We aimed to identify the relation between perioperative cerebrospinal fluid (CSF) drain through lumbar drainage (LD) and development of postoperative (POP) remote intracerebral hemorrhage (rICH) in craniotomy to treat ruptured intracranial aneurysms.
We retrospectively reviewed consecutive patients who underwent craniotomy for ruptured cerebral aneurysms at the authors’ institution between 1998 and 2004. We subsequently compared the incidence and characteristics of POP rICH between the patients who had a perioperative LD and those who did not. All statistical analyses were conducted using the software package SPSS 19.0 (SPSS Inc., Chicago, IL, USA). A
We enrolled 688 patients, of which 80 patients (11.6%) received perioperative LD, and 608 did not. LD and non-LD groups were comparable because although clinical characteristics of the two groups were significantly different considering history of hypertension, timing of surgery, and closed system negative pressure suction drain (SD) placement, none of these three variables was an independent risk factor associated with POP rICH in multivariate analysis. POP rICH incidence was significantly higher in the LD goup (12.5%) than non-LD group (0.8%) (
POP rICH incidence was significantly higher in patients who were managed with perioperative LD than in those who did not. LD insertion in craniotomy for ruptured intracranial aneurysm, should be closely monitored to address the occurrence of POP rICH.
Draining the cerebrospinal fluid (CSF) via lumbar drainage (LD) is frequently performed in numerous neurosurgical settings and to clip the ruptured intracranial aneurysm for primarily obtaining appropriate brain relaxation, following which minimizing brain retraction, avoiding bloody CSF from obscuring the operative field. However, many adverse events from CSF drain have been established and reported. These include the Arnold-Chiari syndrome,
Postoperative (POP) ICH occurrence is one of the most serious complications in almost all neurosurgical procedures. Remote cerebellar hemorrhage was first introduced in 1977 by Yasargil and Yonekawa
Though rICH is relatively rare complication, it may result in significant morbidity and mortality.
Therefore, the immediate goal of this study was to evaluate and demonstrate the most approximate rICH pathogenesis by investigating the relationship between LD and POP rICH specially in the craniotomy for ruptured intracranial aneurysms.
We retrospectively reviewed the medical records and radiographies of consecutive patients who underwent craniotomy for ruptured cerebral aneurysms at our institute from 1998 to 2004. We excluded cases of unruptured cerebral aneurysms, ruptured aneurysms that were treated with both clipping and extraventricular drainage, endovascular embolization or operated using various skull base approaches including orbitozygomatic, lateral suboccipital, or different types of combined skull base approaches.
We identified age, sex, initial Hunt-Hess and Fischer grades, location of ruptured aneurysm, coagulation profiles, timing of surgery (early or delayed), presence or absence of hypertensive-hypervolemic (H-H) therapeutic intervention, history of hypertension, and LD and closed system negative pressure suction drain (SD) usage in each of the patients included in this study. H-H therapy was conducted in compliance with an internationally recommended protocol.
LD duration and the volume of CSF drain were also investigated in patients who had a perioperative LD. Final diagnosis of spontaneous SAH, ruptured cerebral aneurysm, microsurgical techniques, LD and SD management, and perioperative care were performed based on universal standards. The neurosurgeon conducting the procedure solely decided whether LD and suction drainage (SD) needed to be inserted or not, based on each patient’s status including surgical field, initial radiographic findings and the surgeon’s experience. During the study period, we exclusively used a lumbar kit from Integra-NeurosciencesTM (Plainsboro, NJ, USA) to drain of CSF, and Hemovac® (Zimmer Surgical, Inc., Dover, OH, USA) as a SD to drain epidural and/or subgaleal oozing blood and exudates.
For the statistical analysis, commercially available software, statistical package for the social science SPSS 19.0 (SPSS Inc., Chicago, IL, USA) was used. Demographic and clinical data with regard to the LD and rICH were compared using the t-test, [chi]2 test, ANOVA as appropriate. We also conducted multivariate logistic regression analyses upon possible clinical variables. All variables except age were considered as categorical. A
Between 1998 and 2004, total 688 patients were deemed suitable based on inclusion criteria. Of these subjects, 80 patients had perioperative LD. The patients with LD have higher rate of SD placement compared to non-LD group and it was statistically significant (
Among 688 patients, 41 showed several kinds of POP hemorrhages on POP head CT. Of these patients, 17 had an LD and 24 did not. In the LD group (80 patients [
From the total 688 patients, 355 had an SD. Of these 355, 15 demonstrated POP rICH. Namely, all 15 rICH patients in this study had an SD. Subsequently, the rate of rICH was 4.2% (15/355) in patients with an SD (
Among the entire 688 patients, 77 were treated by using an LD and an SD simultaneously (
Mean drained CSF through LD per day was below 50 mL/day in 41 patients, between 50–100 mL/day in 23, and above 100 mL/day in 16. The POP rICHs were developed in 4 patients of <50 mL group (9.8%), 6 of 50–100 mL (26.1%), and none from the >100 mL (0%), in each (
Number of patients that showed POP rICH in relation to LD duration are summarized in
Among 688 patients, 238 had a medical history of hypertension and 450 did not (
Among the included 688 patients, 468 underwent prophylactic or therapeutic H-H therapy, irrespective of its duration. Among these 468 patients, 13 showed POP rICH. The rates of rICH were 2.8% and 0.9% in the group of patients who had H-H therapy and who did not, respectively (
Higher volume of the subarachnoid blood clot (or Fisher grade) indicated an equally greater risk of developing POP rICH, and this correlation was statistically significant (
In a group of 80 patients who underwent LD, 9 exhibited POP rICH in the cerebellum (3, ipsilateral to the operative site; 4, contralateral; 2, bilateral) and 1 developed POP rICH at basal ganglia contralateral to the operative side (
Although LD has frequently been used in a variety of conditions in neurosurgery, it has been clearly understood that the over-drainage of CSF irrespective of the routes, may induce a plethora of complications
Although the characteristics of two groups (LD group and non-LD group) in this study were significantly different in the frequency of history of hypertension, timing of surgery and placement of SD, these variables were not independent risk factors in the multivariate analysis (
In a review of 4992 intracranial procedures, Kalfas and Little identified that rICH accounted for 18% (7/40) of all POP intracranial hemorrhages.
POP rICH incidence (2.2%) according to our study is relatively lower than that after direct surgical repair of ruptured and/or unruptured cerebral aneurysms as reported by others.
Studies have previously demonstrated that certain cases of POP rICH following intracranial aneurysm surgery occurred in the cerebral hemisphere contralateral to the operative site, while other reports suggested that POP rICH typically developed in the contralateral cerebellar hemisphere.
As described before, the overall POP rICH incidence was 2.2% (15/688) in our study and among these POP rICH cases, the incidences were 12.5% (10/80) and 0.8% (5/608) in the patients who had LD and who did not, respectively (
Although the initial Fisher grade of patient was not an independent risk factor associated with the formation of POP rICH in the multivariate analysis, we noted that the initial Fisher grade demonstrated a statistically significant correlation with the risk of developing POP rICH in the univariate analysis (
Unexpectedly, the authors failed to verify that POP rICH incidence was directly proportional to the amount and/or duration of CSF drain via LD in spite of these two parameters (amount and duration of CSF drain via LD) showed statistically significant correlations in the frequency of POP rICH (
According to relatively early period of case reports on the POP rICH, fluctuation or sudden elevation of BP during the craniotomy, initial POP period, vasospasm, H-H therapy, autoregulatory impairment, and perioperative coagulopathy might potentially cause POP rICH.
Alternatively, the consensus that the position of the patient’s head during craniotomy with microsurgery has a certain degree of influence in the development of POP rICH is relatively vague. Compression of internal jugular vein at the transverse process of the first cervical vertebra and resulting intracranial venous hypertension as a consequence of the patient’s head position during the craniotomy may cause POP rICH.
Brain sagging as a basic etiology of POP rICH, was introduced following intraoperative and/or perioperative CSF over-drain in craniotomy.
Recently, a few authors
Given the situation we do not have choice but to accept that the unidentified or unknown POP clinical settings including neurosurgical conditions, which can violently disturb homeostasis or normal internal milieu of the brain may occur beyond the known clinical conditions as specified in
Comprehensively, we propose the pathogenesis of POP rICH considering the results of this study and a thorough review of the literatures is shown in
This study has numerous weaknesses and there may be more drawbacks apart from those mentioned below. First, there are several inherent limitations due to the retrospective natures of this study, including an absence of a corresponding control group, missing data that was neither documented nor checked up. Second, we did not subdivide the volume of rICH in the POP rICH patients and the corresponding volume of CSF loss through the LD. However, this two might be associated with each other. Third, we considered and analyzed CSF drain for only the 24 hours (1 day) basis without checking the velocity of CSF drain via LD within more segmented time periods. Fourth, we did not subdivide the patients into age groups which might have an effect on the frequency, appearance, and volume of POP rICH. Finally, we did not consider CSF drain volume via SD, although it was not an independent risk factor associated with the emergence of POP rICH in the multivariate analysis.
The LD is characteristically used for a variety of neurosurgical procedures including cerebral aneurysm. However, it should be used in only specific and selected conditions, and rapid and/or large amount of CSF drain through LD should be prevented and closely monitored. Additionally, while treating patients with any CSF drain routes, neurosurgeons should be aware of the possibility of POP rICH even after a smooth, uneventful, and successful procedure.
The authors would like to thank Prof. DP Jang (Hanyang University, Korea) for the contribution of statistical analysis and its interpretation.
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Here, we demonstrate and summarize potential pathogenesis and progress associated with the development of rICH and unknown, unidentified neurological conditions. The arrows and lines of dotted, and the arrow and relatively thinner line indicate low and moderate levels of possible pathogeneses, respectively. BP, blood pressure; CSF, cerebrospinal fluid; LD, lumbar drainage; SD, suction drainage. rICH, remote intracerebral hemorrhage.
Suggested pathogenesis of postoperative (POP) remote intracerebral hemorrhage (rICH) and other feasible neurological disorders or phenomena. CSF over-loss (hypovolemia) is the initial event and/or root cause which may trigger diverse neurological phenomena or complications including POP rICH. CSF, cerebrospinal fluid.
Demographic and clinical characteristics of patients with an LD and without an LD
Variables | LD(+) | LD(−) | |
---|---|---|---|
No. of patients (%) | 80 (11.6) | 608 (88.4) | |
Sex (Male:Female ratio) | 31:49 | 202:406 | 0.326 |
Age (years) | 0.057 | ||
Range | 26–67 | 20–79 | |
Mean | 49.88 | 52.52 | |
Hypertension history (%) | 36 (45.0) | 202 (33.2) | 0.037 |
Hunt-Hess grade (%) | 0.109 | ||
1 | 3 (3.7) | 52 (8.5) | |
2 | 40 (50) | 339 (55.8) | |
3 | 17 (21.3) | 116 (19.1) | |
4 | 15 (18.7) | 87 (14.3) | |
5 | 5 (6.3) | 14 (2.3) | |
Fischer grade (%) | 0.295 | ||
1 | 1 (1.2) | 4 (0.7) | |
2 | 10 (12.5) | 123 (20.2) | |
3 | 38 (47.5) | 290 (47.7) | |
4 | 31 (38.8) | 191 (31.4) | |
Location of aneurysms | 0.811 | ||
Anterior circulation | 69 | 524 | |
Posterior circulation | 1 | 14 | |
Multiple | 10 | 70 | |
Coagulopathy | 0 | 2 | 0.607 |
Surgery timing (%) | 0.021 | ||
Early operation | 63 (78.8) | 535 (88.0) | |
Delayed operation | 17 (21.2) | 73 (12.0) | |
Insertion of SD (%) | 77 (96.3) | 278 (45.7) | 0.000 |
H-H therapy (%) | 60 (75) | 408 (67.1) | 0.155 |
Values are presented as number (%, if necessary)
LD(+), Patients who underwent a perioperative lumbar drainage
LD(−), Patients who did not undergo a perioperative lumbar drainage
Operation performed within 72 hours after rupture of cerebral aneurysm
H-H therapy, Hypertensive-Hypervolemic therapy; SD, suction drainage
Comparison of clinical characteristics of POP rICH between patients with and without an LD
Variables | LD(+) | LD(−) | |
---|---|---|---|
No. of patients with rICH (%) | 10 (12.5) | 5 (0.8) | 0.000 |
Location of rICH | 0.591 | ||
Cerebellum | 9 | 4 | |
Contralateral to operative site | 3 | 1 | |
Ipsilateral to operative site | 4 | 1 | |
Bilateral hemispheres | 2 | 2 | |
Cerebral hemisphere | 1 | 1 | |
Contralateral to operative site | 1 | 1 | |
Treatment | 0.143 | ||
Conservative | 10 | 4 | |
Surgical | 0 | 1 | |
Outcome | 0.648 | ||
No residual neurologic deficits | 2 | 1 | |
Temporary neurologic deficits | 4 | 1 | |
Permanent neurologic deficits | 1 | 0 | |
Death | 3 | 3 | |
Suction drainage | 0.000 | ||
Yes | 10 | 5 | |
No | 0 | 0 |
Values are presented as number (%) if necessary
LD(+), Patients who underwent a perioperative lumbar drainage
LD(−), Patients who did not undergo a perioperative lumbar drainage
POP, Postoperative; rICH, remote intracerebral hemorrhage
Clinical features of patients who had an LD and developed rICH
Features | POP rICH (%) (n=10) | |
---|---|---|
Amount of drained CSF (%) | 0.040 | |
< 50 mL/day (n=41) | 4 (9.8) | |
50–100 mL/day (n=23) | 6 (26.1) | |
>100 mL/day (n=16) | 0 (0) | |
Duration of LD (%) | 0.026 | |
Only during surgery (n=7) | 3 (42.9) | |
1 day (n=38) | 3 (7.9) | |
2 days (n=4) | 2 (50) | |
3 days (n=6) | 0 (0) | |
4 days (n=5) | 0 (0) | |
5 days (n=6) | 0 (0) | |
6 days (n= 5) | 2 (40) | |
7 days (n=5) | 0 (0) | |
8 days (n=1) | 0 (0) | |
9 days (n=3) | 0 (0) | |
Hypertension history | 0.089 | |
Yes | 2 | |
No | 8 | |
Lumbar and suction drainage | 0.000 | |
Yes | 10 | |
No | 0 | |
Hypertensive-Hypervolemic | 0.089 | |
Yes | 8 | |
No | 2 |
Values are presented as number (%, if necessary)
Hypertensive-Hypervolemic, Hypertensive-Hypervolemic therapy
LD, lumbar drainage; POP, postoperative; rICH, remote intracerebral hemorrhage; CSF, cerebrospinal fluid
Evaluation of risk factors for postoperative rICH development in this study
Variables | rICH(+) | rICH(−) | |
---|---|---|---|
No. of patients (%) | 15 | 673 | |
Sex (Male: Female ratio) | 8:7 | 225:448 | 0.107 |
Age (years) | 0.433 | ||
Range | 28–70 | 20–79 | |
Mean | 49.87 | 52.27 | |
Hypertension history (%) | 0.057 | ||
Yes | 5 | 233 | |
No | 10 | 440 | |
Hunt-Hess grade (%) | 0.851 | ||
0 | |||
1 | 1 | 54 | |
2 | 7 | 372 | |
3 | 3 | 130 | |
4 | 3 | 99 | |
5 | 1 | 18 | |
Fischer grade (%) | 0.046 | ||
1 | 1 | 4 | |
2 | 2 | 131 | |
3 | 8 | 320 | |
4 | 4 | 218 | |
Coagulopathy | 0 | 2 | 0.833 |
Surgery timing (%) | 0.977 | ||
Early operation | 13 | 585 | |
Delayed operation | 2 | 88 | |
H-H therapy (%) | 0.089 | ||
Yes | 13 | 455 | |
No | 2 | 218 |
Values are presented as number
rICH(+), patients who developed remote intracerebral hemorrhage
rICH(−), patients who did not develop remote intracerebral hemorrhage
Early Operation, Operation performed within 72 hours after rupture of cerebral aneurysm
H-H, Hypertensive-Hypervolemic
Multivariate analysis for the clinical features of remote intracerebral hemorrhage
Variables | OR | 95% CI | |
---|---|---|---|
Sex (Female/Male) | 0.475 | 0.148–1.525 | 0.211 |
Age (years) | 0.998 | 0.958–1.038 | 0.905 |
Hunt-Hess Grade | 1.183 | 0.623–2.246 | 0.607 |
Fischer Grade | 0.477 | 0.215–1.059 | 0.248 |
Surgery timing (Early | 2.083 | 0.408–10.622 | 0.377 |
Hypertension history (No/Yes) | 1.208 | 0.410–3.559 | 0.732 |
Suction drainage insertion (No/Yes) | 0.000 | 0.000 | 0.994 |
Lumbar drainage insertion (No/Yes) | 0.112 | 0.035–0.356 | 0.0002 |
H-H therapy (No/Yes) | 0.344 | 0.074–1.607 | 0.175 |
Early, Operation performed within 72 hours after rupture of cerebral aneurysm
H-H, Hypertensive-Hypervolemic; OR, odd ratio; CI, confidence interval