1623
Definition of Initial Grading, Specific Events,
and Overall Outcome in Patients With
Aneurysmal Subarachnoid Hemorrhage
A Survey
J. van Gijn, MD, FRCPE; J.E.C. Bromberg, MD; K.W. Lindsay, PhD, FRCS;
D. Hasan, MD; M. Vermeulen, MD
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Background and Purpose Scientific communication in medicine can be effective only if reports are based on unequivocal
criteria for clinical conditions or specific diagnoses.
Methods We reviewed all articles about subarachnoid hemorrhage published in nine neurosurgical or neurological journals from 1985 through 1992 and assessed the presence and
the precision of definitions used for reporting the initial grade,
the specific complications of rebleeding, delayed cerebral
ischemia, and hydrocephalus, and the overall outcome. We
identified 184 articles reporting direct observations in at least
10 patients on one or more of these conditions.
Results Of 161 articles reporting the initial condition, only
19% used an unequivocal grading system (World Federation
of Neurological Surgeons Scale or Glasgow Coma Scale); this
proportion did not increase after 1988, when the World
Federation of Neurological Surgeons Scale was introduced.
The specific outcome events of rebleeding, ischemia, and
hydrocephalus (283 instances) were sufficiently defined in only
w
hen I use a word," Humpty Dumpty said, in
rather a scornful tone, "it means just what I
choose it to mean —neither more nor less."
Lewis Carroll
Through the Looking-Glass
The eventual outcome of patients with subarachnoid
hemorrhage is determined by the effects of the initial
hemorrhage and often also by newly developing complications, of which rebleeding, delayed ischemia, and
hydrocephalus are the most important. This multitude
of factors calls for a high degree of accuracy in reports
of research dealing with prognosis or with intervention
aimed at specific complications. Otherwise, the results
of such studies cannot be generalized or compared with
other results. First, the initial assessment (or "grading")
should be unambiguous in describing the selection of
patients who entered the study because this is an
Received January 28, 1994; final revision received March 31,
1994; accepted April 20, 1994.
From the University Department of Neurology, Utrecht (J. van
G., J.E.C.B.), the University Hospital 'Dijkzigt,' Rotterdam
(D.H.), the Academic Medical Centre, Amsterdam (M.V.), the
Netherlands, and the Department of Neurosurgery, Institute of
Neurological Sciences, Southern General Hospital, Glasgow, UK
(K.W.L.).
Reprint requests to J. van Gijn, MD, FRCPE, University
Department of Neurology, University Hospital, PO Box 85500,
3508 GA Utrecht, The Netherlands.
© 1994 American Heart Association, Inc.
31% of instances, incompletely in 22%, and not at all in 47%.
The proportions were similar when the results were analyzed
according to the type of complication, the year of publication,
or per study. The four exclusively neurosurgical journals
featured suitable definitions for any of the three outcome
events in 20% of 209 instances, whereas the five mainly
neurological journals published fewer articles about subarachnoid hemorrhage (74 instances of outcome events) but more
often with precise criteria (65%). Overall outcome was adequately reported in 63% of all articles, with an increase over
the years (54% in 1985 through 1988, 71% in 1989 through
1992).
Conclusions Reports about subarachnoid hemorrhage require closer scrutiny before publication to ascertain whether
the conclusions about specific outcome events are based on
unequivocal criteria. (Stroke. 1994^5:1623-1627.)
Key Words • cerebral ischemia • hydrocephalus •
stroke outcome
important determinant of outcome.1 Second, any subsequent complication should be identified, not so much as
a measure of outcome in itself but rather to provide an
understanding of the pathophysiological chain of
events. Third and last, the eventual outcome should be
recorded in terms that are not only unambiguous, and
therefore consistent between observers, but also relevant from the point of view of the patient.
These methodological requirements are not always
met in published studies about the prognosis and management of patients with ruptured aneurysms. To assess
the extent of this problem, we performed a systematic
review of articles about subarachnoid hemorrhage in
nine relevant periodicals published from 1985 through
1992. We studied not only the definitions for the three
major complications but also the methods used for
grading the clinical condition on admission and for
judging the eventual outcome.
Methods
The year 1985 was arbitrarily chosen as the starting point for
this survey. By that time, computed tomography (CT) equipment had been installed in all major hospitals, and several
publications in international journals of neurology and neurosurgery had stressed the diagnostic importance of serial CT
scanning.2-6 Up to and including the year 1992, we identified
articles about patients with subarachnoid hemorrhage via the
annual indexes (using the key words subarachnoid hemorrhage, hemorrhage, and aneurysm) of the following nine
1624
Stroke
Vol 25, No 8 August 1994
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journals: Journal of Neurosurgery, Neurosurgery, Surgical Neurology, Acta Neurochirurgica, Annals of Neurology, Archives of
Neurology, Neurology, Journal of Neurology, Neurosurgery and
Psychiatry, and Stroke. The first four journals can be regarded
as being directed mainly at a readership of neurosurgeons; the
other five journals are primarily neurological in scope, although there is some overlap for the last two journals. Articles
were included in the study on the basis of the following
criteria: (1) full article (not abstract or letter), (2) direct
observations of patients (not population studies or review
articles), (3) presence of ruptured aneurysm either demonstrated by angiography or strongly suggested by the pattern of
hemorrhage on the CT scan, (4) number of patients 10 or
more, (5) follow-up period of at least 1 week, (6) selection of
patients not determined by outcome or occurrence of specific
events, and (7) outcome criteria not exclusively paraclinical
(eg, blood flow velocity, biochemical substances, or isotope
scanning).
server studies; such studies have been performed for the
Glasgow Outcome Scale" 12 and the Rankin Scale.1314
A definition was considered incomplete if only some of the
above criteria were met, such that other causes of deterioration were not convincingly excluded. This included, for instance, lumbar puncture for the diagnosis of rebleeding,15
"ischemic symptoms" for the diagnosis of ischemia, or a
personal scale distinguishing "good," "fair," and "poor" in the
assessment of outcome. The distinction we proposed between
definite and probable ischemia or rebleeding did not affect the
way in which the articles were classified. If no criteria at all
were given for specific complications or outcome, despite these
being mentioned in the "Results" section, we categorized the
definition as absent. These judgments were made by two of the
authors (J. van G. and J.E.C.B.); disagreements were resolved
by discussion.
The definition of a particular outcome event was normally
found in the "Methods" section of a scientific article, but we
took account of descriptions anywhere in the text, including
figure legends and references to previous publications. Each
article was rated according to the grading system on admission
and also according to the criteria used for defining rebleeding,
delayed cerebral ischemia, acute hydrocephalus, and overall
outcome (usually after 3 to 6 months).
The scale used for the initial assessment of the patient was
simply tabulated, without qualitative judgment at this stage.
For rebleeding, ischemia, and hydrocephalus, we regarded a
definition as adequate if it contained a description of the
clinical features supplemented by repeated CT scanning, the
results of which were compared with a baseline scan. Signs of
clinical deterioration are necessary but usually not sufficient
for diagnosing any of these three outcome events. For instance, a gradual decrease in the level of consciousness
without focal signs may be caused by delayed ischemia6 but
also by hydrocephalus.7 Loss of consciousness with a sudden
onset almost invariably accompanies confirmed episodes of
rebleeding8 but in itself is not sufficient to establish the
diagnosis3; one third of such episodes have to be attributed to
causes other than rebleeding.4 Only a gradually developing
focal deficit is fairly characteristic of ischemia, but unless the
patient has been under continuous supervision rebleeding
ought to be considered as well. For each possible complication,
we considered the following descriptions as precise. (1) Rebleeding was defined as sudden deterioration with fresh hemorrhage on a repeated CT scan or at autopsy compared with a
baseline CT scan (definite rebleeding); or sudden deterioration and death without the possibility of proof by a CT scan or
an autopsy (probable rebleeding). (2) Delayed ischemia was
defined as gradual development of focal neurological signs,
deterioration in the level of consciousness, or both, with
ischemia confirmed by a CT scan or at autopsy (definite
ischemia); or gradual development of focal neurological deficit, with or without deterioration in the level of consciousness,
in the absence of confirmation by CT or autopsy but with
exclusion of other causes of deterioration such as hydrocephalus, electrolyte disorders, or specific surgical complications
(probable ischemia). Because the pathogenesis of delayed
cerebral ischemia after subarachnoid hemorrhage is multifactorial,9 we did not include vasospasm or other specific causal
factors in the "ideal" definition, even apart from difficulties in
demonstrating such factors in any systematic fashion. (3)
Hydrocephalus was defined as some measure of ventricular
size (often a linear measure such as the bicaudate index), with
some threshold of abnormality, preferably the 95th percentile
for age.
We identified 184 articles that fit the inclusion criteria
for this study. Twenty articles mentioned only the
clinical grading on admission, only the overall outcome,
or both. Of the 164 remaining articles, 80 reported only
one of the three specific outcome events (rebleeding,
delayed ischemia, or hydrocephalus); 49 articles reported two events, and 35 articles reported on all three.
A grading system for the clinical condition on admission
was used in 161 articles and a measure of outcome in
137.
For outcome we regarded a measure as adequate if it was
focused on a simple scale of handicap or degree of dependence.10 The scale should have proved reliable in interob-
Results
Table 1 lists the use of different grading systems for
each year for the clinical condition on admission. The
scale according to Hunt and Hess (or, in some cases,
that by Hunt and Kosnik) was by far the most widely
used (71%), with the Glasgow Coma Scale or World
Federation of Neurological Surgeons (WFNS) Scale
used in only a small minority (19%). Over the years
some fluctuations occurred but without a consistent
tendency to change.
Fig 1 illustrates the precision of the definitions per
outcome event for the entire period of 1985 through
1992 and for all nine journals. The proportion of
adequate criteria was around 30% for rebleeding, ischemia, and hydrocephalus and 63% for overall outcome.
An article with no given definition at all occurred most
often for rebleeding (59%) but was only slightly less
common for hydrocephalus (47%) and delayed ischemia
(40%); overall outcome was almost always defined in
some way, although incompletely in 36%.
Fig 2 shows the accuracy of the definitions per journal
for the entire study period. We did not include overall
outcome in this comparison. Because this definition was
adequate in 63%, across the range of journals, inclusion
of this item in the comparison between journals would
dilute any differences in the definition of specific complications. The four typically neurosurgical journals
featured adequate criteria in 20%, and these journals
contained by far the most articles (74% of the event
assessments). The five journals with a primarily neurological background that contained the remaining 26% of
reported events were accurate far more often (65%).
The proportion of accurate definitions per year is
shown for the three specific outcome events in Fig 3. It
is clear that the rate of 31% for adequate definitions for
all three events together is rather stable over the 8 years
of the study, with no discernible tendency to change.
An analysis per article for one or more of the three
specific outcome events showed that the methodological
van Gijn et al Definitions in Subarachnoid Hemorrhage
1625
TABLE 1. Grading Systems Used for Recording the Clinical Condition on Admission of Patients
With Subarachnoid Hemorrhage in 161 Articles in Nine Neurosurgical and Neurological Journals
According to Year of Publication
Hunt and Hess Scale17
(or Hunt and Kosnik)
Year of
Publication
No. of
Articles
Glasgow Coma Scale21
or WFNS Scale (*)*>
Other
System
No.
%
%
No.
%
1985
13
7
54
3
28
3
28
1986
14
12
86
1
7
1
7
1987
25
19
76
2
8
4
16
1988
30
23
77
4(2)*
13
3
10
1989
16
7
44
6(1)*
37
3
19
1990
16
13
81
2(0)*
13
1
6
1991
20
15
75
5(3)*
25
1992
27
18
67
7(4)*
26
2
7
Total
161
114
71
30
19
17
10
No.
Downloaded from http://stroke.ahajournals.org/ by guest on July 28, 2017
WFNS indicates World Federation of Neurological Surgeons.
standards were slightly higher than average for studies
that concentrated on a single outcome event. Of the 80
articles reporting on one outcome event, 33 (41%) used
adequate criteria; an additional 27 (34%) applied other,
though incomplete, definitions.
Table 2 lists the proportion of adequate assessments
of outcome over the years of the study. In this case there
does seem to be a clear trend toward better definitions
over the course of time. This change reflects the widespread adoption of the Glasgow Outcome Scale.
Discussion
It is disquieting that two thirds of the studies of
subarachnoid hemorrhage published in the last 8 years
had incomplete or even no criteria for classifying patients' initial condition or for defining subsequent outcome events (rebleeding, ischemia, and hydrocephalus).
Such ambiguity occurred regularly more than once in
the same article. It is of no less concern that we failed to
find any sign of improvement over the years except for
the Glasgow Outcome Scale, which has become a widely
rebteeolng
(n=75)
J Neurosurg
(n=63)
Neurosurgery
(n=55)
Surg Neural
(n=28)
Acta Neuroch
(n=63)
all neurosurgical [
L
(n=209)
Stroke
(n=52)
Am Neural
(n=6)
Arch Neural
(n=6)
Neurology
(n=4)
JNNP
(n=6)
ischemia
(n=144)
hydrocephalus [~
(n=64)
L.
outcome
(n=i37)
% 0
accepted measure for the overall outcome of patients
with subarachnoid hemorrhage.
Our survey is not without its limitations. First, we did
not include every neurosurgical and neurological journal in the world. Nevertheless, the periodicals we selected have the largest circulation and are most often
cited by authors in the field of neurosurgery and neurology; the wide readership is reflected in a relatively
high journal impact factor.16 Therefore, any selection
bias in the literature reviewed is likely to be in the
direction of good articles rather than poor articles.
Second, the emphasis in our review was not on articles
25
50
75
100
al neurological
(n=74)
%
I I = adequate definition
[ffj = incomplete definition
p i = no definition at al
FIG 1. Bar graph showing definition of specific outcome events
and overall outcome after subarachnoid hemorrhage in 184
articles published from 1985 through 1992 in nine neurosurgical
and neurological journals, n indicates number of times an event
was reported.
0
25
75
50
•
100
= adequate definition
= incomplete definition
= no definition at a l
FIG 2. Bar graph showing definition of specific outcome events
after subarachnoid hemorrhage (rebleeding, ischemia, and hydrocephalus) in 184 articles, according to the journal in which
these were published, n indicates number of times an event was
reported.
1626
Stroke Vol 25, No 8 August 1994
1985
(n=21)
1986
(n=29)
1987
(n=35)
1988
(n=60)
1989
(n=30)
1990
(n=32)
1991
(n=33)
1992
(n=43)
% 0
25
50
75
100
Downloaded from http://stroke.ahajournals.org/ by guest on July 28, 2017
I_J = adequate definition
|#3 = incomplete definition
S = no definition at all
FIG 3. Bar graph showing definition of specific outcome events
after subarachnoid hemorrhage (rebleeding, ischemia, and hydrocephalus) in 184 articles published in nine neurosurgical and
neurological journals according to year of publication, n indicates number of times an event was reported.
as a whole but on the sets of criteria used for defining
initial condition, specific outcome events, and overall
outcome. Most articles contained reports on more than
one of these states or events, on average slightly more
than three per article. One might argue that multiple
definitions within the same article are more likely to be
of the same quality than single definitions from different
articles. We analyzed this per article for the three
specific outcome events and found that the rate of
adequate definitions was only slightly higher in articles
describing single events (41%) than in those reporting
multiple events (31% with precise definitions). In addition, it would have been difficult to apply weighting to
obtain a rating per article instead of per reported item.
A third objection might be that the reviewed articles
included work from our own group, published for the
TABLE 2. Definition of Overall Outcome After
Subarachnoid Hemorrhage in Nine Neurosurgical and
Neurological Journals According to Year of
Publication (1985-1992)
Definition
Adequate
Year of
Publication
No. of
Articles
No.
%
1985
10
5
50
1986
12
4
33
1987
19
10
53
1988
30
19
63
1989
14
11
79
1990
15
9
60
1991
14
11
79
1992
23
17
74
most part in neurological journals, and that therefore
the results of this overview are to some degree based on
circular reasoning. However, given that the 80 studies
focusing on single rather than multiple outcome events
after subarachnoid hemorrhage can be regarded as most
typically representing the "state of the art," our group
contributed only 8 of the 33 articles with precise definitions. Of the 25 other articles with complete definitions of single issues, as many as 18 were published in
neurosurgical journals, which indicates that the use of
our standards for definitions is not confined to the
neurological community.
The initial assessment of the patient's condition was
most often recorded (in two thirds of the studies) on the
scale proposed in 1968 by Hunt and Hess.17 Although
hallowed by tradition, this 25-year-old scale has important drawbacks. These were highlighted by two studies
of observer variability.1819 Both were published before
1985, the first year of our review. When experienced
trainees and neurosurgical specialists were asked to
grade 15 patients with subarachnoid hemorrhage, considerable variation existed with up to four different
grades being selected for the same patient. A similar
variation occurred when written summaries of these 15
patients were submitted to a group of observers from 11
centers throughout Europe, all with a declared interest
in the management of subarachnoid hemorrhage.18 The
second study addressed the interobserver variability in
assessing the separate clinical features from which this
and similar scales were derived (headache, neck stiffness, hemiparesis, level of consciousness). Grading the
severity of headache caused most variability. The consistency was almost as poor for grading the level of
consciousness, which might be expected in view of the
vague terms in which this feature is described in the
Hunt and Hess scale (eg, "drowsiness" and "stupor"). 19
Moreover, a preliminary analysis of the data from 3521
patients entered into the International Study on the
Timing of Aneurysm Surgery showed that, in the presence of a normal level of consciousness, headache or
neck stiffness did not relate to outcome.20 This evidence
prompted an ad hoc committee of the WFNS to propose
a more reliable and valid grading system in 1988. This
WFNS Scale is based on the Glasgow Coma Scale for
the assessment of consciousness level21 in combination
with the presence or absence of focal signs.20 The
interobserver agreement in the use of the Glasgow
Coma Scale has been proved good, as has the agreement
between nurses and physicians.22 It is sobering that in
the subsequent 4 years the rational approach embodied
by the WFNS scale has not perceptibly replaced the
traditional scale.
The description of specific complications is at least as
important as grading the initial condition. Rebleeding,
delayed ischemia, and hydrocephalus each require completely different therapeutic measures. As we pointed
out in "Methods," there are many pitfalls in distinguishing between these events, and serial CT scanning is
mandatory. These difficulties are compounded because
some interventions aimed at preventing or abating one
specific complication can induce another. For example,
prevention of rebleeding with antifibrinolytic drugs increases the risk of ischemic complications,5 and similar
dangers may exist with early surgery.23 Similarly, the
benefits of ventricular drainage aimed at relieving acute
van Gijn et al Definitions in Subarachnoid Hemorrhage
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hydrocephalus are offset by an excessive risk of rebleeding.7-24 It is therefore a cause for concern that these
three events were adequately defined in less than a third
of all instances without any sign of improvement over
the years. Of course, the rating of published definitions
as "adequate" or "inadequate" is slightly subjective. If
anything, we have been too liberal in the classification of
articles. For instance, we accepted relevant clinical
features in combination with CT scanning as sufficient
for the diagnosis of rebleeding or delayed ischemia even
if authors did not specify whether or not a baseline CT
scan was available for comparison. Moreover, no definition at all was given in almost half of all instances in
which events were reported, a fact that cannot be
misinterpreted. The lack of precise criteria was slightly
worse for rebleeding than for hydrocephalus or delayed
ischemia, but these differences were relatively minor.
A much more striking contrast is that between neurosurgical and neurological journals. The four neurosurgical journals reported 209 of the 283 events (74%) with
adequate definitions in only 20% of instances, whereas
the remaining quarter of events, recorded in journals
with a predominantly neurological readership, were
based on adequate criteria in 65%. Apparently reviewers and editors of neurosurgical journals are much more
prepared than their neurological colleagues to accept
such diagnoses on trust and to forego explicit
definitions.
On a more optimistic note, we found increasing use of
a reliable scale for overall outcome: 54% in the period
of 1985 through 1988 versus 70% in 1989 through 1992
(Table 2). In most of these cases the Glasgow Outcome
Scale was used." This is a five-point scale, initially
developed for the follow-up of patients with head injury
and aimed primarily at categorizing the degree of
independence in daily life. Such a global level of measurement can be applied to different categories of
disease and reflects the patient's quality of life far better
than disease-specific impairment scales.10 A very similar
scale is the modified Rankin scale (alternatively called
the Oxford Handicap Scale).13 Both scales have proved
reliable in interobserver studies.12-14
Our survey has uncovered frequent shortcomings in
the precision of reporting on patients with subarachnoid
hemorrhage. Leaders of research groups as well as
reviewers and editors of scientific journals should see
that future articles contain precise definitions of states
and events. This will help to ensure that the conclusions
are based on observation rather than opinion.
Acknowledgments
The authors are indebted to GJ.E. Rinkel, MD, and to LJ.
Kappelle, MD, for their valuable comments on earlier drafts of
this article.
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J van Gijn, J E Bromberg, K W Lindsay, D Hasan and M Vermeulen
Stroke. 1994;25:1623-1627
doi: 10.1161/01.STR.25.8.1623
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