Kulkarni 1998

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J Neurosurg 89:31–35, 1998

Incidence of silent hemorrhage and delayed deterioration


after stereotactic brain biopsy

ABHAYA V. KULKARNI, M.D., ABHIJIT GUHA, M.D., ANDRES LOZANO, M.D.,


AND MARK BERNSTEIN, M.D., F.R.C.S.(C)

Division of Neurosurgery, Toronto Hospital, Toronto, Ontario, Canada; Department of Surgery,


University of Toronto, Toronto, Ontario, Canada

Object. Many neurosurgeons routinely obtain computerized tomography (CT) scans to rule out hemorrhage in
patients after stereotactic procedures. In the present prospective study, the authors investigated the rate of silent
hemorrhage and delayed deterioration after stereotactic biopsy sampling and the role of postbiopsy CT scanning.
Methods. A subset of patients (the last 102 of approximately 800 patients) who underwent stereotactic brain biop-
sies at the Toronto Hospital prospectively underwent routine postoperative CT scanning within hours of the biopsy
procedure. Their medical charts and CT scans were then reviewed.
A postoperative CT scan was obtained in 102 patients (aged 17–87 years) who underwent stereotactic biopsy
between June 1994 and September 1996. Sixty-one patients (59.8%) exhibited hemorrhages, mostly intracerebral
(54.9%), on the immediate postoperative scan. Only six of these patients were clinically suspected to have suffered a
hemorrhage based on immediate postoperative neurological deficit; in the remaining 55 (53.9%) of 102 patients, the
hemorrhage was clinically silent and unsuspected. Among the clinically silent intracerebral hemorrhages, 22 measured
less than 5 mm, 20 between 5 and 10 mm, five between 10 and 30 mm, and four between 30 and 40 mm. Of the 55
patients with clinically silent hemorrhages, only three demonstrated a delayed neurological deficit (one case of seizure
and two cases of progressive loss of consciousness) and these all occurred within the first 2 postoperative days. Of the
neurologically well patients in whom no hemorrhage was demonstrated on initial postoperative CT scan, none experi-
enced delayed deterioration.
Conclusions. Clinically silent hemorrhage after stereotactic biopsy is very common. However, the authors did
not find that knowledge of its existence ultimately affected individual patient management or outcome. The authors,
therefore, suggest that the most important role of postoperative CT scanning is to screen for those neurologically
well patients with no hemorrhage. These patients could safely be discharged on the same day they underwent
biopsy.

KEY WORDS • intracranial hemorrhage • complications • stereotactic biopsy •


computerized tomography scanning

HE use of stereotactic biopsy sampling in the man- review of early symptomatic complications following
T agement of intracranial lesions has been well estab-
lished. However, this relatively less invasive proce-
dure is associated with complication rates ranging from
stereotactic biopsy, which has already been well docu-
mented in previous studies.1,2,5,8,10,12–17
1.2 to 7.2%.1,2,5,8,10,12–17 Given these significant numbers, it
is not an uncommon practice for many neurosurgeons to Clinical Material and Methods
obtain computerized tomography (CT) scans routinely
after uncomplicated stereotactic biopsies. However, there At the Division of Neurosurgery at the Toronto Hospital
is little in the literature to support this practice. To study between June 1994 and September 1996, 102 patients (51
the diagnostic and, ultimately, the therapeutic yield of this men and 51 women) with a mean age of 56.8 years (range
practice, we prospectively obtained CT scans immediate- 17–87 years) in whom frame-based stereotactic biopsies
ly following all frame-based stereotactic biopsies in pa- were obtained prospectively underwent CT scanning
tients beginning in June 1994 and compiled our cumula- within hours of their procedure. All biopsies were per-
tive results. We looked specifically at those patients who formed by surgeons with special expertise and experience
initially had a clinically silent hemorrhage and whether in stereotactic technique and represented only the most
they went on to experience delayed deficit in any pre- recent in a series totaling nearly 800 cases. The systems
dictable fashion. This was not intended to serve as a used were the Brown-Roberts-Wells (Radionics, Burling-

J. Neurosurg. / Volume 89 / July, 1998 31


A. V. Kulkarni, et al.

TABLE 1 TABLE 2
Pathological diagnosis of lesions in 102 patients who underwent Incidence of hemorrhage on routine postoperative CT scans in
stereotactic brain biopsy 102 patients who underwent stereotactic brain biopsy
Diagnosis No. of Patients No. of Patients (%)
Type of
neoplastic 90 Hemorrhage All Hemorrhages Silent Hemorrhages
high-grade astrocytoma 49
low-grade astrocytoma 17 intracerebral
metastasis 9 ,5 mm 23 (22.5) 22 (21.6)
lymphoma 9 5–10 mm 21 (20.6) 20 (19.6)
oligodendroglioma 4 10–30 mm 7 (6.9) 5 (4.9)
other 2 30–40 mm 5 (4.9) 4 (3.9)
infectious 4 subarachnoid 3 (2.9) 2 (2.0)
infarction 1 subdural 1 (1.0) 1 (1.0)
other 4 intraventricular 1 (1.0) 1 (1.0)
nondiagnostic 3 total 61 (59.8) 55 (53.9)

ton, MA), Cosman-Roberts-Wells (Radionics), or Leksell five (8.9%) between 30 and 40 mm (Table 2). Associated
(AB Elekta Instruments, Stockholm, Sweden) stereotactic with these intracerebral hemorrhages were four intraven-
frame systems; all were used with CT guidance. The tech- tricular hemorrhages, two subarachnoid hemorrhages, and
nique of skull penetration was by burr hole or twist drill, one subdural hematoma. In all such cases, the intracere-
based on the surgeon’s preference. A direct trajectory bral component was the major hemorrhage and, therefore,
through a single pial surface was chosen and almost never these seven are listed under intracerebral hemorrhage in
involved transgression of an ependymal surface. All bi- Table 2. There were also three patients with isolated sub-
opsies were performed with a side-cutting needle. Pro- arachnoid hemorrhage, one patient with isolated intraven-
cedures were performed after the patient had been admin- tricular hemorrhage, and one patient with isolated subdu-
istered a local anesthetic agent; this was occasionally ral hematoma.
supplemented with intravenous sedation. Routine preop- Among the more common pathological conditions as-
erative blood work included a platelet count in all cases, sociated with the hemorrhages, postoperative hemorrhage
but further coagulation screening was only performed was seen in 31 (63%) of 49 high-grade astrocytomas,
when clinically indicated. eight (47%) of 17 of low-grade astrocytomas, four (44%)
We reviewed the CT scans and compared preoperative of nine metastases, and four (44%) of nine lymphomas.
and postoperative images. New hemorrhages were classi- The average number of needle biopsy samples taken
fied by location (intraparenchymal, intraventricular, sub- per case was 1.68 (range 1–8). In those cases with post-
arachnoid, subdural, or epidural) and by size (maximum operative hemorrhage, the mean was 1.82 and in those
diameter for intraparenchymal and maximum thickness with no hemorrhage the mean was 1.46. This difference
for subdural or epidural). The clinical charts of all patients did not achieve statistical significance (p = 0.479 using the
were also reviewed to determine if there was any new Mann–Whitney rank-sum test).
neurological deficit associated with the stereotactic pro- Nine patients (8.8%) experienced an early postopera-
cedure. tive neurological deficit, which was defined as a deficit
Patients in whom stereotaxy was performed for func- that presented within hours of the procedure and was pres-
tional procedures, Ommaya reservoir insertion, ventricu- ent at the time of initial postoperative CT scanning. Three
loperitoneal shunt placement, brachytherapy, or cranioto- of the nine patients had no hemorrhage on their post-
my planning were excluded from the study. operative CT and their deficit was attributed to increased
tumor edema and mass effect. Six patients had a new neu-
rological deficit that was associated with postoperative
Results hemorrhage (Table 3). One of these patients, who initially
All 102 patients underwent framed-based stereotactic had left-sided hemiparesis associated with a 20-mm hem-
biopsies and postoperative CT scanning. Preoperative co- orrhage, went on to experience delayed decreased level of
agulation testing revealed only one abnormal result in a consciousness on the 5th postoperative day. At that time
patient with an International Normalized Ratio (INR) of CT scanning revealed evidence of significant new he-
1.46 (normal 0.9–1.1). The technique of skull penetration morrhage. That patient improved after a period of obser-
was by burr hole in 22 patients and by twist drill in 80 pa- vation only.
tients. The pathological characteristics of the lesions that Fifty-five patients who experienced postoperative hem-
were obtained by biopsy sampling are listed in Table 1. orrhages were neurologically unchanged. This group in-
In 41 patients (40.2%) there was no new hemorrhage cluded nine patients with hemorrhages measuring be-
seen on the initial postoperative CT scan. There were a tween 10 and 40 mm (Table 2). The patient with an INR
total of 61 patients (59.8%) in whom hemorrhage was of 1.46 experienced an asymptomatic 5- to 10-mm hem-
visualized on postoperative imaging. Of the 56 hemor- orrhage.
rhages that were intraparenchymal, 23 (41.1%) were less Of the 55 patients who experienced clinically silent
than 5 mm in maximum diameter, 21 (37.5%) between 5 hemorrhages, three developed a delayed neurological
and 10 mm, seven (12.5%) between 10 and 30 mm, and deficit, which was defined as the onset of a new neuro-

32 J. Neurosurg. / Volume 89 / July, 1998


Hemorrhage after biopsy

TABLE 3
Early new neurological deficit associated with hemorrhage in six
patients who underwent stereotactic brain biopsy*
Hemorrhage
Deficit Lesion Size & Location Treatment

increased dysphasia GBM 20 mm, lt temporal observed


decreased LOC MA 40 mm, rt frontal urgent craniotomy,
died
increased confusion MA 10 mm, para–third observed
ventricle
lt leg numbness MA ,5 mm, rt parietal observed
lt hemiparesis GBM 20 mm, rt frontal rebleeding on Day
5, observed FIG. 1. Case 1 from Table 4. Preoperative magnetic resonance
decreased LOC MA massive SAH observed images obtained in a 50-year-old man who presented with seizure
* GBM = glioblastoma multiforme; LOC = level of consciousness; MA = but had no gross neurological deficit. Coronal T1-weighted
malignant astrocytoma; SAH = subarachnoid hemorrhage. gadolinium-enhanced (left) and axial T2-weighted (right) images
showing right frontal oligodendroglioma.

logical deficit beginning after the day of surgery (Table 4). patients with no hemorrhage on the initial postoperative
Case 1 from Table 4 serves as an illustrative example. This CT scan, there were no delayed deteriorations. Therefore,
50-year-old man originally presented with a right frontal of the population of patients who initially were well, with
mass (Fig. 1), but was neurologically intact. He underwent no new neurological deficit (93 patients), the positive pre-
biopsy sampling of what proved to be an oligodendro- dictive value of the initial postoperative CT scan in fore-
glioma. He was neurologically intact postoperatively; casting delayed deterioration was only 5.5%. However,
however, a routine CT scan revealed a 35-mm right frontal the negative predictive value was 100%.
hemorrhage (Fig. 2). On the 1st postoperative day he de-
veloped a seizure, which was easily controlled. Repeated Discussion
CT scanning at that time revealed some increase in the
size of the hemorrhage (Fig. 3); the patient was observed Many neurosurgeons routinely obtain CT scans in pa-
in the hospital for 6 uneventful days, after which he was tients in an attempt to detect occult hemorrhages after
discharged home. uncomplicated stereotactic biopsy. The diagnostic yield in
The patient in Case 2 from Table 4 also had evidence of detecting these occult bleeds is not well known. More
significant new hemorrhage that coincided with his dete- important, one must ask the question: does the finding of
rioration on postoperative Day 1. The patients in Cases 1 an occult hemorrhage have any significant effect on pa-
and 3 were successfully managed with observation alone, tient management or outcome? There is little information
whereas no aggressive therapy was given to the patient in available in the literature regarding this practice.
Case 2 because of his overall poor prognosis; that patient
died shortly thereafter.
There were a total of two biopsy-related deaths in this
group of patients for a mortality rate of 2%.
Overall, the rate of delayed deterioration after stereo-
tactic biopsy was found to be 3.9% (four of 102). The inci-
dence of delayed deterioration after an initially silent hem-
orrhage was 5.5% (three of 55). In neurologically well

TABLE 4
Delayed neurological deficit after silent hemorrhage in three
patients who underwent stereotactic brain biopsy*
Age Initial Hemor-
Case (yrs), Deficit & Pathological rhage Size Treatment
No. Sex Time Condition & Location & Outcome

1 50, M seizure, oligodendro- 35 mm, rt observed,


POD 1 glioma frontal recovered
2 66, M decreased glioblas- 5–10 mm, comfort mea-
LOC, toma rt parietal sures only,
POD 1 died
3 49, F decreased epidermoid 25 mm, lt observed,
LOC, cyst temporal recovered
FIG. 2. Case 1 from Table 4. Initial CT scan obtained hours after
POD 2
biopsy showing a 35-mm hemorrhage. At this time, the patient did
* LOC = level of consciousness; POD = postoperative day. not demonstrate any neurological deficit.

J. Neurosurg. / Volume 89 / July, 1998 33


A. V. Kulkarni, et al.

Uniqueness of the Present Study


The present report represents the first study in which
the true rate of asymptomatic hemorrhage following
stereotactic biopsy was specifically investigated. In this
prospective study of 102 patients, there was, indeed, a
very significant rate of occult, clinically silent hemorrhage
(53.9%), although the majority were very small. At first
glance, this result appears disturbingly high, especially in
the context of most previous studies of stereotactic biopsy
in which hemorrhage and complication rates have been
reported to be below 7 or 8%.1,2,5,8,10,12–17 In fact, in two pre-
vious large, retrospective reviews from this institution a
major morbidity rate of 3% and an overall complication
rate of 6.3% have been reported.2,16 However, the results of
the present study cannot be fairly compared on a purely
quantitative basis with prior results because no previous
study contained a report of every single small, asymp-
tomatic hemorrhage following biopsy. Also, we would not
use the term “complication,” as it has been traditionally
FIG. 3. Case 1 from Table 4. A CT scan obtained on postopera- used, to describe a clinically insignificant hemorrhage.
tive Day 1, after the patient had suffered a seizure, showing evi-
dence of some new hemorrhage with intraventricular extension.
The patient was successfully managed conservatively and was dis- Clinical Relevance of Silent Hemorrhage
charged on postoperative Day 6. Despite the high incidence of postoperative hemorrhage
in our patients, we found that the ultimate clinical impact
of this finding was virtually nil. In three patients with
Incidence Rates in the Literature initially clinically silent hemorrhage, there did develop
The early reports on experience with CT-guided needle delayed clinical deterioration. However, in two of these
biopsies presented some data on the incidence of hemor- patients (Cases 1 and 2 from Table 4) neurological deteri-
rhage following needle placement into the brain, with oration occurred within the 1st postoperative day. Even if
asymptomatic hemorrhages ranging from 0% to 40% in a postoperative CT scans had not been obtained in these
few small series.6,7,11 These procedures, of course, are very patients, their clinical deterioration would have alerted the
different from modern stereotaxy and the results cannot be surgeon while the patients were still in the hospital, be-
reliably extrapolated. cause it was routine practice to keep all patients in the hos-
In modern larger series of stereotactic biopsies, compli- pital for at least 1 day postoperatively. Also, both patients
cation rates range from 1.2 to 7.2%.1,2,5,8,10,12–17 However, in underwent repeated CT scanning at the time of their dete-
all previous studies, only symptomatic complications and rioration, and this certainly would have been performed
hemorrhages were considered. The authors of very few regardless of whether an initial postoperative CT scan had
series even considered asymptomatic hemorrhage as a been obtained. Of further interest is the fact that the CT
reportable event. Voges and colleagues17 found eight post- scan obtained at the time of deterioration in both cases
operative hemorrhages in a series of 338 patients; three showed significant interval increase in hematoma size that
were asymptomatic. Levin9 reported three asymptomatic could not have been predicted based on the initial postop-
hemorrhages in 87 stereotactic biopsies. However, al- erative CT scan. Three additional patients had silent hem-
though not specified, it appears that postoperative CT orrhages similar in size to the one found in the patient in
scans were obtained only in patients in whom there was Case 1; 19 patients had silent hemorrhages similar in size
intraoperative suspicion of bleeding. Bullard, et al.,3 re- to the one found in the patient in Case 2; and four patients
ported finding five small (3–7 mm), asymptomatic hem- had silent hemorrhages similar in size to the one found in
orrhages on 11 postbiopsy CT scans from a series of 44 the patient in Case 3. None of these patients suffered any
patients. In another series, Bullard and associates4 found delayed deterioration. In all such cases, the delayed deficit
that, of four postoperative CT scans obtained because of was either minor and transient or was associated with a
patient complaints of headache or to confirm biopsy loca- hopeless prognosis, rendering all cases suitable for con-
tion, the majority showed evidence of hemorrhage. How- servative management alone. This appears to be the hall-
ever, Niizuma, et al.,13 reported only four cases of asymp- mark characteristic of patients with delayed deterioration
tomatic hemorrhage in a series of 121 biopsies. Clearly after biopsy.
there is no consensus in the literature regarding the fre- Only one patient in the entire series required a cra-
quency of silent hemorrhage. The problem inherent in niotomy for an intracerebral hemorrhage that ultimately
almost all of these series is that the indications for obtain- proved to be fatal. In this case the patient’s clinical deteri-
ing postoperative CT scans were not given and it is not oration was obvious immediately postoperatively, prior to
clear whether all asymptomatic hemorrhages were, in fact, his undergoing routine postoperative CT scanning. This
reported. In no previous study has the frequency of silent likely echoes the experience of most neurosurgeons, in
hemorrhage been considered in the context of a rigid, that those cases in which craniotomy for postbiopsy hem-
prospective study protocol. orrhage is required declare themselves very early in the

34 J. Neurosurg. / Volume 89 / July, 1998


Hemorrhage after biopsy

postoperative course. Those cases in which the patients do pling does not add significantly to patient management or
well initially, although subject to a small incidence of outcome and is not recommended if the results will not
delayed deterioration, usually require only conservative affect earlier discharge policy. The role of early CT scan-
management. ning in selecting patients who are safe for same-day dis-
charge is attractive, both medically and financially, and
Pathological Conditions may be an important aspect of postbiopsy CT scanning in
Among the more common pathological conditions, it the future.
appeared that high-grade astrocytomas had the greatest
tendency to bleed (63%). Low-grade astrocytomas, metas- References
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Manuscript received December 2, 1997.
Conclusions Accepted in final form March 3, 1998.
Address reprint requests to: Mark Bernstein, M.D., F.R.C.S.(C),
Based on our present experience, we believe that ob- Division of Neurosurgery, Toronto Hospital, Western Division, 399
taining a CT scan after routine stereotactic biopsy sam- Bathurst Street, Toronto, Ontario, M5T 2S8 Canada.

J. Neurosurg. / Volume 89 / July, 1998 35

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