JOURNAL OF THE NEUROLOGICAL SCIENCES 307

The Special Clinical Problem of Symptomatic Hydrocephalus

with Normal Cerebrospinal Fluid Pressure
Observations on Cerebrospinal Fluid Hydrodynamics

S. HAKIM AND R. D. ADAMS

Department of Neurology, National University of Bogota (Colombia);

Department of Neurology-Neuropathology, Harvard Medical School, and the Neurology Service,
Massachusetts General Hospital, Boston, Mass. ( U. S. A.)

INTRODUCTION

In recent years we have observed in 3 patients a paradoxical condition of cerebro-

spinal fluid dynamics in which symptomatic hydrocephalus was associated with normal
cerebrospinal fluid pressure. Each of these patients had exhibited aprogressive neurol-
ogical syndrome with prominent mental symptomatology which was evidently
related to a communicating type of hydrocephalus; and, although the initial lumbar
cerebrospinal pressures were normal, a lowering of the pressure by means of repeat-
ed lumbar punctures or the performance of a ventriculo-atrial shunt resulted in
unexpected clinical improvement. These observations are being reported in order
that other neurological physicians and surgeons may avoid the mistake which we
have several times made, of misdiagnosing an occult hydrocephalic state as traumatic
encephalopathy or presenile or senile dementia.
In considering possible explanations of this condition of symptomatic hydro-
cephalus with normal cerebrospinal fluid pressure, an important physical principle
would seem to be involved - - that the effective expansile force within the ventricles
is not equivalent to the intraventricular pressure, but is a product of the ventricular
pressure and ventricular area. From this it follows that the larger the surface area of
the ventricular system, the lower may be the pressure which still is effective in pro-
ducing symptoms of cerebral impairment. This aspect of cerebrospinal fluid hydro-
dynamics appears to have been neglected and we have found no reference to it in the
medical literature.

PRESENTATION OF CASES

Case 1

Male, age 16 years, patient at Hopital San Juan de Dios, Neurological Service. Head
injury in an adolescent. Initial improvement followed by worsening of state of

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308 s. HAKIM, R. D. ADAMS

consciousness and appearance of left hemiparesis. Removal of small right subdurtll

hematoma. Several weeks' period of intermittent impairment of consciousness with
normal CSF pressure. Demonstration of communicating hydrocephalus. Improve-
ment consequent to repeated lumbar punctures with drainage of CSF and finally to
ventriculo-atrial shunt. Full recovery.

History and examination

In late December, 1957 this adolescent boy was struck by a motor car and suffered
a severe head injury. Although immediately rendered unconscious, by the time he
arrived at the hospital (1-2 hr later) his condition had improved somewhat in that he
was then confused and agitated. His pupils were noted to be small and equal and
reacted slightly to light. The eyes moved conjugately from side to side. Blood pressure
was 80/60, pulse 115, respirations 20 and regular. A 3 cm laceration was noted in the
right fronto-temporal region, but X-rays of the skull showed no fracture. There was
edema and bruising of the right cheek.
During the first few hours in the hospital the patient remained alternately agitated
and drowsy. He vomited once. One brief seizure was observed, consisting of a shaking
of the left arm and simultaneous dilatation of the pupils. The tendon reflexes were at
all times difficult to elicit; the plantar reflexes were flexor on right and questionably
extensor on left. His response to painful stimuli on the two sides of the body was approx-
imately the same, though on a few occasions it seemed slightly more active on the
right side. Antibiotic therapy, oxygen, intravenous fluids, and 0.1 g phenobarbital
were administered. At the end of the fourth hour the right pupil had dilated and the
patient was unresponsive, reacting only to very painful stimuli by withdrawal of
limbs. There was now an evident left hemiparesis and the plantar reflex was extensor
on the left side.
In view of this rapid worsening in the patient's condition, a right carotid arterio-
gram was performed with the demonstration of an avascular area over the convexity
of the right hemisphere and a separation of the cortical and meningeal vessels from
the inner table of the skull. The patient was taken at once to the operating room and
a posterior frontal burr-hole was made. The dura appeared bluish and under tension;
and when it was incised, a small amount of blood clot escaped. After the subdural
space was washed with warm saline, the brain was observed to expand. The cerebral
cortex in this region appeared to be contused, and there was subarachnoid hemorrh-
age.
By the following day the patient's condition had improved. He was more responsive
to painful stimuli but still did not speak. He lay with eyes closed. The pupils were of
medium size and reacted to light; the eyes tended to deviate slightly towards the right.
The left plantar was extensor, the right flexor. The blood pressure was now 100/65,
pulse 100, temperature 37.5°C, respirations 18 and regular. Some degree of neck
stiffness on forward bending was noted. The medical regimen now consisted of
terramycin, 100 mg intramuscularly every 6 hours, and 5 % glucose in a quantity
of 1500 ml/day. After the second day he was fed through a stomach tube. The pheno-
barbital was continued in a dose of 50 mg 3 times a day.
Thereafter the patient's condition seemed to stabilize temporarily. Vital signs re-

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 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINALFLUID PRESSURE 309

mained normal. Extraocular movements became full. Pupillary reactions were normal.
At times he opened his eyes, looked at individuals a r o u n d him, moved all four extre-
mities, but still did not vocalize or communicate by speech. Believing that this con-
dition might last for a time, the patient was sent to his home for further convalescence.
However, a m o n t h later he was readmitted to the Neurological Service at the
father's insistence because he had failed to improve further. His mother, who was
charged with feeding him, observed that at times he was so drowsy that she had to
slap his face in order to arouse him to the point where he would eat.
Examination at this time disclosed a semi-comatose boy who opened his eyes but

A B

C D
Fig. 1. Case 1. A: lateral view of right carotid arteriogram showing normally placed vessels. B:
similar view one month later showing bowing of the anterior cerebral artery consistent with ventncular
dilatation. C and D : air studies done at the time of the second arteriogram (B) confirming the presence
of hydrocephalus.

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310 S. H A K I M , R. D, A D A M S

did not look at the examiner or make any effort to speak. His eyes closed in response
to a loud noise. He heeded no spoken command. He withdrew from painful stimuli
but did not initiate any type of movement. Passive movements of his limbs evoked
a mild degree of resistance. The reflexes were more lively than before and the plantar
reflexes were extensor bilaterally. At lumbar puncture the initial pressure of CSF
was 150 mm. The fluid was slightly xanthochromic but contained only one lympho-
cyte; the protein was 60 rag/100 ml. Bilateral carotid arteriograms were performed
and disclosed only a widened sweep of centrally placed anterior cerebral arteries, a
finding suggestive of hydrocephalus (Fig, 1B). Fifteen ml of cerebrospinal fluid were
removed at the time of the lumbar puncture.
The next day the patient was definitely improved. He followed the examiner with
his eyes, would look at his own hands and move them. He mumbled a few words:
He remained incontinent of sphincters. A lumbar pneumoencephalogram was per-
formed the following day and it showed a symmetrical dilatation of the ventricular
system (see Fig. 1, C and D). This procedure seemed to aggravate the patient's
condition. He again became stuporous and was still that way the next day. The
CSF pressure was measured again and was found to be 180 mm. Surmising that the
hydrocephalus might be contributing to the symptomatology, a catheter was intro-
duced into the right lateral ventricle and the cerebrospinal fluid was permitted to
drain. Again there was improvement.

Course o f illness
A ventriculo-atrial shunt was done approximately 6 weeks after the head injury.
After the completion of this operation, the patient showed a dramatic improvement.
He began to talk, though his speech was slightly dysarthric. He now asked simple
questions about what had happened to him. Two days later he seemed much more
alert, followed the examiner with his eyes and obeyed simple commands, but he
was still incontinent of urine and feces. By the fifth postoperative day he was feeding
himself and had regained control of sphincters. His speech was slightly thick and
dysarthric. He was now able to leave his bed and to walk about, though rather un-
steadily. Ten days after operation the spinal fluid pressure was 80 and he was greatly
improved. He left the hospital 15 days after the shunt operation. When seen a month
later in the out-patient clinic he had gained weight and was alert. His gait was essenti-
ally normal. His speech lacked normal inflection, but his choice of words was entirely
correct and he understood all that he heard and read. Three months later he was
judged to be normal, had returned to school and was performing nearly as well as
before the injury.

Comment
The initial unconsciousness was ascribed to the severe concussion and the slight
left hemiparesis to the contusion of convolutions in the right cerebral hemisphere
and the small right subdural hematoma. The failure of the patient to improve but,
more particularly, the episodic worsening of his condition seemed to bear some
relationship to the enlargement of the lateral and third ventricles. Although initially
attributed to irreversible brain injury, since the initial cerebrospinal fluid pressure

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 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 311

was normal, the improvement after lumbar puncture and after drainage of the lateral
ventricle and the apparent aggravation of his condition by pneumoencephalo-
graphy strongly suggested an important hydrocephalic factor. The favorable response
to ventriculo-atrial shunt corroborated this impression.

Case 2

Male, age 52. Private patient (S.H.) at H.M.C. Progressive reduction of alertness,
attentiveness, motility and speech over the period of a year. Neurological status
when first e x a m i n e d - - one of akinetic mutism with sphincteric incontinence and Babin-
ski signs. CSF pressure never above 180 ram. Arteriography and pneumoencephalo-
graphy consistent with communicating hydrocephalus. Ventriculo-atrial shunt follow-
ed by dramatic recovery and return to gainful employment.

History and examination

On February 12, 1958 this patient, a professional trombone player, was brought
to medical attention because of inability to play his musical instrument, gradual fail-
ure of memory, mental dullness and apathy, disinterest in personal appearance,
unsteadiness of balance and stiffness of legs. The disorder of gait and the change in
mentation were of insidious onset and developed simultaneously. The first hint of
the disorder was a slowness in thinking and in speaking during conversation. Often
the thread of the topic being discussed was lost and his associations were not always
logical. This condition slowly increased in severity. Later the patient's wife became
aware of an untidiness in dress. Even more distressing was an incontinence of urine
which began to occur from time to time. The difficulty in locomotion which devel-
oped during this same period was described as a stiffness of the legs. He preferred
to sit much of the time and he talked less than usual. There was a tremor of the
trunk. Despite these obvious changes the patient himself made no complaints about
his condition. According to his wife, he lost all capacity for worry and expressed no
concern about anything that was happening. His appetite was ravenous and he gained
a considerable amount of weight. There was no complaint of headache. His condi-
tion had forced his retirement as a musician; in fact, he had been unoccupied for
several months when first seen medically.
At the time of the initial physical examination the patient was slightly obese and
was uncertain of his whereabouts. He realized that he was in a hospital but did not
know its name. He gave the day, month and year incorrectly. When asked his
complaint, he said either that nothing was the matter or that he could not walk
properly. It was impossible for him to recount the history of his illness. The name of
the musical instrument he had played was not remembered, but the clef in which the
music for this instrument is written was given. Arithmetical calculations were slowly
performed and many mistakes were made. Although slow in finding words and slightly
thick of speech, there was no evidence of aphasia. The gait was unstable, the base
broad, and there was stiffness and possibly slight weakness of legs. The help of two
canes was required in order to walk. A definite lateral nystagmus was evidenced
during right lateral gaze. Both optic discs seemed unnaturally pale, but the eye-

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312 s. HAKIM, R. D. ADAMS

grounds were otherwise not remarkable. The pupils reacted to light but the coll-
striction was slow and incomplete on the right side. Visual acuity was 20/25 in the
right eye, 20/20 in the left; color vision was intact and the visual fields were full.
Ocular motility were normal. Hearing was within limits of normal. A terminal tremor
of the hands was noted in finger to nose test, more pronounced on the left side than
on the right. Response to touch, pinprick, tuning fork, and passive movements of
digits were seemingly within the limits of normal in all four extremities. Tendon
reflexes were a brisk 3 + in the legs and only 2 + in the arms. There was a suggestion
of spasticity in the legs. Ankle clonus was present bilaterally and the plantar reflexes
were extensor.
The remainder of the examination revealed no important abnormalities. Blood
pressure was 140/90 and other vital signs were also normal.

Laboratory data
X-rays of chest revealed a mild emphysema. In x-rays of the skull the pineal body was
noted to be calcified and lay in the midline. The posterior clinoid processes were thin
and decalcified. An electroencephalogram demonstrated ~- and r-waves diffusely
mixed with others of slower frequency in the 5-7 and occasionally 2-3/sec range.
The initial CSF pressure, taken in the lateral decubitus position, was 180 mm. The
fluid contained 6 lymphocytes/mm 8, 15 mg protein and 77 mg glucose/100 ml. The
Hinton, Wassermann and cardiolipine tests were all negative.

Course o f illness
After the lumbar puncture the patient's condition seemed to improve. His wife
remarked that his words came more quickly, that he was less forgetful and walked
more rapidly and with better coordination. The diagnosis at this time was still in
doubt. His condition then worsened to the level at which it was when first seen.
During the following month, two further lumbar punctures were done, again with the
removal of fluid, and each time followed by a slight but definite improvement which
lasted a few days. The spinal fluid pressures were 150 and 170 respectively, and the
sample of CSF from the second of these two lumbar punctures contained 18 cells/
mm 3.
By the latter part of March, 1958, the patient's condition had definitely worsened.
He had become stuporous, his lips were mildly cyanotic, his breathing was stertorous
and the rectal temperature was 37.8°C. The pupillary reactions to light had become
more sluggish than before. Rales were heard over both lung fields. The blood pressure
was now 170/110. The level of responsiveness was reduced to such an extent that it
was necessary to suction saliva from the trachea to keep his airways clear. Oxygen
and antibiotics were given. Since the urine was retained, a Foley catheter had to be
inserted. At this time it was decided to do carotid arteriograms bilaterally in order
to rule out a possible chronic subdural hematoma. The major arteries were observed
to be in their normal lateral position and could be traced to the meningeal surface,
thus excluding a subdural collection of fluid, but in the lateral films there was a
considerable bowing and upward displacement of the anterior cerebral arteries (Fig.
2A). Thereafterwards the patient became even more obtunded. The left eye seemed

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 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 313

A B C

Fig. 2. Case 2. A: right carotid arteriogram showing bowing of the anterior cerebral artery consistent
wit h hydrocephalus. B and C: air studies showing gross hydrocephalus at that time. The enlargement
of the fourth ventricle can be seen in B and C.

slightly more prominent and deviated outwardly. Plantar reflexes were now extensor
bilaterally. The blood pressure remained at 160/110 and the pulse 58.
On March 28 a combined right occipital ventriculogram and lumbar pneumoenceph-
alogram were done under local anesthesia. The films showed a generalized enlarge-
ment of the ventricular system and no air entered the subarachnoid spaces over the
convexities of the cerebral hemispheres (Fig. 2B, C). A No. 10 French catheter was
left in the right lateral ventricle, a procedure which has been used (by Dr. J. Poppen)
in order to avoid an aggravation of the hydrocephalus by the injected air. That
afternoon the patient's condition was better, but the external deviation of the left
eye and weakness in internal rotation of it were still present. A total amount of 25
ml of spinal fluid had drained by 3 p.m. and 72 ml by 9 p.m. By the evening of the
following day he was alert and quiet.
A ventriculo-atrial shunt was performed on March 30 under local anesthesia,
utilizing the burr hole through which the ventriculography had been performed. On
the following day there was a remarkable improvement in the patient's condition.
His anisocoria had disappeared. It was now possible to elicit full conjugate eye move-
ments in all directions of gaze. The left plantar reflex was still extensor, the right
flexor. An indication of his improved state was his spontaneous remark when the
surgeon (S.H.) entered the room: "Doctor, do you think I shall ever walk again?"
It was recorded that he correctly named a series of objects and later remembered most
of them. He spoke more clearly and knew the name of the musical instrument which
he had played.
By April 2 the patient was more alert and responsive than at any time since his
entrance to the hospital. Orientation as to time and place was now perfect. His
leg motions were more quick and the knee and ankle jerks were less lively. The left
plantar reflex was absent and the right, flexor. The patient still had an indwelling
urinary catheter, but he could leave his bed, stand and take a few steps with help.
He still walked on a broad base and relied on a cane. Later the catheter was removed
at his request. On April 4 he was fully conscious, was now feeding himself and walk-
ing with a cane without other assistance. There was still some dribbling of urine. A
lumbar puncture was performed on April 6. The initial pressure was 70.
The improvement in the patient's neurological and mental status continued. His

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314 S. HAKIM, R. D. ADAMS

conversation was lively and his attention span was normal. He was asking question~
about the earlier part of his illness in order to gain a full knowledge of it. As in the
past, he was now neat and clean and concerned about his personal appearance. He
had begun to worry about the economic status of his family. His speech was perfectly
articulated and the choice of words was proper. Control of sphincters was nox~
complete.
By July 13 his mental status was quite normal, but he still felt more confident
when using a cane to help in locomotion. He has continued to remain in perfect
health since that time and now walks with only the slightest difficulty.

Comment
The slowly progressive mental deterioration over a period of one year was the
dominant feature of this case. It was eventually traced to a communicating hydro-
cephalus, the cause of which was never determined. The pressure of the cerebrospinal
fluid never exceeded 180 mm of water on any one of four lumbar punctures. Never-
theless, when a ventriculo-atrial shunt was performed and the pressure lowered,
there was unmistakable improvement and almost complete recovery.

Case 3
Male, age 43, private patient of Dr. Hakim, referred later to the Massachusetts General
Hospital on the services of R. Adams and W. Sweet.
Middle-aged adult suffered a head injury with depressed skull fracture, deep coma,
small pupils and decerebrate posture. With improvement, left hemiparesis in evidence and
laboratory evidence of contusion of right cerebral hemisphere. Wide fluctuations in
alertness, motility, sphincteric control and plantar reflexes in relation to rises in CSF
pressure to 170 ram. After demonstration of communicating hydrocephalus a ven-
triculo-atrial shunt was performed. Stabilization of clinical state and slowimprovement
over a period of months. Now able to work and lead an independent life.

History and examination

This patient had enjoyed good health until July 7, 1961 when, while driving a
jeep on a hunting expedition, he crashed into a bus. He was thrown from the jeep,
struck his head on hard earth and lost consciousness immediately. Four hours later
he was transported by helicopter to a municipal hospital. On arrival there he was
observed to be in deep coma with miotic, almost unresponsive pupils and the trunk
and limbs were set in a posture of decerebrate rigidity, i.e., extension, adduction,
internal rotation of arms, and extension of legs. The plantar reflexes were extensor.
Blood oozed from the right ear. There was a bruise in the right scalp and a depressed
skull fracture in the right temporoparietal region. The blood pressure at this time
was almost unobtainable (art indefinite and uncertain reading of 40 systolic was
once obtained); the heart action was extremely rapid and respirations, fast and
shallow.
The patient was given an injection of a vasopressor drug, a transfusion of whole
blood, corticosteroids and antibiotics, and a tracheostomy was performed immedia-

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 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 315

tely. He responded to these measures and within a few minutes his blood pressure
had risen to 80/40. On the following day, July 8, a right parietal burr hole was perform-
ed. There was no blood either outside or inside the dura. When the depressed bone
fragment was elevated, it was thought that his condition immediately improved;
his pupils reacted better to light, he grimaced, and a few restless movements of the
extremities were observed. A slight right peripheral facial weakness and a mild left
hemiparesis could then be discerned. He coughed vigorously when his trachea was
suctioned. Blood pressure was now normal. Dilantin was given in order to prevent
seizures.
During the following days, July 9 through 20, the patient's state of consciousness
fluctuated from semicoma or light coma to stupor. In: the latter condition he lay
speechless with eyes open, left pupil larger than right, an apparent left hemiparesis,
a probable weakness of the right leg, and bilateral Babinski signs. When semico-
matose he responded only to pinch and painful stimulus with groans and ineffective
withdrawal. Despite this poor state of responsiveness there was gradual improvement
so that the tracheotomy tube could be closed by July 15. His blood pressure had
stabilized and oxygen and antibiotic therapy were no longer needed.
By July 20 his temperature was normal. He looked about the room but did not
speak or obey commands, even the most simple ones. All four extremities were
moved freely. He slept much of the time but could be aroused to open his eyes
when touched and was easily startled by a loud noise. When pinched he would
open his mouth, but no sound came forth. Food given by his wife was sometimes
accepted and masticated, but at other times he would either refuse to open his mouth
or would accept the food and retain it in his mouth for many minutes.
His condition remained like this until July 25 by which time he was slightly more
alert though still incontinent of urine and still completely mute. When left alone
he immediately fell asleep. The tendon reflexes were more lively on the left side than
the right, 3 + compared with 2 + ; the plantar reflexes were extensor bilaterally. The
CSF pressure on this day was 160. Twelve ml were removed, lowering the pressure
to 140. The CSF contained 40 lymphocytes/mm a and a protein of 35 mg/100 ml.
A few hours after the lumbar puncture the patient seemed more alert than at any
time since his injury. He attempted to speak, pronouncing the few uttered words
slowly, and for the first time he obeyed such commands as "Open your eyes" or
"Put out your tongue". He still had to be fed and was still incontinent of urine.
This improvement continued during the following days.
By August 1 he occasionally initiated a conversation, was able to sit in a chair,
but was disoriented, confused and forgetful. The right facial weakness was still
present. The right eye tended to deviate upwards and outward. By August 9 he was
walking on a broad base, leaning slightly to the left. His steps were short and slow,
but his coordination was fairly adequate. The plantar reflexes now were flexor. He
was eating well and had gained some weight. Improvement was maintained from
August 11 to 23, but in the period of August 24 to September 7 he relapsed, being no
longer able to speak or leave his bed or control micturition. His attention span was
virtually nil; much of the time he could not be attracted to a stimulus. Again he might
follow objects with his eyes momentarily. The optic discs were normal. The plantar

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316 S. HAKIM, R. D. ADAMS

reflexes were once more extensor and grasp and sucking reflexes were easily evoked.
There was again slight nuchal rigidity. The vital signs remained stable.
Suspecting that this worsening might be due to a chronic subdural hematoma.
bilateral carotid arteriograms were performed on September 7, 1961. They revealed
an arching and upward displacement of the anterior cerebral arteries indicative of
hydrocephalus, but no sign of subdural hematoma or effusion (Fig. 3A). The CSF"

A B C

Fig. 3. Case 3. A: left carotid arteriogram showing bowing of the anterior cerebral artery. B and
C: air studies showing hydrocephalus.

pressure measured later on this day was 170, and it fell to 100 after the removal of
20 ml. The next day after this procedure there was again a remarkable improvement
in the patient's state of consciousness. For the first time in many days he was able
to feed himself at breakfast. He talked, answered simple questions, but was still
confused and incontinent.
Another lumbar puncture was done on September 9. The pressure at this time
was 180 and after the removal of 15 ml of fluid it fell to 110. The content of the fluid
was essentially normal to chemical and cytologic tests. His improvement continued
on the following day, when the CSF was again re-examined and the pressure found
to have fallen to 120. The removal of another 20 ml of fluid resulted in a fall to 70 mm.
The improvement after this lumbar puncture continued for the next three days.
On September 14 the spinal fluid pressure was re-tested and found to be 70 mm and
after removal of another 13 ml it fell to 60 mm. On September 19 he was alert,
talked freely, his speech was more rapid, his pronunciation had improved. He read
simple passages from the paper, copied a few lines of typescript without mistakes,
and gave correctly the names of 10 objects. For the most part he was jovial and happy,
His gait was still slow but balance was adequate, at which level it continued through
the latter part of September. By then he had improved to the point where he could
follow complicated orders, do simple calculations and explain the meaning of popular
proverbs. If anything, he tended to be loquacious, was rather agitated and somewhat
uninhibited in his behavior. On October 5 he had again relapsed though without
change in vital signs. Once more he refused to speak, seemed indifferent as to what
was happening around him and was incontinent of urine. A lumbar puncture at this
time revealed a pressure of 170 ram, falling to 120 after removal of 12 ml of fluid.

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 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 317

The next day he got out of bed by himself andagainseemedtalkativeand more active.
His CSF pressure on October 8 was 130 mm. At this time and during the next days
he seemed active and was quite happy.
The patient was transferred to the Massachusetts General Hospital to the service
of one of us (RDA) in the early part of November. When first seen there, he was
able to talk slowly but seemed vague and uncertain of himself, was inaccurate as to
details of his history, was able to walk with a somewhat broadened base with a list
to the left, and had bilateral Babinski signs. A pneumoencephalogram was performed
on November 10. It showed a marked bilateral hydrocephalus, the septum pellucidum
being in the midline. The right temporal horn was larger than the left one. The third
ventricle was markedly dilated and the aqueduct and fourth ventricle moderately
enlarged (see Fig. 3C). The patient tolerated this procedure rather poorly and after-
wards spoke very little, was incontinent, had bilateral Babinski signs and slight left-
sided hyperreflexia. For several days he did not wish to leave his bed.
Because of the marked fluctuations in the patient's symptomatology in relation
to rising and falling cerebrospinal fluid pressures, Dr. W. Sweet was consulted and
a ventriculo-atriostomy was performed on November 21, using a McPherson valve.
The procedure was well tolerated, though on the 23rd he had a shaking chill and a
temperature of 103°F. The CSF contained 40 cells/mm 3, all lymphocytes. On Novem-
ber 25 he seemed more active and talkative, quicker in response and less drowsy.
His speech, however, was still rambling and incoherent and he confused what happen-
ed two weeks before with the events of the previous day. His neck was re-explored
on December 30 by Dr. Ojemann and the McPherson valve was replaced. By Jan-
uary 1 he was somewhat more alert and able to feed himself but said little. The plan-
tar reflexes were equivocal. The CSF pressure was still 170 m m and the fluid xantho-
chromic. After removal of an unmeasured amount of CSF the final pressure was
135. On January 15 the patient was much the same as he had been just before
the operation, still dull, slow inattentive, registering poorly what had been recently
presented to him, and incontinent of urine at night. The left hemiparesis was still
present and the plantar reflexes were extensor. The CSF pressure was 170 mm. On
January 19 a lumbar puncture was done with an opening pressure of 275 and it was
clear that the valve was not .functioning properly. Vigorous massage of the valve
resulted in a fall in the pressure to 90 mm. Thereafter the valve continued to function
normally and the pressures remained low.
During the next five months he slowly improved in alertness, mental competence,
initiative, speech and gait. One could not say that any of these changes took place
at a rate which permitted the examiner to be sure of what was happening from week
to week. In fact, we were rather disappointed with the therapeutic result. For a time
we ascribed his poor progress to a salt-losing syndrome which kept serum sodium
and chlorides at levels of 125 and 95 milliequiv./1 respectively, unless extra salt was
ingested. By early June, however, it was evident that he could lead an independent
existence outside the hospital. He still had trouble recalling the name of the city,
the hospital and the doctors. He was more restless and inclined to worry, yet he would
smile frequently. The neurological examination seemed to be more nearly normal.
He walked quite steadily though slowly. His plantar reflexes were flexor. He had

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318 s. H A K I M , R. D. A D A M S

regained control of the vesicular sphincters. All during the spring the CSF pressurc~
had remained in the range of 100-130 ram.
During the summer, after discharge, this improvement continued and by autumn,
1962, the patient was able to return to work and to carry out rather simple secretarial
tasks in an office. He works steadily now and also looks after a small farm which helps
support his family. He has been discharged from the Army. No longer is he the
vivacious, imaginative, highly intelligent man that he had been before his accident.

Comment
This case is much more difficult to interpret. Obviously the patient had a severe
injury with concussion, and contusion and laceration of his right temporal region,
accounting for pyramidal signs of the left. In addition he showed a marked impair-
ment of consciousness, quite prolonged, with some signs pointing to a disorder at
the upper brain stem level. As he improved, however, he entered a state where it was
quite evident that he had a communicating hydrocephalus with pressures at the upper
limits of normal; and further it became clear that a lowering of his CSF pressure
was attended by a definite general improvement in alertness, spontaneity, capacity
for speech and action, continence of urine. Conversely, a rise in CSF pressure up to
170 or 180 mm was attended by a reduction in consciousness, bilateral Babinski signs,
incontinence of urine and an akinetic mutism. The ventriculo-atrial shunt did not
produce the immediate result we had expected, but there was at first some difficulty
in making the valve work properly. In addition he had a brief period of septicemia,
probably caused by Staphylococcus albus. Once this was corrected and the valve
began to work, a slow improvement took place, so gradual that we could hardly be
sure of it until many months had passed. No longer were there fluctuations in his
alertness and psychomotor activity. We could not be sure always whether this was
due to the regression of the effects of cerebral trauma or to the treatment of the
hydrocephalus. We doubted in the weeks following the operation whether he would
ever again be able to function independently. In the final analysis we concluded that
this patient did have a severe head injury with depressed fracture, contusion of brain,
probably some upper brain stem injury, a mild salt-losing syndrome, and, added
to all of this, a communicating hydrocephalus which retarded his recovery. The
"shunt procedure" appeared to contribute to the success of the therapeutic program.

DISCUSSION
Special features o f the clinical state
The three cases reported above are examples of a larger series of cases observed
over the past lO years, in which a demonstrable hydrocephalus of obstructive or
communicating type has been the cause of a characteristic clinical syndrome, the
finer details of which will be described in a later communication. Two of the cases
chosen for this report were traumatic and in the other there was a hydrocephalus
of undetermined type, presumably due to a block in the perimesencephalic region.
In each of these cases a syndrome of impaired consciousness and reduced responsive-
ness of variable degree had been combined with faulty locomotion and sphincteric in-

J. neurol. Sci. (1965) 2:307-327

 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 319

continence. The impairment of consciousness varied from a mild inattentiveness,

with failure of daily events to be registered in mind and later retained, to a state of
virtual coma. In this state the patient often was manifestly unreceptive of stimuli
as well as unresponsive to them. The latter was at times more prominent than the
former. The psychomotor retardation also varied in degree; when mild, a lack ofim-
pulsivity, expressed as apathy, disinterest, and lack of spontaneity, was associated with
reduced levels of verbal and motorial function. When severe, it amounted to total
immobility and absence of consecutive psychic activity, a state akin to akinetic
mutism. The incontinence of sphincters was essentially of cerebral type, the patient
being unaware of the contents of bladder and bowel and incapable of making any
arrangement for the somewhat precipitate action of these organs. The alteration of
gait varied from a mild disorder in which locomotion appeared careless, the steps
slow and somewhat shortened and the balance slightly uncertain, to one in which
there was total incapacity to stand and walk. With the latter the plantar reflexes
were usually extensor and the tendon reflexes brisk, particularly in the legs. An ele-
ment of ataxia seemed to have been present but was always difficult to evaluate, and
clearcut intention tremor and dysmetria were not demonstrable.
The syndrome described in the previous paragraph is, of course, familiar to all
clinicians who have had experience with hydrocephalic patients. Its existence is rela-
ted in some way to the dilatation of the lateral and third ventricles and possibly the
ataxic element of gait in some instances to dilatation of the fourth ventricle. More
precise statements concerning clinical-anatomical correlation are probably impossible.
One can only vaguely speculate in general terms that the dilatation of the ventricles
subjects the major long tracts in the cerebral white matter and corpus callosum to
compression and stretching, with a resultant physiological block of function which
is to a considerable extent reversible when the pressure is reduced. This hypothesis
would be in harmony with the observation that it is the white matter of the cerebrum
which appears to yield maximally to great expansion of the ventricular system.
The feature to which attention is called in this paper is the occurrence of this hydro-
cephalic syndrome in the face of normal CSF pressure. In this regard one must
first examine closely the evidence that the CSF pressure was indeed at all times within
normal limits. In our three cases it is to be noted that the CSF pressures, measured
in the lateral decubitus position, ranged from 130 to 180 mm H20. The latter figure
is usually considered to be at the upper limits of normal, though some authorities
state that pressures below 200 mm may be called normal. The next question to be
raised concerns the reliability of isolated pressure measurements. In Case 1 there were
only two lumbar punctures, one with a pressure of 150 and one with a pressure of
180. In Case 2 there were five lumbar punctures with pressures ranging from 160 to
180. In Case 3 the patient had ten lumbar punctures with pressures from 120 to 180.
Since it has been learned from the informative study of LUNDBERG (1960) that the
ventricular pressure, when measured continuously over a period of days in patients
with intracranial tumors and other conditions causing high pressure, varies widely
from hour to hour (large plateau-like waves of high pressure lasting for many minutes
to hours interspersed with valleys of normal ventricular pressure), could we have by
chance recorded the pressure only during the times when it was within limits of normal

J. neuroL Sci. (1965) 2:307-327

320 s. HAKIM,R. D. ADAMS

and have missed the peaks of pressure that were producing the clinical symptoms?
Against this possibility is the fact that not one of the many pressures was elevated:
and, in Cases 2 and 3, improvement was noted when the pressure fell to the range of
70-120 m m and worsening occurred on more than one occasion when it rose to a
level of 150-180 mm. Moreover, a permanent improvement coincided with a reduc-
tion in pressure to around 130 m m or below by the procedure of ventriculo-atrial
shunt. In Case 3 improvement did not occur after shunting, as long as the pressure
remained in the range of 170-180 mm, the so-called normal level. It is for these reasons
that we have concluded that the pressure measurements were valid and representa-
tive, a symptomatic hydrocephalus occurring with pressures in the 150-180 mm
range.

Other references to this phenomenon o f symptomatic hydrocephalus with normal spinal

fluid pressures
In conversations with other neurologists and neurosurgeons it has been learned
that observations of the type made here are not widely known. In searching the volumi-
nous literature on hydrocephalic states one, of course, finds many references to hydro-
cephalus following subarachnoid hemorrhage, cranial trauma, and other diseases
of more obscure nature. And, it is well known that a marginally compensated hydro-
cephalus of whatever cause may decompensate after injury, infection, lumbar punc-
ture or pneumoencephalography. However, we found no well-studied series of cases
of symptomatic hydrocephalus where repeated lumbar punctures had demonstrated
CSF pressures at the upper limits of normal. A possible exception is one of the cases
of KmLER et al. (1961) where a single pressure was recorded as 160 m m ; but no point
of this fact was made in their paper. FoeTz et al. (1956) noted in their Case 6 a
symptomatic hydrocephalus with normal CSF pressure and stated that ventriculo-
mastoidostomy was nevertheless beneficial. Many of the pressures in published cases,
however, have been only slightly above the upper limits of normal and there is a
general consensus that in these and other more typical cases the reduction of the pres-
sure often has resulted in clinical improvement. The converse of this, that elevations
of pressure above normal exercise a deleterious affect on cerebral function, has recent-
ly been disputed. In the early reports by ADSON AND LILUE (1927) and ETHELBERG
AND JENSEN (1952) attention was drawn to the relatively close correspondence between
a marked rise in intracranial pressure and the occurrence of a cerebral symptoma-
tology, an association which has been confirmed more recently by the studies of
LUNDBERG (1960). These studies tend to cast doubt on the statements of BROWDER
AND MEeERS (1938) and RYDER et al. (1953), that greatly elevated intracranial pres-
sure bears no predictable relationship to any disturbance in nervous function. It
is to be noted that the technique of deliberately raising the intracranial pressure by
the injecting of fluid into the spinal subarachnoid space and observing its effect, which
was the basis of many of these conclusions, is hardly comparable to the rise in intra-
ventricular pressure resulting from hydrocephalus. The point made by BROWDER
AND MEYERS and by RYDER et al. cannot be completely discounted, however, for
changes in intraventricular pressure of sufficient magnitude to alter consciousness
do not cause a regular alteration in the pulse, blood pressure or respiration.

J. neuroL Sci. (1965) 2:307 327

 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 321

An hypothesis concerning the mechanism of symptomatic hydrocephalus with relatively

normal or only slightly raised intracranial pressure
The intracranial pressure, as is well known, represents the composite effect of
several physiological factors. As pointed out by O'CONNELL (1953) and later by RYDER
et al. (1953), the main factor in maintaining intracranial pressure is the arteriolar-
capillary blood pressure, a fact which becomes self-evident during shock and at the
moment of death, when the fall in CSF pressure corresponds to the fall in blood
pressure. Variation in the cerebrovascular resistance offered by arteriolar constric-
tion seems to be the main mechanism by which CSF pressure is modified. When the
vessels are constricted, offering high resistance, the intracranial pressure tends to be
lower; when they are dilated, it rises. In addition, the venous pressure, which regulates
to some extent the volume of blood in the cranial cavity, and the mass of brain
tissue itself and any pathological element which it may contain, also influence the
level of cerebrospinal fluid pressure. Presumably there is at all times a delicate balance
between intracranial vascular volume, quantity of CSF, brain volume, and the force
of arteriolar-capillary pressure. Any hypothesis, therefore, which fails to measure
and take into account all of these factors will not provide more than a partial ex-
planation of the pressure changes in the CSF in any particular disease state.
Let us assume that an intracranial disease which interferes with cerebrospinal
fluid circulation has occurred and the conditions which favor the development of
hydrocephalus now exist. As the pressure within the ventricles rises, the ventricles
themselves enlarge and the brain tissue around the ventricles yields gradually.Except
in infancy, where the head may enlarge, the cerebral hemispheres become compressed
by the rising pressure from within and the resistance offered by the meninges and
cranium from without. If the block in CSF circulation be complete, the pressure

- 120

1t2o
A~ A2
Fig. 4. The hydraulic press effect on the ventricular walls is illustrated in A2. Despite an identical
CSF pressure in both Az and A2, the force (F2) on the ventricular wall is greater and proportional
to the increased surface (see text).

J. neuroL Sci. (1965) 2:307-327

322 s. HAKIM, R. D. ADAMS

within the ventricles rises to such a height as to paralyze the function of the cerebrum
and structures in the upper brain stem, usually with respiratory failure and death.
Fortunately this state of affairs seldom happens. Instead, the block is usually partial;
it causes a rise in ventricular pressure up to a certain point at which CSF formation
and absorption come into a state of equilibrium. Presumably the cerebral arteriolar-
capillary pressure, volume of intracranial blood, volume of CSF reach a balance
under these new conditions. With partial or more complete relief of the cause of the
hydrocephalus (e.g., resorption of subarachnoid blood or suppression of meningeal
inflammation), another even milder hydrocephalic state may prevail - - one in which
the CSF pressure returns to normal but the ventricles remain enlarged and neurol-
ogical symptoms persist. It would seem that the ventricles, once having expanded,
may be maintained in this state by CSF pressures which are lower than those which
caused the initial enlargement. A new mechanism appears to be operating to perpe-
tuate the hydrocephalic cerebral syndrome ( e l our Cases 1 and 3).
To elaborate upon this latter mechanism, we would suggest that the expanded
state of the ventricles themselves plays an important role in determining the effect
of the CSF pressure on the brain. This notion would be in accordance with the law
of PASCAL, enunciated over 300 years ago, that: "the pressure applied to an enclosed
fluid is transmitted undiminished to every portion of the fluid and to the walls of the
containing vessel" (SEARS 1946). A given pressure of CSF would therefore be ex-
pected to have a greater force when applied to the walls of enlarged ventricles than
to small ones. More explicitly, the CSF pressure, defined as that pressure which must be
exerted to prevent any outflow of CSF through a needle inserted in the subarachnoid
space or the ventricle (DAvsoN 1956), represents the force per unit area of ventricular
and subarachnoid surface. The total pressure or force applied to the cerebrum would
then be the pressure multiplied by the area of the walls of the space containing the
CSF (force = pressure × area). To illustrate this point, a CSF pressure of 120 mm
of water means that every m m 2 of the ventricular surface is subjected to the weight

, !
\ /

P = PRESSURE oT
T = ELASTIC TENSION pc,< - ~
r = RAolus

Fig. 5. To illustrate PASCAL'S law applied to a spherical elastic container, Pc~2T/r; with increa~ in
diameter of the balloon, the pressure falls.

J. neurol. Sci. (1965) 2:307-327

 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 323

of a column of water 120 m m high. Ventricles of two different sizes may be under
the same pressure, but the force exerted on the walls of the larger one will be greater.
In the normal sized ventricle (A1) of 20 cm surface area, F1 = 120 x 2), whereas in an
enlarged ventricle (A2) of 40 cm surface area, F2 = 120 x 40. Therefore F1/F2
---- A1/A2. Thus the pressure in both the small and large ventricle is equal, but the
force in the larger ventricle has increased in proportion to its increased surface.
It theoretically follows from this equation that if the product of ventricular pressure
and volume is constant, an increase in ventricular volume should be accompanied
by a decrease in pressure. The principle of increasing force in the ventricle as the area
of it expands might be called the hydraulic press effect (Fig. 4).
Since the ventricular walls and surrounding brain tissue have some property of
elasticity, as evidenced by the slow expansion of ventricles under conditions of in-
creased ventricular pressure and by their later reduction in size and return to normal
volume when the pressure is lowered, one might turn to rubber balloons filled with

Ibs.
51
"i
31

1
I
02 3 4 5 6 7' 8 9 lo II cm
LENGTH OF STRETCH

Fig. 6. The increase in elastic tension with increasing stretch on rubber has been photographed.
The relation of length to elastic tension is shown in the graph below.

J. neuroLScL (1965) 2 : 3 0 7 - 3 2 7
324 S. H A K I M , R. 1). ADAMS

water to study the postulated relationships between force, pressure and area. As
shown in Fig. 5, in any fluid enclosed in a spherical elastic container, the relationship
of pressure (P) to tension (T) and the radius (r) of the sphere is expressed by the
formula: P~x : 2T/R. This is PASCAL'S law applied to a spherical elastic container.
The effect of elastic tension of rubber during stretching is illustrated in Fig. 6. It
can be shown that with increasing stretch the elastic tension (as tested by force
required to stretch it) rises. As the rubber balloon is inflated (Fig. 7), the pressure
increases until the balloon starts to enlarge and then falls with further increase in
size despite the increase of tension of the rubber of the balloon. The increase in
elastic tension is proportional to the amount of the stretch. Everyone who has
attempted to blow up a child's rubber balloon and to indent it with his fingers is
familiar in a practical way with the physics of this problem.
Admittedly the analogy is open to criticism on the grounds that the elasticity
of the brain is different. In the rubber the force required to overcome the elastic
tension increases with stretch, whereas in the brain, where the elasticity of the tissue
is much less, it decreases as the ventricular system continues to enlarge. Further,
the brain is enclosed by resistant membranes and bone, and the balloon only by the
atmospheric pressure. However, to the extent that the ventricles do possess some

A B
mmHg
I00 I

~ 80I
6O

20

0
I
0
I
200
I I
400
I I
600
I I
800
I
mm 2
APPROXIMATE AREA

Fig. 7. The decrease in pressure with increasing diameter of the balloon has been photographed.
A and B show the same pressure despite the fact that B has more elastic tension. The relation of the
pressure to the approximate area on which it is acting is shown in the graph below.

J. neurol. Sci. (1965) 2:307-327

 SYMPTOMATIC HYDROCEPHALUS WITH NORMAL CEREBROSPINAL FLUID PRESSURE 325

degree o f elasticity, the analogy is pertinent. Under any given pressure the walls of
the ventricles will exert an opposing force proportional to the degree o f stretch, and
there will be a point, finally, where the elastic tension o f the ventricular wall will
balance the opposing pressure inside. This pressure forces C S F out and the size o f
the ventricular system then remains constant. I f the pressure exceeds the elastic
tension, then the ventricles again enlarge.

2S LI,. z Lb. r~5 Lb. "1 Lb.

__ "&r>o~,Hao./ -- ~,~ ~-~o

Fig. 8. The relation of the CSF hydrodynamics to the physical principle involved is shown. A pressure
of one pound is supporting 3 times the weight acting on a larger surface area (A). The same principle
applies to the ventricular system (B), where an equal pressure in enlarged ventricles produces a
greater force. Corresponding x-rays are shown in C.

J. neurol. Sci. (1965) 2:307-327

326 s. HAKIM, R. D. ADAMS

One has no way of estimating the degree of elasticity of brain tissue, but some
evidence on this point has been provided by MASSERMAN(t934)who showed that
rapid drainage of a quantity of CSF causes a reduction in ventricular size, begin-
ning immediately after drainage and lasting for 8 hours. Also FOLTZ e t al. (1956)
demonstrated a decrease in ventricular size after lowering of CSF pressure. And, of
course, there are countless numbers of cases of hydrocephalus which come to the
attention of neurosurgeons in which enlarged hydrocephalic ventricles are restored
to a more nearly normal size after the reduction of intraventricular pressure by
shunting procedures.
It is not our intention to argue that the "dynamic press mechanism" of ventricular
expansion is the only factor that need be taken into account in the development of
hydrocephalus. Nonetheless, we feel that the importance of the distinction between
pressure and force within the ventricles has not been appreciated. There is virtually
no reference to a r e a of ventricular system in discussions of hydrocephalus. We
believe that our cases have demonstrated that a pressure of 180 mm of water in en-
larged ventricles is pathological and may be responsible for the maintenance of hydro-
cephalic symptoms. This is summarized in Fig. 8. It is our view that ventricular
size should always be considered in the evaluation of the significance of lumbar,
subarachnoid or intraventricular pressure. This factor of ventricular force probably
plays a role in the formation of infantile hydrocephalus where the head enlarges,
in the development of postoperative meningeal cysts, in certain types of porencephaly
and possibly syringomyelia. It may also explain the sites of greatest enlargement of
the ventricular system, the force being greater in the largest parts such as the anterior
horns of the lateral ventricles.

SUMMARY

In a series of personally observed cases, three of which are reported in detail, the
authors have noted that a state of symptomatic hydrocephalus may exist in the
presence of normal CSF pressure. The patients had exhibited mental dullness, in-
attentiveness, psychomotor retardation, unsteadiness of gait, and incontinence of
urine, a syndrome which may be mistakenly ascribed to a degenerative or traumatic
vascular disease of the cerebrum. Ventriculo-atrial shunt corrected this condition
and permitted recovery by lowering the CSF pressure 20 or more mm of water.
An important factor, heretofore overlooked, in explaining this symptomatic hydro-
cephalus with relatively normal CSF pressure is that the force exerted on the ven-
tricular wall represents a product of pressure times surface area. A given pressure
exerts a greater force in a large ventricular system than in a small one. A pressure of
170 or 180 mm H~O in ventricles that are three times normal size may produce symp-
toms, whereas it would not do so in a normal-sized ventrieular system.
This hydraulic press hypothesis must be applied in all cases of hydrocephalus.
Without some knowledge of ventricular size in this condition, the CSF pressure cannot
be accurately evaluated. This physical principle applies not only to adult hydroce-
phalus but also to infantile hydrocephalus, where the cranium expands, and to certain
types ofporencephaly and postoperative meningeal cysts and possibly syringomyelia.

J. neurol. Sci. (1965) 2 : 3 0 7 - 3 2 7

 SYMPTOMATIC HYDROCEPHALUSWITH NORMAL CEREBROSPINALFLUID PRESSURE 327

ACKNOWLEDGEMENT

This research was s u p p o r t e d in p a r t by the H a r r i n g t o n F u n d f r o m H a r v a r d Med i cal

School.

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J. neurol. Sci. (1965) 2:307-327