatively little protein (ratio of CSF albumin to serum albumin = 6.5 ± 1.9 × 10­3). Its composition differs from that of blood in other respects as well. The cerebrospinal fluid is not an ultrafiltrateofblood;rather,itisactivelysecretedbythechoroidplexus,mainlywithin the lateral ventricles. The blood within the capillaries of the choroid plexus is separated from the subarachnoid space by the so-called blood­CSF barrier, which consists of vascular endothelium, basal membrane, and plexus epithe-

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	Cerebrospinal Fluid and Ventricular System · 407 10
	Interventricular
	foramen
	Corpus callosum	Fornix
		Suprapineal
		recess
		Pineal body
		Collateral
		trigone
Anterior horn of
lateral ventricle		Posterior horn of
	Third ventricle	lateral ventricle
	Optic recess
	Infundibular recess
	Inferior horn of
	lateral ventricle
	Cerebral aqueduct
	and fourth ventricle
	Lateral recess and
	lateral aperture of	Median aperture
Lateral	fourth ventricle
ventricles		of fourth ventricle

Third ventricle

Fourth ventricle

Fig. 10.3Ventricularsystem.aPosition of the ventricular system in the brain. bAnatomical structure.

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10 408 · 10 Coverings of the Brain and Spinal Cord; Cerebrospinal Fluid and Ventricular System

Choroid plexus of the lateral ventricle

	Interhemispheric	Arachnoid
	cistern
		granulations
		Choroid plexus of
		the third ventricle
		Transverse
		cistern

			Ambient
Interven-			cistern
tricular foramen		Vermian cistern
	Chiasmatic cistern
Basal
cistern	Interpeduncular cistern	Choroid plexus of the
	Cerebral aqueduct
		fourth ventricle
	Ponto-	Cerebellomedullary
	medullary cistern

cistern with median aperture of the fourth ventricle

Fig. 10.4 Circulation of the cerebrospinal fluid

lium. This barrier is permeable to water, oxygen, and carbon dioxide, but relatively impermeable to electrolytes and completely impermeable to cells.

The circulating CSF volume is generally between 130 and 150 ml. Every 24 hours 400­500 ml of CSF are produced; thus, the entire CSF volume is exchanged three or four times daily. The CSF pressure (note that the CSF pressure is not the same as the intracranial pressure) in the supine position is normally 70­120 mmH2O.

Infectious or neoplastic processes affecting the CNS alter the composition of the cerebrospinal fluid in characteristic ways, as summarized in Table 10.1.

Circulation. The CSF is produced by the choroid plexus of the lateral ventricles, third ventricle, and fourth ventricle (Fig. 10.4). It flows through the foramina of

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Cerebrospinal Fluid and Ventricular System · 409 10

Tabelle 10.1	CSF Findings in Diseases of the Central Nervous System
Diagnosis	Appearance	Pandy	Cell Count,	Biochemistry	Other Findings
		Reaction	Cytology
Normal lum-	Clear, color-	—	Up to 4 cells/	Lactate	Glucose 50−
bar CSF	less		μl, mainly	2.1 mmol/l.	60 % of blood
			lymphocytes	Albumin quotient:	level
			(85 %)	Adults over 40
				years, 8; under
				40 years, 7;
				children under 15
				years, 5
Purulent	Turbid	+++	Several thou-	Lactate	Demonstration
(bacterial)			sand/μl,	3.5 mmol/l;	of bacteria
meningitis			mainly	albumin quotient
			neutrophils	20 × 10−3
Brain	Clear,	+/-	A few	Albumin quotient	Low glucose,
abscess	occasionally		hundred/μl,	normal or mildly	bacteria
	turbid		mononuclear	elevated	sometimes
			cells and/or		demonstrable,
			neutrophils		local IgA
					synthesis
Encephalitis	Clear, color-	+/-	Normal or	Albumin quotient	IgG, IgM, IgA
(herpes	less		mononuclear	10 × 10-3	elevated; de-
simplex)			pleocytosis		monstration of
			(lympho-		specific Ab, PCR
			cytes)		positive for HSV
Viral	Clear	+	Up to several	Albumin quotient
meningitis			hundred	up to 20 × 10−3;
			mononuclear	lactate
			cells, includ-	3.5 mmol/l
			ing activated
			B lympho-
			cytes

Tuberculous	Yellow-tinged	+++	Up to 1500/	Albumin quotient
meningitis			μl, mixed	20 × 10−3;
			cellular pic-	glucose 50 % of
			ture, mostly	serum glucose
			mononuclear
			cells
Neuro-	Clear or tur-	+/-	Mononuclear
syphilis	bid		pleocytosis

IgG and IgA elevated; mycobacteria demonstrated by culture and PCR

Immunoglobulins elevated, TPHA positive

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10 410 · 10 Coverings of the Brain and Spinal Cord; Cerebrospinal Fluid and Ventricular System

Tabelle 10.1	(Continued) CSF Findings in Diseases of the Central Nervous System
Diagnosis	Appearance	Pandy	Cell Count,	Biochemistry	Other Findings
		Reaction	Cytology
Diagnosis	Appearance	Pandy	Cell Count,	Biochemistry	Other Findings
		Reaction	Cytology
Multiple	Clear, color-	+/-	Up to 40	Albumin quotient	Oligoclonal
sclerosis	less		mononuclear	20 × 10−3	bands revealed
			cells/μl		by isoelectric
					focusing
Acute neu-	Clear		Up to a few	Albumin quotient	Immunoglobu-
roborreliosis			hundred	50 × 10−3	lins elevated,
(Lyme dis-			mononuclear		demonstration
ease)			cells/μl		of antibody
Fungal	Clear		Up to a few		Immunoglobu-
meningitis			hundred		lins elevated,
			mononuclear		demonstration
			cells/μl		of fungi by cul-
					ture and special
					stains
Polyradiculi-	Clear		No more than	Albumin quotient
tis (Guillain-			mild pleocy-	up to 50 × 10−3
Barré syn-			tosis	(“albumino-cyto-
drome)				logical dissocia-
				tion”)

Luschka and Magendie (Figs. 10.3b and 10.4) into the subarachnoid space, circulates around the brain, and flows down into the spinal subarachnoid space surrounding the spinal cord. Some of the CSF is resorbed at spinal levels (see below). The composition of the CSF is the same at all points; it is not more dilute or more concentrated at either end of the pathway.

Resorption. CSF is resorbed (i.e., removed from the subarachnoid space) intracranially and along the spinal cord. Some of the CSF leaves the subarachnoid space and enters the bloodstream through the many villous arachnoid granulations located in the superior sagittal sinus and in the diploic veins of the skull. The remainder is resorbed in the perineural sheaths of the cranial and spinal nerves, where these nerves exit the brainstem and spinal cord, respectively, and across the ependyma and capillaries of the leptomeninges.

Thus, CSF is constantly being produced in the choroid plexuses of the ventricles and resorbed again from the subarachnoid space at various locations.

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Bottlenecks of the CSF circulation. As it flows through the ventricular system, the CSF must traverse a number of narrow passageways: the interventricular foramina, the slender third ventricle, the cerebral aqueduct (narrowest point!), and the exit foramina of the fourth ventricle and the tentorial aperture.

Disturbances of Cerebrospinal Fluid Circulation—

Hydrocephalus

General aspects of pathogenesis. Many different diseases cause an imbalance of CSF production and resorption. If too much CSF is produced or too little is resorbed, the ventricular system becomes enlarged (hydrocephalus). Elevated CSF pressure in the ventricles leads to displacement, and eventually atrophy, of the periventricular white matter, while the gray matter is not affected, at least at first. As animal experiments have shown, hydrocephalus causes seepage (diaedesis) of CSF through the ventricular ependyma into the periventricular white matter. The elevated hydrostatic pressure in the white matter impairs tissue perfusion, causing local tissue hypoxia, damage to myelinated nerve pathways, and, ultimately, irreversible gliosis. The histological and clinical abnormalities caused by hydrocephalus can regress only if the intraventricular pressure is brought back to normal in timely fashion.

Types of Hydrocephalus

Different clinical varieties of hydrocephalus can be conveniently classified by etiology, by the site where CSF flow is blocked, and by the dynamic status of the pathological process (e. g., active hydrocephalus due to congenital aqueductal stenosis).

Classification by etiology and pathogenesis. Hydrocephalus due to obstruction of the CSF pathways is called occlusive hydrocephalus, while that due to inadequate CSF resorption is called malresorptive hydrocephalus (see Fig. 10.6). Occlusive hydrocephalus is typically due to an intracranial space-occupying lesion (e. g., tumor, infarct, or hemorrhage, particularly in the posterior fossa) or malformation (e. g., aqueductal stenosis, colloid cyst of the third ventricle). Malresorptive hydrocephalus often arises in the aftermath of subarachnoid hemorrhage and meningitis, both of which can produce occlusive adhesions of the arachnoid granulations. Hydrocephalus can also result from traumatic brain injury and intraventricular hemorrhage. Hypersecretory hydrocephalus, due to overproduction of CSF, is much rarer; it is usually caused by a tumor (papilloma) of the choroid plexus.

Older, alternative, and essentially synonymous terms for malresorptive and occlusive hydrocephalus are “communicating” and “noncommunicating” hy-

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10 412 · 10 Coverings of the Brain and Spinal Cord; Cerebrospinal Fluid and Ventricular System

drocephalus, respectively. In communicating hydrocephalus, the CSF circulates freely from the ventricular system to the subarachnoid cisterns. In noncommunicating hydrocephalus, there is an obstruction to CSF flow within the ventricular system, so that the connection from the ventricles to the CSF-re- sorbing structures is no longer patent, or can only be kept open under abnormally high pressure.

Classification by dynamics. Hydrocephalus is called active if the intraventricular pressure is continuously elevated. There are two types of active hydrocephalus. In compensated active hydrocephalus, the ventricular size and the patient’s symptoms and signs remain constant over time; in uncontrolled hydrocephalus, the patient’s condition worsens while the ventricles continue to enlarge. Active hydrocephalus is not the same as normal pressure hydrocephalus (see below), in which the CSF pressure is only intermittently elevated.

Normal pressure hydrocephalus (NPH). NPH is a special case among types of hydrocephalus, generally involving communicating hydrocephalus with abnormal CSF flow dynamics and only intermittently elevated intraventricular pressure. The characteristic clinical triad of NPH consists of apraxic gait disturbance, dementia, and urinary incontinence (Case Presentation 1). Its cause is unclear; it may be the common clinical expression of a number of different disease processes (aqueductal stenosis, malresorptive hydrocephalus, etc.).

Differential diagnosis: “hydrocephalus ex vacuo.” Degenerative diseases of the brain, such as Alzheimer disease and Pick disease, cause brain atrophy, with secondary enlargement of the internal and external CSF spaces. This may create the impression of hydrocephalus. Strictly speaking, however, hydrocephalus is present only when the internal CSF spaces (i.e., the ventricular system) are enlarged out of proportion to the external spaces, and not when both are enlarged by atrophy. The older term “hydrocephalus ex vacuo” for the latter condition is, therefore, not recommended. Unlike NPH, in which the ventricles are enlarged but the sulci are of relatively normal width, neurodegenerative diseases cause enlargement of the internal and external CSF spaces to a roughly comparable extent.

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Case Presentation 1: Normal Pressure Hydrocephalus

This retired 80-year-old man suffered for several months from urge incontinence, which was initially attributed to his benign prostatic hypertrophy. Over time, however, other symptoms developed: he felt unsteady while walking, walked with his feet wide apart, and fell multiple times. He sometimes complained that he could barely lift his feet off the ground. His family physician ordered an MRI scan of the head (Fig. 10.5) and, after viewing the images, referred him for admission to the hospital. The patient’s wife, in response to the specific questions of the admitting neurologist, reported that he had become increasingly forgetful and inattentive in recent months. Neurological examination revealed an unsteady, apraxic gait.

The clinical and radiological diagnosis was normal pressure hydrocephalus (NPH).

Transient improvement of gait after removal of a large quantity of cerebrospinal fluid is considered to confirm the diagnosis of NPH. Even in this 80-year-old patient, a lumbar puncture and removal of 40 ml of cerebrospinal fluid resulted in marked improvement of gait, as well as complete resolution of urinary incontinence. His cognitive difficulties were unchanged, however. He was transferred to the neurosurgical service for the insertion of a shunt. In the ensuing months, his gait became normal and his urinary incontinence resolved completely. His cognitive difficulties remained, but did not progress.

a

b

c

Fig. 10.5 Normal pressure hydrocephalus (NPH)

(communicating hydrocephalus), as seen on MRI. Axial T2-weighted FLAIR image (a), coronal image (b), and sagittal T2-weighted spin-echo image (c). The ventricles are disproportionately enlarged in relation to the subarachnoid space. The sagittal image (c) reveals low signal intensity in the aqueduct and neighboring portions of the third and fourth ventricles (arrow) because of rapid CSF flow (“flow void”). Recent studies have shown that CSF pulsatility is greater than normal, as a rule, in patients with NPH. The images are mildly blurred because of patient movement; persons with NPH and other dementing illnesses are often unable to cooperate fully with MRI studies.

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10 414 · 10 Coverings of the Brain and Spinal Cord; Cerebrospinal Fluid and Ventricular System

General Aspects of the Clinical Presentation, Diagnostic Evaluation, and Treatment of Hydrocephalus

Epidemiology. Many types of hydrocephalus begin in childhood, usually accompanying other abnormalities of development, such as the Chiari malformation, spina bifida, or meningo(myelo)cele. The prevalence of hydrocephalus in the first three months of postnatal life is 0.1­0.4%.

Manifestations in children. The cranial sutures do not close until one year after birth; throughout the first year of life, the skull bones can respond to elevated intracranial pressure by spreading wider apart. Thus, the most obvious clinical sign of childhood hydrocephalus is abnormal growth of the head, with disproportionate enlargement of the skull in relation to the face. Further signs include gaping cranial sutures, stasis of the scalp veins, frontal bossing, and tightly bulging fontanelles. Percussion of the head produces a rattling sound (MacEwen sign). The affected children appear well at first, because the intracranial pressure is only mildly raised as long as the sutures are open and the head is still able to expand. Decompensation occurs later, giving rise to signs of intracranial hypertension, including vomiting (including projectile vomiting and dry heaves). These children may also present with the sunset phenomenon (upward gaze paresis) and general failure to thrive.

Diagnostic evaluation in children. At present, hydrocephalus can be diagnosed before birth by routine prenatal ultrasonography. Hydrocephalus arising after birth is detected by routine serial measurement and documentation of the child’s head circumference: if the head grows faster than normal (according to the reference curves on the chart), then hydrocephalus should be suspected, and further diagnostic studies should be done to guide potential treatment. After birth, children with hydrocephalus are evaluated not just with ultrasound but also with CT and MRI. This enables the identification of potential treatable causes of hydrocephalus, as well as other potential causes of disproportionate growth of the head, such as subdural hematomas and hygromas, and familial macrocephaly.

Manifestations in adults. In children with closed sutures, and in adults, hydrocephalus presents with manifestations of intracranial hypertension, including headache, nausea, and vomiting (particularly morning dry heaves and projectile vomiting), and signs of meningeal irritation, including nuchal rigidity, head tilt, opisthotonus, and photophobia. As the condition progresses, further manifestations may include fatigue, cognitive decline, unsteady gait, cranial nerve deficits (particularly abducens palsy), Parinaud syndrome, papilledema, and impairment of consciousness.

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Cerebrospinal Fluid and Ventricular System · 415 10

Diagnostic evaluation in adults. CT and MRI readily demonstrate ventricular enlargement and often reveal the cause of hydrocephalus.

Treatment. If no underlying, treatable cause of hydrocephalus can be identified, the elevated intraventricular pressure can be relieved by the insertion of a cerebrospinal fluid shunt. Many different types of shunts are available; for further information, the reader is directed to textbooks of neurosurgery.

Case Presentation 2: Malresorptive Hydrocephalus after Subarachnoid Hemorrhage (SAH)

This 52-year-old man was admitted to the hospital because of an acute, severe headache— the worst headache of his life—and mild somnolence. A CT scan of the head revealed the cause: acute subarachnoid hemorrhage (SAH). Cerebral angiography showed the source of bleeding to be a ruptured aneurysm of the left

middle cerebral artery. The blood in the subarachnoid space blocked the outflow and resorption of CSF, leading to widening of the ventricles (hydrocephalus, Fig. 10.6). A temporary external ventricular drain was inserted to treat the hydrocephalus, and the aneurysm was then clipped in an open neurosurgical procedure.

a

b

Fig. 10.6 Malresorptive hydrocephalus after aneurysmal subarachnoid hemorrhage (SAH); CT of head. The subarachnoid space is filled with hyperdense (bright) blood (a), which impairs CSF circulation and resorption. The ventricles are dilated, particularly the temporal horns (b). The ventricles are black in the CT scan because they contain very little blood. A small amount of blood has entered the ventricular system by reflux and can be seen in the posterior horns of the lateral ventricles (blood−CSF levels, arrows, b).

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417 11

11 Blood Supply

and Vascular

Disorders of the

Central Nervous

System

Arteries of the Brain . . . . . . . . . . . 419

Veins of the Brain . . . . . . . . . . . . . 435

Blood Supply of the Spinal Cord . 439

Cerebral Ischemia . . . . . . . . . . . . . 443

Intracranial Hemorrhage . . . . . . . 477

Vascular Syndromes

of the Spinal Cord . . . . . . . . . . . . . 489

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11 418

11Blood Supply and Vascular Disorders of the Central Nervous System

Thecerebralbloodsupplyisderivedfromtheinternal carotidandvertebral arteries The internal carotid artery on either side delivers blood to the brain through its major branches, the middle and anterior cerebral arteries and the anterior choroidal artery (anterior circulation). The two vertebral arteries uniteinthemidlineatthecaudalborderoftheponstoformthebasilarartery, whichdeliversbloodtothebrainstemandcerebellum,aswellastopartofthe cerebralhemispheresthroughitsterminalbranches,theposteriorcerebralarteries (posterior circulation). The anterior and posterior circulations communicate with each other through the arterial circle of Willis. There are also many other anastomotic connections among the arteries supplying the brain, and between the intracranial and extracranial circulations; thus, occlusion of amajorvesseldoesnotnecessarilyleadtostroke,becausethebraintissuedistal to the occlusion may be adequately perfused by collateral vessels.

The venous blood of the brain flows from the deep and superficial cerebral veins into the venous sinuses of the dura mater, and thence into the internal jugular veins on both sides.

Protracted interruption of blood flow to a part of the brain causes loss of function and, finally, ischemic necrosis of brain tissue (cerebral infarction). Cerebral ischemia generally presents with the sudden onset of a neurological deficit(hencetheterm“stroke”),duetolossoffunctionoftheaffectedpartof thebrain.Sometimes,however,thedeficitappearsgraduallyratherthansuddenly.Themostcommoncausesofischemiaonthearterialsideofthecerebral circulationareemboli (usuallyarisingfromtheheartorfromanatheromatous plaque,e. g.,intheaortaorcarotidbifurcation)anddirectocclusionofsmallor middle-sizedvesselsbyarteriolosclerosis(cerebral microangiopathy,usually due to hypertension). Cerebral ischemia can also be due to impairment of venous drainage (cerebral venous or venous sinus thrombosis).

Another cause of the stroke syndrome is intracranial hemorrhage, which may be either into the brain parenchyma itself (intracerebral hemorrhage) or into the neighboring meningeal compartments (subarachnoid, subdural, and epidural hemorrhage and hematoma).

Theblood supply of the spinal cord ismainlysuppliedbytheunpairedanteriorspinalarteryandthepairedposterolateralspinalarteriesTheanteriorspinalarteryreceivescontributionsfrommanysegmentalarteries.Likethebrain, the spinal cord can be damaged by hemorrhage or by ischemia of arterial or venous origin.

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Arteries of the Brain · 419 11

Arteries of the Brain

Extradural Course of the Arteries of the Brain

Four great vessels supply the brain with blood: the right and left internal carotid arteries and the right and left vertebral arteries. The internal carotid arteries are of the same caliber on both sides, but the two vertebral arteries are often of very different sizes in a single individual. All of the arteries supplying the brain are anastomotically interconnected at the base of the brain through the arterial circle of Willis. They are also interconnected extracranially through small branches in the muscles and connective tissue, which may become important in certain pathological processes affecting the vasculature, but which are normally too small to be demonstrated.

Thestructuresoftheanteriorandmiddlecranialfossaearemainlysuppliedby the internal carotid arteries (the so-called anterior circulation), while the structuresoftheposteriorfossaandtheposteriorportionofthecerebralhemispheres aremainlysuppliedbythevertebralarteries(theso-calledposteriorcirculation).

Common carotid artery. The internal carotid artery is one of the two terminal branches of the common carotid artery, which, on the right side, arises from the aorticarchinacommon(brachiocephalic)trunkthatitshareswiththerightsubclavian artery (Fig. 11.1). The left common carotid artery usually arises directly from the aortic arch, but there are frequent anatomical variants. In 20% of individuals,theleftcommoncarotidarteryarisesfromaleftbrachiocephalictrunk.

The internal carotid artery originates at the bifurcation of the common carotid artery at the level of the thyroid cartilage and ascends to the skull base without giving off any major branches. It passes through the carotid canal of the petrous bone, where it is separated from the middle ear only by a thin, bony wall, and then enters the cavernous sinus (Fig. 11.1). For its further intracranial course, see p. 421.

Anastomotic connections of the arteries of the brain with the external carotid artery.

The second branch of the common carotid artery, the external carotid artery, supplies the soft tissues of the neck and face. It makes numerous anastomotic connections with the opposite external carotid artery, as well as with the vertebral arteries (see Fig. 11.11, p. 433) and the intracranial territory of the internal carotid artery (e. g., through the ophthalmic artery [Fig. 11.11] or the inferolateral trunk, see p. 432). These connections can dilate in the setting of slowly progressive stenosis or occlusion of the internal carotid artery, thereby assuring continued delivery of blood to the brain.

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11 420 · 11 Blood Supply and Vascular Disorders of the Central Nervous System

	Basilar a.
Posterior cerebral a.	Posterior
	communicating a.
Superior cerebellar a.	Middle cerebral a.
Anterior inferior	Anterior cerebral a.
cerebellar a.
	Ophthalmic a.
	Cavernous sinus
	Internal carotid a.
	Superficial
	temporal a.
	Maxillary a.
	Facial a.
Posterior inferior	Lingual a.
cerebellar a.
Vertebral a.

Superior thyroid a.

Common carotid a.

Subclavian a.

Brachiocephalic

trunk

Aorta

Fig. 11.1 Extracranial course of the major arteries supplying the brain (common carotid artery, vertebral artery)

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