Injury, 5, 265-268 265

Intracranial volume/pressure studies in patients with head injury J. D. Miller and J. D. Pickard Department of Neurosurgery, University of Glasgow

Summary Intracranial volume/pressure compensation was tested in 16 patients with head injury by observing the change in intracranial pressure when 1 ml. of fluid was either injected or withdrawn through the ventricular catheter system used for monitoring intracranial pressure. Carotid angiography was also performed and showed that 8 patients had varying degrees of brain shift. Patients with brain shift had higher levels of baseline intracranial pressure and a greater sensi- tivity of pressure to the induced volume change. The degree of pressure sensitivity correlated more closely with the degree of brain shift (P<0.001) than with the level of baseline intracranial pressure (P<0.01). These findings indicate that this dynamic test during continuous monitoring of intracranial pressure provides additional information of clinical value in making management decisions in patients with head injury.

INTRODUCTION IT is now recognized that in patients with head injury secondary complications of brain swelling and haemorrhage contribute greatly to the morbidity and mortality. Further brain damage is caused by a combination of increased intra- cranial pressure (ICP), cerebral ischaemia, and brain shift. Neuropathological studies in patients dying following head injury (Graham and Adams, 1971; Adams and Graham, 1972) indicate that patchy cerebral ischaemia and the neuro- pathological changes associated with brain shift, particularly tentorial herniation, are common findings.

The technique of continuous monitoring of ICP (Guillaume and Janny, 1951; Lundberg, 1960) has yielded much useful information for the management of patients with head injuries (Lundberg, Troupp, and Lorin, 1965; Johnston, Johnston, and Jennett, 1970; Vapalahti and Troupp, 1971). It is possible to identify high levels of ICP when there is no clinical indication from

heart rate or blood pressure that this is present, and to observe a trend of increasing ICP. The method clearly indicates the effectiveness of agents, such as mannitol, administered to reduce ICP. Conversely, the identification of the patient who has low ICP is also a great help in decisions on patient management (Jennett and Johnston, 1972).

On the other hand, the level of ICP alone cannot be used as a factor in prediction of the outcome of a head injury. Patients with low ICP (<20 mm. Hg) have almost as high morbidity and mortality as those with high ICP (>40 mm. Hg) (Jennett and Johnston, 1972). Furthermore, there is poor correlation between ICP and conscious level (Langfitt, Kumar, James, and Miller, 1971; Miller, Stanek, and Langfitt, 1971), and between ICP levels during life and the presence of brain ischaemia after death (Jennett and John- ston, 1972). Although, in general, patients with brain shift demonstrated by carotid angiography have elevated ICP, some patients with brain shift may have normal ICP (Jennett and Johnston, 1971). Finally, in patients with intracranial space-occupying lesions, yet normal ICP, there is abnormal sensitivity of 1CP to any factor which causes cerebral vasodilatation, such that ICP rises suddenly and sharply with the administra- tion of volatile anaesthetic agents or with an increase in arterial Pco~ (McDowall, Barker, and Jennett, 1966; Jennett, Barker, Fitch, and McDowall, 1969; Lundberg, 1972; Miller and Adams, 1972).

Continous monitoring of ICP in patients with head injuries will certainly record fluctuating levels of ICP as they occur, but the method cannot predict increases in ICP. It seems impor- tant, therefore, not only to establish the baseline level of ICP, but also to try to measure the response of ICP to the stress of an addition to the volume of intracranial contents, such as might be caused subsequently by hypercapnia, hypoxia or

266 Injury: the British Journal of Accident Surgery Vol. 5/No. 3

other agent resulting in cerebrovascular dilata- tion. During continuous monitoring of ICP in neurosurgical patients by means of a catheter placed in the lateral ventricle, we have recently induced changes of 1 ml. in CSF volume with measurement of the resultant change in 1CP as a test of intracranial compensatory capacity (Miller and Garibi, 1972; Miller, Garibi, and Pickard, 1973). As baseline ICP increases, so also does the magnitude of the ICP change in response to withdrawal or infusion of 1 ml. through the ventricular catheter, confirming the logarithmic shape of the intracranial volume] pressure curve. However, there is considerable

Table /.--Resting intracranial pressure and intra- cranial volume/pressure responses in patients with and without brain shift on angiography. Significance of changes assessed by standard t test

Brain sh i f ton angiography

Absent Present ( n = 8 ) ( n = 8 )

Resting I CP mm. Hg 10-1 37.7 (Mean±s.e.) ±0-9 <0-005 ±6.2

Volume/pressure response 1-3 5-8 ram. Hg/ml. I 0 - 2 <0.005 ±1.2

variation in the induced ICP change in different patients at the same baseline level of ICP, and the removal of an intracranial mass lesion such as a turnout or haematoma, has a considerable influence on the volume/pressure response, even where there is little change in baseline ICP. These findings suggest that intracranial volume] pressure testing yields helpful information, which is not available from the normal chart recording of ICP. The present study evaluates this intra- cranial volume/pressure test in patients with head injuries.

P A T I E N T S A N D M E T H O D S

This investigation was carried out in 16 patients with head injury, in whom ICP monitoring was already in progress using an intraventricular catheter (Lundberg, 1960). The 16 patients comprised 8 in whom there was clinical evidence of brain-stem damage with no signs of severe hemisphere damage, 6 patients with cerebral contusion associated with varying degrees of brain swelling and acute subdural haematoma, and 2 patients with extradural haematomata. Cerebral angiography was carried out in all patients and the amount of cerebrovascular shift was measured, concentrating on midline shift and elevation of the middle cerebral artery, indicating a temporal lobe lesion. During the period of ICP

m m H g / t ~ 6 1 - A

1 4 -

1 2 -

1 0 -

8 -

6 -

4 -

2 - •

rs 0 -735 P < 0.01

O o •

16

14

12

10

8

6

4

2

_ B

rs 0 . 9 2 4 " - P< 0.001

• l

0 o

• . ; ÷ i I I I I 6 ~ 0 I i f i s

10 20 3 0 4 0 50 70 0 1-5 5-1010-20

BASELINE I C P ( m m H 9 ) BRAIN SHIFT ( m m )

Fig. 1.---A, Relationship between resting intracranial pressure and the volume/pressure response in 16 patients with head injuries. The figure shown is the Spearman rank correlation coefficient. B, Relationship between angiographic shift and the intracranial volume/pressure response in the same 16 patients. The figure shown is the Spearman rank correlation coefficient which indicates better correlation than in graph A.

Miller and Pickard : Intracranial Volume/Pressure Studies 267

monitoring (24 hours to 5 days) controlled alterations of CSF volume of 1 ml. over 1 second were induced at intervals and the immediate change in 1CP measured (Miller and others, 1973). The change in ICP per volume change in CSF (mm. Hg/ml.), measured on the day of angiography, was compared with the degree of shift and with the resting ICP at the time of measurement. In 4 patients the opportunity was also taken to compare volume/pressure responses before and after decompressive surgery.

RESULTS On the basis of the angiographic appearance, there were 8 patients who had little or no lateral shift of midline structures and no middle cerebral artery displacement, and 8 patients in whom there was midline shift together with varying degrees of middle cerebral artery displacement. The baseline ICP was significantly higher in the group with intracranial shift (P<0.005); this group also showed a significantly greater sensi- tivity of ICP to induced changes of 1 ml. in CSF volume (P<0"005) (Table I). However, it was not the patients with the highest resting ICP (35- 70 mm. Hg) who had the highest volume/pressure sensitivity; instead it was the 4 patients with a lesser degree of intracranial hypertension (20-

35 mm. Hg) who had the highest sensitivity of ICP to induced volume change. Using the Spearman rank correlation coefficient there was, in fact, a better correlation between ranked degrees of angiographic shift and the sensitivity of ICP to volume changes (P<0.001) than between resting ICP and its sensitivity (P<0-01) (Fig. I).

Pressure waves of types B and C (Lundberg, 1960) were seen more often at higher levels of resting ICP, but there was a less well defined relationship between presence of these waves and volume/pressure sensitivity (Table H).

Table //.--Resting intracranial pressure and intra- cranial volume/pressure responses in patients with and without spontaneous intracranial pressure waves (types B and C)

Pressure waves on ICP record

Absent Present ( n = 9 ) ( n = 7 )

Resting ICP mm. Hg 12.9 38-3 (Mean±s.e.) ___2.9 <0.01 ±7 .3

Volume/pressure Not response 2.2 signifi- 5"5 mm. Hg/ml. -}-0.7 cant q-1.5

3 0 -

25 -

20 - ICP

m m Hg

15-

10-

5 -

0

A . L . R . Frontal I.C. Haematoma

/ J

2 9 O c t 72 31Oct 72 1 N o v 7 2 2 N o v 7 2 Fig. 2.--Intracranial pressure responses to 1 m]. change in CSF volume in a patient with a post-traumatic frontal intracerebral haematoma. After the first observations partial aspiration of haematoma was carried out, resulting in reduction of mean pressure and sensitivity on 31 October, 1972; thereafter, both mean pressure and sensitivity increased, requiring formal craniotomy and evacuation of further haematoma.

268 Injury: the British Journal of Accident Surgery Vol. 5/No. 3:

In all 4 patients in whom volume/pressure testing was carried out before and after de- compressive surgery, there were significant reductions in the sensitivity of ICP to changes in C S F volume after decompression (Fig. 2).

Acknowledgement This work was supported by a grant from the Secretary of State for Scotland's Fund for Medical Research.

CONCLUSIONS The change of ICP which results from a 1 ml. change in CSF volume in the lateral ventricle is in effect a measure of lumped intracranial elastance, which is inverse compliance (Shulman and Marmarou, 1971; L6fgren, von Essen, and Zwetnow, 1973; Miller and others, 1973). Measurement of this factor permits identifica- tion of those cases in which intracranial volume compensat ion is becoming exhausted at a stage before resting ICP is greatly increased. By using this test during continuous ICP monitoring, the neurosurgeon may be warned that his patient is liable to suffer a considerable increase in pressure with even a small increment o f intracranial volume. Such an increase in volume of one of the intracranial constituents might be caused by cerebral oedema formation or by cerebral vaso- dilatation due to respiratory obstruction resulting in hypercapnia and hypoxia (Miller and Adams, 1972) or administrat ion of volatile anaesthetic agents (Jennett and others, 1969).

A sharp increase in ICP may result in cerebral ischaemia due to a reduction in cerebral per- fusion pressure, particularly when autoregulation is already disturbed by previous head trauma (Miller and others, 1971). There is also evidence that these additional increases in ICP, caused by cerebral vasodilatation in the presence of an intracraniai mass lesion, can be associated with occurrence or worsening of tentorial herniation even when there is no change in the volume of the mass lesion itself (Fitch and McDowall , 1971).

There is therefore a direct clinical application of the results of this type of test. In patients with temporal lobe contusion, in whom the angio- gram shows a moderate shift and only a small rise in ICP, low sensitivity o f 1CP to induced volume change ( < 2 ram. Hg/ml.) suggests that the patient should cope adequately with any small increase in intracranial compartment volume; in that even decompression is not necessary at this time. High sensitivity on the volume/pressure test ( > 5 mm. Hg/ml.) , on the other hand, indicates that medical or surgical decompression is needed urgently. The volume/ pressure test therefore provides the surgeon with information of direct value in the management of the patient.

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- - - - a n d JOHNSTON, I. H. (1971), 'Raised intra- cranial pressure and brain hypoxia after head injury ', in Brain Hypoxia (ed. BRIERLEY, J. B., and MELDRUM, B. S.), p. 107. London: Heinemann.

(1972), ' The uses of intracranial pressure monitoring in clinical management ', in lntracranial Pressure (ed. BROCK, M., and DIETZ, H.), pp. 353- 357. Berlin: Springer.

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LOFGREN, J., VON ESSEN, C., and ZWETNOW, N. N. (1973), ' The pressure/volume curve of the cerebro- spinal fluid space in dogs ', Acta neurol, scand., in press.

LONOBERG, N. (1960), 'Continuous recording and control of ventricular fluid pressure in neuro- surgical practice ', Acta psychiat, scand., 36, Suppl. 149.

- - - - (1972), ' Monitoring of the intracranial pres- sure ', in Scientific Foundations of Neurology (ed. CRrrCHLEV, M., O'LEARV, J. L., and JENNETT, B.), p. 356. London: Heinemann.

- - - TROUPP, H., and LOR1N, H. (1965), 'Continu- ous recording of the ventricular fluid pressure in patients with severe acute traumatic brain injury ', J. Neurosurg.. 22: 581.

Miller and Pickard : Intracranial Volume/Pressure Studies 269

McDOWALL, D. G., BARKER, J., and JENNETT, B. 0966), 'Cerebrospinal fluid pressure measure- ments during anaesthesia ', Anaesthesia, 21, 189.

MILLER, J. D., and ADAMS, J. H. (1972), 'Physio- pathology and management of increased intra- cranial pressure', in Scientific Foundations o f Neurology (ed. CRITCHLEY, M., O'LEARY, J. L., and JENNE'rr, B.), pp. 308-324. London: Heine- mann.

- - - and GARret, J. (1972), ' Intracranial volume/ pressure relationships during continuous moni tor- ing of ventricular fluid pressure ', in Intraerania! Pressure (ed. BROCK, M., and DIETZ, H.), pp. 270- 274. Berl in: Springer.

and PICKARD, J. D. (1973), ' The effects of

induced changes of cerebrospinal fluid volume during continuous monitoring of ventricular pressure ', Archs Neurol., 28, 265.

- - - STANEK, A. E., and LANCFITT, T. W. (1971), 'Concepts of cerebral perfusion pressure and vascular compression during intracranial hyper- tension ', in Progress in Brain Research, Vol. 35, (ed. MEYER, J. S., and SHAD~, J. P.). Amsterdam: Elsevier.

SHOLMAN, K., and MARMAROU, A. (1971), ' Pressure/ volume considerations in infantile hydrocephalus ', Develop. Med. Child. Neurol., Suppl. 25, 13, 90.

VAPALAHTI, M., and TROUPP, H. (1971), 'Prognosis for patients with severe brain injuries ', BE. med. J., 3, 404.

Requests for reprints should be addressed to:--J. D. Miller Esq., Institute of Neurological Sciences, Glasgow, GSI 4TF.