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ORIGINAL
The risk of hemorrhage in stereotactic biopsy for brain tumors
Yoshifumi Mizobuchi(1), Kohei Nakajima(1), Toshitaka Fujihara(1), Kazuhito Matsuzaki(2), Hideo Mure(1),Shinji Nagahiro(1), and Yasushi Takagi(1)Department of Neurosurgery, Institute of Biomedical Sciences Tokushima University Graduate School, Tokushima, Japan, (2)Department of
Neurosurgery, Tokushima Red Cross hospital, Tokushima, Japan(1)

Abstract : Objective : One major complication associated with STB is intratumoral hematoma, which is also themost common cause of morbidity related to permanent paralysis and mortality in STB. The risk of perioperative
hemorrhage is generally between 1% and 10%, but this could be an underestimation since it is not common formany neurosurgeons to perform CT scans after uncomplicated STBs. In this study, we describe the incidence of
cerebral hemorrhage, including asymptomatic cerebral hemorrhage. Methods : We recently reviewed data on the
diagnosis rate and occurrence of complications, including symptomatic and asymptomatic cerebral hemorrhage,in 80 patients who underwent STB at our facility between 2005 and 2014. Results : Histological diagnosis wasestablished for 75 cases (93.8%), glioma was the most frequently encountered tumor. Symptomatic hemorrhage
was observed in two cases (2.6%), with the symptoms subsiding within two days. The morbidity and mortality
rate was 0%. However, asymptomatic hemorrhages were observed in 23 cases (28.8%). Conclusion : Stereotactic
biopsy is a less invasive procedure for obtaining samples of brain tumors for diagnosis. The bleeding of the tissue-resection cavity that includes asymptomatic hemorrhage occurs at a constant rate. It is important to reduce
the symptomatic bleeding associated with stereotactic biopsy. J. Med. Invest. 66 : 314-318, August, 2019
Keywords : stereotactic biopsy, silent hemorrhage, intratumoral hematoma

INTRODUCTION
Therapeutic strategies for intracranial mass lesions are mosteffective when based on histopathological diagnoses, rather
than upon clinical and radiographic findings alone(4). When thelesions are strongly suspected to be malignant tumors, direct
surgical resection should be considered, because massive tumor
excision has a significant positive impact on prognosis and facilitates histopathological analysis (13). Sometimes, direct surgicalresection is difficult because of multiple lesions, deep-seatedcerebral lesions, and the patient’s age or general condition. However, obtaining tissue for analysis is critical for guide therapy
and the prevention of unnecessary interventions. Presently, stereotactically guided biopsy is commonly used to obtain samples
for the histopathological diagnosis of tumors located in deep or
eloquent areas within the brain. Stereotactic biopsy (STB) has
reduced the morbidity associated with open cranial surgery andnonstereotactic techniques and has minimized disruption tonormally functioning neural structures (1, 5). In fact, computed
tomography (CT)/magnetic resonance imaging (MRI)-assisted
STB is now routinely used for diagnosis and is considered an accurate and relatively safe procedure. Such neuroimaging-based
STB procedures are less invasive, especially for surgically inaccessible lesions and for patients who cannot undergo craniotomy
because of their general condition (9, 11, 14, 17, 20). However,
the risk of perioperative complications remains, with data froma large meta-analysis revealing a major morbidity rate of 3.5%
and a mortality rate of 0.7% (6, 19). In some reports, complication
rates have ranged from 6% to 12% and permanent morbidity
and mortality from 0% to 6.4% (12). Brain edema, seizure, andReceived for publication May 8, 2018 ; accepted July 1, 2019.
Address correspondence and reprint requests to Yoshifumi Mizobuchi
Department of Neurosurgery, Institute of Biomedical Sciences Tokushima University Graduate School Tokushima, 3-18-15, Kuramoto-cho, Tokushima 770-8503, Japan and Fax : +81-88-632-9464.

infection have been reported, although the major complication
associated with STB was intratumoral hematoma. The risk forperioperative hemorrhage was generally found to range from
1% to 10% (1, 3, 5, 9, 14, 17, 21). However, these results may be
an underestimation because it is uncommon for neurosurgeons
to obtain routine CT scans after uncomplicated/asymptomatic
STBs (2). In several studies, silent hemorrhage following uncomplicated STBs was reported to range from 8% to 53.9% (10).
We have performed STBs using a Leksell system in patientswith multifocal, deep-seated cerebral lesions, as well as in elderly
patients or patients whose conditions had deteriorated. During
these STBs, we inserted a drainage tube into the site of tissue
resection after the tissue sample was removed. We use this protocol to prevent morbidity and mortality due to cerebral hemorrhage as a complication by the astriction of extraction cavity andthe draining of the bleeding and to enable the identification of
the resected site using postoperative CT scan. Upon completionof the biopsy, a CT scan is performed in all cases, regardless ofthe symptomatic status, to check for complications such as hemorrhages and to confirm the accuracy in targeting the resection
site. We recently reviewed data on the diagnosis rate and complications, specifically symptomatic and asymptomatic (silent)
cerebral hemorrhage, in 80 patients who underwent STB with
the Leksell system at our facility between 2005 and 2014. In thisstudy, we describe the complications and diagnostic benefits ofneuroimaging-guided STB.

CLINICAL MATERIAL AND METHODS
A retrospective study was conducted with institutional review
board approval from University of Tokushima. Patients wereadmitted to the Division of Neurosurgery at the Tokushima University hospital between November 2005 and December 2014.
Data from 80 patients (44 men and 36 women) with a mean ageof 63.3 years (range : 14–86 years), who underwent stereotactic
biopsy using a Leksell apparatus and prospective CT scanning

The Journal of Medical Investigation Vol. 66 2019

The Journal of Medical Investigation Vol. 66 August 2019within hours of their procedure, were analyzed. Their lesions
were either multifocal, diffuse, or seated in deep intrinsic cerebral areas, and were considered inaccessible for direct removal.
Routine blood tests, including platelet count, prothrombin time(PT), and active partial thrombin time (APTT) were performed
for all patients. The following medical conditions were included
for statistical analysis : hypertension, history of diabetes, recent
aspirin use, and procedures performed under local or generalanesthesia.

STEREOTACTIC BIOPSY TECHNIQUE
All biopsies were performed at our institution by three neurosurgeons who were specialized and experienced in performing
stereotactic techniques and were certified by the Japan Neurosurgical Society. A Leksell model G stereotactic frame system(AB Elekta Instruments, Stockholm, Sweden) was used, with
MRI guidance for stereotactic lesion localization. After placement of the head-frame, all patients underwent MRI with aslice thickness of 1 mm. For biopsy, we usually select one site on
a contrast-enhanced lesion, or a lesion with hyperintensity on
T2-weighted MR images or fluid attenuated inversion recovery(FLAIR). The patient was put under local or general anesthesia
and a burr hole was drilled. The dura was incised in a cruciate
fashion, and whenever possible, biopsy trajectories were designed to avoid entrance through a sulcus, cortical artery, venous
structure, or ventricle. The pia-arachnoid was coagulated withbipolar forceps, and then an incision was made with a small scalpel. A Sedan type, side-cutting aspiration biopsy needle (outer
diameter 2.5 mm) was inserted at the target site, and four tissue
samples were obtained from four different directions. After obtaining the tissue samples, portions of the resected tissue were
submitted to a pathologist for rapid examination. After the tissue
was histologically identified, a silicon drain tube with an outer
diameter of 2.5 mm was inserted into the resection cavity witha Kirschner stainless steel wire (inner sheath) and connectedto the drainage circuit to stop bleeding through the astriction of
the extraction cavity and the draining of the blood (Figure 1 left).
All patients underwent postoperative CT scanning immediately to confirm that the sample was from the target site, andto identify complications such as intracranial bleeding (Figure
1 right). New hemorrhages were classified by size (maximum
intraparenchymal diameter) (Figure 2). The following day, all

5mm <

315

patients underwent CT scanning and the drainage tubes were
removed without cerebral hemorrhage.

Statistical analysis
In each case, medical charts and laboratory results werereviewed to identify factors that may have increased the risk of
post-biopsy intracranial hemorrhage associated with the procedure. Fisher’s exact probability test was used to evaluate therelationship between hemorrhagic complications and potential
risk factors in a univariate model, using P = 0.05 as the threshold of statistical significance. Odds ratios were calculated toestimate the magnitude of risk associated with each significant
categorical variable. Factors evaluated included age and sex ofpatients, platelet count, history of hypertension, diabetes, use of
anticoagulant or antiplatelet medications, location of lesion, partial thromboplastin time, historical diagnosis, and procedures
under local or general anesthesia. All analyses were conductedusing EZR (Saitama Medical Center, Jichi Medical University,
Saitama, Japan) (7).

Figure 1. Drainage tube insertion protocols and sample images.

A silicon drainage tube with an outer diameter of 2.5 mm was inserted using a Kirschner stainless steel wire (inner sheath) into theresection cavity (left). Postoperative computed tomography (CT) can beused to confirm whether the sample was from the target site (right).

5mm >Figure 2. Representative images of stereotactic biopsy-related hemorrhages.

No hemorrhage

Representative computed tomography (CT) images of hemorrhages > 5 mm in size (left panel), hemorrhages < 5 mm (middle panel),and no hemorrhages (right panel).

Y. Mizobuchi, et al. The risk of hemorrhage in stereotactic biopsy

316
RESULTS

Patient population
We analyzed data from 80 patients and their clinical data
are summarized in Table 1. The age of patients ranged from 14
to 86 years, with a mean age of 63.3 years at biopsy. Forty-four
patients (55.0%) were male and 36 patients were female. The
mean platelet count was 25.5 (10.9–72.9) × 104 /µl and the mean
prothrombin time was 11.5 (9.1–31.4) seconds. Pre-existing medical conditions were identified in 35 patients (43.8%), including
a history of hypertension (n = 25) and diabetes (n = 10). In six
patients, antiplatelet agents had already been administered 48
hours before surgery. Twenty-one patients (26.3%) underwent
biopsy under local anesthesia.
Table 1. Prebiopsy characteristics of 80 patients undergoing stereotactic brain biopsy

Characteristic

mean (range)

Age (yrs)

63.3 (14-86)

Sex (% male)

55.0%
25.5 (10.9-72.9)X104/µl

Prothrombin time (secs)

11.5 (9.1-31.4)

History of hypertension

31.3%

History of diabetes

12.5%
7.5%

Local anesthesia

26.3%
N=80

Target lesion
The stereotactically biopsied sites are summarized in Table 2.
Forty cases (50.0%) involved tumors that were localized in the
cerebral hemispheres : 20 cases (25%) involved tumors in thefrontal lobe, 7 cases (8.8%) involved tumors in the temporal lobe,
7 cases (8.8%) involved tumors in the parietal lobe, and 6 cases(7.5%) involved tumors in the occipital lobe. For forty patients(50.0 %), the lesions were located deep in the brain. Lesions werelocated in the basal ganglia, corpus callosum, cerebellum, andbrain stem.
Table 2. Sites of stereotactic biopsies
Location

No. of cases (%)

Frontal lobe

20 (25.0)

Temporal lobe

7 (8.8)

Parietal lobe

7 (8.8)

Occipital lobe

6 (7.5)

Cerebellum

2 (2.5)

Basal ganglia

30 (37.5)

Brain stem

1 (1.3)

Corpus callosum

7 (8.8)

Table 3. Histological diagnosis
Lesion TypeNo. of Patients (%)

Low-grade astrocytoma

6 (7.5)

Anaplastic astrocytoma

5 (6.3)

Glioblastoma multiforme

24 (30.0)

Metastasis

2 (2.5)

Malignant lymphoma

30 (37.5)

Gliosis2 (2.5)

Inflammatory

5 (6.3)Demyelination

1 (1.3)

Nondiagnostic

5 (6.3)
N=80

Platelet count

Recent aspirin use

grade glioma, and five (6.3%) diagnosed as anaplastic glioma.
Thirty tumors (37.5%) were malignant lymphomas and two(2.5%) were metastatic brain tumors (Table 3).

COMPLICATIONS AND INCIDENCE OF HEMORRHAGE ON
ROUTINE POSTOPERATIVE CT SCAN
In the present study, no death was attributable to the stereotactic procedure. The only two minor complications associatedwith STB were transient motor weakness caused by hemorrhage
in the tissue-resection cavity and low level of consciousness
caused by postoperative hemorrhage (2.6%). In the case involving the low level of consciousness, hydrocephalus, caused by intraventricular hemorrhage, occurred. However, these symptoms
were temporary and completely disappeared within 48 hours.
The total operative mortality and morbidity rate was 0% upondischarge (Table 4).
Table 4. Complications directly induced by stereotactic brain biopsy
Minor/Transient

Permanent

Weakness

1 (1.3%)0

Seizure00

Infection00

Lowering of
consciousness

1 (1.3%)0

Total

2 (2.6%)0

In the 25 patients (31.3%) in whom hemorrhage was detectedon routine postoperative CT scan, intraparenchymal hemorrhages were smaller than 5 mm in diameter in 22 patients(27.5%) and larger than 5 mm in three patients (3.8%). In the 23
patients, there were no hemorrhage-related neurological deficits(i.e., all hemorrhages that occurred were silent hemorrhages)(Table 5).

N=80

Table 5. Incidence of hemorrhage on routine postoperative computed tomography scans in 80 patients who underwent stereotactic brain
biopsyNo. of Patients (%)

HISTOLOGICAL DIAGNOSISHistological diagnosis was established for 75 cases (93.8%)
following STB. Of the 67 neoplasm cases, 65 were diagnosed
as primary brain tumors. Histologically, glioma was encountered frequently (35 patients ; 43.8%), with 24 tumors (30%)
determined to be glioblastoma, six (7.5%) determined to be low-

All Hemorrhages

Asymptomatic
hemorrages< 5 mm22 (27.5)

22 (27.5)> 5 mm3 (3.8)1 (1.3)total

25 (31.3)

23 (28.8)

The Journal of Medical Investigation Vol. 66 August 2019
RISK FACTORS INFLUENCING HEMORRHAGE
The results following univariate analysis of the risk of post-biopsy hemorrhage revealed a significant correlation with thedegree to which the prothrombin time was longer than 12.7
seconds (P = 0.014). These patients had a 7.43-fold risk of cerebral hemorrhage including asymptomatic hemorrhage comparedto those with a normal prothrombin time. On the other hand,patients with malignant glioma had a 0.37-fold reduced risk ofhemorrhage (P = 0.049). Variables which were not significantly
correlated with risk include age and sex of patients, platelet
count (< 150000), history of hypertension, history of diabetes,
use of anticoagulant or antiplatelet medications, location oflesion, patients with malignant lymphoma, and procedures performed under local anesthesia or general anesthesia (Table 6).
Table 6. Risk factors that influence hemorrhage
Risk Factor

Hemorrhage Gr No hemorrhage Gr ODDs Ratio P-Value

Age (70 <)

11/32

21/32

1.15

0.811

Gender (male)

16/44

28/44

1.48

0.477

PLT (< 150)

2/5

3/5

0.72

1.0

Hypertension

5/25

20/25

0.41

0.129

Diabetes

3/10

7/10

0.877

1.0

Antiplatelet
agents

4/7

3/7

3.04

0.206

Deep-seatedlesion

14/38

24/38

0.69

0.48

PT > 12.7s

6/8

2/8

7.43

0.014

Malignantglioma

14/30

16/30

0.37

0.049

Malignantlymphoma

7/30

23/30

2.00

0.221

Local
Anesthesia

5/21

16/21

0.57

0.42

Abbreviations : PLT, platelet count ; PT, prothrombin timeDISCUSSION
As specified above, we analyzed data from 80 patients who
underwent STBs using the Leksell system, with insertion of adrainage tube according to our standard protocol. Many of thesepatients were at an advanced age, and the resected tissues were
histologically diagnosed as lymphoma in many cases (37.5%). Ina study by Franzini et al., 100 out of 940 patients had multiple
lesions, which comprised malignant gliomas (37%), primary lymphomas (15%), brain metastases (15%), and low-grade gliomas(12%) (3). The prevalence of malignant lymphomas in our study
is higher than that in the study by Franzini et al., possibly because our patient population comprised patients with multiple ordeep lesions, systemic conditions and therefore cannot undergo
tumor resection by open craniotomy, and advanced age.
The pathological diagnosis rate using tissue samples acquired
using the Leksell system in our institute is 93.8%, which is comparable to the values reported in the literature. However, withbrain tumor biopsy, only part of the entire tumor can be collected. Particularly, in cases involving heterogeneous tumors suchas gliomas, the site of resection does not always represent thetumoral region of high malignancy (15). To improve the precisionof resection and sampling, and thus the diagnostic accuracy, it
may be useful to identify an area with relatively high malignancy by performing 11 C-methionine positron emission tomography

317(met-PET) or thallium scintigraphy. With the precision provided
by the Leksell system, it is quite possible to target the high-density areas visualized using met-PET or thallium scintigraphy.
Alternatively, diagnostic accuracy could be improved by setting
multiple targets or collecting multiple tissue specimens, though
this is viewed negatively by many investigators because of its
increased risk of biopsy-related hemorrhage. At our facility, we
select a single target and collect four tissue samples from thetargeted area.
The incidence of complications has been reported to range
from 6% to 12% after STB, consisting mostly of reports of
intracranial symptomatic hemorrhage. Malone et al. reported
that patients with intracranial hemorrhage were significantly
more likely to die in the hospital or experience a non-routinedischarge. These patients have an in-hospital mortality ratethat is six-fold higher than that for patients without hemorrhage(12). In this study, the mortality and morbidity rate, including
infection and postoperative convulsions, was 0% excluding twocases (2.6%), but the symptoms subsided within two days. In
the literature, the risk of perioperative hemorrhage ranges from
1% to 10% (1, 3, 5, 9, 14, 17, 21). However, these results do notinclude asymptomatic hemorrhage. Asymptomatic hemorrhage
was observed in 23 cases (28.8 %) at our facility. The incidenceof asymptomatic hemorrhage has been reported in other studies
to range from 8% to 53.9% (10, 15, 2). There is no generally
accepted standard for postoperative management, monitoring,and surveillance of patients. Postoperative CT scans are not
performed at many facilities if no symptoms are observed after
biopsy. The studies reported in the literature include studies inwhich a CT scan was performed only in cases where symptoms
were observed after biopsy. Thus, the incidence of hemorrhage
reported in the literature is effectively that of symptomatic hemorrhage only, whereas the true incidence of hemorrhage (including asymptomatic hemorrhage) after biopsy may be higher thanpreviously reported due to cases of asymptomatic hemorrhage.
The present study revealed a correlation between postoperative hemorrhage (including asymptomatic hemorrhage) andprothrombin time. It is therefore advisable to consider this relationship when biopsy is performed. On the other hand, patientswith malignant glioma in our study were at a modestly reduced
risk for hemorrhage. This is in accordance with the results ofMalone et al. (12). However, several authors have reported that
gliomas of the basal ganglia and thalamus are risk factors formorbidity in a frame-based stereotactic biopsy (8, 14, 16, 18).
Therefore, such an intervention should be performed in glioma
patients only following careful preparation and consideration of
the target site. Our study suggests that the surgical risk is not
greater for lesions that are located in deep brain areas, although
this is contrary to the reports of other studies (1, 5, 14, 19).
In order to perform safe biopsies, it is important to avoid
symptomatic hemorrhage. Therefore, careful planning should be
enforced. In the literature, Nishihara et al. emphasized the importance of the selected trajectory for the biopsy. They suggested
that biopsies should be performed in such a way as to avoid thesulci and associated blood vessels, as well as the pyramidal tract,
if it is near the target.

CONCLUSION
Neurosurgeons can be presented with serious problems incases of multiple cerebral lesions, advanced age, or deep-seatedlesions. Intracranial hemorrhage is the most common cause ofmorbidity related to permanent paralysis and mortality in stereotactic biopsy. However, intracranial symptomatic hemorrhage
caused by STBs are rare. Stereotactic biopsy is a less invasive

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Y. Mizobuchi, et al. The risk of hemorrhage in stereotactic biopsy

procedure compared to open craniotomy. However, it can still be
used to obtain the samples of brain tumors needed for diagnosis.

DISCLOSURESWe neither have any sources of financial support to disclose,
nor do we have any potential conflicts of interest.

FUNDINGNo funding was provided for this study.

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