Assessing Consciousness in Critically III Patients

S. Laureys, S. Majerus, and G. Moonen

I Introduction
An accurate and reliable evaluation of the state of consciousness in intensive care
unit (lCU) patients is of primordial importance for their appropriate management.
Altered states of consciousness are commonly encountered in rcus. Even excluding
neurological and neurosurgical rcus, altered states of consciousness are the pri-
mary reason for adult rcu admission in 3 to 7% of cases [1]. Additionally, second-
ary alterations of consciousness due to encephalopathy, seizures, and cerebrovascu-
lar accidents are known to occur in one-eighth of un selected patients admitted to a
medical lCU, and even more frequently in those with sepsis [2, 3]. Up to one-fifth
of patients develop an acute confusional state in the lCU [4].
Consciousness is a multifaceted concept that can be divided into two major com-
ponents: the level of consciousness (i.e., arousal, wakefulness, or vigilance) and the
content of consciousness (i.e., awareness of the environment and of the self) [5]
(Fig. 1). Arousal is maintained by a diffuse system of upper brainstem and thalamic
neurons (called the reticular activating system) and its connections to the cerebral
hemispheres. Therefore, depression of either brain stem or global hemispherical
function may cause reduced wakefulness. Brainstem reflexes are a key to the assess-
ment of the functional integrity of the brainstem's reticular activating system.
Awareness is thought to be dependent upon the functional integrity of the cerebral
cortex and its reciprocal subcortical connections; each of its many aspects resides
to some extent in anatomically defined regions of the brain [6].
Unfortunately, at present, consciousness cannot be measured objectively by any
machine; its estimation requires the interpretation of several clinical signs. Many
scoring systems have been developed for the quantification and standardization of
the assessment of consciousness. The present chapter will discuss the possibilities
and pitfalls of a behavioral assessment of consciousness in patients and review the
most frequently used 'consciousness scales' in the lCU.

I Clinical Evaluation of Consciousness

Both arousal and awareness are not on-off phenomena but are part of a large conti-
nuum. At the patient's bedside, arousal is assessed by the presence of spontaneous
or stimulation-induced eye opening. It ranges from alert waking (spontaneous eye
opening), sleep (eye opening following moderate external stimuli), through stupor
(eye opening following vigorous external stimuli) and coma (no eye opening).
Awareness refers to the collective thoughts and feelings of an individual. Clinically,
716 S. Laureys et al.

Movements
Appropriate
Localized
Abduction

III
III Language -'" Reflexes
Q/
c:
III
Fronto·orbicular
j Vertical oculovestibular
o
·v pupillary light
~ --------, Horizontal oculovestibular
o
u
Oculocardiac

Fig. 1. A simplified scheme of consciousness and of its two major components: arousal and awareness. Note:
the gray area represents the reticular activating system encompassing the brainstem and thalamus; the arrow
near the brainstem denotes the progressive disappearance of brainstem reflexes during rostral-caudal deteriora-
tion

we are limited to the appraisal of the patient's potential to perceive the external
world and to voluntary interact with it (i.e., perceptual awareness). In practice, this
is evaluated by careful and repeated examination of the capacity to formulate re-
producible, voluntary, purposeful and sustained behavioral responses to auditory,
tactile, visual or noxious stimuli. By asking the patient to say or write their name
we can assess awareness of self (self-consciousness); another - much more difficult
- possibility is to evaluate patient self recognition in a mirror [7]. The patient
needs to be aroused in order to perform the cognitive processes required for aware-
ness. Hence, patients in a coma are unaware because they cannot be aroused. How-
ever, as illustrated by patients in a vegetative state, arousal is only a necessary, and
not a sufficient, condition for awareness. Indeed, patients in a vegetative state are
aroused (as shown by preserved spontaneous eye opening and sleep-wake cycles)
but show no sign of awareness.
Consciousness is intimately related to higher functions such as perception, atten-
tion, working memory, declarative memory, cognition, mental imagery, motivation,
emotion, and language. Visual, auditory or somatosensory deficits in our patients
may seriously reduce their perceptual awareness. Attention forms a component of
perception in that it accounts for the selection and directed concentration on pro-
cessing certain information with the exclusion of other competing stimuli or data.
Sensory signals reach the level of consciousness only if they become the target of
selective attention, and only these find their way to declarative memory [8]. Lesions
of the parietal lobe, either of the cortex or of subjacent white matter, may result in
hemi-neglect, hemi-inattention and a tendency not to use the contralateral hand
and arm. Consciousness is bound to the information-containing elements of the ex-
plicit memory trace and is recovered along with the memory. Working memory is
the short-term retention of a limited number of items held in consciousness for im-
mediate use. Conscious recollection is constantly occurring and provides us with a
 Assessing Consciousness in Critically III Patients 717

sense of familiarity and continuity. In contrast, patients without current explicit

memory are "isolated in a single moment of being ... without a past or future,
stuck in a constantly changing, meaningless moment" [9]. Motivational and emo-
tional drives help to determine behavior, once the stimulus has been received, and
to assess its significance relevant to competing internal and external factors. Lan-
guage is a highly developed cognitive activity allowing for internal conversation
and conceptual formulation. Thinking, like consciousness, is difficult to define sat-
isfactorily. The act of thinking depends on all the components of consciousness
previously mentioned and also includes an awareness of one's own cognitive activ-
ity. Confusion is a disorder of the content of consciousness. Any impairment of
cognitive function may cause confusion, i.e., impaired perception, attention, under-
standing, action, or coherence of thought. It may also be the presenting sign in iso-
lated focal dysfunction such as aphasia or visuospatial agnosia. Delirium is synon-
ymous with an acute confusional state accompanied by fluctuating agitation and in-
creased arousal [10].

I Consciousness Scales

Glasgow Coma Scale

Teasdale and Jennett published the Glasgow Coma Scale (GCS) in the Lancet in
1974 as an aid in the clinical assessment of post-traumatic unconsciousness [11]. It
was devised as a formal scheme to overcome the ambiguities that arose when infor-
mation about comatose patients was presented and groups of patients compared.
The GCS has three components: the eye (E), verbal (V), and motor (M) response to
external stimuli. The best or highest responses are recorded. The scale consisted of
14 points, but was later adapted to 15, with the division of the motor category 'flex-
ion to pain' into two further categories (Fig. 2). So far, more than 1500 publications
have appeared to its use (MEDLINE search performed in December 2001, limited to
title and abstract word). It is a component of the Acute Physiology and Chronic
Health Evaluation (APACHE) II score, the (Revised) Trauma Score, the Trauma and
Injury Severity Score (TRISS) and the Circulation, Respiration, Abdomen, Motor,
Speech (CRAMS) Scale, demonstrating the widespread adoption of the scale.
The presence of spontaneous eye opening "indicates that the arousal mecha-
nisms of the brain stem are active" [11]. As stated above, preserved arousal does
not imply the presence of awareness. Patients in a vegetative state have awakened
from their coma but remain completely unaware of their environment and self.
Most comatose patients who survive will eventually open their eyes, regardless of
the severity of their cerebral injuries [12]. Indeed, less than 4% of head-injured pa-
tients never open their eyes before they die [13]. The eye opening in response to
speech tests the reaction "to any verbal approach, whether spoken or shouted, not
necessarily the command to open the eyes" [11]. Again, this response is observed
in vegetative patients who can be awakened by non-specific auditory stimulation.
In these patients, it is recommended to differentiate between a reproducible re-
sponse to command and to non-sense speech. Eye opening in response to pain
should be tested by a stimulus in the limbs, because the grimacing associated with
supraorbital or jaw-angle pressure may cause eye closure.
After arousing the patient, the presence of verbal responses indicates the restora-
tion of a high degree of interaction with the environment (i.e., awareness). An ori-
718 S. Laureys et al.

C. Not assessable
8
----------------------------------------------------------------------
c:n
c:
c:
4. Spontaneous
9
8
QJ
~
o 3. To speech
QJ
>-

8
QJ
Pain
2. To pain
w ~.

1. None

T. Not assessable
8 ~
Pain

QJ
\1\
c:
o
~
\1\ 4. Confused speech
....
QJ

Q
iO
...
..c
QJ
3. Inappropriate words

>
>
I
2. Incomprehensible sounds Ql Groan]

1. None

6. Obeys simple commands

8 1----------J
QJ
S. Localizes pain
\1\
C
o
~ 4. Withdraws (normal flexion)
\1\
....
QJ
....
....oo 3. Stereo typed flexion

E
I
2. Stereotyped extension
:E

1. None
 Assessing Consciousness in Critically III Patients 719

ented conversation implies awareness of the self (e.g., the patient can answer the
question: "What is your name?") and environment (e.g., the patient correctly an-
swers the questions: "Where are we?" and "What year/month is it?"). Confused
speech is recorded when the patient is capable of producing language, for instance
phrases and sentences, but is unable to answer the questions about orientation.
When the patient presents intelligible articulation but exclaims only isolated words
in a random way (often swear words, obtained by physical stimulation rather than
by a verbal approach) this is scored as 'inappropriate speech'. Incomprehensible
sounds refer to moaning and groaning without any recognizable words. This rudi-
mentary vocalization does not necessitate awareness and is thought to depend on
subcortical functioning as it can be observed in anencephalic children and vegeta-
tive patients.
The motor response first assesses whether the patient obeys simple commands,
given in verbal, gestural, or written form. A non-specific sound stimulus may in-
duce a reflex contraction of the patient's fingers or alternatively such a reflex re-
sponse can result from the physical presence of the examiner's fingers against the
palm of the patient (i.e., grasping reflex). Before accepting that the patient is truly
obeying commands, it is advised to test that the patient will also release and
squeeze again to repeated commands. If there is no response a painful stimulus is
applied. First, pressure is applied to the fingernail bed with a pencil. If flexion is
observed stimulation is then applied to other sites (applying pressure to the su-
praorbital ridge, pinching the trapezium or rubbing the sternum) to differentiate
between localization (i.e., a stimulus at more than one site causes a limb to move
so as to attempt to remove it by crossing the midline), withdrawal flexion (i.e., a
rapid flexion of the elbow associated with abduction of the shoulder) or 'abnormal'
flexion (i.e., a slower stereotyped flexion of the elbow with adduction of the
shoulder that can be achieved when stimulated at other sites). Stereotyped flexion
responses are the most common of the motor reactions observed in severely brain-
injured patients; they are also the most enduring [14]. Extensor posturing is more
easily distinguished and is usually associated with adduction, internal rotation of
the shoulder, and pronation of the forearm. The term 'decerebrate rigidity' should
be avoided because it implies a specific physioanatomical correlation. Abnormal
flexion and extension motor responses often co-exist [15]. It is important to ap-
preciate that it is the best response that should be scored and that abduction move-
ments reflect some residual awareness while stereotyped postures do not. The pres-
ence of asymmetrical responses are significant in indicating that there is a focal as
well as a diffuse disturbance of brain function, and this should be noted separately.
The side showing the impaired response locates the site of the focal brain damage
and the level of the best response of the better side reflects the extent of general
depression in brain function. The scale of responses to pain is applicable to the
movements of the arms. The movements of the legs are not only more limited in
range, but may take place on the basis of a spinal withdrawal reflex (e.g., in brain
death, a spinal reflex may still cause the legs to flex briskly in response to pain ap-
plied locally [16]).
It is very tempting to sum the three components of the GCS (E-V-M) into a total
score, ranging from 3 to 15. However, given the increased use of intubation, ventila-
tion, and sedation of patients with impaired consciousness before arrival at special-

Fig. 2. Glasgow Coma Scale (GCS). (Adapted from [11] with permission)
720 S. Laureys et al.

ists units, and even before arrival at hospital [17], patients might wrongly be
scored as GCS 3/15 rather than being more appropriately reported as impossible to
assess or score. In a recent study of 1005 patients with head injuries in European
centers, assessment of each of the three components of the GCS was possible only
in 61% of patients before hospital, in 77% on arrival at the first hospital, in 56%
on arrival in the neurosurgical unit, and in 49% 'post-resuscitation' [18]. The inap-
propriate scoring of absent responsiveness as 3, has led to some data indicating
that the mortality of patients with a score of 3 is apparently lower than that of
those with a score of 4. Summing GCS components has also been criticized on a
purely mathematical basis. Because there are only four units assigned to the eye re-
sponses, versus five to the verbal and six to the motor responses, the scale incorpo-
rates a numerical skew toward motor response. This problem can be tackled by
weighting individual scores for eye, verbal and motor responses in such a way that
each has a minimum contribution of one and a maximum of five [19]. This
approach, however, is too complicated for practical use. Moreover, this effort to
provide mathematical parity for the three components has abutted against studies
that have stressed the particular importance of the motor portion of the GCS. In-
deed, the motor score is more important than either of the other two components
in predicting the magnitude of neurological injury for patients with severe head in-
jury [20], while verbal and eye scores are more pertinent in patients who are not,
in fact, comatose. It is a widespread but erroneous usage to define mild brain in-
jury as a summed score ranging from 13-15, moderate injury, 9-12, and severe in-
jury, 3-8. Indeed, in the persistent vegetative state, patients open their eyes sponta-
neously (E4) and may make moaning sounds (V2) or flex abnormally to pain
(M3), while their condition hardly reflects 'moderate' brain injury. For clinical pur-
poses, summation of the GCS is too imprecise [21]. To achieve a total score of 6 to
12 there are more than 10 simple combinations of variables, each with very differ-
ent clinical profiles. In Glasgow, patients are always described by the three separate
responses and never by the total [22]. It is, therefore, good practice to communi-
cate the GCS in terms such as 'patient scored E2, VT, M4' and only sum its three
components for research applications.

Glasgow liege Scale

One of the most frequently expressed reservations regarding the GCS has been its
failure to incorporate brainstem reflexes. A number of investigators have disagreed
with Teasdale and Jennett that spontaneous eye opening is sufficiently indicative of
brain stem arousal systems activity and have proposed coma scales that include
brain stem responses [23]. Many coma scales that include brain stem indicators have
been proposed (e.g., the Comprehensive Level of Consciousness Scale [24], the Clin-
ical Neurologic Assessment Tool [25], the Bouzarth Coma Scale [26], the Maryland
Coma Scale [27]) but none have known a widespread use. These scales generally
have been more complex than the GCS.
A simpler system is the Glasgow Liege Scale (Fig. 3). It was developed in 1982 in
Liege and combines the Glasgow Scale with a quantified analysis of five brain stem
reflexes: fronto-orbicular, vertical oculocephalic, pupillary, horizontal oculocephalic,
and oculocardiac [28]. The fronto-orbicular reflex is considered present when per-
cussion of the glabella produces contraction of the orbicularis oculi muscle. The
oculocephalic reflexes (doll's head) are scored as present when deviation of at least
one eye can be induced by repeated flexion and extension (vertical) or horizontal
 Assessing Consciousness in Critically III Patients 721

R - brain stem reflexes

~
5. Fronto - orbicular
g --~ g-
"""
4. Vertical oculovestibular
(~(~
3. Pupillary light 00 - -..· 00
\11
Light

2. Horizontal oculovestibular

1. Oculocardiac

o. None Braindead

Fig. 3. GlasgOW-liege Scale (GLS). Note: when oculocephalic reflexes (doll's eyes) cannot be tested or are ab-
sent, the (vertical and horizontal) oculovestibular reflexes (ice water testing) should be evaluated. (Adapted from
[28] with permission)

neck movement (horizontal). If the reflexes are absent or cannot be tested (e.g., im-
mobilized cervical spine), an attempt is made to elicit ocular motion by external
auditory canal irrigation using iced water (i.e., oculovestibular reflex testing). With
cold-water irrigation of the head at 30 elevation from the horizontal, the eyes de-
0

viate tonically toward the ear irrigated (horizontal). When cold water is injected si-
multaneously into both ears canals, the eyes deviate tonically downwards; the re-
verse occurs with bilateral irrigation of warm water (vertical). The oculocardiac re-
flex is scored as present when pressure on the eyeball causes the heart rate to slow
down. As for the GCS, the best response determines the brainstem reflex score (R).
The selected reflexes disappear in descending order during rostral-caudal deteriora-
tion. The disappearance of the last reflex, the occulo-cardiac, coincides with brain
death.

Reaction Level Scale

The Reaction Level Scale (RLS85) was developed in Sweden in 1985 as an eight-
grade scale for the assessment of patients in the ICU [29]. Its numeric values are
not necessarily separated by steps of equal value. The information content of the
GCS and the RLS85 is similar, though their construction differs (Table 1). By com-
bining eye, verbal, and motor responses into a single-line ordinal scale it has a bet-
722 S. Laureys et al.

Table 1. Reaction Level Scale (RLS85). (From [29] with permission)

Clinical descriptor Responsiveness Score

Alert No delay in response 1

Drowsy or confused Responsive to light stimulation 2
Very drowsy or confused Responsive to strong stimulation 3
Unconscious Localizes but does not ward off pain 4
Unconscious Withdrawing movements on pain st.imulation 5
Unconscious Stereotype flexion movements on pain stimulation 6
Unconscious Stereotype extension movements on pain stimulation 7
Unconscious No response on pain stimulation 8

ter discriminatory ability, greater accuracy, and higher inter-observer agreement

than the GCS [23] and can be applied to patients who are intubated or whose eyes
are swollen shut. There is a high correlation between the two scales, indicating a
similar ranking order of neurologic defect severity. The Swedish Societies of Inten-
sive Care, Anesthesiology and Neurosurgery have recommended replacement of the
GCS with the RLS85 in that country's hospitals.

Innsbruck Coma Scale

The Innsbruck Coma Scale (ICS), also developed for assessment of victims of trau-
ma, was published in 1991 [30]. The total score is analogous to that of the GCS in
having a number of separate assessments that are scored separately but can be
added for an aggregate score (Table 2). Its eight items allow for a maximal score of
23. It is similar to the GCS, but excludes verbal response and contains pupillary
size and reaction, movement and position of the eyes, and oral automatisms. An
anomaly is that the score rates dilated fixed pupils of greater severity (lower score)
than midposition nonreactive pupils [31]. Thus, a patient with brain death (where
midposition pupils are generally the rule) would achieve a better score than one
who is not brain dead.

Edinburgh-2 Coma Scale

The Edinburgh-2 Coma Scale (E2CS) is a single-line scoring system [32]. The best
response is the one that is used in tabulating the score which is inversely related to
consciousness (Table 3). The disadvantage of this score is that it cannot be applied
to patients who are unable to give an oral response.

I Pitfalls Encountered in ICU Patients

Untrained or inexperienced observers produce unreliable scoring of consciousness
[33]. In one study, one in five ICU workers was mistaken when asked to make judg-
ments as to whether patients were 'conscious' or 'unconscious', [34]. Consciousness
needs considerable skill to evaluate and the observer should be aware of the pitfalls
encountered in ICU settings. It is also well known that the preceding score of the
 Assessing Consciousness in Critically III Patients 723

Table 2. Innsbruck Coma Scale (lCs). (From [30] with permission)

Item Factor Score

Eye opening Spontaneous 3

To acoustic stimuli 2
To painful stimuli 1
None 0
Reaction to acoustic stimuli Turning towards stimuli 3
Better-than-extension movements 2
Extension movements 1
None 0
Reaction to pain Defensive movements 3
Better-than-extension movements 2
Extension movements 1
None 0
Body posture Normal 3
Better-than-extension movements 2
Extension movements 1
None 0
Pupil size Normal 3
Narrow
Dilated ,
2

Completely dilated 0
Pupil response to light Sufficient 3
Reduced 2
Minimum 1
None 0
Position and movements of the eyeballs Fixing of the eyes 3
Sway of eyeballs 2
Divergent 1
Divergent fixed 0
Oral automatisms Spontaneous 2
To external stimuli 1
None 0

Note: Maximum total score is 23.

Table 3. Edinburgh-2 Coma Scale (E2Cs). (From [32] with permission)

Stimulation (maximal) Response (best) Score

Two sets of questions: Answers correctly to both o

1. Month? Answers correctly to either 1
2. Age? Incorrect for both 2
Two sets of commands: Obeys correctly to both 3
1. Close and open hands Obeys correctly to either 4
2. Close and open eyes Neither correct 5
Strong pain Localizing 6
Flexion 7
Extension 8
None 9
724 S. Laureys et al.

patient frequently influences the examiner when rating the patient's present state of
consciousness. Therefore, scoring should be done in a 'blinded' manner.
Obviously, problems arise when the eyes are swollen shut, either following peri-
orbital edema, direct ocular trauma, facial injury, craniotomy, cranial nerve VII in-
jury, or neuromuscular blockade. In these circumstances, enforced closure of the
patient's eyes should be recorded on his chart by marking 'c' (=eyes closed) [35].
In deep coma, flaccid eye muscles will show no response to stimulation yet the eyes
remain open if the lids are drawn back. Such opening should be recorded as unre-
sponsive. It is important to stress that although opening of the eyes implies arousal,
it does not necessarily mean that the patient is aware.
Continued speechlessness may be due to causes other than unawareness (e.g.,
neuromuscular blockade, intubation via the oropharynx or through a tracheostomy,
fractured mandible or maxillae, edematous tongue, deafness, foreign language, dys-
phasia, confusion or delirium). The evaluation of verbal responses is also biased
when patients are sedated, alcohol or drug intoxicated, or too young to speak. As
discussed above, the use of early intubation and administration of neuromuscular
paralyzing agents in the pre-hospital phase of care has rendered verbal and motor
responses unmeasurable in these cases. Early treatment was uncommon when the
GCS was first described, but has since gained greater acceptance. The RLS85, which
does not include a verbal response criterion, is the most notable alternative for
scoring intubated patients. Several other techniques have been proposed to desig-
nate the verbal score in intubated patients. Some have proposed to assign an arbi-
trary score of one point to all intubated patients [36]. Others have created a pseu-
do-score by averaging the testable scores and adding this calculated score to the
sum in lieu of the verbal score [37]. Linear regression predication of the verbal
scores based on the other two scores has also been utilized [38].
The best alternative is to report separate responses, using a non-numerical des-
ignation of 'T' (= intubated) when the verbal score cannot be assessed and not to
sum the responses [17]. The patient's verbal response may also be impaired as a re-
sult of a single focal lesion of the speech areas in the dominant hemisphere, that is,
aphasia. The assessment of such a patient's language ability requires a specialized
evaluation (i.e., written instructions and written replies in the case of motor dys-
phasia). The level of verbal response should still be indicated but an appropriate
note may be made that the impairment is considered to be due to dysphasia
('D'= dysphasia) [35]. Motor responses cannot be reliably monitored in cases of
spinal cord, plexus or peripheral nerve injury or in the presence of splint or immo-
bilization devices. As previously stated, one must take care not to interpret a grasp
reflex or postural adjustment as a response to command.
In most scoring systems, awareness is assessed as the level of obedience to com-
mands. This approach cannot be applied to cases where the patient is clinically or
pharmacologically paralyzed yet alert (e.g., locked-in syndrome, severe polyneuro-
pathy, or use of neuromuscular blocking agents) or those with psychogenic unre-
sponsiveness. It is important to stress that special effort should be made to identify
and exclude these rare causes of pseudo-coma. The GCS has also been critiqued for
lacking reliability in monitoring levels of consciousness in patients with moderate
brain injury [23]. More detailed scales are recommended for the assessment of
awareness in these patients [39, 40]. Finally, we remain with a theoretical limitation
to the certainty of our clinical assessment of consciousness, since we can only infer
the presence or absence of conscious experience in another person [41]. Finally, as
consciousness is a subjective first person experience, we remain with a theoretical
 Assessing Consciousness in Critically III Patients 725

limitation as to the certainty of our clinical assessment of consciousness (since the

clinician can only infer the presence or absence of conscious experience in another
person) [41].

I Conclusion

Despite its drawbacks, the GCS remains the most universally utilized consciousness
scale worldwide. The eye opening score (E) directly relates to the level of con-
sciousness (i.e., arousal) but does not test the content of consciousness (i.e., aware-
ness). In minor and moderate brain-injured patients, the verbal (V) and motor (M)
score covaries with the level of awareness of self and environment. The observation
of a verbal response (except for groaning and moaning) or of a localizing or abduc-
tion movement witnesses the presence of awareness. Stereotyped flexion or worse
denotes severe brain dysfunction. Appending the brainstem reflexes (R), such as in
the GLS, permits a better evaluation of the brains tern arousal systems. Finally, even
if the GCS is the most widely used and validated tool to evaluate the state of con-
sciousness, it also is the most frequently misused. One recent study showed that
51 % of patients were incorrectly assessed [42]. It is also important to stress that
for clinical use, patients should be characterized by the three separate scores (E, V,
M and R) and never by the total sum. If eye or verbal responses cannot be evalu-
ated, this should be indicated by marking a 'C' (eyes closed) or 'T' (intubated), re-
spectively. By virtue of its simplicity the GCS seems destined to be used in inten-
sive care and emergency medicine for some time.

Acknowledgements. This work was supported by grants from the Fonds National de
la Recherche Scientifique de Belgique (FNRS), the Special Funds for Scientific Re-
search of the University of Liege and by the Queen Elisabeth Medical Foundation.
SL and SM are respectively Postdoctoral Researcher and Research Fellow at the
FNRS.

References
1. Groeger JS, Strosberg MA, Halpern NA, et al (1992) Descriptive analysis of critical care
units in the United States. Crit Care Med 20:846-863
2. Bleck TP, Smith MC, Pierre-Louis SJ, et al (1993) Neurologic complications of critical med-
ical illnesses. Crit Care Med 21 :98-1 03
3. Papadopoulos MC, Davies DC, Moss RF, Tighe D, Bennett ED (2000) Pathophysiology of
septic encephalopathy: a review. Crit Care Med 28:3019-3024
4. Dubois MJ, Bergeron N, Dumont M, Dial S, Skrobik Y (2001) Delirium in an intensive care
unit: a study of risk factors. Intensive Care Med 27:1297-1304
5. Plum F, Posner JB (1983) The Diagnosis of Stupor and Coma. FA Davis, Philadelphia
6. Llinas R, Ribary U, Contreras D, Pedro arena C (1998) The neuronal basis for conscious-
ness. Philos Trans R Soc Lond B Bioi Sci 353:1841-1849
7. Gallup GG Jr (1997) On the rise and fall of self-conception in primates. Ann N Y Acad Sci
818:72-82
8. Moscovitch M (1995) Models of consciousness and memory. In: Gazzaniga MS (ed) The
Cognitive Neurosciences. Bradford Book MIT Press, Cambridge, pp:1341-1356
9. Sacks 0 (1985) The Man who Mistook his Wife for a Hat. Summit Books, New York
10. American Psychiatric Association. Task Force on DSM-IV (2000) Diagnostic and statistical
manual of mental disorders: DSM-IV-TR. American Psychiatric Association, Washington,
DC
726 S. Laureys et al.

II. Teasdale G, Jennett B (1974) Assessment of coma and impaired consciousness. A practical
scale. Lancet 2:81-84
12. Jennett B (1972) Prognosis after severe head injury. Clin Neurosurg 19:200-207
13. Bricolo A, Turazzi S, Feriotti G (1980) Prolonged posttraumatic unconsciousness: therapeu-
tic assets and liabilities. J Neurosurg 52:625-634
14. Born JD (1988) The Glasgow-Liege Scale. Prognostic value and evaluation of motor re-
sponse and brain stem reflexes after severe head injury. Acta Neurochir 95:49-52
IS. Bricolo A, Turazzi S, Alexandre A, Rizzuto N (1977) Decerebrate rigidity in acute head in-
jury. J Neurosurg 47:680-689
16. Ivan LP (1973) Spinal reflexes in cerebral death. Neurology 23:650-652
17. Marion DW, Carlier PM (1994) Problems with initial Glasgow Coma Scale assessment
caused by prehospital treatment of patients with head injuries: results of a national survey.
J Trauma 36:89-95
18. Murray LS, Teasdale GM, Murray GD, et al (1993) Does prediction of outcome alter patient
management? Lancet 341: 1487 -1491
19. Bhatty GB, Kapoor N (1993) The Glasgow Coma Scale: a mathematical critique. Acta Neu-
rochir 120:132-135
20. Jagger J, Jane JA, Rimel R (1983) The Glasgow coma scale: to sum or not to sum? Lancet
2:97
21. Bozza Marrubini M (1984) Classifications of coma. Intensive Care Med 10:217-226
22. Teasdale G, Jennett B, Murray L, Murray G (1983) Glasgow coma scale: to sum or not to
sum. Lancet 2:678
23. Segatore M, Way C (1992) The Glasgow Coma Scale: time for change. Heart Lung 21:548-
557
24. Stanczak DE, White JG 3rd, Gouview WD, et al (1984) Assessment of level of consciousness
following severe neurological insult. A comparison of the psychometric qualities of the
Glasgow Coma Scale and the Comprehensive Level of Consciousness Scale. J Neurosurg
60:955-960
25. Crosby L, Parsons LC (1989) Clinical neurologic assessment tool: development and testing
of an instrument to index neurologic status. Heart Lung 18:121-129
26. Bouzarth WF (1968) Neurosurgical watch sheet for craniocerebral trauma. J Trauma 8:29-
31.
27. Salcman M, Schepp RS, Ducker TB (1981) Calculated recovery rates in severe head trauma.
Neurosurgery 8:301-308
28. Born JD (1988) The Glasgow-Liege Scale (GLS). Act Neurochir (Wien) 91:1-11
29. Starmark JE, Stalhammar D, Holmgren E, Rosander B (1988) The Reaction Level Scale
(RLS85). Manual and guidelines. Acta Neurochir (Wien) 91:12-20
30. Benzer A, Mitterschiffthaler G, Marosi M, et al. (1991) Prediction of non-survival after
trauma: Innsbruck Coma Scale. Lancet 338:977-978
31. De'Clari F (1991) Innsbruck coma scale. Lancet 338:1537
32. Sugiura K, Muraoka K, Chishiki T, Baba M (1983) The Edinburgh-2 coma scale: a new
scale for assessing impaired consciousness. Neurosurgery 12:411-415
33. Rowley G, Fielding K (1991) Reliability and accuracy of the Glasgow Coma Scale with ex-
perienced and inexperienced users. Lancet 337:535-538
34. Teasdale G, Jennett B (1976) Assessment and prognosis of coma after head injury. Acta
Neurochir (Wien) 34:45-55
35. Teasdale G (1975) Acute impairment of brain function-I. Assessing 'conscious level'. Nurs
Times 71:914-917
36. Marshall LF, Becker DP, Bowers SA, et al. (1983) The National Traumatic Coma Data Bank.
Part 1: Design, purpose, goals, and results. J Neurosurg 59:276-284
37. Grahm TW, Williams FC Jr, Harrington T, Spetzler RF (1990) Civilian gunshot wounds to
the head: a prospective study. Neurosurgery 27:696-700
38. Meredith W, Rutledge R, Fakhry SM, Emery S, Kromhout-Schiro S (1998) The conundrum
of the Glasgow Coma Scale in intubated patients: a linear regression prediction of the Glas-
gow verbal score from the Glasgow eye and motor scores. J Trauma 44:839-844
39. Majerus S, Van der Linden M, Shiel A (2000) Wessex Head Injury Matrix and Glasgow/Glas-
gow-Liege Coma Scale: A validation and comparison study. Neuropsych Rehab 10:167-184
 Assessing Consciousness in Critically III Patients 727

40. Ansell BJ, Keenan JE (1989) The Western Neuro Sensory Stimulation Profile: A tool for as-
sessing slow to recover head injured patients. Arch Phys Med Rehabil 70:104-108
41. Bernat JL (1992) The boundaries of the persistent vegetative state. J Clin Ethics 3:176-180
42. Crossman J, Bankes M, Bhan A, Crockard HA (1998) The Glasgow Coma Score: reliable
evidence? Injury 29:435-437.