J Neurosurg 47:503-516, 1977

Significance of intracranial hypertension in severe head injury J. DOUGLAS MILLER, M.D., PH.D., F.R.C.S., DONALD P. BECKER, M.D., JOHN D. WARD, M.D., HUMBERT G. SULLIVAN, M . D . , WILLIAM E. ADAMS, M.D., AND MICHAEL J. ROSNER, M . D .

Division of Neurological Surgery, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia L,, Measurements of intracranial pressure (ICP) were begun within hours of injury in 160 patients with severe brain trauma, and continued in the intensive care unit. Some degree of increased ICP (> 10 mm Hg) was present on admission in most cases (82%), and in all but two of the 62 patients with intracranial mass lesions requiring surgical decompression; ICP was over 20 mm Hg on admission in 44% of cases, and over 40 mm Hg in 10%. In patients with mass lesions only very high ICP (> 40 mm Hg) on admission was significantly associated with a poor neurological picture and outcome from injury, while in patients with diffuse brain injury any increase in ICP above 10 mm Hg was associated with a poorer neurological status and a worse outcome. Despite intensive measures aimed at prevention of intracranial hypertension, ICP rose over 20 mm Hg during the monitoring period in 64 of the 160 patients (40%). Postoperative increases in ICP over 20 mm Hg (mean) were seen in 52% of the patients who had had intracranial masses evacuated, and could not be controlled by therapy in half of these cases. Even in patients without mass lesions, ICP rose above 20 mm Hg in a third of the cases, despite artificial ventilation and steroid therapy. Of the 48 patients who died, severe intracranial hypertension was the primary cause of death in nearly half and even moderately increased ICP (> 20 mm Hg) was associated with higher morbidity in patients with mass lesions and those with diffuse brain injury. Measurement of ICP should be included in management of patients with severe head injury. KEY WORDS head injuries 9 pressure-volume response 9

INCE the introduction into neurosurgical practice of continuous monitoring of intracranial pressure (ICP), 7,13 several reports have indicated that extremely high levels of I C P ( > 40 m m Hg or 550 m m H20) may be encountered in patients with severe head trauma, and that such sustained i n t r a c r a n i a l h y p e r t e n s i o n has a p o o r prognosis? '~~ Beyond that, however, the picture is clouded because many patients who were deeply comatose from diffuse or

s

J. Neurosurg. / Volume 47 / October, 1977

9 intracranial pressure

9

mass lesion

brain-stem injury and who also fared badly have been found to have normal I C P ? Because of this a poor correlation has been reported between I C P and outcome. Neuropathological studies of patients dying from head injury have suggested, per contra, that most of these patients have at some time been subject to intracranial hypertension or at least to brain shift? Clinical recordings of I C P in head injury have mostly been made in heterogeneous groups of patients, and have been of 503

J. D. Miller, varying duration, often starting several days after injury, so that it is hard to judge the frequency and severity of intracranial hypertension in severe head injury from available reports, let alone estimate its significance in determining the outcome from injury. The techniques of monitoring ICP are not without risk; 21,24 correct interpretation of the findings often requires additional physiological information (such as arterial pCO2 and blood pressure), and all methods involve expenditure in terms of equipment, time, and trained personnel. It is important, therefore, to evaluate with care the role of ICP monitoring in management of patients with severe head injury, as conflicting claims have already been made. z,6 Johnston and Jennett 9 have summarized the uses of ICP monitoring as being in diagnosis, management, and prognosis, and evaluation ought to be made of all three aspects before conclusions can be fairly reached. More information is, in any case, required as to the frequency with which intracranial hypertension is encountered, the levels of ICP that should be considered significant, and how often raised ICP really creates a problem for head-injured patients. For the past 4 years, we have made a policy of measuring ICP in severely head-injured patients immediately upon arrival in the emergency room, and continuing ICP monitoring in the intensive care unit. This has been combined with a uniform protocol aimed at early detection and evaluation of intracranial mass lesions and prevention of raised ICP, which has been described fully elsewhere. 2 As a result, we have a series of 160 patients whose clinical course and outcome have been carefully followed, and in all of whom ICP measurements have been made, so that it is possible to determine the frequency, extent, and significance of intracranial hypertension, and to evaluate the place of ICP monitoring in these patients. Clinical Material and Methods

Study Population The criterion for admission to the study was blunt head injury resulting in depression of the level of consciousness with inability to obey commands or worse, but excluding patients who met the criteria of brain death. In 46% of the group the best motor response to pain on admission was decorticate, 504

et al.

decerebrate, or nil; in 40% of cases the oculocephalic response was impaired or absent; and in 21% of cases the pupillary light response was bilaterally absent.

Management In all patients a 9/64 in. frontal twist-drill hole was made while in the emergency room as soon as stable airway and hemodynamic conditions had been obtained and respiratory abnormalities corrected as determined by blood-gas measurement. The frontal horn of the lateral ventricle was punctured with an 18G cannula or a polyethylene catheter connected to a long fluid-filled manometer.* Thus ICP measurement was delayed until possible hypoxia or hypercapnia had been corrected. After a stable pulsatile meniscus had been verified, the initial measurement of ICP was recorded, then 7 to 10 ml of air was injected and brow-up films taken. All patients with 5 mm or more of midline brain shift on the ventriculogram were immediately treated by wide craniotomy for removal of intracranial mass lesions. Patients with no shift, but increased ICP (> 15 mm Hg; 200 mm H20), were referred for a further study (angiography or computerized tomography (CT) scan) to ~.xclude bilateral lesions. Patients with no shift and ICP below 15 mm Hg were admitted directly to the intensive care unit but underwent angiography or CT scan within 48 hours. Sixty-two patients were found to have mass lesions requiring surgical decompression, 12 epidural and 26 acute subdural hematomas, while 24 patients had cerebral contusion a n d / o r hematoma affecting the frontal and/or temporal lobes. The average midline shift in these patients was 9 mm. Surgical decompression consisted of large craniotomy, removal of all blood clot, and removal of necrotic, contused frontal and/or temporal tip. In the 24 patients without extraaxial clot a more generous frontal and/or temporal lobectomy was carried out including evacuation of intracerebral hematoma if this had been detected on CT scan, found during brain resection, or located by needling the swollen area. As a matter of policy, bone flaps were replaced with reliance on the internal decom*Glass manometer, No. 4003, manufactured by Bard-Parker, Rutherford, New Jersey.

J. Neurosurg. / Volume 47 / October, 1977

Intracranial hypertension in head injury pression. Only in a few extreme cases was it necessary to remove the bone flap to permit closure. In the remaining 98 patients there was little or no midline shift, and their trauma was designated " d i f f u s e brain injury," although we appreciate that many of those patients with mass lesions and brain shift have diffuse brain injury as well. All patients were intubated and artificially ventilated with conversion to tracheostomy by the third day if intubation was still required. Arterial pCO2 was kept between 25 and 35 mm Hg. All patients received dexamethasone, 10 mg on admission and 4 mg every 6 hours for the first 3 days, tailing thereafter unless otherwise indicated. Phenytoin 100 mg three times daily was given to all patients. Most patients did not receive muscle relaxants but had chlorpromazine 25 mg or morphine 1 to 3 mg as required to phase them into the volume respirator, which was set at a slow rate (10 to 12/minute) and large tidal volume (15 ml/kg). Patients were nursed with their heads slightly raised (10~ or flat if dictated by other injuries, such as leg fractures. Intracranial pressure was monitored in all patients either by a polyethylene cannula in the ventricle or by subarachnoid screw, inserted in the e m e r g e n c y room, in the operating room after surgery, or in the intensive care unit. We prefer to tunnel ventricular cannulas bringing them through the scalp at least 1 in. from the incision for the twistdrill hole. Measurement of I C P was by an external arterial range pressure transducert mounted on a disposable plastic manifold system~ attached to the intravenous fluid pole at the bedside (Fig. 1). This manifold also has ports for a fluid manometer, fluid reservoir, tuberculin syringe for flushing and performing volume-pressure response tests, and a drainage bag which can be elevated to any desired hydrostatic pressure. The system can therefore remain closed yet permit recalibration, fluid drainage, and other manipulations. Monitoring of ICP was continued for at least 48 hours in nearly all patients and at tPressure transducer manufactured by Statham Instruments, 2230 Statham Boulevard, Oxnard, California. :~Manifold system manufactured by Cobe Laboratories East, Inc., 180 Penrod Lane, Glen Burnie, Maryland. J. Neurosurg. / Volume 47 / October, 1977

FIG. 1. Equipment used for bedside monitoring of intracranial pressure. The disposable manifold permits recalibration, CSF drainage, and pressurevolume testing within a closed system.

present is routinely continued for 3 days. Thereafter, because the risk of infection increases, a decision is made each morning to continue or desist depending on the clinical value of the information obtained. 21 Indications for treating raised I C P were a sustained increase over 40 mm Hg (this threshold was down to 30 mm Hg by the end of this study), or any increase in I C P that appeared to be associated with neurological deterioration. After ruling out changes in body or head position or in blood gases as a cause o f increased ICP, treatment was by further hyperventilation with an increased tidal volume, by closed ventricular drainage against a positive pressure of 15 to 20 m m Hg or by intravenous mannitol given in most cases as a bolus of 1 g m / k g body weight in l0 to 15 minutes, but in some cases continuous mannitol infusion has been used. The eventual outcome of these patients was classified according to the scheme of Jennett and Bond as good r e c o v e r y , m o d e r a t e l y disabled, severely disabled, vegetative, or d e a d ) 505

J. D . M i l l e r , et al. TABLE 1 Intracranial pressure on admission in 160 patients

Intracranial Pressure (mm Hg)

Diagnosis

0-10

acute epidural hematoma acute subdural hematoma acute intracerebral mass lesion all intracranial mass lesions diffuse brain injury all head injuries

11-20 21-30 31-40 41-50

51-60

Total

0 0

3 5

3 7

5 5

1 4

0 5

12 26

2*

9

6

3

2

2

24

17 44 61

16 19 35

13 7 20

7 1 8

7 1 8

62 98 160

2 26 28

*Two patients with CSF rhinorrhea.

Summary of Cases Incidence o f lntracranial Hypertension on Admission All but two of the 62 patients with intracranial mass lesions had some increase in I C P ( > 10 m m Hg) when first evaluated in the emergency room; the two patients with normal I C P both had C S F rhinorrhea (Fig. 2, Table 1). In 69% of these patients initial I C P was more than 20 m m H g mean, and in 23% it was over 40 m m Hg. Severe early intracranial hypertension was m o s t evident in the patients with acute subdural h e m a t o m a , 35% of whom had initial I C P levels of more than 40 m m Hg.

t,~ I-Z I.t.I

50

-

n~

4.0 -

I.l. 0

30

Intracroniol Mass Lesion F - ' - ] Diffuse Brain Injury

-

~_ 20 Z W ~ W

I0

i 0 - I0

,1 II - 2 0

21-30

31-40

41-50

51- 6 0

INTRACRANIAL PRESSURE mmHg FIG. 2. Distribution of intracranial pressures in 160 patients with severe head injury on admission to hospital, contrasting intracranial mass lesions in 62 patients (cross-matched) with 98 patients who had diffuse brain injury. 506

O f the 98 patients with diffuse brain injury, only 26% had unequivocally normal I C P (0 to 10 m m Hg); 45% had slightly elevated I C P (11 to 20 m m Hg) and in 26% I C P lay between 20 and 40 m m Hg despite the absence of brain shift. Only two patients had initial I C P levels over 40 m m Hg. Overall, however, the a s s o c i a t i o n between m a s s lesions and intracranial hypertension was significant (x 2 = 25.59; p < 0 . 0 0 1 ) . Thus when first seen in the hospital soon after injury, 82% of this series of patients had some elevation of I C P above 10 m m Hg, 44% had I C P levels over 20 m m Hg, and 10% were over 40 m m Hg.

Initial I C P and Midline Brain Shift There was a trend toward higher I C P as midline brain shift increased but not a strong one. N o r m a l I C P (0 to 10 m m Hg) was not seen in any patient with 5 m m or m o r e midline shift, and there was a strong association between I C P greater than 20 m m H g and shift o f 5 m m or m o r e (X 2 = 28.79; p < 0.001). Beyond this, however, there was not a significant association between higher I C P and greater degrees of shift. Also, lack of midline shift did not imply normal I C P . Four patients with no midline shift had I C P levels over 40 m m Hg; only two of these had bilateral mass lesions; 10 patients with no shift had I C P greater than 30 m m Hg.

Initial I C P and Neurological Dysfunction In the 62 patients with mass lesions requiring s u r g e r y , there was no a p p a r e n t relationship between neurological dysfunction and the levels of I C P on admission tak-

J. Neurosurg. / Volume 4 7 / October, 1977

Intracranial hypertension in head injury TABLE 2 Relationship between neurological signs and intracranialpressure on admission Diagnosis intracranial mass lesions total diffuse brain injury total

ICP on Motor Response Admission (mm Hg) Normal Abnormal 0-10

11-20

1

9

1 (50%)

Oculocephalic Response Present 1

Imp/Absent 1 (507o)

Pupil Light Reaction Present Bilat. Absent 2

0

8 (47 ~o)

9 17 2 29

8 (47%) 12 (41%) 12 (86%) 33 (53 ~)

12 23 2 39

5 (29%) 6 (21%) 12 (86%) 23 (37 %)

23 30

5 (18%) 12 (40%) 12 (46 %) 2 (100~o) 31 (32%)

27 36 24 0 87

1 (4~o) 6 (14%) 2 (8 %) 2 (100%) 11 (117o)

21-40 41-60 +

15 2 27

14 (48%) 12 (86%) 35 (56%)

0-10 11-20 21-40 41-60 +

18 30 11 0 59

10 (36%) 12 (40%) 15 (58%) 2 (100~o) 39 (40%)

ing blocks of 10 m m Hg between 0 and 40 mm Hg (Table 2). The incidence of abnormal m o t o r responses to pain (decorticate, decerebrate, or flaccid) ranged between 38% and 56%, the incidence of impaired or absent oculocephalic responses between 37% and 50%, and the incidence o f bilateral loss of the pupillary light reaction between 0 and 29%. When initial ICP was over 40 mm Hg in these patients, however, there was a sharp increase in the incidence of neurological dysfunction with the incidence o f a b n o r m a l m o t o r response, impaired oculocephalics, and loss of pupillary reaction all increased to 86% (x 2 = 4.86, 6.07, 15.72 respectively; p < 0.05, < 0.02, < 0.001). In the 98 patients with diffuse brain injury the findings were quite different (Table 2). With every 10 m m Hg increase in ICP there was a progressive increase in the incidence of abnormal neurological function through the entire range of pressures from 0 to over 60 mm Hg. The incidence of abnormal motor responses rose from 36% to 100%, of impaired oculocephalic response from 18% to 100%, and o f loss of pupillary light reactions from 4% to 100%. Early Intracranial Hypertension and Outcome f r o m Injury If the entire group of 160 patients was considered together, only severe intracranial hypertension (mean ICP > 40 mm Hg) on admission was associated with a poor outcome (there was a 69% mortality, and only J. Neurosurg. / Volume 47 / October, 1977

14

0 67

25% of patients finished as a good recovery or moderately disabled; • = 9.07; p < 0.01) (Table 3). Conversely, unequivocally normal ICP (0 to 10 m m Hg) on admission was associated with a low mortality (14%), and a higher proportion of patients (78%) who made a good r e c o v e r y or were only moderately disabled (X2 = 4.88; p < 0.05). Between these extremes, however, initial ICP did not apparently influence outcome. The relationship between ICP and outcome becomes much clearer when the two groups of patients with and without intracranial mass lesions are considered separately. Patients with intracranial mass lesions tended to have a greater degree of neurological dysfunction than those with diffuse injury, 2 mortality in these patients (40%) was higher than in those patients with diffuse injury (23%; X2 = 5.14; p < 0.02), and, as stated, ICP tended to be higher in the patients with mass lesions. Despite this, there was no significant correlation between initial ICP and outcome in the patients with mass lesions; thus even in those patients with mass lesions whose initial ICP was greater than 40 m m Hg, 28% made a good recovery or were only moderately disabled. Presumably, other factors such as p r i m a r y brain dysfunction, d y s f u n c t i o n secondary to brain herniation, and the timing of surgical d e c o m p r e s s i o n relative to deterioration have an over-shadowing influence on outcome. By contrast, in the patients with diffuse brain injury, initial ICP seemed to be closely 507

J. D. Miller, et al. TABLE 3 Outcome from head injury related to level of intracranial pressure on admission* Diagnosis intracranialmass lesions

total diffuse brain injury

total

ICP on Admission (ram Hg)

Outcome Dead

Total

GR/MD

SD/Veg

0-10 11-20 21-40 41-60 +

0 7 (41 70) 20 (697o) 4 (50~o) 31 (5070)

0 2 (1270) 3 (1070) 1 (770) 6 (10~o)

2 (10070) 8 (4770) 6 (21 ~) 9 (64~o) 25 (4070)

2 17 29 14 62

0-10 11-20 21-40 41-60 +

22 (85 70) 28 (64~) 15 (5870) 0 65 (6670)

2 (8 70) 5 (11 7o) 3 (1170) 0 10 (1070)

2 (8 ~o) 11 (2570) 8 (31 70) 2 (10070) 23 (2370)

26 44 26 2 98

*Outcome is graded as good recovery (GR), moderate disability (MD), severe disability (SD), vegetative and dead.

related to outcome. With normal I C P (0 to 10 m m Hg), 85% of patients made a good recovery and 8% died; 7% were left severely disabled or vegetative. With even a slight elevation of I C P (11 to 20 m m Hg), mortality increased to 25%, and severe morbidity to 11%, with a corresponding decrease in the proportion of patients who made a good recovery or were moderately disabled to 64% (X 2 = 5.30; p < 0.02). Further increases in I C P were associated with a correspondingly worse outcome. It appears, therefore, that in this group of patients who have no mass lesion and no brain shift, any increase in I C P is significant in its relationship with outcome. This m a y reflect the total volume of brain tissue that has been damaged, or the extent of cerebral blood volume alteration induced by t r a u m a , or the degree of structural alteration of the brain sufficient to change pressurev o l u m e relationships. This r e l a t i o n s h i p between initial I C P and outcome is restricted to patients with neurological dysfunction. In those patients with diffuse injury who exhibited a b n o r m a l m o t o r responses (decorticate, decerebrate, or flaccid), I C P levels in excess of 10 m m Hg were associated with a higher percentage of poor outcomes. When I C P was 0 to 10 m m Hg on admission, the proportion of patients with abnormal m o t o r responses who finished severely disabled, vegetative, or who died was 43%; when I C P was higher than this, the proportion of bad outcomes rose to 83% (X2 = 5.05; p < 0.05). The significant cut-off point for I C P in this 508

respect appeared to be at 10 m m Hg, not at any higher level. In patients with purposeful m o t o r responses, increased I C P on admission was not significantly related to outcome. Course o f I C P During Continuous Monitoring

The goal of the m a n a g e m e n t protocol for these patients was to prevent severe intracranial hypertension but, despite this, the regimen was not always successful. Increased I C P in the intensive care unit was in the form of both p r e s s u r e w a v e s and sustained elevations. Plateau waves as defined by Lundberg 13 were rarely seen but it must be recalled that measures were taken to reduce I C P if it exceeded 40 m m Hg (and later 30 m m Hg), even if no neurological deficit was seen. Severe waves o f increased I C P associated with systemic vasopressor responses were seen in m o s t cases of fatal intracranial hypertension, however, and will be referred to below. Sharply peaked, brief B waves 13 were seen both in patients with mass lesions and diffuse brain injury, but did not appear to be related to neurological dysfunction. These waves were less c o m m o n while patients were being artificially ventilated. We believe that sustained elevations of I C P are of greater pathological significance than pressure waves in head injury, and have therefore analyzed carefully the course of all patients following surgery and/or m a i n t e n a n c e on artificial ventilation at J. Neurosurg. / Volume 47 / October, 1977

Intracranial hypertension in head injury TABLE 4 Numbers of patients showing course of httracranial pressure during monitoring in intensive care unit after surgical decompression and/or institution o f artificial ventilation

Diagnosis

Total

acute epidural hematoma acute subdural hematoma acute intracerebral mass lesion

12 26 24

all intracranial mass lesions diffuse brain injury

62 98

Group I Groups II &III Group II Group III (ICP Below (ICP Over (Controlled) (Not Controlled) 20 mm Hg) 20 mm Hg) 3 2 1 9 12 8 4 14 17 7 10 7 30 66

moderate hypocapnia. In this part of the study we have chosen to consider sustained elevations of ICP in excess of 20 mm Hg mean as abnormal. O f the 62 patients who had mass lesions, ICP remained low after surgical removal in 30, despite the fact that initial ICP had been higher than 20 mm Hg in 24 of these 30 patients (Table 4). Clearly, decompressive surgery had been successful in these cases; eight patients had had an epidural hematoma, 11 an acute subdural hematoma, but only five an intracerebral mass lesion. In 32 of the 62 operated cases, ICP either remained over 20 m m Hg or rose again after a temporary reduction. By the use of increased ventilation, C S F drainage, or mannitol, it was possible to control ICP and reduce it below 20 mm Hg in 17 cases (Table 4). In the remaining 15 patients, intracranial hypertension persisted despite therapy leading to a fatal outcome. Thus, in just over half of the operated cases, ICP remained high or rose again despite surgical decompression, artificial ventilation, and steroids, and in half of these cases the intracranial hypertension proved fatal. In these patients with mass lesions there was not a predictable relationship between initial ICP and the occurrence of high ICP postoperatively. It was clear, however, that this problem was much more prevalent in the group of patients with intracerebral mass lesions, 71% of whom had postoperative intracranial hypertension compared with 39% of those with acute epidural and subdural hematomas (x 2 = 4.60; p < 0.05). Also, of the patients with intracerebral mass lesions who developed raised ICP after surgery, it could not be controlled in 59% compared with 33% in the patients with acute h e m a t o m a s . Thus, postcompressive brain swelling was a less frequent J. Neurosurg. / Volume 4 7 /

October, 1977

32 32

17 24

15 8

cause of persistent or recurrent raised ICP, than primary brain damage; this may be a result of our policy of early evacuation of hematomas. The pattern of ICP in the 98 patients with diffuse brain injury was rather different. Sixty-six patients had normal ICP during the postinjury course, and 56 of these patients had had normal ICP to start with. In 24 patients, 13 of whom had high ICP initially, ICP ran over 20 m m Hg but could be controlled by therapy. In a further eight patients, five of whom had high ICP from the start, ICP rose inexorably and could not be controlled by treatment. Thus in the whole group of 160 patients, despite vigorous surgical and medical treatment aimed at the prevention and control of intracranial hypertension, increased ICP required further measures in 64 patients (40%) and in 23 of these cases ICP could not be controlled. Persistent or recurrent intracranial hypertension was a greater problem in patients with mass lesions and brain shift on admission, affecting 52% of cases, a significantly higher proportion than affected the patients with diffuse injury (32%; X2 = 5.69; p < 0.02). Nevertheless, one-third of the patients with diffuse injury had problems with intracranial hypertension, and when this did occur there was a 25% chance of it terminating fatally. Course o f I C P a n d O u t c o m e

The outcome o f the patients was compared against the three patterns of ICP observed in the monitoring period (Table 5). Clearly, the third category o f uncontrollable intracranial hypertension was o f serious p r o g n o s t i c significance since all affected patients died. 509

J. D. Miller, et al. TABLE 5 Outcome from head injury related to course of intracranial pressure during monitoring

Diagnosis

ICP Group*

GR/MD

Outcomet SD/Veg

Dead

Total

intracranial mass lesions

I II III

23 (777o) 8 (477o) 0 31

2 (7~o) 4 (23%) 0 6

5 (177o) 5 (297o) 15 (1007o) 25

30 17 15 62

diffuse brain injury

I II Ill

52 (7970) 13 (54~o) 0 65

6 (9~o) 4 (177o) 0 10

8 (127o) 7 (29~0) 8 (100 7o) 23

66 24 8 98

*Group I = ICP remained below 20 mm Hg; Group II = ICP rose above 20 mm Hg but was controlled by therapy; Group III = ICP rose above 20 mm Hg but could not be controlled by therapy. tGR = good recovery; MD = moderate disability; SD = severe disability; Veg = vegetative. Even an increase in I C P that could be controlled, the second category, was of adverse significance, however. This was associated with a higher proportion of poor outcomes (se~,ere disability, vegetative, or dead) than when I C P r e m a i n e d n o r m a l (the first category) both in patients with mass lesions (53% vs 23%) and those with diffuse injury (46% vs 21%) (x 2 = 4.24 and 5.32; p < 0.05 and < 0.02, respectively). Further information on the significance of sustained or recurrent intracranial hypertension e m e r g e s w h e n the subgroup of patients with normal m o t o r responses on admission is considered. In these patients, when I C P remained normal only 5% had a poor outcome (severely disabled, vegetative, or dead). When I C P was elevated, however, 46% fared badly (X 2 = 22.50; p < 0.001); this remained true even when the intracranial hypertension could be controlled by therapy when 33% had a p o o r result (x 2 = 12.26; p < 0.001). In the other subgroup of patients, who had a b n o r m a l m o t o r responses (decorticate, decerebrate, or flaccid) this overshadowed the effect of I C P on prognosis. Thus 52% of these patients with normal I C P had a poor o u t c o m e compared with 70% of those whose I C P had risen but was controlled. This difference was not significant (X2 = 1.75; not significant). Intracranial P r e s s u r e - V o l u m e Studies

Serial, t w i c e - d a i l y assessments of intracranial cerebrospinal fluid (CSF) volume compensation were m a d e in 34 patients in this 5]0

series; 15 patients had had mass lesions evacuated (no studies were made before decompressive surgery), and 19 patients had diffuse brain injury. This assessment, the volume-pressure response (VPR), was m a d e by measuring the immediate change in I C P produced by the injection of 1 ml saline into the lateral ventricle in 1 second via a ventricular catheter. 17,1s It should be noted that the technique cannot be used safely with the subarachnoid screw. In all but two of the patients the averaged V P R was normal or only slightly increased (range 0 to 4 m m H g / m l ) . This was true even in patients with increased ICP, in fact in some patients with very high ICP, approaching the level of arterial pressure, we encountered surprisingly low values for the V P R of 1 or 2 m m H g / m l . When this occurred, the I C P wave showed a very large pulse pressure. We have observed this phenomenon experimentally also.12,2a The two patients in whom consistently high values of V P R were found both had unsuspected intracranial mass lesions that required further surgical decompression. A 15year-old girl, who had a frontal epidural h e m a t o m a evacuated, showed a persistently high value of V P R at 8 to 11 m m H g / m l on the second postoperative day. This was followed later in the day by an increase in I C P f r o m 14 to 35 m m Hg; C T scan revealed an u n s u s p e c t e d contralateral epidural h e m a t o m a . The other patient was an 18-yearold girl, who had resection of a frontal lobe contusion. Twelve hours after surgery I C P remained between 15 and 25 m m H g but the J. Neurosurg. / Volume 4 7 /

October, 1977

Intracranial hypertension in head injury VPR, which had been 2 to 3 m m H g / m l , rose to 6 to 8 m m H g / m l ; cerebral angiography showed a large intracerebral h e m a t o m a . It must be emphasized that all patients were studied after surgical decompression had been completed, midline shift reversed, and the patients were being artificially ventilated. The low incidence of high values of the V P R is understandable on this basis, and the technique, although simple, was able to detect two patients with unsuspected mass lesions. TM

Intracranial Hypertension as a Cause o f Death Following Head Injury Forty-eight (30%) of this series of patients died (Table 6). In evaluating the terminal events in these patients, a determination was made as to the principal cause of death. In 22 of the 48 fatal cases, death was considered to be due to u n c o n t r o l l a b l e i n t r a c r a n i a l hypertension, in which I C P rose toward the level of arterial blood pressure with or without r e a c t i v e a r t e r i a l h y p e r t e n s i o n ("Cushing response") followed eventually by declining arterial pressure. These waves of increased arterial pressure were never accompanied by neurological i m p r o v e m e n t and had

o__|

TABLE 6 Mortality rates and cause of death Diagnosis acute epidural hematoma acute subdural hematoma acute intracerebral mass lesion all intracranial mass lesions diffuse brain injury all head injuries

Cause of Death Total Deaths Increased Medical ICP Causes 12

1 (87o)

1

0

26

11 (4270)

4

7

24

13 (54 70)

9

4

62

25 (4070) 14

11

98

23 (2370)

8

15

48 (30 70) 22

26

160

a uniformly bad prognosis. As I C P reached within 20 m m H g of arterial pressure and effective cerebral perfusion pressure was insufficient to sustain cerebral blood flow, TM we repeatedly observed, in order, loss of all m o t o r activity, bilateral pupillary dilatation, and loss of electroencephalographic activity (Fig. 3). In the remaining 26 patients, death was caused by systemic medical complica-

|

BOTH PUPILS DILATED

|

* FLACCID

EEG FLAT ,+

16o

O. ~

40

0

4

8

12

16

20

24

28

32

36

40

44

I

I 48

HOURS

Fro. 3. Death from uncontrollable intracranial hypertension. Chart showing arterial pressure (upper trace) and intracranial pressure (lower trace) in a 20-year-old man with generalized brain swelling following injury. Ventricular drainage (D) was possible for decreasing periods of time due to ventricular collapse, and intravenous mannitol I gm/kg (M) had a diminishing effect. Finally, as ICP reached to within 20 mm Hg of arterial pressure both pupils dilated; the motor response, which had been decerebrate, was lost completely, and the electroencephalogram (EEG) became flat. Angiography and cerebral blood flow measurement at this final stage showed no flow, confirming the clinical diagnosis of brain death.

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J. D. Miller, et al. abnormally high by most people. In the genesis of raised ICP by brain compression from an expanding lesion, considerable volumetric addition may take place before a significant rise in ICP occurs because of spatial compensation, so that any increase at all in ICP may be of significance.11 We have noted in our own experiments 12,23and in those of others 11that during expansion of a mass lesion, ICP does not remain absolutely normal; there is always a small rise in ICP during the phase of volumetric compensation, so that the "flat portion" of the pressure-volume curve is not completely fiat. It is in this special circumstance that intracranial pressure-volume studies have an application in the management of head injury, when relatively low ICP may be falsely reassuring. 16-18The selection of a threshold pressure of 10 mm Hg gives added security, however. In patients with diffuse brain injury any increase in ICP over 10 mm Hg was associated with worsening of the neurological status and a poorer outcome so that this threshold does appear to have real clinical significance. In making a decision as to whether further diagnostic measures are needed immediately, we deliberately chose a slightly higher cut-off pressure of 15 mm Hg, and in classifying ICP levels during the monitoring period in the intensive care unit we defined levels over 20 mm Hg mean as indicative of unequivocally raised ICP. This last was done for the purpose of Discussion this review and these different choices of ICP Increased ICP is a common occurrence level do not alter our belief that any ventricsoon after serious head injury, and this study ular or supratentorial (subarachnoid, subsuggests that if measurements are made early, dural, or epidural) pressure over 10 mm Hg virtually all patients with intracranial mass should be regarded with suspicion. Based on lesions and brain shift will have raised ICP. these definitions we find that raised ICP is This contrasts with other reports where nor- still a frequent occurrence even after early mal ICP has been recorded in the presence of surgical decompression and the institution of substantial brain shift.9,1~ Central to this ap- artificial ventilation. In 14% of the total series parent difference are definitions of normal and 46% of the fatalities, death was and raised ICP, and the timing of ICP associated with fulminating intracranial measurement. In most reports, mean levels of hypertension, which could not be controlled 15 or 20 mm Hg have been taken as by surgical or medical measures. On the thresholds for definition of intracranial grounds of frequency and severity, therefore, hypertension,e,~,~~ We have deliberately raised ICP constitutes an important factor in chosen l0 mm Hg as our upper limit of nor- the clinical course of the patient with severe mality for patients on admission and would head injury. defend this on several grounds. First, intraA crucial issue here is the relationship ventricular pressures between 0 and 10 mm between intracranial hypertension and brain Hg can be unequivocally regarded as normal. damage and dysfunction. Does brain damage A sustained ventricular pressure of 18 mm Hg cause high ICP, or does high ICP cause brain mean (250 mm H20) would be regarded as damage? Somewhat unsatisfactorily, the

tions, including pulmonary embolism or sepsis, septicemia, and renal failure. Of the 25 patients with mass lesions who died, 14 (56%) succumbed to uncontrollable intracranial hypertension, compared with eight of the 23 patients (35%) who died following diffuse brain injury. This difference is not statistically significant (X2 = 2.17). The proportion of fatalities due to increased ICP rose with increasing levels of ICP on admission; thus, of the four patients with normal initial ICP who died, only one (25%) died of high ICP, while 37% of those fatal cases whose ICP on admission was 11 to 20 mm Hg and 57% of those whose ICP on admission was 21 to 40 mm Hg died because of uncontrollable intracranial hypertension. Clearly, other factors also weigh heavily in determining which patients die from head injury, notably those other parameters that define the severity of the initial injury. Thus, of the 48 patients who died, 79% were decorticate, decerebrate, or flaccid on admission compared with 46% of the overall series, 73% had impaired or absent oculocephalic responses compared with 40% of the overall series and the pupillary light response was absent bilaterally in 50% of the fatal cases as against 17% frequency of this finding in the 160 cases. All of these differences are highly significant (x 2 > 25; p < 0.001).

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Intracranial hypertension in head injury answer to both of these questions is affirmative. In the final sequence of events in those patients with severe intracranial hypertension who died, we observed such a clear relationship between progressive brain dysfunction and the diminishing difference between arterial and intracranial pressure, that we concluded this to be an instance where ICP per se was a cause of neurological deterioration, which if it persisted would cause brain damage. (It must be emphasized that this statement is restricted to traumatic brain injury; its validity for other forms of intracranial hypertension would need to be separately examined). At an earlier stage, however, before ICP became a limiting factor for cerebral perfusion, we considered ICP to be only one of several indicators of the severity and extent of brain damage caused by multiple factors, including primary injury, tissue swelling, vascular dilatation, or congestion. In the sphere of diagnosis, high levels of ICP (> 40 mm Hg) soon after injury should alert the surgeon to the likelihood of an expanding intracranial mass lesion, particularly acute subdural hematoma, and indicate an urgent need for localizing diagnosis and surgical decompression. Conversely, recording of an ICP level below 10 mm Hg is reassuring that a mass lesion of surgical significance is unlikely, although CSF rhinorrhea or otorrhea will cause a falsely low ICP value. During the monitoring period, a secondary increase in ICP indicates the urgent need to rule out causes of secondary brain insult such as hypoxia, hypercarbia, or hyperthermia. Even B waves, which in themselves do not damage the brain, can be valuable clues to periodic respiration related in turn to cerebral or pulmonary dysfunctionY~ When simple causes for increased ICP such as positional or blood-gas changes have been ruled out, then increased ICP indicates the urgent need for repeat study such as CT scan, angiography, or, if the patient cannot be moved due to multiple injuries, by ventriculography if there is a ventricular catheter in place. Even before ICP is increased significantly, a VPR of 5 mm Hg/ml or more should likewise be regarded as an urgent indication for repeat study of the patient. TM The relative merits of clinical evaluation of patients and continuous monitoring of ICP have been frequently discussed and the situaJ. Neurosurg. / Volume 47 / October, 1977

tion has been clouded by statements that in certain patients ICP can rise almost to the level of arterial blood pressure with no evident clinical deterioration. 1~ This applies mainly to patients with benign intracranial hypertension and obstructive hydrocephalus. It does not apply to patients with head injury in whom an increase in ICP over 40 mm Hg has virtually always in our experience been associated with some clinical deterioration; not infrequently lesser elevations of ICP have also had an ill effect, this being one of the factors that led us to take 30 mm Hg as a threshold for therapy of intracranial hypertension in the intensive care unit. A special problem of the comatose patient with head injury who is exhibiting decorticate or decerebrate motor responses and may have abnormal eye movement and pupillary function is that any clinical deterioration from this point will suddenly render the patient flaccid and unresponsive with dilated pupils, a state in which brain death is only minutes away. In such patients, therefore, we hold that ICP monitoring is invaluable to detect adverse processes before irreversible clinical deterioration occurs. Finally, in determining the place of ICP in diagnosis it must be stated emphatically that we regard the magnitude of brain shift as always more important than the height of ICP in determining the urgency of a course of action. The relationship between displaceable (CSF and venous blood) volume and masslesion volume and the elastic properties of the brain and spinal contents will determine the rate and extent to which ICP rises during brain compression; some degree of compression will always precede the first major rise in ICP. First priority, therefore, must be given to an investigation that reliably informs the neurosurgeon about the presence of intracranial mass lesions and brain shift. In management, effectiveness of therapy for raised ICP can be judged only by measuring ICP. Clinical signs are a poor guide? In certain patients, for instance those with chest injuries or severe pulmonary problems, who require muscle relaxants and positive endexpiratory pressure, ICP monitoring is the only continuously available guide to intracranial events. (Most patients in this study were not paralyzed but phased into the ventilator by means of small sedative doses of morphine or chlorpromazine, and thus 513

J. D. Miller, et al. remained accessible for neurological evaluation.) The advocate of ICP monitoring in head injury is often asked what the overall payoff in the management of patients is likely to be. This is a hard judgement to make on what is essentially a preventative measure. Broadly, the outcome from severe head injury is primarily determined by the severity of initial injury and modified by the subsequent management regimen. Thus neurological signs that relate to the extent and severity of brain damage, such as abnormal motor function or disorders of eye movement, correlate more closely with outcome than ICP in overall terms; increased ICP in these patients on admission appears to be a further parameter of brain damage. The success of the management scheme is better measured by how few patients deteriorate after injury for reasons that are preventable, and it is in this light that ICP monitoring ought, in our opinion, to be judged. Even if only a handful of patients have early and effective therapy initiated as a result of information from ICP measurements, this must be accounted a benefit. Against this must be set the risks, which are that some patients may deteriorate because of intracranial hematoma induced by placement of the subarachnoid screw or ventricular catheter (which did not occur in this series) or intracranial infection, which occurred in 4% of the patients, but in no patient monitored for 3 days or less? 1 In pursuing the evaluation of the role of ICP monitoring in prognosis of head injury we find it to be of value in patients with diffuse brain damage; when signs of brain shift do not cloud the picture, ICP levels on admission provide a valuable guide to the expected outcome, and the higher the ICP is on admission in such patients the greater is the risk of persistent or recurrent intracranial hypertension. Of most importance, recurrent or persistent intracranial hypertension in patients with purposeful motor responses is associated with a poorer outcome. This we believe supports our contention that secondary insults materially influence outcome and ICP monitoring detects these processes. If used as sole indicants of outcome in all patients with head injury, however, ICP levels are of less significance than clinical signs of severe cerebral and brain-stem dysfunction, which in many cases are a compound of both primary and secondary (shift-related, hypox514

ic, or ischemic) damage. High ICP will also be a poor prognostic indicator in those patients with mass lesions who have a good outcome if decompression is achieved before signs of secondary shift-related dysfunction are established. ~ It should therefore come as no surprise that ICP levels do not correlate closely with outcome in all patients with head injury, and this is certainly not a valid reason for condemning ICP monitoring in head injury as others have done. 8 We consider that some of the questions posed in this paper concerning the value of ICP monitoring in head injury have been answered, and that during this study the information yielded from ICP measurement has justified the expenditure of time, equipment, and personnel, at an acceptably low risk. Only in the last 9 months of the study, however, has the CT scan been available to us as a diagnostic tool. Until that point, the alternative to immediate twist-drill ventriculography was carotid angiography, which carries a certain amount of risk. What we must now compare is the risk of ventricular puncture and instillation of air in the emergency room against the transport of the patient for CT scanning and possibly the risk of sedation or anesthesia in order to obtain an artifact-free scan. Air ventriculography increases ICP, and when a mass lesion is present these increases may be large indeed. 4,5 That we have never observed neurological deterioration as a result of air ventriculography we ascribe to the practice of aspirating air from the ventricles where possible, and then the rapid administration of mannitol before transport to the operating room for surgical decompression in all patients with significant midline shift. Surprisingly, failure to locate the lateral ventricle in a maximum of three passes has been an infrequent problem. In such an event, however, we monitor ICP with a subarachnoid screw. At the present time, given the choice, we prefer the ventricular catheter since it offers the opportunity of controlling ICP by CSF drainage and of assessing intracranial pressure-volume relationships and there is no difference in infection risk? 1 The information yielded from ICP monitoring is of value only when it is accurate (< + 1 mm Hg), reliable (easily checked and recalibrated), and accompanied by other clinical and physiological information and a reasonJ. Neurosurg. / Volume 47 / October, 1977

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able understanding of the processes of brain compression. For these reasons, the technique should, in our view, be restricted to neurosurgical centers with intensive care facilities and trained personnel (medical and nursing) available to check, calibrate, interpret, and act on I C P measurements on an around-the-clock basis. What of the future? In this paper we have emphasized a high index of suspicion over even small elevations of I C P , and discussed briefly the use of pressure-volume measurements to try to detect those situations in which a rather low I C P measurement is falsely reassuring because any further volumetric increase in the craniospinal contents will push I C P sharply upward. The methods available for assessing the related parameters of I C P instability, elastic properties of the intracranial contents, C S F outflow resistance, and CSF production rate 15,1va3a5 should be investigated in patients with head injury, to determine their validity and their value. We believe that much i m p o r t a n t physiological data remain to be gathered from the results of controlled perturbations of the CSF system, data of immediate relevance to the management of the severely head-injured patient. References 1. Adams H, Graham DI: The relationship between ventricular fluid pressure and the neuropathology of raised intracranial pressure, in Brock M, Dietz H (eds): lntracranial Pressure. Berlin/Heidelberg/New York: Springer-Verlag, 1972, pp 250-253 2. Becker DP, Miller JD, Ward JD, et al: The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 47:491-502, 1977 3. Becker DP, Vries JK, Young HF, et al: Controlled cerebral perfusion pressure and ventilation in human mechanical brain injury: prevention of progressive brain swelling, in Lundberg N, Pont6n U, Brock M (eds): lntracranial Pressure II. Berlin/Heidelberg/ New York: Springer-Verlag, 1975, pp 480-484 4. Chawla JC: Changes in intracranial dynamics during ventricUlography. J Neurol Neurosurg Psychiatry 32:632, 1969 (Proceedings) 5. Cronqvist S, Lundberg N, Pont6n U: Cerebral pneumography with continuous control of ventricular fluid pressure. Acta Radinl (Diagn) 1:558-564, 1963 6. Fleischer AS, Payne NS, Tindall GT: Continuous monitoring of intracranial pressure in J. Neurosurg. / Volume 47 / October, 1977

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severe closed head injury without mass lesions. Surg Neurol 6:31-34, 1976 Guillaume J, Janny P: Manom6trie intracranienne continue: Int6r6t de la m6thode et premiers r6sultats. Rev Neurol 84:131-142, 1951 Jennett B, Bond M: Assessment of outcome after severe brain damage. A practical scale. Lancet 1:480-484, 1975 Johnston IH, Jennett B: The place of continuous intracranial pressure monitoring in neurosurgical practice. Acta Neurochir 29: 53-63, 1973 Johnston IH, Johnston JA, Jennett B: Intracranial-pressure changes following head injury. Lancet 2:433-436, 1970 Langfitt TW: Increased intracranial pressure. Clin Neurosurg 16:436-471, 1969 Leech P J, Miller JD: The intracranial volumepressure relationships during experimental brain compression in patients. I. Pressure responses to changes in ventricular volume. J Neurol Neurnsurg Psychiatry 37:1093-1098, 1974 Lundberg N: Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Acta Psychiatr Neurol Scanfl 36 (Suppl 149):1-193, 1960 Lundberg N, Troupp H, Lorin H: Continuous recording of the ventricular-fluid pressure in patients with severe acute traumatic brain injury. A preliminary report. J Neurosurg 22:581-590, 1965 Marmarou A, Shulman K, LaMorgese J: Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 43:523-534, 1975 Miller JD: Pressure and volume in the craniospinal axis. Clin Neurosurg 22:76-105, 1975 Miller JD, Garibi J, Pickard JD: Induced changes of cerebrospinal fluid volume. Effects during continuous monitoring of ventricular fluid pressure. Arch Neuroi 28:265-269, 1973 Miller JD, Pickard JD: Intracranial volume pressure studies in patients with head injury. Injury 5:265-268, 1974 Miller JD, Stanek A, Langfitt TW: Concepts of cerebral perfusion pressure and vascular compression during intracranial hypertension. Prog Brain Res 35:411-432, 1972 North JB, Jennett S: Abnormal breathing patterns associated with acute brain damage. Arch Neurol 31:338-344, 1974 Rosner M J, Becker DP: ICP monitoring: complications and associated factors. Clin Neurosurg 23:494-519, 1976 Rossanda M, Collice M, Porta M, et al: Intracranial hypertension in head injury, clinical significance and relation to respiration, in 5"15

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New York: Springer-Verlag, 1975, pp 475-479 23. Sullivan HG, Miller JD, Becker DP, et al: The physiological basis of intracranial pressure change with progressive epidural brain compression. An experimental evaluation in cats. J Neurosurg 47:532-550, 1977 24. Sundb~irg G, Kjallquist A, Lundberg N, et al: Complications due to prolonged ventricular fluid pressure recording in clinical practice, in Brock M, Dietz H (eds): lntraeranial Pressure. Berlin/Heidelberg/New York: SpringerVerlag, 1972, pp 348-352 25. Szewczykowski J, Dytko P, Kunicki A, et al: Determination of critical ICP levels in neurosurgical patients: a statistical approach, in Lundberg N, Pont6n U, Brock M (eds): In-

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Pressure II. Berlin/Heidelberg/ New York: Springer-Verlag, 1975, pp 392-393 26. Troupp H: Intraventricular pressure in patients with severe brain injuries. J Trauma 5:373-378, 1965 27. Vapalahti M, Troupp H: Prognosis for patients with severe brain injuries. Br Med J 3:404-407, 1971 tracranial

This work was supported by NIH Grant 1 P50 NS12587. Address reprint requests to." J. Douglas Miller, M.D., Division of Neurosurgery, P.O. Box 758, Virginia Commonwealth University Medical College of Virginia, Richmond, Virginia 23298.

J. Neurosurg. / Volume 47 7 October, 1977