Bram (1976), 99, 331-346
CEREBROSPINAL FLUID PRESSURE CHANGES IN RESPONSE TO COUGHING by BERNARD WILLIAMS
INTRODUCTION
THE pressure of the cerebrospinal fluid (CSF) is subject to continual variation, and the role of such pulsation in producing damage has been subject to much speculation but little systematic study. When excessive, or maldirected, pulsations probably cause or aggravate some diseases by the imposition of forces which may produce distension of cavities or injection of fluid into tissue planes. Such mechanisms may occur in hydrocephalus, porencephalic cysts, arachnoid cysts and syringomyelia. Two sources of pulsation in CSF pathways are the arterial pulse wave and the venous changes consequent upon change of posture, respiration, coughing, muscular exertion and so on. The arterial pulse has received attention from Bering (1955), Laitinen (1968) and Dereymaeker, Stevens, Rombouts, Lacheron and Pierquin (1971), but the venous pulses have largely been neglected, although two comprehensive monographs have appeared on Queckenstedt's test (Gilland, 1966; Lakke, 1969); and movements within the CSF pathways in response to venous'and arterial pulsation have been reported by Du Boulay, O'Connell, Currie, Bostick and Verity (1972). The venous pressure is transmitted to the CSF pathways more readily than the arterial because the CSF and venous blood are in a state of balance across venous membranes (Bedford, 1935). Pressure swings in response to venous changes are big and easy to demonstrate and this study shows features of this type of pulsation. The pulsation itself is only of importance inasmuch as it transmits energy to tissue and it is the difference between pressures of adjacent areas which is important. The propagation of a wave depends upon a moving difference in pressure. Two sampling sites were therefore chosen at points where clinical puncture of the CSF pathways is normally carried out, the lumbar region and the cisternal, and the differences were studied by direct subtraction of the cisternal pressure from the lumbar.
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(From the Midland Centre for Neurosurgery and Neurology, Holly Lane, West Midlands, B67 7JX)
332
BERNARD WILLIAMS
The only measurements possible in this study were pressure and time. The timing of the venous pulse is a factor which has apparently not previously been measured. Williams (1969) suggested that under certain circumstances coughing might produce a rise in pressure which begins in the head before it begins in the spine; although radiological observations tend to suggest that the movement of myodil is always initially upwards after coughing (Du Boulay et ah, 1972).
Because the greater part of active human exercise is undertaken in the upright position measurements were taken from patients sitting erect.
METHODS Sixteen patients, all with disease in the cervical region and requiring myelography, were studied. Pressure recordings were made with 3^ in. 18 gauge needles in the lumbar region and the cisterna magna. In all cases the mean pressures were identical if they were referred to atmospheric zero at the manubriosternal joint. The patients were all tested with sharp coughs of short duration and limited amplitude. Recordings were taken with a Statham P23H differential manometer which gave two pressure recordings and the difference. The 60 cm tubes which connected the needles to the transducers had a natural frequency around 23 Hz, despite restraint by adhesive tape. Attenuation of high frequencies by a 15 Hz filter lessened the vibrations from the connecting lines and did not much alter the shape of the trace.
RESULTS
Clinical details are given in Table 1. The traces have been analysed for amplitudes, slopes and the areas between the curves and the resting baselines as shown in fig. 1. The differential pulse waves were measured from zero in the middle of the trace. The description and analysis of results will be readily followed by frequent reference to fig. 1. Individual pulse shapes, although they tended to be similar for any one patient, differed between one patient and another. Sometimes inhalation before the cough produced a fall of the baseline, sometimes a slight elevation preceded the main cough pulse, apparently produced by tensing the abdominal muscles.
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It seemed likely that the pulse wave produced by coughing would be attenuated during its passage up the spinal canal; and that the attenuation would reflect any blockage or narrowing of that pathway more effectively than Queckenstedt's test, because of the more rapid changes and higher amplitudes involved. Attenuation might be expected to diminish the amplitude of the ascending pulse, lessen its area, lower the rates of rise and fall (slopes) and to delay its passage. Such measurements were therefore made in patients in whom the information provided would be of at least potential clinical value even though the method, at first, was unproven.
CSF PRESSURE WAVES
333
70 r
=>
70
I 1
7. V
CO CO
LLJ
IT
a.
35 r
35 L
I I
I I I I I i i I i > i ' i i i i i I i i i i i i
i i i I i i i i i i i i
i I i i i
i i i i i i
1 SECOND1
FIG. 1. Illustration of the methods of analysis of results (Case 7). The dotted areas were measured only up to the crossover point, X-X. The coughs on the right have been used to illustrate the methods of measuring amplitudes and slopes. Slopes were not taken from the steepest part of the curve but from the fastest rise in 1/10 of a second in order to eliminate artefacts due to oscillations in connecting lines. Oscillations at around 5 Hz are visible in this trace.
Amplitudes The mean amplitudes in the lumbar region were between 19 and 97 mmHg above the baseline. Although amplitudes above 100 mmHg could be produced by most subjects, the records were ragged and the coughs were often preceded by abdominal tension and followed by minor coughs or gulps. The cisternal pulses were always lower in amplitude than the lumbar. From each patient ten coughs were analysed and the range, mean and standard deviations calculated. The values in Table 2 therefore give the range of the means and the means of the mean values of ten coughs for each of 16 patients. The standard deviations of the means are also given. Correlation coefficients in Table 2 have also been calculated from the means of ten coughs for each patient. The amplitude of the differential pulse upwards was usually greater than that downwards but not invariably.
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E
334
BERNARD WILLIAMS TABLE 1. CLINICAL ASPECTS OF CASES Radiology
Diagnosis 1 2 3
Severe pain neck and arm Myelopathy, undiagnosed Cervical myelopathy due to spondylosis
4 5
Severe neck pain Cervical myelopathy due to spondylosis Post-traumatic quadnparesis
6 7
9 10 11 12 13
14 15
16
due to due to
due to
Gross narrowing of spinal canal Partial block at C5-6
due to
Almost complete block C5-6
with disc
Compression from C5-6 disc
due to
Narrow spinal canal with C4-5 disc protrusion
due to
Cervical myelopathy due to spondylosis Multiple sclerosis with advanced cervical spondylosis Cervical myelopathy due to spondylous
Narrow spinal canal compression from C3-C7 No blockage—wide spinal canal Narrow spinal canal C4-5 disc protrusion
Post-operative result
_ Decompressive laminectomy
Recovery Unchanged Improvement
— Decompressive laminectomy
Recovery Improvement
Anterior fusion for instability of subluxation Decompressive laminectomy
No change
Due removed and anterior fusion Decompressive laminectomy
Improvement
Anterior fusion
Improvement
Laminectomy and lateral disc removal Anterior cervical fusion and disc removal Decompressive laminectomy followed later by anterior fusion Decompressive laminectomy
Recovery
Improvement
Unchanged
Improvement Improvement after each operation Unchanged Unchanged
Decompressive laminectomy
Improvement
Slopes The slopes of rise of the lumbar, cisternal and differential upwards pressures were all taken as the fastest change within any one-tenth of a second. Drawing a tangent to the steepest part of the curve gave higher results but these were questionable because of resonance in the manometer tubing. The slope of the fall of these three curves was also recorded; the rise was given a positive and the descent a negative sign. The return of the downward part of the differential to the baseline was often so shallow and marred by resonance that measurements could not be made. Timing The cisternal pulse was always later than the lumbar pulse. The time-lag was difficult to measure because of the irregular pulse shapes; there was sometimes a flattening or a double peak (fig. 1). The time delay was always over 004 s and the greater the attenuation of the cisternal pulse the later it arrived. The duration of the main cough impulse was around 0-6 to 0-9 s but the disturbance from the start of the cough to the end was sometimes very much longer.
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8
Cervical myelopathy spondylosis Cervical myelopathy spondylosis Cervical myelopathy spondylosis Cervical myelopathy spondylosis Cervical myelopathy large single disc Cervical myelopathy protrusion Cervical myelopathy spondylosis
Normal Normal Marked osteophyte encroachment of spinal canal Normal Multiple disc protrusion but wide canal, slight kyphos No blockage on myelography unstable subluxation Severe narrowing of spinal canal C2-7 Central disc protrusion C5-6
Operation
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TABLE 2. MEANS OF TEN RESULTS FROM EACH OF THE 16 PATIENTS
Correlation coefficients
Range
g T
E •3
Si
1
\
3
U T
Q
X
U
T
Q
wards
d 5?
|
-j
19-97 10-70 6-45 0-5—21 24-91
46-37 28 81 2712 - 9 24 60-95
1890 16 15 11-27 4-92 19-68
10 0-84 0 63 0 34 0-26
10 . * * 0-23 10 0-58 002 10 0-57 0-29 0 50 10
Arbitrary Arbitrary Arbitrary Arbitrary Ratio Ratio
104-677 48-333 60-483 15-213 1-44-6-18 0-44-43-4
351 152 198 94 3-37 7 77
134 80 100 64 1 72 11-10
017 0-24 016 000 0-39 0-20
004 0-44 008 017 0 63 0 06
013 0-21 0-40 0 28 0 09 0-49
0-25 0-49 007 0 62 0-59 0-30
0 10 0-45 0 38 0-37 0-71 0 27
10 0-52 0 72 0-55 0-09 0-10
10 011 0 55 0 65 010
• • 10 0 20 10 0-52 0-29 10 0-01 0 50 003
10
mmHg in the fastest 1/10 of a second
10-70 - 1 1 — 63 4-39 -5—42 5-56 _7—44
0-79 0-85 0 63 0-61 0-47 0-39
0-61 0-79 0-69 0-74 0-26 0 28
0 65 0 38 0-24 0 12 0-69 0 53
0 04 0-23 0 16 0 17 016 006
0-30 0-36 0 56 0-54 008 0-22
002 0 01 0-09 011 0-11 0 06
007 0-22 0-04 019 0 10 0 07
0 12 003 0 06 0 18 002 003
0 21 0-20 006 002 0-26 0-26
Lumbar Cisternal Differential upwards Differential downwards Cisternal amplitude as a percentage of the lumbar
mmHg mmHg mmHg mmHg %
ALX ACX ADu ADd ALX/ACX ADu/ADd
Lumbar upwards Lumbar downwards };_ Cisternal upwards 55 Cistcrnal downwards Differential upwards Differential downwards
Mean
Standard deviation of means
11 1J
32 -27 19 -18 23 -22
18 13 11 12 14 10
•
*
* Significant at the 5 per cent level, P < 005
012 008 008 010 0-29 0-24
|
•a •5
1 •1 | *
I
§•
•3 •a
O *
•3
1
•§
iff
p
i §•
iff
-8
Slopes
Areas
ist
Amplitudes
Q
oVI •n
*
tn VI
*
0-22 0 36 0-31 0-43 008 0 12
C 7> tn
tn VI
1-0 0-82 0-77 0-68 0-84 0 71
• 10 0-78 0-83 0 45 0 49
• • 1 0 0 92 0-57 0-74
• •
•
•
* • * 10 • 0-45 10 * 0-64 0 84 10
336
BERNARD WILLIAMS
Areas When the lumbar pressure exceeded the cisternal there was a force tending to move cerebrospinal fluid upwards; after the lumbar pressure dropped below the cisternal the pressure gradient within the spine was reversed. The point at which they became equal was referred to as the crossover point, X-X (fig. 1). The area between the curve and the baseline is a measure of impulsive force and has dimensions of pressure and time. It was measured by the method of
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273 100
r
8 Q 50
50
100
ACX x100 ALX FIG. 2. All points represent the mean of ten recordings for one of the 16 cases. ADd is usually less than ADu and increases in size in relatively unblocked cases, i.e. when ACX is large relative to ALX. (Correlation coefficient 0-43.) For definition of these areas see fig. 1.
CSF PRESSURE WAVES
337
counting squares up to crossover for both the lumbar and cisternal pulses (ALX and ACX, fig. 1). In the differential traces the areas were measured both before and after the crossover (fig. 1, ADu and ADd). The range and mean of the means is given in Table 2. The ratios of the areas beneath the curves ACX/ALX and ADu/ADd are plotted against each other in fig. 2. The cases with the greatest attenuation as defined by ACX/ALX are to the left on the horizontal axis. ADd increases as a proportion of ADu in cases with less attenuation; the correlation coefficient Downloaded from http://brain.oxfordjournals.org/ at University of Lethbridge on October 2, 2014
100 \ \ \
\ \ \
8 50
\ \ \ \ \ \ \ \
50
100
ACX x100 ALX FIG. 3. Each point represents the mean often recordings for each of 16 patients. If the recordings were error free they would all lie on the dotted line. Although there is a scatter of results, there is no evidence of bias and the regression curve fits the dotted line almost exactly.
338
'
BERNARD WILLIAMS
is 0-43. It can be seen that all values of ACX are less than 70 per cent of ALX but that the same restriction does not apply to ADd which may be larger than ADu. Further correlation coefficients are given in Table 2.
Complications were as for lumbar puncture or cisternal puncture. Some patients complained of headache for a day. In 2 cases the injection of contrast medium at the end of the procedure was into the subdural space, possibly due to exertions allowing the collection of fluid between the arachnoid and the dura. Myelography was successfully completed following a subsequent puncture. There were no neurological sequels.
DISCUSSION
Origin of the Pulse Wave The origin of the pressure pulse is almost certainly a surge of blood into the epidural venous plexus from the abdominal and thoracic cavities which squeezes the dura. There is an extensive anastomosis through valveless veins all around the vertebral bodies, the transverse processes and the spines (Henriques, 1962). The cisternal pressure pulse is probably caused by a wave of cerebrospinal fluid passing upwards in the subarachnoid space (fig. 4). Part of the pressure pulse at the cistern could theoretically be due to an increase in venous pressure around the cistern. Limitations of the Curves The pressure traces are samples from points within a complex system and care must be taken to avoid simplistic interpretation. There is no point of origin for the cough impulse because the lumbar and thoracic dura is squeezed almost simultaneously. The fact that the lumbar wave is earlier and higher does not mean that it is representative of the origin of the wave. Despite appearances it cannot be assumed that there is a wave generated at or below the lumbar needle which is moving upwards and which then passes the cisternal needle with some separation of the wave components and attenuation of the amplitude.
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Error in measurement was not great except for the areas. This arose because of difficulty in placing the baselines by eye. A minor displacement of the baseline produced a large change in area. Note that ADu should equal ALX minus ACX and therefore that ADu as a percentage of ALX plus ACX as a percentage of ALX should always reach 100 per cent of ALX. A check was therefore available in the graph given as fig. 3. The points should lie on the line linking 0 and 100 per cent, and the degree of scatter can be seen. The regression for these points fits the theoretical line almost exactly indicating a random distribution of error.
CSF PRESSURE WAVES
339
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FIG. 4. Left: the likely situation when the differential trace is upward, i.e. before crossover point. Right: the expected situation after the crossover point, i.e. during ADd (fig. 1) when there is a pressure gradient available to movefluiddownwards. M
340
BERNARD WILLIAMS
The 15 Hz filter may have distorted the waves, lessening the slope of the upward rise and the amplitude. Some lower frequency oscillations remain (fig. 1) and it is probable that these are a genuine intraspinal phenomenon caused by fluid reverberating up and down the spinal canal (Lockey, Poots and Williams, 1975). Some artefacts were noted: the lumbar needle would sometimes produce a flat-topped wave presumably due to a nerve root flapping over the needle tip. Repositioning of the needle would prevent this. Accidental introduction of air made the cisternal pressure higher than the lumbar until it passed up into the head.
The area under the lumbar trace is related to the potential energy required to move CSF. The area under the cisternal curve is probably a result of kinetic energy and accompanied by distension of the pathways, as in fig. 4. The areas under either curve, however, are not a measure of potential or kinetic energy, or of total energy, because the movements of CSF are not measured. They are not interpretable as work done and the slopes are not a measure of power because of this same limitation. Capacitance The capacitance of the CSF pathways is the ability to absorb a given extra volume with a proportional rise of pressure. A high capacitance is the state where a relatively large volume can be absorbed for a small pressure increase and the converse state is a low capacitance. The capacitance of the venous system must also be considered, and as both capacitances are located within the same spinal canal and cranium they are therefore mutually dependent. The two fluids are in balance across membranes within a relatively rigid structure bounded by bones and the ligamenta flava, with relatively little possibility of movement of epidural fat through the intervertebral foraminae. The degree of filling of the veins and of the CSF pathways prior to the cough is of importance in determining the outcome of the coughing. For a more extensive discussion see Williams (1974) and Lockey et al. (1975). If the spine is considered as an organ pipe it can neither be analysed as an open-ended pipe nor a closedended one because the skull with its capacitance provides the closure. The capacitance of the CSF pathway at the top of the spine is likely always to be great unless the foramen magnum is blocked or there is an intracranial space-occupying lesion. This is because the head contains a large number of compressible veins. Because of the difference in capacitance between the upper and lower end of the spine it could be anticipated that the cisternal cough pulse would be small in comparison with the lumbar pulse. There are two opposing theoretical factors to consider. One is that the pressure wave produced by CSF moving up the spine might be accompanied by venous distension and augmented by this. However,
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Energy, Work Done and Power
CSF PRESSURE WAVES
341
The Significance of the Slopes Since none of the cases had a complete blockage of the spinal subarachnoid space it may be assumed that fluid moved in proportion to the pressure difference and that work has been done. The rate of performing work is power. The power of the impulses is therefore probably best expressed by, but not accurately measured by, the slope of the curves. The power is of importance because it is the rate of absorption of energy by the tissues that is important rather than the total amount absorbed. The power of the cough impulse lessens as it ascends, the upstroke is always steeper in the lumbar than the cisternal curves and only in one case did the mean of the downward gradients of the cisternal pulses exceed that of the lumbar. The slope of the differential downwards, however, was steeper than the lumbar downwards in 3 cases and steeper than the cisternal in 10 cases although it was never as steep as the lumbar upward. Thus the power of the rebound downwards from the head to the spine may exceed that of the initial upward impulse, although the total energy of the rebound will be less. Since the slopes are derived from maxima and not from identical points in time, slope lumbar minus slope cisternal is not equal to slope differential. The Significance of ADu and ADd (fig. 1) The relationship between the pressure wave and volume shifts offluidis complex. If there is free communication and a pressure difference then fluid will move. ADu and ADd (fig. 1) represent an upward impulsive force and a downward impulsive force respectively, but the crossover point (X, fig. 1) does not represent reversal of flow. The inertia of the upward movement of fluid momentarily continues to carry it upwards against the pressure gradient. The kinetic energy is then converted back into potential energy which drives the fluid downwards once more. If a total block were present and no transmission from veins occurred above the block, then ADu would be equal to ALX and there would be no ACX and no
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the capacitance of the veins in the neck and around the head is high in the sitting position, and many of the neck veins are empty. Secondly a wave travelling upwards may be reflected from the head so that the pressure rise at the cisternal end is the summation of two waves, the incident wave and the reflected wave. A summation of such pressure waves would not necessarily have a great energy value because the fluid at the tip of the needle need not be in a state of rapid movement. Thus, although loss of energy is inevitable as the wave moves up the CSF pathways, lessening of amplitude is not similarly inevitable. That a cisternal amplitude higher than the lumbar was not observed suggests that in the erect posture the capacitance of the veins of the upper thorax and neck is sufficient to absorb the upward thrust of venous distension, at least over the short sharp coughs used in this study, and that the intracranial capacitance is also high.
342
BERNARD WILLIAMS
ADd (seefig.1). Conversely if there was complete freedom offlowthen ALX would equal ACX and there would be no differential pressure either upwards or downwards. Plainly, although complete block is feasible, lack of resistance is impossible and ADd is higher when blockage is least (fig. 2). It is notable that ADd rises steeply and can exceed 100 per cent of ADu.
Baseline Shifts The cord is surrounded by a subarachnoid space with a cross-sectional appearance like an annulus. The force moving CSF is proportional to the pressure gradient multiplied by the area of the annulus. The frictional restraint of movement of fluid and to the passage of the pressure wave is inversely proportional to the area of the annulus. The area at any point varies because of the elasticity and compressibility of the dura. Drainage of CSF will exaggerate the effects of blockage on performing Queckenstedt's test and inflation of the pathway will make such a blockage less evident (Gilland, 1966). When a wave of pressure is generated in the lumbar region and passes up the CSF pathways it may produce a wave of distension passing in a similar direction in the dura (fig. 4). This wave may therefore pass some obstructions more readily than a less energetic rebound wave. The result may be that fluid which readily moves upwards past an obstruction returns only slowly. Such considerations are relevant to the baseline shifts shown in fig. 5. Perhaps the development of a low pressure below a partial block in Froin's syndrome may be due to evacuation of the lumbar CSF space by muscular exertion. Baseline shifts may also result from valvular mechanisms. A valve is produced by cerebellar ectopia at the foramen magnum when the cerebellar tonsils protrude downwards into the spinal canal. This herniation when congenital may be very advanced and form the Arnold-Chiari malformation. Upward passage of fluid is relatively easy but the downward rebound from the head towards the
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Diseases Associated with Pulsatile Movement The upward thrust of CSF may cause enlargement of intracranial arachnoid pouches (Williams and Guthkelch, 1974). Either upward or downward pulsation may be responsible for filling spinal subarachnoid cysts, depending upon the local anatomy. Pressure pulses may be transmitted across spinal cord walls in syringomyelia causing the syrinx fluid to be driven upwards. Such a phenomenon may be partly responsible for the predominance of syringomyelic cavities at the upper end of the spinal cord. It is also the probable explanation for syringobulbia and the upward spread of fluid from the site of the cord lesion which causes syringomyelia above a paraplegia. The observation that the lumbar pressure pulse always precedes the cisternal appears to dispose of Williams'first(1967) hypothesis about syrinxfillingin response to venous engorgement of the head, and demands its replacement by the hypothesis that it is the downward movement, that is, the phase represented by ADd (fig. 1) which fills the syrinx (Williams, 1971, 1973a).
CSF PRESSURE WAVES
343
90
3
CD
x E
90
to (J
50
40 sec 60
FIG. 5. Marked dissociation between cisternal and lumbar needles produced by a sequence of eight coughs. Note that the lumbar baseline drops progressively after each cough with little increase in the resting cisternal level. The failure of the cisternal baseline pressure to rise reflects the greater capacitance of the top end of the spinal canal. Note that the evacuation of the lumbar sac produces a gross diminution of the arterial pulsation which does not return until the baseline has reached the normal levels.
spine may cause tissue to jam in the foramen magnum. A pressure difference is thus generated between the head and the spine or a pre-existing difference may be exaggerated. If the tonsils are engaged in the foramen magnum repeated attacks of 'jamming' may occur in response to the ebb and flow of fluid through the foramen magnum. The tonsils would then become progressively further impacted (Williams, 1971). This explanation was offered for cough headache by Gardner (1945). Permanent relief of cough headache has been reported after air encephalography (Symonds, 1956) and this could be explained by disimpaction at the foramen magnum. Measurements of difference of pressure between the head and the spine engendered by coughing and straining have been reported (Williams, 1973a), and the suggestion made that craniospinal pressure dissociation may be responsible for filling the syrinx in cases of communicating syringomyelia. It is of interest that communicating syringomyelia may occur from arachnoiditis (Barnett, Foster and Hudgson, 1973); the dissociation in pressure may therefore take place without a valve as it has done across the area of cervical spondylosis illustrated in fig. 5. In infants with spina bifida changes in the capacitance of the lumbar CSF sac following removal of a meningocele may allow cough impulses, or the pressure pulses produced by crying, to exaggerate craniospinal pressure differences.
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DC Q.
344
BERNARD WILLIAMS
Incipient hydrocephalus may thus be precipitated (Williams, 1971, 1974). Raised intracranial pressure after coughing and straining could be responsible for exacerbation of hydrocephalus due to stenosis of the aqueduct.
Two limitations are obvious. Results on cough testing may be invalid when blockage is present below the cervical region because of venous compression of the subarachnoid space above the block by the venous pressure rise in the thorax on coughing. More important, Queckenstedt's test is now largely supplanted by myelography because of the additional anatomical information which the latter gives.
SUMMARY
CSF pressure recordings have been taken from the lumbar region and the cisterna magna of 16 patients during coughing in the sitting position. Isolated coughs of low amplitude have been studied. The lumbar pressure waves occur sooner, rise higher and faster than the cisternal pressure waves and fall faster, sooner and lower. Thus there is a phase during which the lumbar pressure exceeds the cisternal, followed by one in which the cisternal exceeds the lumbar. These phenomena may be conveniently displayed on a differential trace. The phase during which the cisternal pressure exceeds the lumbar may be protracted.
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Comparison with Queckenstedt's Test It was at first hoped that since this test provided a form of 'impulse testing' of the patency of the CSF pathways with a high energy and a rapid rise and fall, it might prove of greater value than Queckenstedt's test which has a relatively low energy and a separate rise and fall. In testing with cough the rate of change is very much sharper than in Queckenstedt's test. There is a pulse to measure and the area, amplitude and slopes are all available. The accuracy of the measurements show marked factional losses even in the normal but the limits of normality are not denned. It seems that when ACX (fig. 1) is less than half ALX, it is then abnormally attenuated. A normal cisternal amplitude should probably be above 70 per cent of the lumbar. Further study might be expected to show which measurement would have the greatest value in expressing blockage. This study is limited because no cases of complete blockage are included since all such cases had been diagnosed before being referred for neurosurgery. Attempts to correlate myelographic findings with these results have failed because of the difficulty in grading the myelograms. Radiological blockage varies with positioning of the head and is subjective. It seems probable that this test is potentially superior to either Queckenstedt's test or myelography as an assessment of a degree of blockage of the spinal canal, but further work is necessary.
CSF P R E S S U R E WAVES
345
The merits and limitations of cough impulse as a clinical test for spinal blockage are discussed, and the suggestion is made that after further evaluation they may provide a more sensitive indication of spinal blockage than Queckenstedt's test. ACKNOWLEDGEMENTS Reckitt and Colman Limited and the Association for Spina Bifida each provided a Devices M19 recorder for the Hull Royal Infirmary and both were used in this study. The Hull Branch of the Association for Spina Bifida and Hydrocephalus gave the P23H transducer and the Wellcome Foundation provided technical help. Miss P. Willey carried out the pressure recordings and help with statistical analysis has been provided by Mr. T. Sorahan and Dr. J. R. Jackson.
REFERENCES BARNETT, H. J. M., FOSTER, J. B., and HUDGSON, P. (1973) Syringomyelia. London: W. B. Saunders.
BEDFORD, T. H. (1935) The effects of increased intracranial venous pressure of the cerebrospinal fluid. Brain, 58, 427-447. BERING, E. A., JR. (1955) Choroid plexus and arterial pulsation of CSF. Demonstration of choroid plexus as a CSF pump. Archives of Neurology and Psychiatry, Chicago, 73, 165-172. DEREYMAEKER, A., STEVENS, A., ROMBOUTS, J. J., LACHERON, J. M., and PIERQUIN, A. (1971) Study
of the influence of the arterial pressure upon the morphology of cisternal CSF pulsation. European Neurology, 5, 107-114. Du BOULAY, G. H., O'CONNELL, J., CURRIE, J., BOSTICK, T., and VERITY, P. (1972) Further investigations
on pulsatile movements in the cerebrospinal fluid pathways. Ada Radiologica (Stockholm), 13, 496-523. GARDNER, W. J. (1945) Cerebrospinal fluid: Dynamics. In: Medical Physics. Edited by O. Glaser. Chicago: Year Book Co., pp. 148-152. GILLAND, O. (1966) CSF Dynamic Diagnosis of Spinal Block. Stockholm: Almqvist and Wiksell. HENRIQUES, C. Q. (1962) The veins of the vertebral column and their role in the spread of cancer. Annals of the Royal College of Surgeons of England, 31, 1-22. LAITINEN, L. (1968) Origin of the arterial pulsation of cerebrospinal fluid. Ada Neurologica Scandinavica, 44, 168-176. LAKKE, J. P. W. F. (1969) Queckenstedt's Test. Amsterdam: Excerpta Medica. LOCKEY, P., POOTS, G., and WILLIAMS, B. (1975) Theoretical aspects of the attenuation of pressure pulses within the CSF pathways. Medical and Biological Engineering, 14, 861-869.
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It is suggested that Froin's syndrome, central subarachnoid pouches and syringobulbia may be associated with upward pressure waves. Cough headache, the filling stages of communicating syringomyelia and tonsillar herniation may be associated with valve-like blockage at the foramen magnum which produces craniospinal pressure dissociation by interfering with downward or rebound pulsation. Decompensation of hydrocephalus after birth may be related to pulsation in association with crying; also after removal of a meningocele sac decompensation may be related to the effects of similar pulsation modified by changes in capacitance following operation. The cord destruction of syringomyelia, and the mechanisms which fill spinal subarachnoid cysts may be related to pressure waves directed both upwards and downwards.
346
BERNARD WILLIAMS
{Received September 5, 1974)
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SYMONDS, C. P. (1956) Cough headache. Brain, 79, 557-568. WILLIAMS, B. (1969) The distending force in the production of communicating syringomyelia. Lancet, 2, 189-193. (1971) Further thoughts on the valvular action of the Amold-Chiari malformation. Developmental Medicine and Child Neurology, Supplement, 25, 105-112. (1973a) The valvular action of the Arnold-Chiari malformation. In: Proceedings of the 1st International Conference on Intracranial Pressure. Edited by M. Brock and H. Dietz. Berlin: Springer Verlag, pp. 338-342. (19736) Is aqueduct stenosis a result of hydrocephalus? Brain, 96, 399-412. (1974) A demonstration analogue for ventricular and intraspinal dynamics. Journal of the Neurological Sciences, 23, 445-461. and GUTHKELCH, A. N. (1974) Why do central arachnoid pouches expand? Journal of Neurology, Neuroswgery and Psychiatry, 37, 1085-1092.
CEREBROSPINAL FLUID PRESSURE CHANGES IN RESPONSE TO COUGHING by BERNARD WILLIAMS
INTRODUCTION
THE pressure of the cerebrospinal fluid (CSF) is subject to continual variation, and the role of such pulsation in producing damage has been subject to much speculation but little systematic study. When excessive, or maldirected, pulsations probably cause or aggravate some diseases by the imposition of forces which may produce distension of cavities or injection of fluid into tissue planes. Such mechanisms may occur in hydrocephalus, porencephalic cysts, arachnoid cysts and syringomyelia. Two sources of pulsation in CSF pathways are the arterial pulse wave and the venous changes consequent upon change of posture, respiration, coughing, muscular exertion and so on. The arterial pulse has received attention from Bering (1955), Laitinen (1968) and Dereymaeker, Stevens, Rombouts, Lacheron and Pierquin (1971), but the venous pulses have largely been neglected, although two comprehensive monographs have appeared on Queckenstedt's test (Gilland, 1966; Lakke, 1969); and movements within the CSF pathways in response to venous'and arterial pulsation have been reported by Du Boulay, O'Connell, Currie, Bostick and Verity (1972). The venous pressure is transmitted to the CSF pathways more readily than the arterial because the CSF and venous blood are in a state of balance across venous membranes (Bedford, 1935). Pressure swings in response to venous changes are big and easy to demonstrate and this study shows features of this type of pulsation. The pulsation itself is only of importance inasmuch as it transmits energy to tissue and it is the difference between pressures of adjacent areas which is important. The propagation of a wave depends upon a moving difference in pressure. Two sampling sites were therefore chosen at points where clinical puncture of the CSF pathways is normally carried out, the lumbar region and the cisternal, and the differences were studied by direct subtraction of the cisternal pressure from the lumbar.
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(From the Midland Centre for Neurosurgery and Neurology, Holly Lane, West Midlands, B67 7JX)
332
BERNARD WILLIAMS
The only measurements possible in this study were pressure and time. The timing of the venous pulse is a factor which has apparently not previously been measured. Williams (1969) suggested that under certain circumstances coughing might produce a rise in pressure which begins in the head before it begins in the spine; although radiological observations tend to suggest that the movement of myodil is always initially upwards after coughing (Du Boulay et ah, 1972).
Because the greater part of active human exercise is undertaken in the upright position measurements were taken from patients sitting erect.
METHODS Sixteen patients, all with disease in the cervical region and requiring myelography, were studied. Pressure recordings were made with 3^ in. 18 gauge needles in the lumbar region and the cisterna magna. In all cases the mean pressures were identical if they were referred to atmospheric zero at the manubriosternal joint. The patients were all tested with sharp coughs of short duration and limited amplitude. Recordings were taken with a Statham P23H differential manometer which gave two pressure recordings and the difference. The 60 cm tubes which connected the needles to the transducers had a natural frequency around 23 Hz, despite restraint by adhesive tape. Attenuation of high frequencies by a 15 Hz filter lessened the vibrations from the connecting lines and did not much alter the shape of the trace.
RESULTS
Clinical details are given in Table 1. The traces have been analysed for amplitudes, slopes and the areas between the curves and the resting baselines as shown in fig. 1. The differential pulse waves were measured from zero in the middle of the trace. The description and analysis of results will be readily followed by frequent reference to fig. 1. Individual pulse shapes, although they tended to be similar for any one patient, differed between one patient and another. Sometimes inhalation before the cough produced a fall of the baseline, sometimes a slight elevation preceded the main cough pulse, apparently produced by tensing the abdominal muscles.
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It seemed likely that the pulse wave produced by coughing would be attenuated during its passage up the spinal canal; and that the attenuation would reflect any blockage or narrowing of that pathway more effectively than Queckenstedt's test, because of the more rapid changes and higher amplitudes involved. Attenuation might be expected to diminish the amplitude of the ascending pulse, lessen its area, lower the rates of rise and fall (slopes) and to delay its passage. Such measurements were therefore made in patients in whom the information provided would be of at least potential clinical value even though the method, at first, was unproven.
CSF PRESSURE WAVES
333
70 r
=>
70
I 1
7. V
CO CO
LLJ
IT
a.
35 r
35 L
I I
I I I I I i i I i > i ' i i i i i I i i i i i i
i i i I i i i i i i i i
i I i i i
i i i i i i
1 SECOND1
FIG. 1. Illustration of the methods of analysis of results (Case 7). The dotted areas were measured only up to the crossover point, X-X. The coughs on the right have been used to illustrate the methods of measuring amplitudes and slopes. Slopes were not taken from the steepest part of the curve but from the fastest rise in 1/10 of a second in order to eliminate artefacts due to oscillations in connecting lines. Oscillations at around 5 Hz are visible in this trace.
Amplitudes The mean amplitudes in the lumbar region were between 19 and 97 mmHg above the baseline. Although amplitudes above 100 mmHg could be produced by most subjects, the records were ragged and the coughs were often preceded by abdominal tension and followed by minor coughs or gulps. The cisternal pulses were always lower in amplitude than the lumbar. From each patient ten coughs were analysed and the range, mean and standard deviations calculated. The values in Table 2 therefore give the range of the means and the means of the mean values of ten coughs for each of 16 patients. The standard deviations of the means are also given. Correlation coefficients in Table 2 have also been calculated from the means of ten coughs for each patient. The amplitude of the differential pulse upwards was usually greater than that downwards but not invariably.
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E
334
BERNARD WILLIAMS TABLE 1. CLINICAL ASPECTS OF CASES Radiology
Diagnosis 1 2 3
Severe pain neck and arm Myelopathy, undiagnosed Cervical myelopathy due to spondylosis
4 5
Severe neck pain Cervical myelopathy due to spondylosis Post-traumatic quadnparesis
6 7
9 10 11 12 13
14 15
16
due to due to
due to
Gross narrowing of spinal canal Partial block at C5-6
due to
Almost complete block C5-6
with disc
Compression from C5-6 disc
due to
Narrow spinal canal with C4-5 disc protrusion
due to
Cervical myelopathy due to spondylosis Multiple sclerosis with advanced cervical spondylosis Cervical myelopathy due to spondylous
Narrow spinal canal compression from C3-C7 No blockage—wide spinal canal Narrow spinal canal C4-5 disc protrusion
Post-operative result
_ Decompressive laminectomy
Recovery Unchanged Improvement
— Decompressive laminectomy
Recovery Improvement
Anterior fusion for instability of subluxation Decompressive laminectomy
No change
Due removed and anterior fusion Decompressive laminectomy
Improvement
Anterior fusion
Improvement
Laminectomy and lateral disc removal Anterior cervical fusion and disc removal Decompressive laminectomy followed later by anterior fusion Decompressive laminectomy
Recovery
Improvement
Unchanged
Improvement Improvement after each operation Unchanged Unchanged
Decompressive laminectomy
Improvement
Slopes The slopes of rise of the lumbar, cisternal and differential upwards pressures were all taken as the fastest change within any one-tenth of a second. Drawing a tangent to the steepest part of the curve gave higher results but these were questionable because of resonance in the manometer tubing. The slope of the fall of these three curves was also recorded; the rise was given a positive and the descent a negative sign. The return of the downward part of the differential to the baseline was often so shallow and marred by resonance that measurements could not be made. Timing The cisternal pulse was always later than the lumbar pulse. The time-lag was difficult to measure because of the irregular pulse shapes; there was sometimes a flattening or a double peak (fig. 1). The time delay was always over 004 s and the greater the attenuation of the cisternal pulse the later it arrived. The duration of the main cough impulse was around 0-6 to 0-9 s but the disturbance from the start of the cough to the end was sometimes very much longer.
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8
Cervical myelopathy spondylosis Cervical myelopathy spondylosis Cervical myelopathy spondylosis Cervical myelopathy spondylosis Cervical myelopathy large single disc Cervical myelopathy protrusion Cervical myelopathy spondylosis
Normal Normal Marked osteophyte encroachment of spinal canal Normal Multiple disc protrusion but wide canal, slight kyphos No blockage on myelography unstable subluxation Severe narrowing of spinal canal C2-7 Central disc protrusion C5-6
Operation
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TABLE 2. MEANS OF TEN RESULTS FROM EACH OF THE 16 PATIENTS
Correlation coefficients
Range
g T
E •3
Si
1
\
3
U T
Q
X
U
T
Q
wards
d 5?
|
-j
19-97 10-70 6-45 0-5—21 24-91
46-37 28 81 2712 - 9 24 60-95
1890 16 15 11-27 4-92 19-68
10 0-84 0 63 0 34 0-26
10 . * * 0-23 10 0-58 002 10 0-57 0-29 0 50 10
Arbitrary Arbitrary Arbitrary Arbitrary Ratio Ratio
104-677 48-333 60-483 15-213 1-44-6-18 0-44-43-4
351 152 198 94 3-37 7 77
134 80 100 64 1 72 11-10
017 0-24 016 000 0-39 0-20
004 0-44 008 017 0 63 0 06
013 0-21 0-40 0 28 0 09 0-49
0-25 0-49 007 0 62 0-59 0-30
0 10 0-45 0 38 0-37 0-71 0 27
10 0-52 0 72 0-55 0-09 0-10
10 011 0 55 0 65 010
• • 10 0 20 10 0-52 0-29 10 0-01 0 50 003
10
mmHg in the fastest 1/10 of a second
10-70 - 1 1 — 63 4-39 -5—42 5-56 _7—44
0-79 0-85 0 63 0-61 0-47 0-39
0-61 0-79 0-69 0-74 0-26 0 28
0 65 0 38 0-24 0 12 0-69 0 53
0 04 0-23 0 16 0 17 016 006
0-30 0-36 0 56 0-54 008 0-22
002 0 01 0-09 011 0-11 0 06
007 0-22 0-04 019 0 10 0 07
0 12 003 0 06 0 18 002 003
0 21 0-20 006 002 0-26 0-26
Lumbar Cisternal Differential upwards Differential downwards Cisternal amplitude as a percentage of the lumbar
mmHg mmHg mmHg mmHg %
ALX ACX ADu ADd ALX/ACX ADu/ADd
Lumbar upwards Lumbar downwards };_ Cisternal upwards 55 Cistcrnal downwards Differential upwards Differential downwards
Mean
Standard deviation of means
11 1J
32 -27 19 -18 23 -22
18 13 11 12 14 10
•
*
* Significant at the 5 per cent level, P < 005
012 008 008 010 0-29 0-24
|
•a •5
1 •1 | *
I
§•
•3 •a
O *
•3
1
•§
iff
p
i §•
iff
-8
Slopes
Areas
ist
Amplitudes
Q
oVI •n
*
tn VI
*
0-22 0 36 0-31 0-43 008 0 12
C 7> tn
tn VI
1-0 0-82 0-77 0-68 0-84 0 71
• 10 0-78 0-83 0 45 0 49
• • 1 0 0 92 0-57 0-74
• •
•
•
* • * 10 • 0-45 10 * 0-64 0 84 10
336
BERNARD WILLIAMS
Areas When the lumbar pressure exceeded the cisternal there was a force tending to move cerebrospinal fluid upwards; after the lumbar pressure dropped below the cisternal the pressure gradient within the spine was reversed. The point at which they became equal was referred to as the crossover point, X-X (fig. 1). The area between the curve and the baseline is a measure of impulsive force and has dimensions of pressure and time. It was measured by the method of
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273 100
r
8 Q 50
50
100
ACX x100 ALX FIG. 2. All points represent the mean of ten recordings for one of the 16 cases. ADd is usually less than ADu and increases in size in relatively unblocked cases, i.e. when ACX is large relative to ALX. (Correlation coefficient 0-43.) For definition of these areas see fig. 1.
CSF PRESSURE WAVES
337
counting squares up to crossover for both the lumbar and cisternal pulses (ALX and ACX, fig. 1). In the differential traces the areas were measured both before and after the crossover (fig. 1, ADu and ADd). The range and mean of the means is given in Table 2. The ratios of the areas beneath the curves ACX/ALX and ADu/ADd are plotted against each other in fig. 2. The cases with the greatest attenuation as defined by ACX/ALX are to the left on the horizontal axis. ADd increases as a proportion of ADu in cases with less attenuation; the correlation coefficient Downloaded from http://brain.oxfordjournals.org/ at University of Lethbridge on October 2, 2014
100 \ \ \
\ \ \
8 50
\ \ \ \ \ \ \ \
50
100
ACX x100 ALX FIG. 3. Each point represents the mean often recordings for each of 16 patients. If the recordings were error free they would all lie on the dotted line. Although there is a scatter of results, there is no evidence of bias and the regression curve fits the dotted line almost exactly.
338
'
BERNARD WILLIAMS
is 0-43. It can be seen that all values of ACX are less than 70 per cent of ALX but that the same restriction does not apply to ADd which may be larger than ADu. Further correlation coefficients are given in Table 2.
Complications were as for lumbar puncture or cisternal puncture. Some patients complained of headache for a day. In 2 cases the injection of contrast medium at the end of the procedure was into the subdural space, possibly due to exertions allowing the collection of fluid between the arachnoid and the dura. Myelography was successfully completed following a subsequent puncture. There were no neurological sequels.
DISCUSSION
Origin of the Pulse Wave The origin of the pressure pulse is almost certainly a surge of blood into the epidural venous plexus from the abdominal and thoracic cavities which squeezes the dura. There is an extensive anastomosis through valveless veins all around the vertebral bodies, the transverse processes and the spines (Henriques, 1962). The cisternal pressure pulse is probably caused by a wave of cerebrospinal fluid passing upwards in the subarachnoid space (fig. 4). Part of the pressure pulse at the cistern could theoretically be due to an increase in venous pressure around the cistern. Limitations of the Curves The pressure traces are samples from points within a complex system and care must be taken to avoid simplistic interpretation. There is no point of origin for the cough impulse because the lumbar and thoracic dura is squeezed almost simultaneously. The fact that the lumbar wave is earlier and higher does not mean that it is representative of the origin of the wave. Despite appearances it cannot be assumed that there is a wave generated at or below the lumbar needle which is moving upwards and which then passes the cisternal needle with some separation of the wave components and attenuation of the amplitude.
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Error in measurement was not great except for the areas. This arose because of difficulty in placing the baselines by eye. A minor displacement of the baseline produced a large change in area. Note that ADu should equal ALX minus ACX and therefore that ADu as a percentage of ALX plus ACX as a percentage of ALX should always reach 100 per cent of ALX. A check was therefore available in the graph given as fig. 3. The points should lie on the line linking 0 and 100 per cent, and the degree of scatter can be seen. The regression for these points fits the theoretical line almost exactly indicating a random distribution of error.
CSF PRESSURE WAVES
339
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FIG. 4. Left: the likely situation when the differential trace is upward, i.e. before crossover point. Right: the expected situation after the crossover point, i.e. during ADd (fig. 1) when there is a pressure gradient available to movefluiddownwards. M
340
BERNARD WILLIAMS
The 15 Hz filter may have distorted the waves, lessening the slope of the upward rise and the amplitude. Some lower frequency oscillations remain (fig. 1) and it is probable that these are a genuine intraspinal phenomenon caused by fluid reverberating up and down the spinal canal (Lockey, Poots and Williams, 1975). Some artefacts were noted: the lumbar needle would sometimes produce a flat-topped wave presumably due to a nerve root flapping over the needle tip. Repositioning of the needle would prevent this. Accidental introduction of air made the cisternal pressure higher than the lumbar until it passed up into the head.
The area under the lumbar trace is related to the potential energy required to move CSF. The area under the cisternal curve is probably a result of kinetic energy and accompanied by distension of the pathways, as in fig. 4. The areas under either curve, however, are not a measure of potential or kinetic energy, or of total energy, because the movements of CSF are not measured. They are not interpretable as work done and the slopes are not a measure of power because of this same limitation. Capacitance The capacitance of the CSF pathways is the ability to absorb a given extra volume with a proportional rise of pressure. A high capacitance is the state where a relatively large volume can be absorbed for a small pressure increase and the converse state is a low capacitance. The capacitance of the venous system must also be considered, and as both capacitances are located within the same spinal canal and cranium they are therefore mutually dependent. The two fluids are in balance across membranes within a relatively rigid structure bounded by bones and the ligamenta flava, with relatively little possibility of movement of epidural fat through the intervertebral foraminae. The degree of filling of the veins and of the CSF pathways prior to the cough is of importance in determining the outcome of the coughing. For a more extensive discussion see Williams (1974) and Lockey et al. (1975). If the spine is considered as an organ pipe it can neither be analysed as an open-ended pipe nor a closedended one because the skull with its capacitance provides the closure. The capacitance of the CSF pathway at the top of the spine is likely always to be great unless the foramen magnum is blocked or there is an intracranial space-occupying lesion. This is because the head contains a large number of compressible veins. Because of the difference in capacitance between the upper and lower end of the spine it could be anticipated that the cisternal cough pulse would be small in comparison with the lumbar pulse. There are two opposing theoretical factors to consider. One is that the pressure wave produced by CSF moving up the spine might be accompanied by venous distension and augmented by this. However,
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Energy, Work Done and Power
CSF PRESSURE WAVES
341
The Significance of the Slopes Since none of the cases had a complete blockage of the spinal subarachnoid space it may be assumed that fluid moved in proportion to the pressure difference and that work has been done. The rate of performing work is power. The power of the impulses is therefore probably best expressed by, but not accurately measured by, the slope of the curves. The power is of importance because it is the rate of absorption of energy by the tissues that is important rather than the total amount absorbed. The power of the cough impulse lessens as it ascends, the upstroke is always steeper in the lumbar than the cisternal curves and only in one case did the mean of the downward gradients of the cisternal pulses exceed that of the lumbar. The slope of the differential downwards, however, was steeper than the lumbar downwards in 3 cases and steeper than the cisternal in 10 cases although it was never as steep as the lumbar upward. Thus the power of the rebound downwards from the head to the spine may exceed that of the initial upward impulse, although the total energy of the rebound will be less. Since the slopes are derived from maxima and not from identical points in time, slope lumbar minus slope cisternal is not equal to slope differential. The Significance of ADu and ADd (fig. 1) The relationship between the pressure wave and volume shifts offluidis complex. If there is free communication and a pressure difference then fluid will move. ADu and ADd (fig. 1) represent an upward impulsive force and a downward impulsive force respectively, but the crossover point (X, fig. 1) does not represent reversal of flow. The inertia of the upward movement of fluid momentarily continues to carry it upwards against the pressure gradient. The kinetic energy is then converted back into potential energy which drives the fluid downwards once more. If a total block were present and no transmission from veins occurred above the block, then ADu would be equal to ALX and there would be no ACX and no
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the capacitance of the veins in the neck and around the head is high in the sitting position, and many of the neck veins are empty. Secondly a wave travelling upwards may be reflected from the head so that the pressure rise at the cisternal end is the summation of two waves, the incident wave and the reflected wave. A summation of such pressure waves would not necessarily have a great energy value because the fluid at the tip of the needle need not be in a state of rapid movement. Thus, although loss of energy is inevitable as the wave moves up the CSF pathways, lessening of amplitude is not similarly inevitable. That a cisternal amplitude higher than the lumbar was not observed suggests that in the erect posture the capacitance of the veins of the upper thorax and neck is sufficient to absorb the upward thrust of venous distension, at least over the short sharp coughs used in this study, and that the intracranial capacitance is also high.
342
BERNARD WILLIAMS
ADd (seefig.1). Conversely if there was complete freedom offlowthen ALX would equal ACX and there would be no differential pressure either upwards or downwards. Plainly, although complete block is feasible, lack of resistance is impossible and ADd is higher when blockage is least (fig. 2). It is notable that ADd rises steeply and can exceed 100 per cent of ADu.
Baseline Shifts The cord is surrounded by a subarachnoid space with a cross-sectional appearance like an annulus. The force moving CSF is proportional to the pressure gradient multiplied by the area of the annulus. The frictional restraint of movement of fluid and to the passage of the pressure wave is inversely proportional to the area of the annulus. The area at any point varies because of the elasticity and compressibility of the dura. Drainage of CSF will exaggerate the effects of blockage on performing Queckenstedt's test and inflation of the pathway will make such a blockage less evident (Gilland, 1966). When a wave of pressure is generated in the lumbar region and passes up the CSF pathways it may produce a wave of distension passing in a similar direction in the dura (fig. 4). This wave may therefore pass some obstructions more readily than a less energetic rebound wave. The result may be that fluid which readily moves upwards past an obstruction returns only slowly. Such considerations are relevant to the baseline shifts shown in fig. 5. Perhaps the development of a low pressure below a partial block in Froin's syndrome may be due to evacuation of the lumbar CSF space by muscular exertion. Baseline shifts may also result from valvular mechanisms. A valve is produced by cerebellar ectopia at the foramen magnum when the cerebellar tonsils protrude downwards into the spinal canal. This herniation when congenital may be very advanced and form the Arnold-Chiari malformation. Upward passage of fluid is relatively easy but the downward rebound from the head towards the
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Diseases Associated with Pulsatile Movement The upward thrust of CSF may cause enlargement of intracranial arachnoid pouches (Williams and Guthkelch, 1974). Either upward or downward pulsation may be responsible for filling spinal subarachnoid cysts, depending upon the local anatomy. Pressure pulses may be transmitted across spinal cord walls in syringomyelia causing the syrinx fluid to be driven upwards. Such a phenomenon may be partly responsible for the predominance of syringomyelic cavities at the upper end of the spinal cord. It is also the probable explanation for syringobulbia and the upward spread of fluid from the site of the cord lesion which causes syringomyelia above a paraplegia. The observation that the lumbar pressure pulse always precedes the cisternal appears to dispose of Williams'first(1967) hypothesis about syrinxfillingin response to venous engorgement of the head, and demands its replacement by the hypothesis that it is the downward movement, that is, the phase represented by ADd (fig. 1) which fills the syrinx (Williams, 1971, 1973a).
CSF PRESSURE WAVES
343
90
3
CD
x E
90
to (J
50
40 sec 60
FIG. 5. Marked dissociation between cisternal and lumbar needles produced by a sequence of eight coughs. Note that the lumbar baseline drops progressively after each cough with little increase in the resting cisternal level. The failure of the cisternal baseline pressure to rise reflects the greater capacitance of the top end of the spinal canal. Note that the evacuation of the lumbar sac produces a gross diminution of the arterial pulsation which does not return until the baseline has reached the normal levels.
spine may cause tissue to jam in the foramen magnum. A pressure difference is thus generated between the head and the spine or a pre-existing difference may be exaggerated. If the tonsils are engaged in the foramen magnum repeated attacks of 'jamming' may occur in response to the ebb and flow of fluid through the foramen magnum. The tonsils would then become progressively further impacted (Williams, 1971). This explanation was offered for cough headache by Gardner (1945). Permanent relief of cough headache has been reported after air encephalography (Symonds, 1956) and this could be explained by disimpaction at the foramen magnum. Measurements of difference of pressure between the head and the spine engendered by coughing and straining have been reported (Williams, 1973a), and the suggestion made that craniospinal pressure dissociation may be responsible for filling the syrinx in cases of communicating syringomyelia. It is of interest that communicating syringomyelia may occur from arachnoiditis (Barnett, Foster and Hudgson, 1973); the dissociation in pressure may therefore take place without a valve as it has done across the area of cervical spondylosis illustrated in fig. 5. In infants with spina bifida changes in the capacitance of the lumbar CSF sac following removal of a meningocele may allow cough impulses, or the pressure pulses produced by crying, to exaggerate craniospinal pressure differences.
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DC Q.
344
BERNARD WILLIAMS
Incipient hydrocephalus may thus be precipitated (Williams, 1971, 1974). Raised intracranial pressure after coughing and straining could be responsible for exacerbation of hydrocephalus due to stenosis of the aqueduct.
Two limitations are obvious. Results on cough testing may be invalid when blockage is present below the cervical region because of venous compression of the subarachnoid space above the block by the venous pressure rise in the thorax on coughing. More important, Queckenstedt's test is now largely supplanted by myelography because of the additional anatomical information which the latter gives.
SUMMARY
CSF pressure recordings have been taken from the lumbar region and the cisterna magna of 16 patients during coughing in the sitting position. Isolated coughs of low amplitude have been studied. The lumbar pressure waves occur sooner, rise higher and faster than the cisternal pressure waves and fall faster, sooner and lower. Thus there is a phase during which the lumbar pressure exceeds the cisternal, followed by one in which the cisternal exceeds the lumbar. These phenomena may be conveniently displayed on a differential trace. The phase during which the cisternal pressure exceeds the lumbar may be protracted.
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Comparison with Queckenstedt's Test It was at first hoped that since this test provided a form of 'impulse testing' of the patency of the CSF pathways with a high energy and a rapid rise and fall, it might prove of greater value than Queckenstedt's test which has a relatively low energy and a separate rise and fall. In testing with cough the rate of change is very much sharper than in Queckenstedt's test. There is a pulse to measure and the area, amplitude and slopes are all available. The accuracy of the measurements show marked factional losses even in the normal but the limits of normality are not denned. It seems that when ACX (fig. 1) is less than half ALX, it is then abnormally attenuated. A normal cisternal amplitude should probably be above 70 per cent of the lumbar. Further study might be expected to show which measurement would have the greatest value in expressing blockage. This study is limited because no cases of complete blockage are included since all such cases had been diagnosed before being referred for neurosurgery. Attempts to correlate myelographic findings with these results have failed because of the difficulty in grading the myelograms. Radiological blockage varies with positioning of the head and is subjective. It seems probable that this test is potentially superior to either Queckenstedt's test or myelography as an assessment of a degree of blockage of the spinal canal, but further work is necessary.
CSF P R E S S U R E WAVES
345
The merits and limitations of cough impulse as a clinical test for spinal blockage are discussed, and the suggestion is made that after further evaluation they may provide a more sensitive indication of spinal blockage than Queckenstedt's test. ACKNOWLEDGEMENTS Reckitt and Colman Limited and the Association for Spina Bifida each provided a Devices M19 recorder for the Hull Royal Infirmary and both were used in this study. The Hull Branch of the Association for Spina Bifida and Hydrocephalus gave the P23H transducer and the Wellcome Foundation provided technical help. Miss P. Willey carried out the pressure recordings and help with statistical analysis has been provided by Mr. T. Sorahan and Dr. J. R. Jackson.
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of the influence of the arterial pressure upon the morphology of cisternal CSF pulsation. European Neurology, 5, 107-114. Du BOULAY, G. H., O'CONNELL, J., CURRIE, J., BOSTICK, T., and VERITY, P. (1972) Further investigations
on pulsatile movements in the cerebrospinal fluid pathways. Ada Radiologica (Stockholm), 13, 496-523. GARDNER, W. J. (1945) Cerebrospinal fluid: Dynamics. In: Medical Physics. Edited by O. Glaser. Chicago: Year Book Co., pp. 148-152. GILLAND, O. (1966) CSF Dynamic Diagnosis of Spinal Block. Stockholm: Almqvist and Wiksell. HENRIQUES, C. Q. (1962) The veins of the vertebral column and their role in the spread of cancer. Annals of the Royal College of Surgeons of England, 31, 1-22. LAITINEN, L. (1968) Origin of the arterial pulsation of cerebrospinal fluid. Ada Neurologica Scandinavica, 44, 168-176. LAKKE, J. P. W. F. (1969) Queckenstedt's Test. Amsterdam: Excerpta Medica. LOCKEY, P., POOTS, G., and WILLIAMS, B. (1975) Theoretical aspects of the attenuation of pressure pulses within the CSF pathways. Medical and Biological Engineering, 14, 861-869.
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It is suggested that Froin's syndrome, central subarachnoid pouches and syringobulbia may be associated with upward pressure waves. Cough headache, the filling stages of communicating syringomyelia and tonsillar herniation may be associated with valve-like blockage at the foramen magnum which produces craniospinal pressure dissociation by interfering with downward or rebound pulsation. Decompensation of hydrocephalus after birth may be related to pulsation in association with crying; also after removal of a meningocele sac decompensation may be related to the effects of similar pulsation modified by changes in capacitance following operation. The cord destruction of syringomyelia, and the mechanisms which fill spinal subarachnoid cysts may be related to pressure waves directed both upwards and downwards.
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BERNARD WILLIAMS
{Received September 5, 1974)
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SYMONDS, C. P. (1956) Cough headache. Brain, 79, 557-568. WILLIAMS, B. (1969) The distending force in the production of communicating syringomyelia. Lancet, 2, 189-193. (1971) Further thoughts on the valvular action of the Amold-Chiari malformation. Developmental Medicine and Child Neurology, Supplement, 25, 105-112. (1973a) The valvular action of the Arnold-Chiari malformation. In: Proceedings of the 1st International Conference on Intracranial Pressure. Edited by M. Brock and H. Dietz. Berlin: Springer Verlag, pp. 338-342. (19736) Is aqueduct stenosis a result of hydrocephalus? Brain, 96, 399-412. (1974) A demonstration analogue for ventricular and intraspinal dynamics. Journal of the Neurological Sciences, 23, 445-461. and GUTHKELCH, A. N. (1974) Why do central arachnoid pouches expand? Journal of Neurology, Neuroswgery and Psychiatry, 37, 1085-1092.
