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To cite this article: Munchi Choksey, H. Alan Crockard & Michael Sandilands (1993) Acute
traumatic intracerebral haematomas: Determinants of outcome in a retrospective series of 202
cases, British Journal of Neurosurgery, 7:6, 611-622, DOI: 10.3109/02688699308995090
Article views: 18
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British Journal of Neurosurgery (1993) 7 , 61 1-622
ORIGINAL ARTICLE
The Royal London Hospital, Whitechapel, London E2 1BB and *Department of Surgical
Neurology, The National Hospital for Neurology and Neurosurgey , Queen Square, London, UK
Abstract
A retrospective study was carried out of 202 patients with traumatic intracerebral haematomas (TICH) noted on
CT, to determine which factors most affected outcome. There were 151 (75%) males and 51 (25%) females,
whose ages ranged from 1 to 84 years. One-hundred-and-two (51%) had a good outcome (Glasgow Outcome
Score 1 and 2). Thirty-five (17%) were vegetative or severely disabled and 65 (32%) died. Of the 169 with a
single haematoma, 98 (58%) had a good outcome, while only 20% of patients with two clots fared well. No
patient with three or more haematomas had a good outcome.
Single factor logistic regression analysis identified Glasgow Coma Score (GCS), haematoma volume and
difficulty with airway maintenance or poor arterial oxygenation as important factors in determining outcome. A
four-factor logistic regression analysis model was developed which revealed that, when all other factors had been
taken into consideration, craniotomy significantly improved the probability of a good outcome.
Key words: Head injuries, intracerebral haematoma, craniotomy, logistic regression analysis, outcome, CT.
61 1
612 M. Choksey, H. A. Crockard & M. Sandilands
TABLE I. The distribution of patients, the approximate percentage of total head injury admissions they represented
and the periods for which the records were available at the different centres
Note: Cambridge is both a primary and secondary referral centre for head injury.
computerized databases. In Landon, the infor- patients could deteriorate in other ways, such
mation was retrieved by weekly consultation as developing pupillary abnormalities or later-
with the neurosurgical centres (Table I). The alizing signs, these parameters were ignored
clinical data (Table I) included age, sex, mode when analyzing the data, for reasons discussed
of injury, neurological state at both referring later.
hospital and neurosurgical unit (NSU), the Many patients, in either the referring hospi-
radiological findings, the treatment and finally tal or the NSU, were unable to maintain their
the outcome. Patients with spontaneous in- airway, had poor arterial oxygenation or inade-
tracranial haemorrhage, multiple injuries and quate ventilation. These patients were
compound depressed fractures were excluded, classified as having respiratory insufficiency.
as were 35 patients with incomplete case Surgical removal of the haematomas was
records. Overall, these patients represented classified as definitive if the patient had a cran-
approximately 3% of all admissions for head iotomy. Burr hole aspiration was not included
injury to the respective neurosurgical centres in ‘surgical removal’.
(Table I). Note that Cambridge, in contrast to Outcome was assessed between 6 months
all the other centres, was both a primary and and 1 year, using the Glasgow Outcome Score
secondary head injury referral centre. (GOS).4 Good outcomes were defined as GOS
1-2, bad outcomes were 3-5.
Haematoma was considered to exist when
Definitions
the predominant C T lesion was a high attenu-
Age, as a factor, was grouped at four levels: ation intracerebral mass, characteristic of
0-20, 21-40, 41-64 and 64 + years old. clotted blood. Surrounding areas of oedema
The principal index of the neurological state were ignored, as their borders blended imper-
was the Glasgow Coma Score (GCS) ranging ceptively with more normal brain. The
from 3 to 15, as recorded on admission to the haematoma location was recorded as either
neurosurgical unit. The GCS was then peripheral (frontal, parietal, temporal, occipi-
grouped at three levels: scores from 3 to 7 tal) or central.
(Group I), 8 to 11 (Group 11) and 12 to 15 Haematoma volume was calculated by mea-
(Group 111). The case records from the Acci- suring the area occupied on each slice of the
dent and Emergency Unit or referring hospital C T scan, multiplying by the slice thickness
were often incomplete, and thus we elected to and summing the volumes so obtained on con-
use the neurosurgical data alone. tiguous slices. The haematoma volumes were
Clinical deterioration was defined as a fall in divided into four groups-less than 5, 6-15,
the GCS of two points or more. Although 16-35 and over 35 ml.
Traumatic intracerebral haematomas 6 13
TABLE
11. The factors and the levels at which they operated, considered for the logistic regression
model. The actual patient numbers in each subgroup are given, together with the number ("1%)
that had a good outcome
No. of Good
Factor Code Levels patients outcome
different levels of each factor. The relation- They were commoner in the elderly (65 + )
ships-and similarities-between probability, age group, accounting for 25/47 (53%) of pa-
odds and log odds are explained in Appendix tients; in contrast, only 7/57 (12.5%) of the
2. 0-19 age group had falls. The mode of trauma
had no effect on outcome.
Results (Table 11)
There were 151 (75%) males and 51 (25%) Age
females in the study group, aged from 1 to 84
Initially, age appeared to have no direct effect
years. One-hundred-and-two (5 1%) had a
on the outcome, which was surprising. How-
good outcome (GOS 1-2). Thirty-five (17%)
ever, a significantly high proportion of young
were left severely disabled or vegetative (GOS
patients (0-20 years) had a low GCS, and a
3-4) and 65 (32%) died.
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TABLE
111. Changes in deviance associated with insertion of factors singly into the logistic
regression model
GM 280.01 - 20 1 -
GCS 234.13 45.88 199 2
Volume 262.19 17.82 198 3
NUM 249.51 30.50 199 2
LOC 264.63 15.38 197 4
DET 229.44 50.57 199 2
RI 263.36 16.65 200 1
AGE 275.27 4.74 198 3
SEX 277.10 2.91 200 1
CRAN 279.24 0.77 200 1
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were intubated and ventilated. The remaining haematoma location and respiratory in-
five were deemed too severely injured to war- sufficiency were all significant in single factor
rant further treatment. Of the 30 patients models, whereas age, sex and craniotomy were
ventilated, only seven (20%) had a good out- not (Table 111).
come. However, since the outcome was affected by
Eighty-one patients were ventilated because many factors, different combinations were
it was thought that they had raised intracranial tried. A model which well described the out-
pressure. Thirty-three of these (41%) had comes of patients included these four factors:
good outcomes. Ninety-one patients were not the GCS, the haematoma volume, the pres-
ventilated and of these 62 (68%) made good ence of respiratory insufficiency and the
recoveries. surgical management. The quantitative effects
on outcome of each of these factors in the
Other features logistic regression model is summarized in
Other clinical and radiological features were Table IV. An explanation of the statistical
studied. The presence of pupillary abnormali- terms used is given in Appendix 1. Qualita-
ties paralleled almost exactly the GCS, so their tively, what Table IV illustrates is that the
inclusion conveyed no further useful informa- GCS has a very large influence on outcome.
tion. The presence of lateralizing signs was not However, following its incorporation into the
significant, nor were skull fractures. model haematoma volume still remained an
important determinant of outcome, as did res-
Surgey piratory insufficiency and surgical removal.
Although their influences were not equal,
Eighty-four patients underwent definitive each of these four factors therefore had an
surgery for removal of their haematoma. Of important effect on outcome.
these, 52 (62%) had good outcomes, 32 The actual effect of the different levels of
(38%) bad. Patients differed widely in other these factors on the outcome is illustrated in
respects, however, and logistic regression was Table V, which requires some explanation,
used to establish the effect of surgery on out- best done by example (see also Appendix 2 ) .
come. Take two patients, A and B. Both have a GCS
in level one, haematoma volume in level one,
Lqistic regression
and neither has had surgery. However, they
GCS, haematoma volume, deterioration, differ in that patient A has no recorded res-
616 M. Choksey, H. A. Cmckard & M. Sandilands
TABLE IV.A four-variable logistical regression model best described our patients. This
incorporating the GCS, haematoma volume, respiratory insufficiency and surgery.
Mean 280.0 20 1 - -
+ GCS 234.1 199 45.9 (5.99) 2
+Volume 214.2 196 19.9 (7.82) 3
Deg. freedom = degrees of freedom; Ch. deviance = change in deviance; Ch. deg. free-
dom = change in degrees of freedom. The figures in brackets in the Ch. deviance column
refer to the level at which the change would have been deemed significant at the 5% level.
Note the very large change in deviance associated with insertion of GCS into the model,
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followed by a large change associated with insertion of volume. However, the insertion
of respiratory insufficiency and surgery subsequent to these two factors reduced the
deviance still further, indicating that these two factors operated independently.
Surgery 0 + 0.98 - -
1.0-
0.9-
0.8-
0.7 -
0.6-
0.5 -
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0.4-
0.3-
0.2-
0.1-
0 1 I I I I I I I I I I
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Probability without craniotomy
FIG.1. A comparison of probabilities of a good outcome, without and with a craniotomy (for the model including
GCS, volume, respiratory insufficiencyand craniotomy, based on data from all the patients). Curve B (D) gives the
baseline of probability of a good outcome without a craniotomy. Curve A (A) shows the increase in probability of
a good outcome associated with a craniotomy. For example, patient 0 has an increase from 0.1 to 0.22. patient P
has an increase from 0.40 to 0.65. patient Q has an increase from 0.78 to 0.90.
Holbourn14 predicted a different swirling with compromised airways and, from reading
mechanism for central haematomas. Here, in the accounts of their initial assessment and
support, only one patient had both a central transfer, it would appear that the problem had
and a peripherally sited haematoma. Central been present for some considerable time. It
haematomas were associated with a poor prog- was our impression that many of these patients
nosis; less than 20% had a good outcome. could have benefited from intubation and ven-
Patients who developed what we have tilation earlier in their management,
termed ‘respiratory insufficiency’ fared particularly prior to transfer.
badly-the log odds of a good outcome fell by The use of multi-variate analysis in the in-
1.516, after allowing for GCS, size of vestigation of factors determining outcome is
haematoma and surgical management (Table now well established.’ The problem of bias in
V). Note that this effect persisted after al- such studies is always present, and this is par-
lowance for both the GCS and the haematoma ticularly so in the evaluation of therapeutic
size: it was not merely a reflection of a poor manoeuvres. Foulkes et a1.I5 stated that, ide-
GCS. It re-emphasizes the importance of ally, patient groups defined by an intervention
avoiding the ‘second injury’ as emphasized by (e.g. surgery versus no surgery) should be
so many other authors, for a large number of matched in all respects save that of interven-
these patients arrived at the neurosurgical unit tion. Non-randomization implies that other
Traumatic intracerebral haematomas 6 19
0-20 44 4 8 56
21-40 30 15 9 54
41-64 20 11 13 44
65 + 18 15 15 48
explanations may be sought for observed ef- The counter-argument-that surgery was
f e c t ~ Similar
.~ limitations apply to the use of only reserved for 'better' patients, does not
historic controls. hold, as three adverse factors-the GCS,
Some of these objections can be countered haematoma size and the presence of respira-
by the form of logistic regression analysis we tory insufficiency were already incorporated in
have used. Provided patients are matched for the model.
risk factors that make 'neurosurgical sense', Our findings may be surprising to some and
the effect of one form of treatment can be we expect our view to be contested. However,
investigated. The argument-database analy- all we can re-emphasize is that the study was
sis versus randomized prospective trial-still retrospective, and that none of the authors had
continues. There are some who believe that any influence on the management. Interest-
the randomized prospective clinical trial is a ingly, most of the neurosurgeons who kindly
'Gold Standard', and the only way truly to allowed us to study their patients thought that
evaluate different management strategies. these haematomas were removed 'only infre-
However, it is unlikely that any large group of quently'-perhaps because of their sporadic
neurosurgeons would agree to a randomized occurrence. This study shows that 84 pa-
prospective trial of best medical treatment ver- tients-over 4O0h-underwent craniotomy, so
sus best medical treatment plus surgery. In the surgical removal is 'not uncommon' in the
absence of this 'Gold Standard', the next best United Kingdom.
approach is analysis of large data banks. While There was a marked association between
the conclusions obtained can only cautiously the volume of the haematoma and the proba-
be extrapolated to patients with TICH, un- bility of late deterioration. It is tempting to
equivocally significant factors may reasonably draw the conclusion that early, pre-emptive
be allowed to influence neurosurgical manage- surgery may be beneficial in TICH. There
ment. have been other attempts to establish guideli-
There can be no single 'true' model that nes for the pre-emptive removal of these
explains all the observed results. However, the haematomas. Cooper'' advocated their re-
four factors used in our model do make 'neu- moval if consciousness was clouded, or if there
rosurgical sense'; that the GCS, haematoma were focal neurological signs. Andrews et ul.'"
volume and respiratory insufficiency affect the suggest that the haematoma volume or its lo-
outcome would surprise few neurosurgeons. cation are guides-30 ml and a temporal
What emerged quite clearly was that the surgi- haematoma were their specific recommenda-
cal removal of these haematomas was tions for removal. Galbraith & Teasdale16
associated with a more favourable outcome. suggested that the ICP was a good guide: their
Patients who underwent a craniotomy had an series included five patients with a purely in-
increase in log odds of a good outcome of tracerebral haematoma. If the ICP was over
0.98. about 30 mmHg, they stated that the patients
620 M. Choksey, H. A. Crockard & M . Sandilands
TABLE
W.
Model Deviance Deg. freedom Ch. deviance Ch. deg. freedom
invariably needed an operation. However, this patients aged over 65 years. This broadly
method is not infallible, for Bullock et al.” matches the results reported by Vollmer et al.
found that the ICP remained low in a who showed a steep rise in mortality in pa-
significant number of patients with tients over 55 years.
haematomas who eventually deteriorated and Establishing the risk factors that govern out-
died. They reported that effacement of the come may or may not be clinically useful. In
basal cisterns was associated with high ICP. In their book, Jennett & Teasdale” state “It is
our own small series of TICH studied with seldom realised how little help it is to the
Single Photon Emission Tomography clinician to know that an individual patient
(SPET),13 we found that patients who subse- under his care has one or more features known
quently deteriorated had large perfusion to be associated with a bad or a good out-
defects that were surrounded by hypo-per- come.” In the coming age of clinical audit, this
fused brain, in marked contrast to those who may no longer be true. In this study we have
remained stable. established that the presence and level of cer-
In this study TICH was found in all age tain risk factors, when taken together,
groups, at all locations. There was a tendency accurately predict the outcome of TICH. In
for these haematomas to be larger in the older future, clinicians may use these data as a guide
age group (65 + years). Yet age was not ini- to their own management, and investigate
tially found to correlate with the outcome. thoroughly cases where the outcome was
This was because, in this series, there was a markedly different from that predicted. It may
preponderance of young patients who were also be a help for them to know that in our
more severely injured. This contrasts with the series certain features-such as the presence of
study composition reported by Vollmer et al.,I2 three or more haematomas-made a bad out-
where no correlation was found between age come inevitable. Creating this baseline of
and injury severity. When the effect of the expected outcome may thus serve a very useful
GCS was allowed for in the regression analy- purpose.
sis, age became a significant feature. All other In summary, TICH remains a troublesome
factors being equal, the log odds of a good clinical problem, one which C T has increas-
outcome decreased by 1.6, but only for ingly brought to the neurosurgeon’s attention.
Traumatic intracerebral haematomas 621
In this series, over 40% of patients eventually Grant, Richard Hayward and Michael
underwent a craniotomy, in most cases after Powell.
clinical deterioration, so conservative manage- London, Royal Free Hospital: Robert
ment is not overwhelmingly the norm. Maurice-Williams and Ken Lindsay.
Deterioration is particularly common with London, St Bartholomew's Hospital: John
large haematomas, especially in the elderly. Currie and Farhad Afshar.
What can we learn from this study? The
Glasgow Coma Score is still a major determi-
nant of outcome. Patients with large Address for correspondence: H. Alan Crockard,
haematomas deteriorate. Poor ventilatory Lkptirtrrirnt 01 Surgical Neurtrlogy, 'TIie
function has a significant adverse effect. Hav- National Hospital for Neurology and
ing allowed for these factors, there is no doubt Neurosurgery, Queen Square, London WC 1N
3BG, UK
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14 Holboum AHS. Mechanisms of head injury. In qualitative terms, what this implies is that, for
Lancet 1943; ii:438-41. patients matched from Glasgow Coma Score,
15 Foulkes MA, Eisenberg HM, Jane JA, Marmarou haematoma size and the presence of respiratory in-
A, Marshall LF. The Traumatic Coma Data Bank: sufficiency, surgical removal materially increases the
design, methods, and baseline characteristics. J probability of a good outcome.
Neurosurg 1991; 75:S8-13.
16 Galbraith S, Teasdale GM. Predicting the need for
operation in the patient with an occult traumatic in- Appendix 2
tracranial haematoma. J Neurosurg 1981; 5575-81. The probability p that a give outcome will occur is the
17 Bullock R, Golek J, Blake G. Traumatic intracere- number of times such an outcome can be expected,
bra1 haematoma-which patients should undergo viz. p = 0.6 means six times out of 10.
surgical evacuation? C T scan features and ICP The odds are =p/l-p, viz: 0.6/14.6 = 1.5:l or 3:2.
monitoring as a basis for decision making. Surg Conversely, p = ODDS/l-ODDS
Neurol 1989; 32:181-7. The log odds are the natural logarithm of pll-p; here
18 Jennett B, Teasdale G. Management of head in- log 1.5 = 0.4054.
juries. Philadelphia: FA Davis, 1981, 327. What does this Table AI indicate? First, the general
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patients matched for Glasgow Coma Score and Respiratory insufficiency - 1.5 16
Table AI.
Level 1 Level 2 Level 3 Level 4
GCS 0 1.69 2.78 -
Volume 0 - 1.625 -2.32 - 2.85
Respiratory insufficiency 0 - 1.5 16
Surgery 0 + 0.98
The general mean = 2.39