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www.jkns.or.kr http://dx.doi.org/10.3340/jkns.2014.55.1.

26 Print ISSN 2005-3711 On-line ISSN 1598-7876

J Korean Neurosurg Soc 55 : 26-31, 2014 Copyright © 2014 The Korean Neurosurgical Society

Clinical Article

Significance of Intracranial Pressure Monitoring


after Early Decompressive Craniectomy in Patients
with Severe Traumatic Brain Injury
Deok-ryeong Kim, M.D.,1 Seung-Ho Yang, M.D.,2 Jae-hoon Sung, M.D.,2 Sang-won Lee, M.D.,2 Byung-chul Son, M.D., Ph.D.3
Department of Neurosurgery,1 Eulji University School of Medicine, Eulji General Hospital, Seoul, Korea
Department of Neurosurgery,2 St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Suwon, Korea
Department of Neurosurgery,3 Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea

Objective : Early decompressive craniectomy (DC) has been used as the first stage treatment to prevent secondary injuries in cases of severe trau-
matic brain injury (TBI). Postoperative management is the major factor that influences outcome. The aim of this study is to investigate the effect of
postoperative management, using intracranial pressure (ICP) monitoring and including consecutive DC on the other side, on the two-week mortality
in severe TBI patients treated with early DC.
Methods : Seventy-eight patients with severe TBI [Glasgow Coma Scale (GCS) score <9] underwent early DC were retrospectively investigated.
Among 78 patients with early DC, 53 patients were managed by conventional medical treatments and the other, 25 patients were treated under the
guidance of ICP monitoring, placed during early DC. In the ICP monitoring group, consecutive DC on the other side were performed on 11 patients
due to a high ICP of greater than 30 mm Hg and failure to respond to any other medical treatments.
Results : The two-week mortality rate was significantly different between two groups [50.9% (27 patients) and 24% (6 patients), respectively,
p=0.025]. After adjusting for confounding factors, including sex, low GCS score, and pupillary abnormalities, ICP monitoring was associated with a
78% lower likelihood of 2-week mortality (p=0.021).
Conclusion : ICP monitoring in conjunction with postoperative treatment, after early DC, is associated with a significantly reduced risk of death.

Key Words : Brain injuries · Intracranial pressure monitoring · Decompressive craniectomy · Mortality.

INTRODUCTION last report for treating uncontrollable ICP17,19,22). However, the


time from injury to DC was reported to be the factor with the
Traumatic brain injury (TBI) is the leading cause of death greatest influence on the outcomes of severe TBI19,22,25). Authors
and disability around the world, despite improvements in of several studies advocate that DC should be performed as
emergency care, imaging, critical care, medical and surgical soon as possible after trauma, in order to prevent secondary in-
treatment options, and rehabilitation15,32). In US alone, an esti- juries that may occur during unsuccessful ICP or other medical
mated 1.5 million people sustain TBI each year, resulting in treatments2,12,22,25,35). Even in case of early DC and maximal
more than 50000 deaths and another 500000 individuals with postoperative medical treatments, uncontrollable ICP due to
permanent neurological sequelae14). Despite more than 25 post-traumatic edema may progress. In this case, better decom-
pharmaceutical trials for TBI that have failed to show efficacy, pression and suitable ICP decrease may be achieved if consecu-
the mainstay of treatment for severe TBI targets the reduction tive DC is performed on the other side of the brain as well25,36).
of elevated intracranial pressure (ICP) and the maintenance of Evidence-based guidelines for severe TBI recommended ICP
adequate cerebral blood flow and oxygenation7). monitoring in patients with severe TBI and link the degree as
Decompressive craniectomy (DC) has been perceived as a well as duration of intracranial hypertension with increased

• Received : June 14, 2013 • Revised : October 2, 2013 • Accepted : December 16, 2013
• Address for reprints : Byung-chul Son, M.D., Ph.D.
Department of Neurosurgery, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Korea
Tel : +82-2-2258-6122, Fax : +82-2-594-4248, E-mail : sbc@catholic.ac.kr
• This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0)

which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

26
Significance of ICP Monitoring after Early DC | DR Kim, et al.

mortality rates4). Patients who responded to ICP-lowering treat- tra-cerebral clots were also evacuated. After meticulous hemo-
ment showed a significantly reduced risk of death at 2 weeks stasis around injured lesions, a subdural ICP monitoring cathe-
than those who did not respond after adjusting for factors that ter (Integra NeuroSciences, San Diego, CA, USA), zeroed relative
independently predict risk of death7). ICP monitoring on the to atmospheric pressure, was placed underneath the incised
initial decompression area may provide pertinent diagnostic in- dura, at the posterior temporal bone margin and secured with
formation leading to more appropriate postoperative medica- dura sutures, to prevent displacement (Fig. 1). The dura was
tion reducing ICP or to timely treatment with invasive proce- then expanded with the synthetic dural substitute to allow the
dures like consecutive DC on the other side. brain to bulge outward. The temporalis muscle and skin flap
The purpose of this study is to evaluate the influence of post- were then re-approximated with sutures. The bone flap was
operative ICP monitoring, placed during early DC, on two-week maintained in wet gauze at -70°C and cranioplasty was per-
mortality in patients who underwent early DC for severe TBI. formed 3-6 months after surgery for surviving patients.

MATERIALS AND METHODS Postoperative management


All patients underwent primary resuscitation and stabiliza-
Study design and assessment tion, according to the Brain Trauma Foundation (BTF) guide-
From January 2010 through December 2012, A retrospective lines4), and were assessed for age, gender, GCS, and pupillary re-
analysis was made of 92 patients with severe traumatic brain in- sponse. These patients were transferred to an operating room
jury [Glasgow Coma Scale (GCS) score <9] underwent early within a maximum of 12 hours after their initial CT scans. Af-
DC. On admission, they received an initial cranial computed ter the decompressive surgery, conventional medical therapies,
tomography (CT) scan and were diagnosed as having type III, including hyper-osmotic agents, hyperventilation, or sedation
IV, or non-evacuated mass lesion of Marshall CT classifica- were used as needed to reduce intracranial hypertension in
tion18). Within this group, we excluded patients according to the both groups. These medical treatments were determined, ac-
following criteria : under 18 years old, severe extra-cranial le- cording to the CT scan, in correlation with neurological deteri-
sions such as cardiovascular, pulmonary or abdominal injuries, oration for Group 1 patients, while ICP monitoring was added
hemodynamic shock, transfer to our hospital more than 12 to the considerations for Group 2 patients. Consecutive DC on
hours after the initial injury, or admission with the diagnosis of the other side of the brain was performed, when ICP increased
brain death. Ultimately, 78 patients were included in this study. to greater than 30 mm Hg, for a period longer than 15 minutes,
The subjects were arranged into two groups. Group 1 contained and when the patient failed to respond to the maximal medical
53 patients who were given postoperative management, with- treatment mentioned above (Fig. 2). Body temperature, respira-
out ICP monitoring. Group 2 contained 25 patients treated tory rate, heart rate, blood pressure, cardiac rhythm, oxygen sat-
postoperatively with subdural ICP monitoring, placed during uration, and ICP for group 2 patients were monitored continu-
DC. With the hospital ethics committee’s approval, we reviewed ously. ICP measurements were recorded using a monitoring
medical records and radiology of all patients. The following pa- device (Integra NeuroSciences, San Diego, CA, USA) and ICP
rameters were recorded and analyzed : patient’s age, sex, initial values were collected on an hourly basis, with additional values
GCS score, pupillary response, and two-week mortality. The included if there were any meaningful changes. Normal ICP
two week time frame was selected because over 85% of deaths was defined as an ICP of 0-20 mm Hg.
occur within two weeks after injury8).

Decompressive surgical procedures


The patient was induced for general anesthesia endotracheal-
ly. The unilateral decompression procedure involved making a
large curvilinear incision in the fronto-temporo-parietal region.
This was followed by preparing a myocutaneous flap and crani-
ectomy, elevating large bone flaps, with a diameter of at least 12
cm, including the frontal, parietal, temporal, and parts of the
occipital squama. Additional bone was removed at the tempo-
ral region, down to the floor of the middle fossa, to release the
compression of the basal cistern. The dura mater was attached
to the craniotomy edge, to prevent epidural bleeding. The dura
was then opened at the temporal base, in a stellate fashion, to
provide additional space for brain swelling. When the dura was
Fig. 1. Lateral plain radiograph of the skull shows subdural Intracranial
opened, the underlying brain or hematoma typically herniated pressure monitoring sensor (arrow), placed at the posterior temporal
outward. The contused brain tissue was gently removed and ex- bone margin, after the initial decompressive craniectomy.

27
J Korean Neurosurg Soc 55 | January 2014

erally fixed and dilated pupils, with no


response to light, and 14 patients had bi-
laterally fixed pupils at admission. A to-
tal of 25 patients (32.1%) had ICP moni-
toring placed during their early DC.

Use and outcomes of ICP


monitoring
A B C Patients were further divided into two
Fig. 2. Pre- and postoperative computed tomography (CT) scans of an illustrative case. A :
groups after early DC; one included pa-
Preoperative CT scan showing diffuse brain swelling and obliterated basal cisterns. B : Initial post- tients treated with an ICP monitor and
operative CT scan showing early decompressive craniectomy (DC). C : Postoperative CT scan show- the other included patients not treated
ing consecutive bilateral DC at an interval of eight hours. an ICP monitor. The clinical characteris-
tics of the two groups are listed in Table
Table 1. Characteristics of the study population 1. For group 1, which was patients treat-
No ICP monitoring ICP monitoring ed without an ICP monitor, the mean
p-value
[n=53 (67.9%)] [n=25 (32.1%)] age was 45.2±18.24 years, 44 patients
Age were male (83%), twenty-eight patients
Mean±SD 45.2±18.24 42.9±16.65 0.597 (52.8%) had initial GCS scores lower
Sex (%) than 6, and twenty-six patients (49.1%)
Male 44 (83) 20 (80) 0.759 had fixed and dilated pupils with no re-
Female 9 (17) 5 (20) sponse to light, regardless of bilateral-
Initial GCS (%) ism. For group 2, which included pa-
6-8 25 (47.2) 15 (60.0) 0.290 tients treated with an ICP monitor, the
3-5 28 (52.8) 10 (40.0) mean age was 42.9±16.65 years, twenty
Pupillary response (%) patients were male (80.0%), fifteen pa-
Yes 27 (50.9) 12 (48.0) 0.808 tients (60.0%) had GCS scores lower
No 26 (49.1) 13 (52.0) than 6, and thirteen patients (52.0%)
2 week mortality (%) had fixed and dilated pupils with no re-
Alive 26 (49.1) 19 (76.0) 0.025 sponse to light. The differences between
Dead 27 (50.9) 6 (24.0) the groups in terms of age, initial GCS
GCS : Glasgow Coma Scale, ICP : intracranial pressure, SD : standard deviation score, and pupillary response were not
statistically significant. The 2-week mor-
Statistical analysis tality rate, however, was 50.9% (27 patients) for group 1, com-
Comparisons between groups were analyzed using the chi- pared with 24.0% (6 patients) for group 2 with a statistically sig-
square test, Fisher’s exact test, and Student’s t-test. The means are nificant difference (p=0.025).
expressed as mean±standard deviation. Logistic regression analy-
ses, controlled for sex, pupillary status, and initial GCS scores, Factors predicting two-week mortality
were used to evaluate the association between ICP monitoring Multivariable logistic regression models predicting two-week
status and two-week mortality. The odds ratios, 95% confidence mortalities are shown in Table 2. After adjusting for confounding
intervals, and p values of the covariates were reported. All statisti- factors, including sex, low GCS score, and pupillary abnormali-
cal tests were two-sided, and p<0.05 was considered statistically ties, ICP monitoring was associated with a 78% lower likelihood
significant. Analyses were performed using the statistical soft- of 2-week mortality (adjusted odds ratio 0.22, 95% confidence in-
ware SPSS (ver. 17.0; SPSS Inc., Chicago, IL, USA). terval 0.059-0.790, p=0.021). To identify factors independently
associated with the two-week mortality, including using an ICP
RESULTS monitor, differences in all available covariates were examined,
and we concluded that women were associated with significant-
Characteristics of the study population ly increased mortality.
Sixty-four patients were male (82.0%). Motor vehicle related
accidents were the cause of 38 cases (48.7%). The patients were Outcome of consecutive decompressive surgery
44±17.6 years old (range 18-80 years). The GCS scores ranged In group 2, where patients were treated with the ICP monitor,
from 3 to 8, including 38 patients with GCS scores of 3-5, and 40 patients were further divided into two groups, depending on
patients with a GCS score of 6-8. Twenty-five patients had unilat- whether they received consecutive DC on the other side. Table

28
Significance of ICP Monitoring after Early DC | DR Kim, et al.

3 shows the clinical characteristics of Table 2. Logistic regression analyses predicting two-week mortalities for all 78 patients
the two groups. Patients who had con- Crude Adjusted*
Variables
secutive DC on the other side, showed OR 95% CI p-value OR 95% CI p-value
significantly higher mean ICP values Age (yr)
right after early DC (p<0.001) and sig- <50 1.000 0.5
nificantly lower initial GCS values (<6, ≥50 1.373 0.551-3.418
p<0.049) than those who did not receive Sex
additional surgeries. The two-week Female 1.000 0.01 1.000 0.007
mortality rate of the consecutive de- Male 0.143 0.036-0.566 0.118 0.025-0.559
compression group was 45.5% (five pa- Initial GCS
tients). The result was lower than that
6-8 1.000 0.01 1.000 0.153
for patients with GCS score of 3-5
3-5 3.625 1.406-9.343 2.506 0.712-8.822
(57.8%) although there was no statisti-
Pupillary response
cal significance (p>0.05). The median
Yes 1.000 0.01 1.000 0.314
interval of time between initial and con-
No 3.924 1.284-8.448 1.922 0.539-6.849
secutive DC was 23.2±22.1 hours (range
Bilateral
4 to 76).
Yes 1.161 0.322-4.184
No 1.000 0.820
DISCUSSION ICP monitoring
Significance of early decompres- Yes 0.301 0.105-0.881 0.216 0.059-0.790
sion No 1.000 0.028 1.000 0.021
DC has become a valuable tool in *Adjusted by Sex, Pupil, GCS. OR : odds ratio, CI : confidence interval, GCS : Glasgow Coma Scale, ICP : intra-
cranial pressure
managing severe head injury since Ko-
cher3) first introduced decompressive Table 3. Characteristics of the group with intracranial pressure monitoring
surgery to alleviate intracranial hyper- Unilateral (n=14) Bilateral (n=11) p-value
tension. The optimal technique, timing, Initial ICP
indications, and outcomes for decom- Mean±SD 13±7.48 30±7.81 <0.001
pressive craniectomy remain controver- Age
sial. The role of DC in severe neurotrau- Mean±SD 46±18.8 38±13.2 0.296
ma has not been proven scientifically, as Initial GCS (%)
the pathophysiological process of post- 6-8 11 (78.6) 4 (36.4) 0.049
traumatic brain swelling is complicated 3-5 3 (21.4) 7 (63.6)
and not fully understood1,11,28,29). In Pupillary response (%)
many neurosurgical guidelines, indica- Yes 9 (64.3) 3 (27.3) 0.111
tion for DC includes dilated pupils, un-
No 5 (35.7) 8 (72.7)
responsiveness to light, uncontrollable
ICP : intracranial pressure, GCS : Glasgow Coma Scale, SD : standard deviation
ICP values (greater than 30 mm Hg) for
a period longer than 15 minutes and failure to respond to medi- Postoperative ICP monitoring
cal treatments10,22,25). DC is often perceived as a last resort for Measuring ICP is a milestone in TBI management. ICP mon-
treating uncontrollable ICP, which restricts many of its positive itors maintain adequate cerebral perfusion and oxygenation in
effects. Several clinical reports demonstrate that early evacuation situations of intracranial hypertension, in order to avoid sec-
of a hematoma and decompression reduce mortality. Addition- ondary brain injuries during the recovery period. According to
ally, accumulating experimental evidence shows that very early the best practice, evidence-based guidelines of the BTF4), using
decompression significantly reduces secondary brain inju- an ICP monitor is recommended for all patients with head in-
ry5,22,24,37). Thus, it seems reasonable to assume that in patients juries who have a GCS of 3 to 8 after resuscitation and an ab-
with a severe brain injury, an early decompression may prevent normal head CT scan, as well as in patients with severe TBI and
secondary injuries that would occur during unsuccessful ICP normal head CT scans, if two or more of the following features
treatment with conventional methods. Thus patients given early are present on admission : age greater than 40, unilateral or bi-
decompressions will have a better outcome than those that have lateral posturing, or systolic blood pressure less than 90 mm Hg.
a later decompression. In this study, we performed early DC in Several evidence-based studies show that ICP monitoring,
severe TBI patients who had abnormal findings in their CT when used in a protocol-based manner in neurosurgical inten-
scans. sive care units, leads to improved outcomes in adjusted mortali-

29
J Korean Neurosurg Soc 55 | January 2014

ty rates for patients with severe TBI6,9,23). In addition, a meta- level of statistical significance.
analysis of clinical studies since 1970 found that patients who
were aggressively monitored for ICP, after severe TBI, had a Limitations of this study
12% lower mortality rate, and 6% more favorable outcomes, This study has some limitations mostly stemming from its
when compared with patients who were less intensely moni- small sample size and retrospective design. Methodological
tored30). There is still debate over the effect of ICP monitoring weaknesses include the following : 1) retrospectively collected
on outcomes, despite increasing evidence that its implementa- data, 2) lack of selection parameters influencing the decision to
tion leads to improved outcomes. The findings of this study monitor, 3) baseline differences between groups in other dis-
suggest that post-decompression treatment with subdural ICP ease characteristics and therapeutic factors known to affect out-
monitoring improves outcome, as measured by the two-week come following TBI. Knowing the rationale for decisions to
adjusted mortalities. Two-week mortality was chosen as the monitor or not is a topic requiring investigation. Besides, Two-
end point of this study because this early time point accounts week adjusted mortality rather than 6-month Glasgow Out-
for over 85% of all TBI-related mortality and more appropriate- come Scale score was used as the primary outcome measure.
ly reflects the severity of the injury as well as the efficacy of early Although our data indicate that ICP monitoring after early DC
intervention26), whereas later time points such as 30-day mor- yields good outcomes, the retrospective design and short term
tality include complications or associated comorbidities due to outcome are prone to bias. Therefore, future research of corre-
ICU and hospital length of stay27). The age and GCS of the pa- sponding randomized controlled trials and outcome assess-
tient are major factors that influence the DC effectiveness. It is ment to include long-term functional status is warranted to fur-
generally reported that outcomes for patients younger than 50, ther explore the role of this procedure.
or those with an initial GCS score of 6 or more, are significantly
better than that for older patients, or those with an initial GCS CONCLUSION
score lower than 611,16,21,22,25). The characteristics of the patients
in this study that were treated for intracranial hypertension with The present study suggests that ICP monitoring, in conjunc-
monitoring, versus those treated without a monitor did not dif- tion with postoperative treatment after early DC, is associated
fer with regard to age, sex, initial GCS score, or pupillary re- with a significantly reduced risk of death. This is the first study
sponse. The two-week mortalities, however, were significantly that statistically evaluated two-week mortalities in patients who
improved if the post-decompression treatment was coupled had ICP monitoring as part of their postoperative treatment,
with the use of an ICP monitor. We speculate that the reason compared to patients treated without ICP monitoring. In addi-
for this improvement is that ICP monitoring ensures that the tion, we speculate that consecutive DC on the other side may
patients receive treatment with a better speed and accuracy. be a favorable treatment for patients who show high ICP’s of
greater than 30 mm Hg, and fail to respond to maximal medi-
Consecutive decompressive surgery cal treatment after early DC.
Bilateral DC was first described by Miyazakib et al.20) in 1966,
and was popularized in 197113). For patients with diffuse brain References
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