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Acta Neurochir (Wien) (2005) 147: 1157–1162

DOI 10.1007/s00701-005-0584-5

Clinical Article
The risk of rebleeding after external lumbar drainage
in patients with untreated ruptured cerebral aneurysms

A. C. J. Ruijs1 , C. M. F. Dirven1 , A. Algra2 , I. Beijer2, W. P. Vandertop1 , and G. Rinkel2

1
Department of Neurosurgery, VU University Medical Center, Amsterdam, The Netherlands
2
Department of Neurology, University Medical Center Utrecht, Utrecht, The Netherlands

Received February 24, 2005; accepted June 1, 2005; published online July 25, 2005
# Springer-Verlag 2005

Summary related DCI [8, 10, 17, 25]. Ventricular drainage may
Background. Does continuous external lumbar CSF drainage before cause decrease of flow of fresh CSF through the basal
aneurysm repair in patients with aneurysmal subarachnoid hemorrhage cisterns [12, 23]. Therefore, drainage of CSF via a lumbar
increase the risk of rebleeding? external catheter would be a more efficient way to ‘‘wash
Method. The study population, consisting of 18 patients treated by
External Lumbar Drainage (ELD) after SAH before aneurysm repair,
out’’ the blood products from the cisterns than via a ven-
was compared with an independent control group of 324 SAH patients tricular catheter. To reach the maximal beneficial effect of
treated in another clinic. Control patients were selected for not being prevention of DCI, lumbar CSF drainage should start as
treated for the ruptured aneurysm yet and not having undergone any
early as possible after SAH. However, drainage before
form of CSF drainage during the exposure time in the case patients. We
calculated hazard ratios with the Cox regression model, adjusted for repair of the ruptured aneurysm may cause an increase
age, and clinical condition on admission and hydrocephalus. of transmural pressure over the aneurysm wall and there-
Findings. The cox regression analysis shows a non-adjusted hazard ra- fore a higher risk of a rebleed [18]. In some studies an
tio of 2.1 (95% CI 0.8 to 5.3) in the model with 5 rebleedings in 18 patients.
Adjustment for age, clinical condition on admission and hydrocephalus increased rebleed risk after CSF drainage before aneur-
did not alter the hazard ratio estimate importantly in either analyses. ysm repair has been reported [4, 11, 22] whereas others
Conclusions. An increased risk of rebleeding by external lumbar demonstrated an equal frequency of rebleed in groups
drainage in the acute phase after aneurysmal SAH could not be con-
firmed, but the data are too imprecise to rule out an increased risk. The
with and without CSF drainage [14, 15, 20]. In none of
potential benefits of early drainage should be weighed against the risks if these studies was the comparison between groups with
the aneurysm is not occluded before or early after the start of drainage. and without CSF drainage controlled for factors that
Keywords: Continuous CSF drainage; external lumbar drainage; determine the risk of rebleeding. Important factors that
SAH; ruptured aneurysm; rebleeding. determine the risk of rebleeding are duration of exposure
to CSF drainage, time lapse since onset of SAH and the
neurological status of the patient after initial hemorrhage,
Introduction
reflected in the WFNS score [1, 3, 7, 21]. In this study we
Delayed cerebral ischemia (DCI) and hydrocephalus compared the risk of rebleeding in patients with and with-
are among the most important factors that determine out- out external lumbar drainage while taking into account all
come after aneurysmal subarachnoid hemorrhage (SAH). known risk factors for rebleeding.
Commonly used methods to treat hydrocephalus in the
acute phase of SAH are lumbar punctures and in case of
Methods and materials
ventricular or parenchymal hemorrhage continuous drain-
age of CSF by a ventricular drain. Continuous drainage of Study population
CSF and blood and its products from the arachnoid cis- Between 1995 and 1997, 107 patients with aneurysmal SAH were
terns after SAH may decrease the risk of vasospasm- admitted to the VU University Medical Center, Amsterdam, The
1158 A. C. J. Ruijs et al.

Netherlands. The clinical diagnosis of SAH was confirmed by the pre- ventricular system measured on CT, moment and duration of ELD inser-
sence of extravasated blood in the basal cisterns on a CT scan or, if the tion calculated from onset of SAH, occurrence of a rebleed, timing of
CT was negative, on xanthochromia of cerebrospinal fluid. Conventional treatment of aneurysm, and death. Hydrocephalus was measured by means
angiography, CT- or MR angiography were performed to detect an of the relative bicaudate index [4]. We quantified the size of the frontal
aneurysm. If angiography could not be performed, a patient was con- horns of the lateral ventricles by means of the bicaudate index (BCI) on all
sidered to have an aneurysmal SAH if the CT scan showed a typical CT’s made within 72 hours after SAH. To calculate age-adjusted relative
aneurysmal pattern of haemorrhage. To treat symptoms of increased sizes, the bicaudate indexes were divided by the corresponding upper limit
intracranial pressure, 18 patients received an external lumbar drain per age group (95th percentile for age). Hydrocephalus was defined as an
(ELD) before surgical or endovascular aneurysm repair, in some cases age-adjusted relative BCI above 1. Acute hydrocephalus was considered
preceded or followed by external ventricular (EV) drainage. Nineteen to be present if any of the CT scans performed within the first 72 hours
patients who received EV drainage only and 70 patients who did not after the hemorrhage met these criteria.
undergo CSF drainage before aneurysm repair, were excluded from this
study. The indication for ELD treatment in this cohort of patients was the
presence of severe headache or other symptoms of elevated intracranial Evaluation of rebleeding
pressure, such as lowered consciousness, in combination with enlarged Rebleeding was defined as a sudden clinical deterioration with evi-
ventricles on CT but without intraventricular extension of the haemor- dence of new blood on a CT scan in comparison with a previous scan. To
rhage. In cases of intraventricular extension of the haemorrhage an assess the risk of rebleeding, the duration of ELD-drainage was re-
external ventricular drain was inserted. Insertion of an external lumbar corded. The exposure time is the time period between insertion of the
drain was typically performed by an experienced neurosurgeon. Care was ELD and the endpoint. The endpoint is defined as the moment when one
taken to avoid outflow of large amounts of CSF by means of an initial of the following events occurred: rebleeding, removal of ELD, insertion
outflow level of 20 cm. above Monro, which would be lowered to 15 cm of other CSF draining method (EVD, LP), repair of aneurysm (surgical
after 24 hours and a draining volume of maximally 10 ml CSF=hour. or endovascular) or death. Time is measured in 6 hour periods or
quarters of days, the day of SAH is defined as day 0 (Fig. 1).

Data collection
Control group
Characteristics and clinical data of the patients were collected, with
special attention to the time of initial SAH, clinical grade according to the To acquire a control group, we used the database of a consecu-
World Federation of Neurological Surgeons (WFNS) scale [2], size of tive series of 546 patients with aneurysmal SAH admitted from 1993

Fig. 1. Time lines of patients undergoing external lumbar drainage. This Fig. shows the data of the individual patients. Legend: # marks insertion of
the ELD. The time-period of lumbar drainage is measured until one of the following events occurred: " removal of the ELD,  Surgical or
endovascular definitive aneurysm treatment, r rebleeding from ruptured aneurysm or y Death.  Insertion and  removal of other CCSF drainage
method. The patients with a rebleed during lumbar drainage are marked with an  . @ Rebleed caused by unintended over drainage
Lumbar drainage after SAH and risk of rebleeding 1159

through 2000 within 72 hours after aneurysmal SAH to the Department Table 2. Characteristics of patients with rebleeding in ELD group
of Neurology of the University Medical Center Utrecht (UMCU). The
first criterion used to find controls in the UMCU database was the Number Age Gender Location WFNS Hypertension
moment and duration of exposure to CSF drainage, thus control patients
3 78 F A comm. 4 yes
who had not yet been treated for the ruptured aneurysm and had not
8@ 54 M A comm. 1 yes
undergone any form of CSF drainage (ventricular drainage, lumbar
10 51 F P comm. 4 no
puncture etc.) during the exposure time in the case patients. Secondly,
12 72 F P comm. 2 no
we selected those with a WFNS score as close as possible to the WFNS
13 76 F A comm. 4 no
score of the ELD patient.
This table shows the characteristics of the 5 patients in which rebleeding
occurred. Location describes the location of the ruptured aneurysm
Data analysis
(anterior communicating artery or posterior communicating artery).
To assess the relative risk of rebleeding in the patients treated with Patient number 3 and 8 had a medical history for hypertension. In
ELD as compared with the matched control group we first calculated the number 8 (@), a rebleed occurred after unintended drainage of a large
cumulative incidence ratio based on the tabular data. In order to account amount of CSF during induction of anesthesia for the clipping procedure.
for the time of follow-up for each patient, a hazard ratio was computed
with the Cox regression model. For that purpose exposure time was
taken as the time variable. Precision of the hazard ratio estimate was Table 3. Results of Cox regression analysis for risk of rebleeding (for 4
described with a 95% confidence interval, also derived from the Cox and 5 rebleeds respectively)
model. To address potential incomparability with regard to covariates
known to be related to the risk of rebleeding (age, clinical condition on Model 4 rebleeds 5 rebleeds
admission and hydrocephalus) between the ELD patients and their Exp (95% CI) Exp (95% CI)
matched controls adjusted hazard ratios were calculated. Non-adjusted 1.7 (0.6–4.7) 2.1 (0.8–5.3)
WFNS 1.5 (0.5–4.1) 1.9 (0.7–4.7)
Age 1.7 (0.6–4.9) 2.2 (0.9–5.5)
Results Hydrocephalus 1.7 (0.6–4.7) 2.1 (0.8–5.3)
WFNS þ Age þ HC 1.5 (0.5–4.4) 2.0 (0.8–5.0)
The characteristics of the patient group and the control WFNS þ Age 1.5 (0.5–4.4) 2.0 (0.8–5.0)
group are shown in Table 1. The study population consists
These are the results of the cox-regression analysis. The non-adjusted
of the 18 patients treated by external lumbar drainage. model has been adjusted for several variables: WFNS, age and the
There were 12 female (67%) and 6 (33%) male patients presence of hydrocephalus on the first CT-scan. The adjustments do
with an average age of 59 years (range 30–78). Six patients not have a strong influence on the significance of the results. Furthermore,
the first column shows the analysis with 4 rebleeds, assuming that one
were in poor neurological condition on arrival (WFNS
rebleeding could have been prevented using a strict protocol. In the second
grade IV and V). The time from aneurysmal bleeding un- column the results of the analysis are shown for all of the 5 rebleeds. The
til insertion of the ELD averaged 3.9 days (0.25–16 days). results do not differ significantly between these two groups.
The duration of lumbar drainage averaged 3.9 days (range
0.25–19 days). Four of 18 patients had a rebleed during the the basis of 5 patients with rebleeding in the ELD group,
period of external lumbar drainage (Table 2) and 44 of the which includes the patient with the adverse event, and a
324 control patients during the exposure time interval. A second on the basis of 4 patients with rebleeding in the
fifth patient had a rebleeding during induction of anesthe- ELD group. The Cox regression analysis shows a non-
sia for a clipping procedure, after unintended excessive adjusted hazard ratio of 2.1 (95% confidence interval
drainage of CSF due to an accidentally open drain with 0.8 to 5.3) in the first analysis (with 5 patients with ELD
the reservoir at a level of 60 cm below the head of the and rebleeding) and 1.7 (95% CI 0.6–4.7) in the sec-
patient. We performed two different analyses: a first on ond analysis (with 4 patients with ELD and rebleeding).
Adjustment for age, clinical condition on admission and
Table 1. Characteristics of the study population versus the control
hydrocephalus did not alter the hazard ratio estimate im-
group
portantly in either analyses (Table 3).
Variable ELD group Control group

Number 18 324
Mean age (SD) 59 (14.2) 56 (13.7)
Discussion
Male (percentage) 6 (33%) 98 (30%)
Drainage of CSF in the acute phase after SAH is a
Hydrocephalus present 9 (50%) 164 (51%)
on first CT-scan well-accepted treatment for acute hydrocephalus and
WFNS Grade I & II 8 (45%) 188 (58%) increased intracranial pressure. However, continuous
– Grade III 4 (22%) 32 (10%) drainage of CSF in the acute phase after SAH, before
– Grade IV & V 6 (33%) 104 (32%)
aneurysm repair, is generally thought to be associated
Rebleed (percentage) 4 or 5 (22% or 28%) 44 (14%)
with an increased risk of aneurysm rebleeding. In this
1160 A. C. J. Ruijs et al.

Table 4. Studies on CSF drainage before treatment of the ruptured aneurysm

Author Study design Drainage group Control group Results


N (rebleeding %) N (rebleeding %)

Van Gijn 1985 [4] pre-op VD, Acute HC, TA 9 (44%) 25 (8%) 5.5X
Hasan 1989 [6] pre-op VD 32 (43%) 441 (15–20%) 2–3X
Kawai 1997 [11] pre-op VD, grade V WFNS 28 (54%) 39 (21%) 2.5X
Kusske 1973 [14] pre-op VD 11 (0%) 9 (0%) matched ¼
McIver 2002 [15] pre-op VD >24 h before repair 45 (4.4%) 259 (5.4%) ¼
Milhorat 1987 [16] pre-op EVD 35 (0%) 165 (0%) ¼
Ochiai 2001 [20] pre-op LD (þ15 cm Monro) 33 (9%) 17 (12%) ¼
Pare 1992 [22] pre-op VD 20 (30%) 108 (8%) 2.5X#
Raimondi 1973 [23] pre-op shunting (VP=VJ) 21 (52%) – 
Rajshekar 1992 [24] pre-op VD, 9x in OR or after repair 52 (14%) – 

In study design the setup of the research is explained. For example the first study administered Ventricular Drainage in patients with acute
Hydrocephalus. Their patients were also included into a clinical study for the effects of tranexamic acid. Results show the multiplication factor of
rebleeding in the drainage group compared to the control group. Footnotes: There was no difference in rebleeding rate between the two groups; # the
association of ventricular drainage with rebleeding was limited to patients with severe hydrocephalus and  significant improvement of clinical status
after drainage. Legend. LD Lumbar Drainage, VD Ventricular Drainage, EVD External Ventricular Drainage, TA Tranexamic acid trial, VP
Ventriculoperitoneal, VJ Ventriculojugular.

study we could not confirm an increased risk of rebleed- The significance strength of our study is that it eval-
ing from continuous drainage by ELD in patients with uates rebleeding risks after continuous drainage while
unrepaired aneurysms. taking into account the timing since SAH and the dura-
Several studies have addressed the effects of contin- tion of the drainage, and also the clinical condition on
uous CSF drainage after SAH on the risk of rebleeding admission, amount of extravasated blood, and ventricu-
(Table 4). Some studies claim a higher rate of rebleeding lar size. Furthermore, in this study the case group and
after continuous ventricular or lumbar drainage [4, 6, 11, control group are derived from two different treating
22] whereas other studies provide no evidence of a centers in which other treatment strategies for SAH
higher rebleeding risk [14–16, 20, 24]. Assessment of patients are similar. Although the numbers of patients
the rebleeding risk in groups of patients with or without treated by continuous drainage before aneurysm occlu-
drainage of CSF requires careful control for factors that sion is relatively large, in an absolute sense the numbers
determine the rebleeding risk in both groups. Time lapse are too small to provide very precise estimates. Although
since onset of the SAH is a very important factor in the in this study an increased risk for rebleeding after con-
risk of rebleeding. The rebleeding rate is highest on the tinuous CSF drainage with ELD before aneurysm repair
day of the initial hemorrhage, then diminishes, and could not be confirmed, an increased risk could not be
increases slightly again during the second week [1]. ruled out either.
Four studies found no increased risk of rebleeding from Continuous CSF drainage after SAH has recently
continuous CSF drainage. In 2 of these studies aneur- gained new interest as a means of removal of cisternal
ysms were repaired acutely [14, 16], in a third the mean blood, thus decreasing the occurrence of DCI [12]. Also
time interval between ventriculostomy and repair of the use of continuous cisternal drainage in the post-
aneurysm was 3.8 days [15]. In the fourth rebleeding operative period, often combined with fibrinolytic local
after lumbar drainage occurred in 3 of 33 patients, in 1 therapy has been reported to decrease the risk of DCI
patient 7 hrs after drain insertion and in the other 2 after [13]. Furthermore, it has been shown in animal models
4 and 5 days respectively [20]. Other factors that deter- that removal of blood clots from the basal cisterns in
mine the rebleeding risk are clinical condition on admis- order to reduce the risk of DCI needs to be performed at
sion, amount of extravasated blood, and hydrocephalus. a very early stage after SAH [5, 19]. These observations
In one study the observation of increased rebleeding risk support a possible role for early continuous CSF drain-
in patients with ventricular drains was limited to patients age by ELD before aneurysm repair. The results of our
with severe hydrocephalus, defined by radiological cri- study indicate that the potential benefits of early drain-
teria with a cerebral-ventricular index greater than the age should be weighed against the risks if the aneurysm
95th percentile [22]. is not occluded before or early after the start of drainage.
Lumbar drainage after SAH and risk of rebleeding 1161

In one patient a rebleed occurred under circumstances 11. Kawai K, Nagashima H, Tamura A, Sano K (1997) Efficacy and risk
of ventricular drainage in cases of grade V subarachnoid hemor-
of unintended over drainage. During induction of an- rhage. Neurol Res 19: 649–653
esthesia the external drain reservoir was accidentally 12. Klimo P Jr, Kestle JR, MacDonald JD, Schmidt RH (2004) Marked
lowered to a very low level below the patients head reduction of cerebral vasospasm with lumbar drainage of cere-
brospinal fluid after subarachnoid hemorrhage. J Neurosurg 100:
and had drained a large amount of CSF within an hour
215–224
time. This serious adverse event shows the necessity of 13. Kodama N, Sasaki T, Kawakami M, Sato M, Asari J (2000)
caution in handling patients with an external CSF drain. Cisternal irrigation therapy with urokinase and ascorbic acid for
prevention of vasospasm after aneurysmal subarachnoid hemor-
Extreme care must be taken to prohibit over drainage
rhage. Outcome in 217 patients. Surg Neurol 53: 110–117
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8. Inagawa T, Kamiya K, Matsuda Y (1991) Effect of continuous This is a well written and interesting paper. The authors are correct
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28: 56–59 continuous drainage while taking into account its timing since aneurysm
1162 A. C. J. Ruijs et al.: Lumbar drainage after SAH and risk of rebleeding

rupture, the duration of the lumbar drainage, the clinical condition on ‘‘drained’’ group =WFNS Grade III, IV, V= – rebleeding is common in
admission, the amount of extravasated blood, and the ventricular size. It the acute stage, and in severe conditions!).
would also enforce the conclusion of the authors that the group having An increased risk of rebleeding due to insertion of lumbar drainage
undergone lumbar drainage and the control group were derived from two before aneurysm closure could not be confirmed or excluded.
different treating departments in which other treatment strategies for T. Doczi
SAH patients were similar. Pecs
Unfortunately, the number of patients treated with continuous drain-
age before aneurysm occlusion was relatively small to provide very Correspondence: Clemens M. F. Dirven, VU University Medical
precise prognostic estimates. (Drainage was started in the acute stage Center, Department of Neurosurgery, P.O. Box 7057, 1007 MB
of SAH only in 10 out of 18; there were more severe patients in the Amsterdam, The Netherlands. e-mail: C.Dirven@vumc.nl

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