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REVIEW
published: 25 January 2019
doi: 10.3389/fneur.2019.00011
Frontiers in Neurology | www.frontiersin.org 1January 2019 | Volume 10 | Article 11
Edited by:
Stephen Honeybul,
Sir Charles Gairdner Hospital,
Australia
Reviewed by:
J. Marc Simard,
University of Maryland, Baltimore,
United States
Jacek Szczygielski,
Universitätsklinikum des Saarlandes,
Germany
Johannes Lemcke,
Unfallkrankenhaus Berlin, Germany
*Correspondence:
Gregory Hawryluk
gregory.hawryluk@hsc.utah.edu
Specialty section:
This article was submitted to
Neurotrauma,
a section of the journal
Frontiers in Neurology
Received: 05 September 2018
Accepted: 07 January 2019
Published: 25 January 2019
Citation:
Shah A, Almenawer S and Hawryluk G
(2019) Timing of Decompressive
Craniectomy for Ischemic Stroke and
Traumatic Brain Injury: A Review.
Front. Neurol. 10:11.
doi: 10.3389/fneur.2019.00011
Timing of Decompressive
Craniectomy for Ischemic Stroke and
Traumatic Brain Injury: A Review
Aatman Shah 1, Saleh Almenawer 2and Gregory Hawryluk 1
*
1Department of Neurosurgery, University of Utah School of Medicine, Salt Lake City, UT, United States, 2Division of
Neurosurgery, Hamilton Health Sciences and McMaster University, Hamilton, ON, Canada
While studies have demonstrated that decompressive craniectomy after stroke or
TBI improves mortality, there is much controversy regarding when decompressive
craniectomy is optimally performed. The goal of this paper is to synthesize the data
regarding timing of craniectomy for malignant stroke and traumatic brain injury (TBI)
based on studied time windows and clinical correlates of herniation. In stroke patients,
evidence supports that early decompression performed within 24 h or before clinical
signs of herniation may improve overall mortality and functional outcomes. In adult TBI
patients, published results demonstrate that early decompressive craniectomy within
24 h of injury may reduce mortality and improve functional outcomes when compared
to late decompressive craniectomy. In contrast to the stroke data, preliminary TBI
data have demonstrated that decompressive craniectomy after radiographic signs
of herniation may still lead to improved functional outcomes compared to medical
management. In pediatric TBI patients, there is also evidence for better functional
outcomes when treated with decompressive craniectomy, regardless of timing. More
high quality data are needed, particularly that which incorporates a broader set of
metrics into decision-making surrounding cranial decompression. In particular, advanced
neuromonitoring and imaging technologies may be useful adjuncts in determining the
optimal time for decompression in appropriate patients.
Keywords: TBI, stroke, decompressive hemicraniectomy, timing, herniation
INTRODUCTION
Decompressive craniectomy has been used to treat elevated intracranial pressure (ICP) resulting
from various etiologies, especially ischemic and traumatic brain injuries. Given the inflexible
confines of the skull, brain swelling from stroke or TBI can result in a compartment syndrome,
increasing intracranial pressure (ICP). This can reduce cerebral perfusion pressure (CPP), cerebral
blood flow (CBF), and oxygenation (1). If not acted upon, this can lead to brain ischemia, infarction,
herniation, and death. There are various management strategies to treat elevated ICPs which
include sedation, hyperventilation, hyperosmolar therapy, paralysis, hypothermia, barbiturates,
and cerebrospinal fluid drainage (2). Decompressive craniectomy is a treatment option generally
reserved for ICP elevation refractory to less invasive treatments (3).
Although decompressive craniectomy has been shown to effectively reduce ICP (4), there
remains much controversy regarding its effect on overall clinical outcome, especially following TBI
(5). Additionally, it is becoming clear that factors such as timing of decompressive craniectomy may
Shah et al. Timing of Decompressive Craniectomy
play a significant role in determining the therapeutic benefit of
this procedure. There are various studies providing insight into
the optimal timing of decompressive craniectomy for victims of
TBI and ischemic stroke and it is important for neurosurgeons
to be aware of this data. The goal of this paper is to synthesize
published findings regarding optimal timing for craniectomy for
both malignant stroke and TBI in relation to time from injury
and in relation to cerebral herniation.
TIMING OF CRANIECTOMY AFTER
ISCHEMIC STROKE
Decompressive Craniectomy for Stroke in
the Animal Model
Some animal data have suggested that early decompressive
craniectomy could yield better functional outcomes than
late decompression or non-operative management. In two
animal studies with standardized experimental conditions, rats
undergoing decompressive craniectomy after MCA infarction
had a significantly better outcome and had a reduction in infarct
size when compared to the non-surgical groups (6,7). These
studies were based on the hypothesis that avoiding herniation
and mesencephalic ischemia would improve prognosis. Doerfler
et al. concluded that the decompressive craniectomy groups
demonstrated better mortality and neurologic outcome when
compared to the non-surgical group (6). It was further concluded
that the animals treated with very early decompression (within
4 h) demonstrated significantly better neurologic outcomes and
smaller infarct size compared to animals treated with later
decompression. Forsting et al. also found that decompressive
craniectomy improved outcomes, mortality, and infarct size
when compared to the non-surgical group regardless of when the
decompression occurred (7).
Decompressive Craniectomy Within 48 h of
Ischemic Stroke
Decompressive craniectomy following acute ischemic stroke has
been studied in three relatively recent human randomized
controlled trials. These studies analyzed the effects of
decompressive surgery on mortality and functional outcome
after malignant hemispheric stroke. The subsequent pooling
and meta-analysis of these studies has generated very important
insights as will be described.
DECIMAL (Decompressive Craniectomy in Malignant
Middle Cerebral Artery Infarcts) was published in 2007. It
assigned 38 patients to undergo surgery or medical management
within 30 h of their initial stroke (8) (see Table 1). When
compared to the medical therapy cohort, the cohort that
underwent decompressive craniectomy demonstrated a
mortality rate that was more than halved, and a 50% increase in
the proportion of patients with only moderate disability.
DESTINY (Decompressive Surgery for the Treatment of
Malignant Infarction of the Middle Cerebral Artery) was also
published in 2007. It enrolled 32 patients within 36 h of stroke (9).
This randomized study demonstrated that craniectomy reduces
mortality in large hemispheric stroke. Like DECIMAL, this study
demonstrated a reduction in death rates in the surgical cohort,
but also like DECIMAL the sample size of the DESTINY trial was
not sufficient to draw conclusions regarding functional outcome.
Because the above studies were underpowered to
assess differences in functional outcomes, the HAMLET
(Hemicraniectomy After MCA Infarction With Life Threatening
Edema Trial) trial was initiated. This third RCT was published in
2009 and was crucial in adding to the body of literature regarding
decompressive surgery following acute ischemic stroke (10).
HAMLET enrolled 64 patients up to 96 h after stroke. This RCT
demonstrated that when decompressive craniectomy is delayed
up to 96 h, there was no improvement in functional outcomes in
survivors. The percentage of patients with a mRS score less than
or equal to three at 1 year follow up were comparable between
the decompressive craniectomy and control group (25% in both
groups). It should be noted that three patients in the surgical
group and three patients in the medical group had a fixed and
dilated pupil on enrollment which means that roughly 20% of
the study population demonstrated signs of herniation prior to
treatment. Because 20% of this study population had already
demonstrated signs of herniation, it can be argued that delayed
craniectomy may be too late to impart any functional benefit.
A meta-analysis of the three studies was performed by Vahedi
et al. on the patients treated with surgery within 48 h in the
DECIMAL and DESTINY trials as well as the first 23 patients
of the HAMLET trial (11). In this meta-analysis of 93 patients
crossover was minimal: there was only one crossover from non-
operative treatment to decompressive surgery included in this
analysis from the DESTINY trial. The results demonstrated
increased favorable functional outcome compared to the medical
cohort (11). In this paper, 43% of the decompressive craniectomy
group had a modified Rankin scale (mRS) score of 0–3 compared
to 21% in the control group. It should be noted that from the
human studies presented thus far, there have been no direct
comparisons between outcomes of early vs. late decompressive
craniectomy.
The findings from the meta-analysis performed by Vahedi
et al. was further corroborated by the findings of Vibbert et al.
This study contained 64 patients with acute ischemic stroke in
the MCA territory who presented within 96 h of symptom onset.
The patients were randomized to receive medical management or
surgical intervention (3). The primary outcome was the modified
Rankin scale (mRS) at 12 months which was stratified as good
outcome (0–3) and severe disability or death (4–6). Twenty-
four out of 32 patients in each arm had a mRS score >3 at 12
months, and rates of severe disability were also similar between
groups. The risk of death was significantly reduced in the surgical
group (absolute risk reduction of 38%; P=0.002). The authors
performed subgroup analyses of patients who underwent surgery
in <48 h and patients who underwent surgery after 48 h. For
patients who underwent surgery within 48 h of stroke, the risk
of death and an mRS score >4 were reduced (respectively: ARR,
59%; 95% CI, 33–84; ARR 30%; 95% CI, 1–59) (3).
Vibbert et al. then performed an updated meta-analysis with
their cohort of patients and patients from the aforementioned
DECIMAL, DESTINY, and HAMLET trials who underwent
decompressive surgery within 48 h (3). Corroborating their prior
Frontiers in Neurology | www.frontiersin.org 2January 2019 | Volume 10 | Article 11
Shah et al. Timing of Decompressive Craniectomy
TABLE 1 | Decompressive craniectomy for stroke studies.
Author Study
design
Patients Selection
criteria
Treatment Total no
of
patients
Time
to DC
Mortality
n(%)
Functional
outcome
at 6 months
Functional
outcome
at 12 months
Conclusions
Stroke Vahedi et al.
(8)
Randomized
controlled trial
Adult patients
with MCA
infarction
Patient age 18–55 years,
within 24 h of a malignant
MCA infarction, NIHSS ≥
16,; >50% of the MCA
territory involved on CT; DWI
infarct volume >145 cm3
DC 20 Avg 20.5 ±8.3 h
(range, 7–43 h)
5 (25) mRS score ≤3:
25%
mRS score ≤3:
50%
When compared to medical
management, the DC group
demonstrated an increase in
the number of patients with
moderate disability by more
than half and demonstrated
a reduction in the mortality
rate by more than half.
Medical
management
18 NA 14 (78) mRS score ≤3:
5.6%
mRS score ≤3:
22.2%
Juttler et al.
(9)
Randomized
controlled trial
Adult patients
with MCA
infarction
Patient age 18–60 years, at
least 2/3 of MCA territory
infarction with basal ganglia
involvement, NIHSS >18 for
non-dominant hemisphere,
NIHSS >16 for dominant
hemisphere, symptoms >
12 h but <36 h before
possible DC
DC 17 Within 36 h after
stroke
2 (11.8) mRS score ≤3:
47%
mRS score ≤3:
47%
DC reduces mortality in
large hemispheric stroke.
Functional outcomes at 6
and 12 months were
comparable between both
groups
Medical
management
15 NA 8 (53.3) mRS score ≤3:
27%
mRS score ≤3:
27%
Hofmeijer
et al. (10)
Randomized
controlled trial
Adult patients
with MCA
infarction
Patient age 18–60, at least
2/3 of MCA territory stroke
within 96 h of treatment,
NIHSS score >16 right
sided lesions or >21 left
sided lesions,
DC 32 Within 96 h after
stroke
7 (22) NA mRS score
≤3:25%
DC can improve fatality and
functional outcomes when
performed within 48 h;
however, when delayed up
to 96 h, there was no
improvement in functional
outcomes.
Medical
management
32 19(59) NA mRS score
≤3:25%
Vibbert et al.
(3)
Randomized
controlled trial
Adult patients
with MCA
infarction
Patient age 18–60, at least
2/3 of MCA territory stroke
within 96 h of treatment,
NIHSS score >16 right
sided lesions or >21 left
sided lesions,
DC 32 Within 96 h after
stroke
NA NA mRS score
≤3:25%
DC can improve fatality
(absolute risk reduction of
38%); however, there was
no improvement in
functional outcomes.
Medical
management
32 NA NA mRS score
≤3:25%
Schwab et al.
(12)
Prospective
cohort
Adult patients
with MCA
infarction
Patients younger than 70,
>50% MCA territory
infarction noted on CT
imaging
Early DC 31 Within 24 h after
stroke
5 (16) Avg Barthel Index
Score: 68.8
NA Earlier DC was associated
with lower mortality. There
was a trend toward better
functional outcomes, and
the patients spent less time
in the ICU
(Continued)
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Shah et al. Timing of Decompressive Craniectomy
TABLE 1 | Continued
Author Study
design
Patients Selection
criteria
Treatment Total no
of
patients
Time
to DC
Mortality
n(%)
Functional
outcome
at 6 months
Functional
outcome
at 12 months
Conclusions
Late DC 32 >24 h after stroke 11 (34.4) Avg Barthel Index
Score: 62.6
NA
Medical
management
55 43 (78) Avg Barthel Index
Score: 60
NA
Wang et al.
(13)
Retrospective
cohort
Adult patients
with MCA
infarction
Patients with 1st stroke
>90% MCA infarction
Early DC 11 Within 24 h after
stroke
3 (27) Mean Glasgow
Outcome Score:
2.5
NA While the mortality rates
were comparable between
groups, severe disability
may be reduced in early
treated patients
Late DC 10 >24 h after stroke 3 (30) Mean Glasgow
Outcome Score:
2.45
NA
Medical
management
41 9 (22) Mean Glasgow
Outcome Score:
2.73
NA
Cho et al. (14) Retrospective
cohort
Adult patients
with MCA
infarction
Patients with >50% MCA
infarction with NIHSS score
>20
Ultra-early DC 12 Within 6 h after
stroke
1 (8.3) Avg Barthel Index
Score: 70
NA DC before neurologic
compromise may reduce
the mortality rate and
increase the conscious
recovery rate
Delayed DC 30 >6 h after stroke 11 (36.7) Avg Barthel Index
Score: 52.9
NA
Medical
management
10 8 (80) Avg Barthel Index
Score: 55
NA
Mori et al. (15) Retrospective
cohort
Adult patients
with MCA
infarction
Patients <85 years of age
with patients with embolic
hemispheric infarction
volume >than 200 cm3
Early DC 21 DC before brain
herniation
4 (19.1) Avg Barthel Index
Score: 52.9
NA Early DC before the onset of
brain herniation should be
performed to improve
mortality and functional
recovery. DC after signs of
herniation may be too late
for functional benefit
Late DC 29 DC after brain
herniation
8 (27.6) Avg Barthel Index
Score: 26.9
NA
Medical
management
21 15 (71.4) Avg Barthel Index
Score: 28.3
NA
Elsawaf et al.
(16)
Prospective
cohort
Adult patients
with MCA
infarction
Patients with malignant
MCA infarction
DC based on
clinical status
27 DC with
deterioration of
consciousness
14 (52) Mean mRS Score:
4.7
NA Early prophylactic DC yields
better clinical and
radiographic outcomes than
DC based on clinical status
Early DC 19 DC within 6 h of
stroke
2 (10.5) Mean mRS Score:
3.5
NA
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Shah et al. Timing of Decompressive Craniectomy
findings, the data suggest a significant reduction in risk of
death (ARR, 49.9%; 95% CI, 33.9–65.9) and in the risk of
severe disability at 12-months (ARR, 41.9%; 95% CI, 25.2–58.6).
While not statistically significant, there was a notable trend
toward reduction in risk of poor outcome (12 month mRS score
>3—ARR, 16.3%; 95% CI, −0.1–33.1).
In summary, decompressive craniectomy within 96 h of
malignant MCA stroke did not reduce poor outcomes at 1
year; however, there seems to be a trend toward reduction
in death and moderate-to-severe disability (mRS score>4)
when surgery was performed within 48 h from the stroke. It
is possible that a significant portion of patients 96 h from
an acute ischemic stroke may already exhibit herniation,
and decompressive craniectomy at this time may be too
late to impart functional benefit. Unfortunately, analysis of
outcome in relation to herniation events was insufficiently
described in these studies, and it is not possible to determine
whether early surgery is beneficial due to avoiding herniation
or whether there is a benefit to early surgery independent
of herniation. The benefit of early surgery in the cohort
by Vibbert et al. was not as great in magnitude as in
HAMLET; however, this may have been due to a longer interval
between symptom onset and surgical treatment in HAMLET
(mean 31 h) than in DECIMAL (mean 16 h) and DESTINY
(mean 24 h).
Decompressive Craniectomy Within 24 h of
Ischemic Stroke
Other data have suggested that early decompressive craniectomy
within 24 h of stroke could yield even better functional outcomes.
Schwab et al. conducted a prospective observational trial where
the patient population was stratified by early craniectomy
(<24 h after symptom onset) and late craniectomy (>24 h), with
additional comparison to a natural history group (12). Patients
were included in the study if they had >50% MCA territory
infarction noted on CT imaging. The mean time between
symptoms and surgery was 21 h (range, 8–42 h) in the early
craniectomy group and 39 h (range, 6–112 h) in the late group.
This difference approached statistical significance (p=0.07).
Mortality was 16% (5/31) in the early group, 34.4% (11/32)
in the late group, and 78% (43/55) in the historical controls
(12). The late group demonstrated uncal herniation in 24 of
32 patients (75%) whereas only 4 of 31 patients (13%) in the
early group demonstrated uncal herniation. Length of stay in
the ICU was 7.4 days for the early group and 13.3 days in the
late treated group (p=0.05). Functional outcome measured by
the Barthel Index (BI) demonstrated a higher mean score for
the early group with an average score of 70 vs. 62.6 in the late
group. There was a trend toward better outcomes with early
craniectomy, however, the data were not statistically significant.
Overall, this study demonstrated that early craniectomy was
an efficacious approach for treating malignant MCA infarction
when the patients were treated before signs of herniation.
The mortality rate was lower, there was a trend to better
functional outcome, and the patients spent less time in
the ICU.
The data presented by Schwab et al. were further corroborated
by smaller series published by Wang et al. and Cho et al. In
a retrospective study of 21 patients, Wang et al. compared the
outcomes of early decompression (<24 h) to late decompression
(>24 h) (13). While the mortality rate was comparable, Wang
et al. demonstrated that severe disability may be reduced in early
treated patients. Cho et al. further corroborated this data, and
demonstrated the positive results in association with ultra-early
decompression defined as decompression within 6 h of symptom
presentation (14). The Cho et al. study reported only a cohort
of 52 patients and demonstrated that the acute mortality rate
was statistically lower for the ultra-early group (8.3%) compared
to the delayed decompression group (>6 h) and the no surgery
group (36.7 and 80%, respectively, all p-values <0.001). The
ultra-early group also had better prognosis for conscious recovery
(91.7%) compared to the delayed decompression group and the
no surgery group (55 and 0%, respectively). While more data
are needed, the published data give credence to the idea that
early craniectomy performed within 24 h yields better mortality
and functional outcomes. Moreover, this study suggests that the
benefit to early surgery may not merely stem from an avoidance
of herniation.
Decompressive Craniectomy for Ischemic
Stroke Based on Clinical Correlates of
Herniation
While the previous studies demonstrated benefit from early
decompression, a key limitation was insufficient delineation of
the role of herniation events in distinction to merely performing
early surgery. Indeed, there have been more recent studies that
indicate that the timing of craniectomy should be based on
clinical features rather than on a strict temporal scale given
the variations in when herniation events occur in the clinical
course of different patients. A retrospective study by Mori et al.
analyzed the outcomes of 71 patients with embolic hemispheric
infarctions (infarct volume >200 cm3) who were stratified into 3
groups: non-operative management, decompressive craniectomy
after brain herniation (late surgery group), and decompressive
craniectomy before brain herniation (early surgery group) (15).
This study utilized the Glasgow Coma Scale (GCS), changes in
mental status, and anisocoria as clinical indicators for herniation.
The mortality at 1 and 6 months in the non-operative group was
61.9 and 71.4%, respectively. The mortality at 1 and 6 months in
the late surgery group was 17.2 and 27.6%, respectively, (p=0.01)
and was even better in the early surgery group −4.8 and 19.1%,
respectively. The Glasgow Outcome Scale (GOS) and Barthel
Index (BI) were employed as functional outcome measures at 6
months. The GOS scores of the early surgery group were better
than those of the late surgery group (p=0.05). The average BI
score of the early surgery group (52.9 ±34.2) were improved
from those of the late surgery group (26.9 ±30.4) (p=0.05).
The late surgery group had a comparable BI score to the non-
operative group (28.3 ±42.2), which indicates that surgery after
signs of herniation may be too late to yield functional benefit.
Mori et al. thus concluded that an effort should be made to
perform early decompressive craniectomy before the onset of
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Shah et al. Timing of Decompressive Craniectomy
brain herniation in patients with malignant cerebral infarction.
Mori et al. also concluded that embolic stroke patients with >200
cm3volume of infarction and shift of the midline structures on
a follow-up CT 2 days after ictus are more likely to herniate and
would benefit from decompressive craniectomy.
Mori et al. advanced the field by conceptualizing outcome in
relation to clinical indicators of herniation. With this in mind,
Elsawaf et al. published a recent and important prospective
study comparing outcomes of early decompression (within 6 h
of presentation) and decompression based on clinical features
of deterioration. Forty-six patients with large hemispheric MCA
infarction were divided randomly into two groups: Group I
in which patients were followed until deterioration of level of
consciousness, and Group II in which patients were operated
within 6 h of presentation regardless of clinical signs of
deterioration or radiographic features (16). While both groups
demonstrated improvement in conscious level, motor power,
and functional outcome, there was significant improvement
(p<0.05) in functional outcome in group II based on the
mRS. Group I demonstrated increased progression of infarct
volume when compared to Group II, and also had a morality
of 52% due to delay in surgery compared to 10% in Group
II. This study found better clinical and radiographic outcomes
for patients with large hemispheric MCA infarction who were
operated on prophylactically within 6 h of infarction without
waiting for deterioration of level of consciousness.
While there are concerns that very early decompression
surgery might potentially be unnecessary, the presented data
demonstrate that decompression after the onset of herniation
symptoms is less effective, or may even be ineffective in reducing
mortality and improving neurological outcome. While more data
are required, current studies suggest that stroke patients with
malignant infarction >200 cm3and follow up CT at 2 days from
symptom onset which demonstrate shift of the midline structures
are likely to herniate and would benefit from early decompressive
craniectomy.
TIMING OF CRANIECTOMY AFTER
TRAUMATIC BRAIN INJURY
Decompressive Craniectomy for Traumatic
Brain Injury (TBI) in the Animal Model
Preliminary data from TBI animal models treated with
decompressive craniectomy have suggested that decompressive
craniectomy could reduce edema formation and prevent
secondary expansion of the original contusion when compared
to non-operative management. Zweckberger et al. utilized
a controlled cortical impact model of TBI in a cohort of
mice to study the influence of decompressive craniectomy on
secondary contusion expansion and brain edema formation, and
to determine optimal timing of decompressive craniectomy (25).
It was determined that in the surgical groups, there was no
secondary expansion of the original contusion and there was
a 52% reduction of brain edema compared to the non-surgical
group. These benefits were seen with decompressive craniectomy
when performed up to 3 h after the initial trauma. Tomura et al
utilized a fluid percussion injury model of TBI in a cohort of
rats to investigate the influence of decompressive craniectomy
on post traumatic brain edema formation. It was found that the
non-surgical group demonstrated less cortical water content and
greater AQP4 expression when compared to the decompressive
craniectomy group.
Decompressive Craniectomy More Than
24 h After TBI
Although there is some controversy regarding the use of
decompressive craniectomy in ischemic stroke patients, the
use of decompressive craniectomy following human TBI has
certainly been more controversial. Three RCTs have analyzed the
outcomes of TBI patients after late decompressive craniectomy
(more than 24 h from the injury) (see Table 2). The DECRA
(Decompressive Craniectomy in Diffuse Traumatic Brain Injury)
trial published by Cooper et al. in 2011 was a landmark RCT
which informed the outcomes of TBI patients with diffuse
injuries who were treated with decompressive craniectomy
within 72 h of injury (17). In this study, 155 patients with
refractory ICPs >20 mmHg for 15 min within a 1-h period
were randomized into a decompressive craniectomy group
(bifrontal decompressive craniectomy) or a maximal medical
management group. On average, the time from injury to surgery
was 38.1 h, with a range of 27.1–55.0 h. In this study, Cooper
et al. determined that bifrontal decompressive craniectomy
decreases ICP and the length of stay in the intensive care unit,
but is associated with more unfavorable outcomes. There are,
however, some criticisms involving the DECRA trial. First, the
randomization was uneven between the 2 groups. There were
more patients with non-reactive pupils in the decompressive
craniectomy group than the medical therapy group (27 vs. 12%,
respectively [p=0.04]). It can be argued that more patients
in the decompressive craniectomy group already demonstrated
signs of herniation prior to treatment which may obfuscate
the therapeutic benefit from a decompressive craniectomy.
Indeed, the harm associated with decompression was no longer
statistically significant when a statistical control for unreactive
pupils was performed. Other issues included the relatively small
sample size and that only bifrontal decompressive craniectomy
without falx sectioning was allowed. Some researchers believe
DECRA was too aggressive and that ICP elevations should have
been sustained for longer durations prior to considering surgery.
Lastly, there were no standardized rehabilitation protocol for the
enrolled patients.
After the DECRA trial, the therapeutic effect of decompressive
craniectomy in TBI patients remained unclear, particularly in
patients with focal pathology and when a lateral decompression
is performed. In 2016, Hutchinson el al. published a multicenter
(48 centers, 19 countries) RCT study named RESCUEicp
(Trial of Decompressive Craniectomy for Traumatic Intracranial
Hypertension) in which a cohort of 408 patients with TBI
and refractory elevated ICP (>25 mmHg for at least 1 h)
were randomized into a decompressive craniectomy group or a
maximal medical therapy group (18). In this pragmatic study,
44% of patients were enrolled after 72 h. RESCUEicp was
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Shah et al. Timing of Decompressive Craniectomy
TABLE 2 | Decompressive craniectomy for TBI studies.
Author Study
design
Patients Treatment Total no
of
patients
Time to DC Mortality
n(%)
GOS at 6 months GOS at 12
months
TBI Cooper et al.
(17)
Randomized
controlled trial
Adults with
TBI
Age 15–59 years,
severe,
non-penetrating
brain trauma,
DC 73 Performed within 72 h
after injury; a large
bifrontotemporoparietal
craniectomy with
bilateral dural opening
14 (19) Median =3 (IQR
2–5)
NA DC decreases ICP and
the length of stay in the
intensive care unit, but
is associated with more
unfavorable outcomes.
Medical
management
82 NA 15 (18) Median =4 (IQR
3–5)
NA
Hutchinson
et al. (18)
Randomized
controlled trial
Adults with
TBI
Age 10–65,
abnormal CT scan
of the brain,
intracranial-
pressure monitor
already in place,
and have raised
intracranial
pressure (>25 mm
Hg for 1–12 h)
DC 202 Performed at any time.
44% were enrolled after
72 h
59 (30.4) Favorable
outcomes
(upper severe
disability or better):
42.8%
Favorable
outcomes
(upper severe
disability or
better):
45.4%
When compared to
medical management,
DC resulted in lower
mortality and higher
rates of vegetative
state, lower severe
disability, and
upper severe disability.
The rates of moderate
disability and good
recovery were
comparable between
both groups.
Medical
management
196 NA 93 (52) Favorable
outcomes
(upper severe
disability or better):
34.6%
Favorable
outcomes
(upper severe
disability or
better):
32.4%
Qiu et al. (19) Randomized
controlled trial
Adults with
TBI
Patient age 18–65,
acute
post-traumatic
brain swelling on
CT with >5 mm
midline shift,
contusions
<25 ml,
compressed basal
cisterns, and GCS
8 or less
Unilateral DC 37 DC for all patients
within 2 to 24 h after
admission
10 (27) 1: 10 (27%); 2: 1
(3%); 3: 5 (14%);
4: 6 (16%); 5: 15
(41%)
4 or 5 (56.8%) Unilateral DC is
superior to control
temporoparietal
craniectomy in lowering
ICPs, reducing the
mortality rate, and
improving neurological
outcomes.
Control (unilateral
routine
temporoparietal
craniectomy)
37 DC for all patients
within 2 to 24 h after
admission
21 (57) 1: 21 (57%); 2: 0
(0%); 3: 4 (11%);
4: 7 (19%); 5: 5
(14%)
4 or 5 (32.4%)
(Continued)
Frontiers in Neurology | www.frontiersin.org 7January 2019 | Volume 10 | Article 11
Shah et al. Timing of Decompressive Craniectomy
TABLE 2 | Continued
Author Study
design
Patients Treatment Total no
of
patients
Time to DC Mortality
n(%)
GOS at 6 months GOS at 12
months
Taylor et al.
(20)
Randomized
controlled trial
Pediatric
patients with
TBI
DC 13 DC was performed at a
median of 19.2 h (range
7.3–29.3 h).
3 (23.1) Favorable: 7
(53.8%);
Unfavorable: 6
(46.2%)
NA DC may be superior to
medical management
of in children with TBI in
reducing ICP and
improving functional
outcome and quality of
life.
Cianchi et al.
(21)
Retrospective
cohort
Adults with
TBI
186 patients with
TBI were
retrospectively
studied from
2005–2009
Early DC 41 DC was performed
within 24 h of TBI
12 (29.3) Average
GOS =3.3
NA Hospital mortality rates
and Glasgow Outcome
Scale at 6 month follow
up were comparable
between all groups
Late DC 21 DC was performed
after 24 h of TBI
6 (28.6) Average
GOS =3.0
NA
Medical
management
124 30 (24.2) Average
GOS =3.6
NA
Bagheri et al.
(22)
Prospective
cohort
Adults with
TBI
Severe TBI
patients with
midline shift >
5 mm and who
were candidates
for DC according
to their initial brain
CT scan from
2011–2014.
Early DC 61 DC performed 4.5 ±
2 h after trauma
NA GOS >3, 54.1%
(33 patients)
NA Patients whose age
was >60 and a GCS
<5 did not benefit from
early decompressive
craniectomy
Jagannathan
et al. (23)
Retrospective
cohort
Pediatric
patients with
TBI
23 patients age <
18 who underwent
DC for Trauma
were analyzed
1995–2006
DC 23 DC performed on avg
68 h (range 24–192)
7 (30.4) NA Avg GOS at 2
years =4.2
(median 5)
Although the mortality
rate remains high, DC
is effective in reducing
ICP and is associated
with good outcomes in
survivors (81%
returning to school)
Shackelford
et al. (24)
Retrospective
cohort
Adults with
TBI
Patients with
combat-related
brain injury
between 2005 and
2015 who
underwent DC at
deployed surgical
facilities
DC 486 Quintile 1: DC
30–152 min after TBI;
Quintile 2: DC
154–210 min after TBI;
Quintile 3 DC
212–320 min after TBI;
Quintile 4: DC
325–639 min after TBI;
Quintile 5: DC
665–3,885 min after
TBI
Quintile 1:
23; Quintile
2:7%;
Quintile 3:
7%;
Quintile 4:
19%;
Quintile 5:
14%
NA NA Mortality was
significantly lowered
when time to
craniectomy occurred
within 5.33 h of injury
Frontiers in Neurology | www.frontiersin.org 8January 2019 | Volume 10 | Article 11
Shah et al. Timing of Decompressive Craniectomy
intended to study a distinct population of patients as compared
with DECRA. The DECRA trial looked at decompression within
72 h after diffuse TBI, whereas the RESCUEicp trial analyzed
decompressive craniectomy as salvage therapy for refractory
intracranial hypertension. Moreover, patients with intracranial
hematoma were not included in DECRA trial, but accounted for
about 20% of the RESCUEicp trial. Unilateral craniectomy was
not permitted in DECRA trial but was allowed in the RESCUEicp
trial. At 6 months, the patients in RESCUEicp’s decompressive
craniectomy group exhibited lower mortality but higher rates
of vegetative state, “lower severe” disability, “upper severe”
disability, and comparable rates of moderate disability and
“good recovery” when compared to the medical management
group. It should also be noted that in the subgroup analysis
comparing decompressive craniectomy performed before 72 h
and at 72 h or more, there were no differences noted in functional
outcomes. In interpreting this trial it is important to consider
that 37.2% (73 patients) of the patients in the medical group
ultimately underwent decompressive craniectomy. Notably, ten
patients were excluded from analysis due withdrawal/lack of
valid consent. Seven additional patients in the medical group
were lost to follow-up. It is particularly important to consider
that the majority of the patients in the RESCUEicp trial
had diffuse injuries (78.6% of all study patients between the
surgical and medical therapy groups) and underwent bifrontal
decompressions (81.3% of the surgical group) despite the intent
to enroll a distinct population from DECRA. With this in mind,
the authors of this manuscript view RESCUEicp as confirming
the findings of DECRA without substantially informing the use
of decompressive craniectomy in patients with focal pathology,
and the role of lateral decompressions.
Due to the paucity of data analyzing the importance of timing
of decompressive craniectomy in outcomes of TBI patients, a
meta-analysis published by Zhang et al. demonstrated that early
decompressive craniectomy within 36 h could result in better
prognosis based on the Glasgow Outcome Scale scores at 6
months when compared to patients operated on >36 h from
the initial injury (5). The meta-analysis included 10 studies with
four randomized controlled trials. On sub-group analysis, Zhang
et al. determined that decompressive craniectomy could reduce
mortality rate, lower ICPs, decrease ICU stay, but could also
increase complication rate.
Decompressive Craniectomy Within 24 h of
TBI
While the aforementioned studies analyzed outcomes following
decompressive craniectomy performed more than 24 h from time
of injury, there have been efforts to analyze outcomes in TBI
patients treated with early decompressive craniectomy within
24 h of injury. To that end, Cianchi et al. published their findings
from a retrospective analysis which looked at the outcomes of
early vs. late decompressive craniectomy compared to maximal
medical management in treating TBI patients (21). In this
study, 186 TBI patients were divided into early decompressive
craniectomy (surgery within 24 h of TBI), late decompressive
craniectomy (surgery after 24 h, on average 7.7 days after TBI),
and maximal medical management groups. Hospital mortality
rates and Glasgow Outcome Scale at 6 month follow up were
comparable between all groups; however, the 6 month mortality
rate was significantly less for the maximal medical management
group compared to the early and late decompressive craniectomy
groups (29, 48.8, 42.9%, respectively [p=0.02]) (21). One of
the main limitations of this analysis is the retrospective study
design. Inherently, patients in the control group had intracranial
pressures that were adequately treated with medical therapy
whereas patients who received decompressive craniectomy failed
medical therapy. It is therefore reasonable to conclude that
the patients who underwent decompressive craniectomy had,
on average, a more severe TBI. A more appropriate control
group would include patients who were non-responders to
medical treatment who were not treated with late decompressive
craniectomy; however, there are obvious ethical considerations
limiting such a study design.
To better address the importance of early decompressive
craniectomy in TBI patients, Qiu et al. published an RCT
analyzing the outcomes of early decompressive craniectomy
in TBI patients (19). Seventy-four patients were randomized
to either unilateral decompressive craniectomy or a control
group which consisted of a unilateral routine temporoparietal
craniectomy. All surgery occurred between 2 and 24 h (average
5.8 h) after admission. Enrolled patients needed to demonstrate
>5 mm of midline shift on CT and compression of the basal
cisterns. In this RCT, the entire cohort had progressed to
some form of radiographic herniation. The mortality rates at 1
month after treatment were 27% in the unilateral decompressive
craniectomy group and 57% in the control group. At 1 year
follow up, good neurological outcome (GOS Score of 4–5) were
56.8% for the decompressive craniectomy group and 32.4% for
the control group (p=0.035). In contrast to the previous stroke
studies which demonstrated that decompressive craniectomy
after herniation does not confer any functional benefit, Qiu
et al. concluded that unilateral decompressive craniectomy
after radiographic signs of herniation may be superior to the
control group at lowering ICPs, reducing the mortality rate, and
improving functional outcome. It should be reiterated that all
surgeries were performed within 24 h which is considered to be
“early” compared to the timing of decompression reported in
most of the TBI in the literature.
Bagheri et al. corroborated the findings of Qiu et al. and
published their findings from a prospective study of 61 patients
who underwent rapid decompressive craniectomy (within 4.5 ±
2 h) after trauma to assess factors associated with prognosis and
outcome (22). Of the 61 patients, 54.1% demonstrated favorable
functional outcomes; however, patients with ages older than
60 years, bilateral non-reactive mydriasis, critical head injury
(GCS<5), or with >1 cm midline shift had worse outcomes.
Bagheri argued that patients whose age was >60 and a GCS <5
did not benefit from early decompressive craniectomy.
Lastly, a large retrospective review involving 486 patients with
combat related TBI who underwent decompressive craniectomy
demonstrated that decompression within 5.33 h from TBI was
associated with improved survival (24). The mortality of the
patients were reported by time interval related quintiles: quintile
Frontiers in Neurology | www.frontiersin.org 9January 2019 | Volume 10 | Article 11
Shah et al. Timing of Decompressive Craniectomy
1 was defined as decompressive craniectomy 30–152 min after
TBI, quintile 2 was defined as decompressive craniectomy 154–
210 min after TBI, quintile 3 was defined as decompressive
craniectomy 212–320 min after TBI, quintile 4 was defined as
decompressive craniectomy 325–639 min after TBI, and quintile
5 was defined as decompressive craniectomy 665–3,885 min
after TBI. The postoperative mortality was 23, 7, 7, 19, and
14% respectively. Mortality was significantly lowered when
time to craniectomy occurred within 5.33 h of injury. While
providing some insight into the possible importance of ultra-
early decompressive craniectomy on survival, the retrospective
design and the lack of long term functional outcome data limits
the conclusions that can be drawn from this study.
Although more research is needed, decompressive
craniectomy remains a frequently performed treatment—
generally of last resort—for many patients with severe TBI.
Much additional research is needed to optimize how and when
this surgery is performed. In contrast to the findings in the
stroke data, preliminary data for TBI studies demonstrate that
decompressive craniectomy after acute herniation may still be
beneficial in improving mortality and functional outcomes.
Although more data are needed, TBI patients treated with early
decompressive craniectomy seem to have lower mortality and
potentially better functional outcomes than TBI patients treated
with late decompressive craniectomy. As with the stroke data,
the analysis of outcome for TBI patients in relation to herniation
events was insufficiently described in relevant studies, and it is
not possible to determine whether early surgery is beneficial
due to avoiding herniation or whether there is a benefit to
early surgery independent of herniation. While the larger RCTs
indicate that decompressive craniectomy may increase the
survival rate and concomitantly increase rates of severe disability
including vegetative state, subsequent trials with a shorter
duration to decompressive craniectomy have demonstrated
improved functional outcomes and less mortality.
Early Decompressive Craniectomy in
Pediatric TBI Patients
Some published data demonstrate that early decompressive
craniectomy may be beneficial in the pediatric population.
To that end, Taylor et al. published the only RCT analyzing
outcomes of early decompressive craniectomy in the pediatric
population (20). Twenty-seven children who had sustained ICP
elevation after TBI were randomized to the medical management
group or the decompressive craniectomy group. Early bitemporal
decompressive craniectomy was performed for the surgical group
at a median of 19.2 h (range 7.3–29.3 h) from the time of
TBI. Outcome was assessed 6 months after the TBI using a
modification of the Glasgow Outcome Score (GOS) and the
Health State Utility Index. At 6 months, 54% of children in the
decompressive craniectomy group had good outcomes or mild
disability at 6 months compared to 14% of children in the control
group. Taylor et al. concluded that in pediatric TBI patients
with refractory ICPs, patients treated with early decompressive
craniectomy are more likely to have reduced ICPs and improved
functional outcome than children treated with maximal medical
therapy alone. While this is the only RCT published regarding
decompressive craniectomy in the pediatric population, this
study has received some criticism because it involved an unusual
decompressive surgery in which the dura was not opened, and
because it accrued a small number of patients over a long study
period.
Jagannathan et al. corroborated the findings from Taylor et al.
in their retrospective review on the outcomes of 23 pediatric
patients who underwent decompressive craniectomy for TBI
(23). The time to decompressive craniectomy was on average 68 h
(range 24–192). Despite having longer time to decompressive
craniectomy compared to Taylor et al., the mean GOS score at
the 2-year follow-up examination was 4.2 (median 5). At latest
follow up, 81% of the patients returned to school, and only
18% were dependent on caregivers. It should be noted that the
outcomes in the Taylor et al. cohort were analyzed at 6 months,
whereas the outcomes in the manuscript by Jagannathan et al.
were analyzed at 2 year follow up, substantially confounding a
comparison of the two trials. Although more data are needed, it
is possible that earlier decompression may not be as important in
improving long term outcomes in the pediatric population as has
been shown in the adult population.
With the limited data at hand, it appears that the pediatric
population has better functional outcomes with decompressive
craniectomy regardless of timing when compared to medical
management. Unfortunately, direct comparisons between early
and late decompressive craniectomy have not been made in the
pediatric population. Larger RCTs with direct comparisons will
be needed to determine if timing plays a role improving outcomes
in the pediatric population.
Future Directions: Decompressive
Craniectomy Based on Biologic and
Radiographic Metrics
While there are data validating the benefits of early craniectomy
based on specific time windows and clinical correlates of
herniation, there are growing data that there may be other
biologic and radiographic metrics to help guide timing of
decompressive craniectomy for TBI and stroke. Strict control
of intracranial pressures and cerebral perfusion pressures alone
does not necessarily prevent cerebral hypoxia (26). Recent data
have demonstrated that measurement of brain tissue oxygen
tension (PbtO2) may more precisely measure the adequacy of
cerebral perfusion, and could be a useful adjunct for deciding
on the timing of decompressive craniectomy (27). A PbtO2
below 20 mmHg has been associated with poor outcomes in TBI
patients (28). Reithmeier et al. published data on the effects of
decompressive craniectomy on ICPs and PbtO2based on the
continuous monitoring of 15 patients and determined that PbtO2
monitoring could serve as a useful tool for timing craniectomy
(2). One criticism of PbtO2is that its measurements are based
on data from the confines of a small volume of brain tissue
which may not adequately reflect the oxygenation of a larger
expanse of compromised brain. Other potentially useful biologic
metrics include the pressure reactivity index (PRx) which is
the correlation coefficient between mean intracranial pressure
Frontiers in Neurology | www.frontiersin.org 10 January 2019 | Volume 10 | Article 11
Shah et al. Timing of Decompressive Craniectomy
(ICP) and mean arterial blood pressure. This could be used as a
surrogate marker of cerebrovascular impairment (29). There have
also been preliminary data suggesting that surrogates for blood-
brain-barrier disruption, defined by a ratio of total CSF protein
concentrations to total plasma protein concentration, may also
be useful for prognosis and treatment (30). Advances in imaging
modalities may also be utilized to guide the treatment trajectory.
The infarct growth rate (IGR) between two CT scans may also
be a useful tool for timing craniectomy. Kamran et al. published
a retrospective, multicenter cross-sectional study of 182 patients
to identify factors for selecting the timing of craniectomy (31).
The IGR on the second CT was one of the five factors identified
as having the strongest association with craniectomy. Patients
who survived without surgery had the slowest IGRs. On another
retrospective cohort of 137 patients, Kamran et al. demonstrated
that IGR was identified as an independent predictor of early
surgery (32). The second infarct growth rate [IGR2] >7.5 ml/hr
was associated with surgery under 48 h. Both first infarct growth
rate [IGR1] and second infarct growth rate [IGR2] were nearly
double in patients with early surgery within 48 h. Although more
data are needed, monitoring the infarct growth rate could help
determine when a neurosurgeon should pursue decompression.
While promising, these biologic and radiographic metrics still
require more data before they are used to counsel patients
regarding treatment course and prognosis.
CONCLUSION
Although there is much controversy surrounding optimal
timing of decompressive craniectomy in patients with stroke
and TBI, data have suggested that early decompression within
24 h has a tendency to improve mortality and functional
outcomes for both conditions when compared to decompression
performed after 24 h. In stroke patients, decompression
before clinical signs of herniation yields improved functional
outcomes when compared to decompression after clinical
signs of herniation. Surgery after clinical deterioration may
be too late to impart any functional benefit in stroke patients.
In contrast to the stroke data, preliminary TBI data have
demonstrated that decompressive craniectomy after signs of
herniation may still lead to improved functional outcomes
compared to medical management. In adult TBI patients, early
decompressive craniectomy within 24 h may improve mortality
and functional outcomes when compared to decompressive
craniectomy performed >24 h. In fact, data from RCTs suggest
that late decompressive craniectomy for TBI may result in
worse functional outcomes than maximal medical therapy.
In pediatric TBI patients, patients also had better functional
outcomes when treated with decompressive craniectomy
regardless of timing. High quality studies better informing
the timing and indications for decompressive craniectomy
are needed for both ischemic stroke and TBI. The additional
data provided by imaging and advanced neuromonitoring
could also be useful adjuncts in guiding decision
making.
AUTHOR CONTRIBUTIONS
AS: Conceptualization of the manuscript, literature review, data
analysis, and manuscript writing. SA: Data analysis and revision
consultant. GH: Supervised, edited/wrote the manuscript and
literature/data analysis.
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
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Frontiers in Neurology | www.frontiersin.org 12 January 2019 | Volume 10 | Article 11
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