Original Article
Surgical Management of Moderate Basal Ganglia Intracerebral Hemorrhage: Comparison
of Safety and Efficacy of Endoscopic Surgery, Minimally Invasive Puncture and
Drainage, and Craniotomy
Chuhua Fu, Ning Wang, Bo Chen, Pingli Wang, Huayun Chen, Wangwang Liu, Lijun Liu
- OBJECTIVE: To date, no standard surgical procedure has
been proven effective for intracerebral hemorrhage (ICH),
particularly deep hematomas. This retrospective study
evaluated the effectiveness and safety of endoscopic sur-
gery, minimally invasive puncture and drainage, and
craniotomy for treating moderate basal ganglia ICH.
- METHODS: Patients with basal ganglia ICH (N [ 177)
were divided into 3 groups based on therapeutic inter-
vention as follows: endoscopic surgery group (n [ 61),
minimally invasive puncture and drainage group (n [ 60),
and craniotomy group (n [ 56). Patient characteristics at
admission were recorded. Operative time; blood loss dur-
ing operation; evacuation rate; postoperative complications
secondary to perihematomal edema, including rebleeding,
infectious meningitis, pulmonary infection, gastrointestinal
bleeding, and epilepsy; mortality; and Glasgow Outcome
Scale scores were compared among the 3 groups.
- RESULTS: Minimally invasive puncture and drainage
was the least traumatic procedure and had the shortest
operative time, but it could not remove the hematoma
quickly; moreover, it had the highest rebleeding rate.
Craniotomy was effective in removing the hematoma but
resulted in marked trauma and had the highest incidence of
pulmonary infection. Endoscopic surgery was safer and
more effective than the other 2 surgical methods, with
greater improvement in neurologic outcomes and no
change in mortality.
Key words
- Basal ganglia
- Deep hematoma
- Endoscopic surgery
- Spontaneous intracerebral hemorrhage
Abbreviations and Acronyms
CT: Computed tomography
ES: Endoscopic surgery
GCS: Glasgow Coma Scale
HV: Hematoma volume
ICH: Intracerebral hemorrhage
MIPD: Minimally invasive puncture and drainage
STICH: Surgical Trial in Lobar Intracerebral Haemorrhage
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- CONCLUSIONS: Minimally invasive neuroendoscopic
management has the advantages of direct vision, efficient
hematoma evacuation, and relatively good results. Endo-
scopic surgery may be a more promising approach for the
treatment of moderate basal ganglia ICH.
INTRODUCTION
S pontaneous intracerebral hemorrhage (ICH), the most
common type of hemorrhagic stroke,1 remains a leading
cause of stroke-related mortality and morbidity2 and
poses a huge economic burden to society.3 Among the several
common regions affected by spontaneous ICH, the basal ganglia
are the most frequently affected.4 Theoretically, surgical
treatment of ICH is beneficial in reducing secondary injuries
associated with hematomas. However, 2 prospective randomized
controlled trials (Surgical Trial in Lobar Intracerebral
Haemorrhage [STICH] and STICH II) have reported no benefit
of craniotomy resection compared with conservative
management.5,6 With advances in technology, minimally inva-
sive surgery, including endoscopic surgery (ES) and minimally
invasive puncture and drainage (MIPD), is expected to be one of
the most promising surgical procedures for the treatment of
spontaneous ICH, particularly deep hematomas.7,8 Among the
different treatment strategies, endoscopic hematoma evacuation is
being gradually acknowledged as an effective method for treating
ICH.9-14 Even so, compared with open surgical evacuation, no
definitive trials have been completed for minimally invasive
Department of Neurosurgery, Xiangyang No. 1 People’s Hospital, Hubei University of
Medicine, Xiangyang, China
To whom correspondence should be addressed: Lijun Liu, M.D.
[E-mail: 87848946@qq.com]
Chuhua Fu and Ning Wang are coefirst authors.
Citation: World Neurosurg. (2019) 122:e995-e1001.
https://doi.org/10.1016/j.wneu.2018.10.192
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CHUHUA FU ET AL.
approaches for ICH evacuation,15 and related literature is
scarce.16,17 Therefore, we conducted a retrospective study to
analyze and compare the therapeutic effectiveness of ES, MIPD,
and craniotomy in the treatment of spontaneous ICH in the basal
ganglia.
MATERIALS AND METHODS
Patients
A retrospective analysis of patients with basal ganglia ICH who
underwent ES, MIPD, and craniotomy for hematoma evacuation
between March 2015 and December 2017 was performed at the
Department of Neurosurgery, Xiangyang No. 1 People’s Hospital,
Hubei University of Medicine. All study procedures were approved
by the Institutional Investigational Review Board and Research
Ethics Committee of this hospital. Informed consent was obtained
from all patients or their families.
All patients underwent brain computed tomography (CT)
angiography to exclude the presence of aneurysms, abnormal
arteriovenous malformations, fistulas, or other vascular lesions.
The patients were categorized into 3 groups: ES group (n ¼ 61),
MIPD group (n ¼ 56), or craniotomy group (n ¼ 60). The baseline
characteristics of all patients at the time of admission were
recorded for each patient, including sex; age; systolic blood
pressure; hematoma volume (HV); presence of intraventricular
hemorrhage; Glasgow Coma Scale (GCS) score; National In-
stitutes of Health Stroke Scale score; blood coagulation status;
history of hypertension, hyperlipidemia, and diabetes; and time to
operation after the ictus.
The inclusion criteria for the study were as follows: 1) basal
ganglia ICH; 2) HV, 30e60 mL; 3) GCS score, 4e14; 4) age 18
years; and 5) interval between stroke and hematoma evacuation
<24 hours. The exclusion criteria were as follows: 1) ICH caused
by aneurysms, trauma, intracranial tumors, infarction, or other
intracranial lesions; 2) coagulation dysfunction or history of
anticoagulant drug use; 3) multiple intracranial hemorrhages; 4)
infectious meningitis and pulmonary or general infection; 5)
enlarged pupils (one or both sides); 6) coexisting severe systemic
diseases and important organ dysfunction; and 7) incomplete or
lost follow-up information.
Interventions
Baseline Treatment. All study patients received medical manage-
ment according to the guidelines of the American Heart Associ-
ation/American Stroke Association Stroke Council for the
treatment of spontaneous ICH in adults,18 including treatment for
controlling blood pressure, cerebral edema, and glycemia; gastric
protection; nutritional support; and prevention of complications.
As there is no standard unified surgical treatment protocol for
spontaneous ICH in the basal ganglia, the surgical criteria for
the treatment decision in each case was determined by the
treating stroke team on duty. In general, this discussion was
held for patients with decreased consciousness and hematoma
volumes >30 mL, especially if CT scan showed a space-
occupying effect on the surrounding normal brain tissue and/or
midline shift. The final treatment decision for each patient was
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ORIGINAL ARTICLE
SURGICAL MANAGEMENT OF MODERATE BASAL GANGLIA ICH
influenced by many factors, such as neurologic impairment, sur-
gical risks, and the wishes of the patient or family.
Endoscopic Surgery. The surgical procedure was similar to the
method described by Wang et al.11 The middle frontal gyrus
approach was used for hematoma evacuation. Kocher entry
point was used for safe access. Before surgery, the hematoma
size, entry direction, and depth were evaluated by 3D Slicer
software (http://www.slicer.org) (Figure 1). Typically, the patient
was placed in the supine position after general anesthesia, and a
linear scalp incision (4e5 cm) was made at the entry site
(Figure 2A and B). Subsequently, craniotomy (diameter of 2.5e3
cm) was performed, and the dura was opened in a cruciate
manner. A 1-cm cortical incision with bipolar cauterization was
made, and a ventricular catheter with a sutured glove (Figure 2C)
was inserted. The glove was ballooned, and the entry tract was
created. Thereafter, a transparent sheath (Goldbov
Optoelectronic Technology Co., Ltd., Wuhan, China) was
inserted into the hematoma cavity. An endoscope (Richard Wolf
GmbH, Knittlingen, Germany) was introduced into the space,
and the hematoma was evacuated under direct vision
(Figure 2D). After adjusting the endoscope and the transparent
sheath, the hematoma was gradually removed. Hemostasis was
maintained using a bipolar cautery and hemostatic materials.
After removal of the hematoma, a soft catheter was inserted into
the hematoma cavity to drain any residual liquid hematoma, the
bone flap was reset and fixed, and the scalp was closed.
Minimally Invasive Puncture and Drainage. The procedure was
based on the method described by Mould et al.19 Under general
anesthesia in the operating room, we placed a soft catheter into
the hematoma through a burr hole. The entry point was
determined using image guidance to avoid functional domains
and blood vessels. Clot aspiration was performed with a 5-mL
syringe until there was no longer any fluid component of the
clot in the aspirate or until resistance was felt. Postoperative CT
was performed to confirm positioning of the soft catheter and
to look for residual hematoma. The hematoma was continuously
liquefied by a fibrinolysis agent (containing 20,000 U urokinase/
5 mL saline solution) for 2e4 days. Routine follow-up CT was
performed 24 hours postoperatively and 72 hours before catheter
removal.
Craniotomy. After general anesthesia, a horseshoe-shaped skin
incision was made on the temporal scalp. The dura mater was
opened after skin incision, and a bone flap was removed. A
cortical surgical route was used from the superior or middle
temporal gyrus hematoma evacuation site, and active bleeding was
controlled with the assistance of an operative microscope using
standard neurosurgical techniques. After hematoma removal, the
dura mater was closed with tension sutures. Bone flap decom-
pression was performed depending on the degree of intraoperative
brain pressure and the patient’s preoperative condition. If intra-
operative brain pressure was high and the preoperative GCS score
was <8, bone flap decompression was performed. If ICH was
accompanied by ventricular hemorrhage or hydrocephalus, an
extraventricular drain was inserted before or after the operation.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.10.192

CHUHUA FU ET AL.
Figure 1. (AeD) Entry point (A and C) and direction and
depth (B and D) for endoscopic surgery were evaluated
by 3D Slicer software. The red area represents the
Observation Indices of Therapeutic Effect
The therapeutic effect of the surgical techniques was evaluated by
operation efficiency, perioperative complications, and outcomes.
Follow-up information about the study patients was obtained by
interviews conducted by telephone or in person. All evaluation
parameters of the 3 groups were compared and analyzed.
Operation Efficiency. Data regarding operative time; intraoperative
blood loss; evacuation rate; and postoperative perihematomal
edema, which was calculated by 3D Slicer software20 according to
the re-examined CT scan 24 hours after operation, were collected.
Perioperative Complications. The incidence of perioperative com-
plications, including postoperative rebleeding, infectious menin-
gitis, pulmonary infection, gastrointestinal bleeding, and epilepsy,
was noted.
Outcome. Mortality and Glasgow Outcome Scale score were
assessed at 6 months after the ictus.
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SURGICAL MANAGEMENT OF MODERATE BASAL GANGLIA ICH
hematoma, and the yellow column represents the
operative passage.
Statistical Analyses
Patient data were evaluated with SPSS Version 13.0 (SPSS, Inc.,
Chicago, Illinois, USA). Normally distributed data are expressed as
mean  SD. Demographic and clinical characteristics and Glas-
gow Outcome Scale score at 6 months after surgery were
compared among the groups using one-way analysis of variance.
Categorical data were compared using the c2 test. P < 0.05 was
considered statistically significant.
RESULTS
After considering the inclusion and exclusion criteria, 177 patients
with ICH in the basal ganglia were examined in this study. As
shown in Table 1, 61 patients were enrolled in the ES group, 56 in
the MIPD group, and 60 in the craniotomy group. All 3 groups
were well matched for baseline characteristics. The ES group
comprised 61 patients (30 men and 31 women) with a mean age
of 61.6  9.2 years (range, 35e73 years). The mean preoperative
hematoma volume was 49.8  11.3 mL (range, 31e56 mL), and
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 ORIGINAL ARTICLE
CHUHUA FU ET AL. SURGICAL MANAGEMENT OF MODERATE BASAL GANGLIA ICH

Table 1. Clinical Baseline Parameters

Clinical ES MIDP Craniotomy
Parameter (n [ 61) (n [ 56) (n [ 60) P

Sex, male 30 (76.1) 25 (44.6) 28 (46.7) 0.885

Age, years 61.6  9.2 65.6  8.8 63.2  9.4 0.764
HV, mL 49.8  11.3 45.4  15.6 50.8  12.4 0.502
GCS score 8.0  2.9 8.4  3.1 7.9  2.8 0.281
SBP, mm Hg 182  13.7 172  15.8 178  14.5 0.945
9
Platelets, 10 /L 233.2  49.2 245.2  46.1 231.9  54.4 0.408
INR 1.0089  0.063 1.0035  0.058 1.0056  0.072 0.624
IVH 8 (13.1) 5 (8.9) 6 (10.0) 0.746
NIHSS score 23.4  5.0 22.9  4.5 24.1  4.9 0.379
Hypertension 48 (78.7) 42 (75.0) 46 (76.7) 0.894
Diabetes 14 (23.0) 11 (19.6) 12 (20.0) 0.888
Hyperlipidemia 11 (18.0) 10 (17.9) 12 (20.0) 0.946
Time to 9.1  3.1 10.2  3.5 9.5  3.2 0.683
operation, hours

Values are presented as mean  SD or number (%).

ES, endoscopic surgery; MIPD, minimally invasive puncture and drainage; HV, hematoma
Figure 2. Steps to remove the hematoma by endoscopic surgery. (A)
Front 5-cm-long skin incision. (B) Side 5-cm-long skin incision. (C) volume; GCS, Glasgow Coma Scale; SBP, systolic blood pressure; INR, international
Establishment of the surgical channel. 1, set of puncture needles with normalized ratio; IVH, intraventricular hemorrhage; NIHSS, National Institutes of
rubber fingernails; 2, disposable syringes; 3, frontal cortex under 3-cm Health Stroke Scale.
bone window. (D) Removal of hematoma under endoscope after a
transparent sheath was introduced into the hematoma cavity.

craniotomy group (165.4  45.2 minutes, 189.3  72.1 mL, and

the median preoperative GCS score was 8.0  2.9. The MIPD
group comprised 56 patients (25 men and 31 women) with a
mean age of 65.6  8.8 years (range, 43e74 years). The mean
preoperative hematoma volume was 45.4  15.6 mL (range, 30e
57 mL), and the median preoperative GCS score was 8.4  3.1.
The craniotomy group comprised 60 patients (28 men and 32
women) with a mean age of 63.2  9.4 years (range, 39e71
years). The mean preoperative hematoma volume was 50.8 
12.4 mL (range, 35e60 mL), and the median preoperative GCS
score was 7.9  2.8. No significant differences were observed
among all 3 groups in the other baseline data, including sex;
age; systolic blood pressure; incidence of intraventricular
hemorrhage; blood coagulation status; National Institutes of
Health Stroke Scale score; history of hypertension,
hyperlipidemia, and diabetes; and time to operation.
Operation Efficiency
There were significant differences among the 3 groups with
respect to the operative time, blood loss, evacuation rate, and
perihematomal edema (P < 0.001), as shown in Table 2; the MIPD
group had the shortest operative time (38.1  18.6 minutes) and
least blood loss (32.5  12.3 mL) and perihematomal edema
(20.4  3.5 mL), followed by the ES group (87.2  28.9
minutes, 67.1  29.2 mL, and 23.6  5.8 mL) and the
31.9  6.2 mL). However, the evacuation rate was lower in the
MIPD group (35.2%  9.4%) compared with the other 2 groups
(ES, 90.8%  7.9%; craniotomy, 87.3%  8.5%; P < 0.001)
(Figure 3).
Perioperative Complications
The rebleeding rate in the MIPD group was significantly higher
than in the other 2 groups (P ¼ 0.026). Patients in the craniotomy
group had the highest incidence of pulmonary infection (P ¼
0.034). No significant differences were observed regarding other
complications, including infectious meningitis, gastrointestinal
bleeding, and epilepsy, among the 3 groups (Table 2).
Outcomes
The fatality rate was 1.6% (1 of 61 patients) in the ES group, 3.6%
(2 of 56 patients) in the MIPD group, and 5.0% (3 of 60 patients) in
the craniotomy group. The cumulative mortality was not signifi-
cantly different among the 3 groups (P ¼ 0.591). The ES group had
a higher Glasgow Outcome Scale score (4.1  0.9) compared with
the MIPD group (3.8  0.8) and the craniotomy group (3.7  1.0)
(P ¼ 0.012). A pairwise comparison showed statistical differences
between the ES and MIPD groups and between the ES and
craniotomy groups, whereas no statistical difference was observed
between the MIPD and craniotomy groups (Table 2).

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 ORIGINAL ARTICLE
CHUHUA FU ET AL. SURGICAL MANAGEMENT OF MODERATE BASAL GANGLIA ICH

brain, whereas MIPD gradually clears the hematoma (complete

Table 2. Comparison of Observation Indices Between the 3 removal takes at least 48 hours). Damage to the brain tissue in-
Groups creases with the compression time. Secondary clinical neurologic
Observation ES MIDP Craniotomy deterioration occurs approximately 12 hours after the onset of
Index (n [ 61) (n [ 56) (n [ 60) P supratentorial ICH,25 and research shows that ischemia can be
present 24 hours after hematoma onset,24 which may worsen
Operative time, minutes 87.2  28.9 38.1  18.6 165.4  45.2 <0.001 the degree of motor impairment in patients with stroke.26
Blood loss, mL 67.1  29.2 32.5  12.3 189.3  72.1 <0.001 Moreover, some blood products that appear after delayed lysis
increase blood-brain barrier permeability, contributing to
Evacuation rate, % 90.8  7.9 35.2  9.4 87.3  8.5 <0.001
edema.24 Therefore, early removal of hematoma may improve the
Perihematomal edema, mL 23.6  5.8 20.4  3.5 31.9  6.2 <0.001 prognosis of patients with spontaneous ICH. However, ultra-early
Rebleeding 2 (3.3) 8 (14.3)* 2 (3.3) 0.026 operation to remove the hematoma (<6 hours) also increases the
risk of rebleeding27 owing to instability of the hematoma; hence,
Infectious meningitis 2 (3.3) 5 (8.9) 3 (5.0) 0.402
surgery at 6e12 hours is considered optimal, and this timing was
Pulmonary infection 3 (4.9) 4 (7.1) 11 (18.3)* 0.034 used in our research.
Gastrointestinal bleeding 3 (4.9) 2 (3.6) 6 (10.0) 0.313 There is currently no standard and unified assessment method
Epilepsy 1 (1.6) 2 (3.6) 5 (8.3) 0.191
for brain tissue trauma caused by surgery. In this study, the
range of edema around the hematoma at 24 hours after the
Mortality 1 (1.6) 2 (3.6) 3 (5.0) 0.591 operation was used to determine the side effects of surgery on
GOS score 6 months 4.1  0.9* 3.8  0.8 3.7  1.0 0.012 brain tissue based on the following considerations: 1) Surgical
after surgery injury to brain tissue is usually a mechanical injury or caused by
thermal effects, including incision, aspiration, and electro-
Values are presented as mean  SD or number (%).
ES, endoscopic surgery; MIPD, minimally invasive puncture and drainage; GOS, Glasgow
coagulation fever. This type of brain edema appears to peak
Outcome Score. about 24 hours after surgery, similar to brain trauma.28,29 (2)
*Represents P < 0.05 compared with other groups. Early edema after spontaneous ICH is usually caused by
compression and ischemia in the brain tissue surrounding the
hematoma and peaks after 48 hours.30 Therefore, edema around
the hematoma at 24 hours after operation can reflect the degree
of trauma caused by surgery.
DISCUSSION ES and MIPD currently represent the most reliable alternatives
This study aimed to evaluate and compare the therapeutic effects to craniotomy for evacuating deeply located hematomas while
of ES, MIPD, and craniotomy to identify the best surgical treat- preventing surgical trauma.16 As shown in our study, the
ment. The results suggested that ES is safer and more effective in edematous areas observed after ES and MIPD were less
evacuating basal ganglia ICH with HV of 30e60 mL than the other compared with craniotomy, which indicates that a minimally
2 surgical methods and has a lower rate of perioperative compli- invasive surgery may cause less damage to the tissue around the
cations and better neurologic outcomes. hematoma than would craniotomy.
ICH induces primary and secondary injury. Primary injury is The outcome of patients with ICH is closely related to the
mainly a result of the mechanical mass effect of the hematoma, location of the hematoma, hematoma volume, duration of the
and secondary injury may be caused by a cascade of events presence of hematoma, and complications.31 Open craniotomy
initiated by the primary injury, the tissue response to the hema- is associated with shortcomings such as a long duration of
toma, and the release of clot components.2 Theoretically, surgery, massive blood loss, high incidence of perioperative
hematoma clearance is beneficial because it reduces hematoma complications, and a potential for a series of pathophysiologic
volume,21 lowers intracranial pressure,22 and improves perfusion changes after craniotomy. Careful hemostasis can be achieved
in the surrounding brain tissue.23 Clot removal may also prevent by coagulation in minimally invasive procedures such as ES,
secondary neurotoxic edema owing to thrombin and hematoma whereas it is impossible to stop the bleeding during MIPD.
degradation products.24 To date, craniotomy has been the most Hence, the rebleeding rate, a serious complication of ICH,
commonly used surgical intervention for spontaneous ICH, but was significantly higher with MIPD than with ES. In addition,
it has shown no significant benefit compared with optimal the duration of the presence of hematoma was longer with
medical management strategies,5,6 probably because craniotomy MIPD, increasing the adverse effects of the hematoma on
causes substantial trauma to the perihematomal brain tissue and brain tissue and influencing the efficacy of MIPD. ES has the
thus negates the benefits of hematoma evacuation.7 Hence, advantages of being less invasive than craniotomy and more
urgent and complete clot removal, with the least amount of effective than MIPD with fewer surgery-related complications,
surgical brain trauma, remains the ideal goal of surgical thus allowing good hemostasis and longer trajectories owing to
treatment for ICH. a more direct and multiangle vision.32 Thus, ES appears to be
Both ES and craniotomy can quickly remove the hematoma and the optimal surgical treatment modality for ICH with HV of
avoid hematoma-induced sustained damage to the surrounding 30e60 mL.

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Figure 3. Patient specimens in the 3 groups. (AeD) Case 1. A 63-year-old
man with an acute spontaneous left basal ganglia hemorrhage treated with
endoscopic evacuation. (A) Preoperative computed tomography.
(B) Preoperative hematoma volume calculated by 3D Slicer software was
53.4 cm3. (C) Postoperative computed tomography. (D) Postoperative
hematoma volume calculated by 3D Slicer software was 3.6 cm3.
(EeH) Case 2. A 52-year-old woman with an acute spontaneous right basal
ganglia hemorrhage treated with minimally invasive puncture and drainage.
(E) Preoperative computed tomography. (F) Preoperative hematoma
volume calculated by 3D Slicer software was 47.2 cm3. (G) Postoperative
computed tomography. (H) Postoperative hematoma volume calculated by
3D Slicer software was 25.8 cm3. (IeL) Case 3. A 65-year-old man with an
acute spontaneous right basal ganglia hemorrhage treated with
craniotomy. (I) Preoperative computed tomography. (J) Preoperative
hematoma volume calculated by 3D Slicer software was 58.1 cm3.
(K) Postoperative computed tomography. (L) Postoperative hematoma
volume calculated by 3D Slicer software was 10.4 cm3. The
perihematomal edema was semiautomatically threshold-based,
segmented, and outlined with green (C, G, and K). A, anterior; S, superior;
P, posterior; I, inferior.

Our results confirmed that compared with classical craniotomy
and MIPD, ES achieved better outcomes. However, this pre-
liminary study has several limitations. This was a retrospective
study, it included a limited number of patients, and the results
were obtained from a single center. Furthermore, we cannot
guarantee that patients with ICH were randomized to receive a
particular surgical procedure. The patients in this study were
specifically selected, and the choice of surgical procedure was
sometimes affected by the opinions of patients and their families.
Therefore, a well-designed prospective trial with a larger number
of cases is essential to compare and establish the safety and
neurologic outcomes of these 3 surgical procedures for the treat-
ment of spontaneous ICH in the basal ganglia.
CONCLUSIONS
This retrospective case series analyzed and compared the safety
and efficacy of ES, MIPD, and craniotomy for treatment of mod-
erate basal ganglia ICH. We found that ES is a more promising
approach with effective hematoma clearance, minimal trauma,
better functional neurologic outcomes, and low rate of
complications.

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CHUHUA FU ET AL.
REFERENCES
1. Qureshi AI, Mendelow AD, Hanley DF. Intrace-
rebral haemorrhage. Lancet. 2009;373:1632-1644.
2. Keep RF, Hua Y, Xi G. Intracerebral haemorrhage:
mechanisms of injury and therapeutic targets.
Lancet Neurol. 2012;11:720-731.
3. Wang W, Jiang B, Sun H, Ru X, Sun D, Wang L,
et al. Prevalence, incidence, and mortality of
stroke in China: results from a nationwide
population-based survey of 480,687 adults. Circu-
lation. 2017;135:759.
4. McCarron MO, Nicoll JA. Spontaneous intracere-
bral hemorrhage. N Engl J Med. 2001;345:769
[author reply: 770].
5. Mendelow D, Gregson BA, Fernandes HM,
Murray GD, Teasdale GM, Hope DT, et al. Early
surgery versus initial conservative treatment in
patients with spontaneous supratentorial intra-
cerebral haematomas in the International Hae-
morrhage (STICH): a randomised trial. Lancet.
2005;365:387-397.
6. Mendelow AD, Gregson BA, Rowan EN,
Murray GD, Gholkar A, Mitchell PM, et al. Early
surgery versus initial conservative treatment in
patients with spontaneous supratentorial lobar
intracerebral haematomas (STICH II): a rando-
mised trial. Lancet. 2013;382:397-408.
7. Fiorella D, Arthur A, Bain M, Mocco J. Minimally
invasive surgery for intracerebral hemorrhage:
rationale, review of existing data and emerging
technologies. Curr Neurol Neurosci Rep. 2016;18:34.
8. Rennert RC, Signorelli JW, Abraham P,
Pannell JS, Khalessi AA. Minimally invasive
treatment of intracerebral hemorrhage. Expert Rev
Neurother. 2015;15:919-933.
9. Yao Z, Hu X, You C, He M. Effect and feasibility of
endoscopic surgery in the spontaneous intrace-
rebral hemorrhage: a systematic review and meta-
analysis. World Neurosurg. 2018;113:348-356.e2.
10. Ma L, Hou Y, Zhu R, Chen X. Endoscopic evac-
uation of basal ganglia hematoma: surgical tech-
nique, outcome, and learning curve. World
Neurosurg. 2017;101:57-68.
11. Wang WH, Hung YC, Hsu SP, Lin CF, Chen HH,
Shih YH, et al. Endoscopic hematoma evacuation
in patients with spontaneous supratentorial
intracerebral hemorrhage. J Chin Med Assoc. 2015;
78:101-107.
12. Longatti P, Basaldella L. Endoscopic management
of intracerebral hemorrhage. World Neurosurg.
2013;79:1-7.
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SURGICAL MANAGEMENT OF MODERATE BASAL GANGLIA ICH
13. Zhao Y, Chen X. Endoscopic treatment of hyper-
tensive intracerebral hemorrhage: a technical re-
view. Chronic Dis Transl Med. 2016;2:140-146.
14. Miller CM, Vespa P, Saver JL, Kidwell CS,
Carmichael ST, Alger J, et al. Image-guided
endoscopic evacuation of spontaneous intracere-
bral hemorrhage. Surg Neurol. 2008;69:441.
15. Dey M, Stadnik A, Awad IA. Spontaneous intra-
cerebral and intraventricular hemorrhage: ad-
vances in minimally invasive surgery and
thrombolytic evacuation, and lessons learned in
recent trials. Neurosurgery. 2014;1:142-150.
16. Li Z, Li Y, Xu F, Zhang X, Tian Q, Li L. Minimal
invasive puncture and drainage versus endoscopic
surgery for spontaneous intracerebral hemorrhage
in basal ganglia. Neuropsychiatr Dis Treat. 2017;13:
213-219.
17. Eroglu U, Kahilogullari G, Dogan I, Yakar F,
Esm AB, Ozgural O, et al. Surgical management of
supratentorial intracerebral haemorrhages: endo-
scopic versus open surgery. World Neurosurg. 2018;
9:261-266.
18. Hemphill JC 3rd, Greenberg SM, Anderson CS,
Becker K, Bendok BR, Cushman M, et al. Guide-
lines for the Management of Spontaneous Intra-
cerebral Hemorrhage: A Guideline for Healthcare
Professionals From the American Heart Associa-
tion/American Stroke Association. Stroke. 2015;46:
2032-2060.
19. Mould WA, Carhuapoma JR, Muschelli J, Lane K,
Morgan TC, Mcbee NA, et al. Minimally invasive
surgery plus recombinant tissue-type plasminogen
activator for intracerebral hemorrhage evacuation
decreases perihematomal edema. Stroke. 2013;44:
627-634.
20. Xu X, Chen X, Zhang J, Zheng Y, Sun G, Yu X,
et al. Comparison of the Tada formula with soft-
ware slicer: precise and low-cost method for vol-
ume assessment of intracerebral hematoma.
Stroke. 2014;45:3433-3435.
21. Lopez VE, Hernandez LA, Calandre L, Grau M,
Cabello A, Gomezescalonilla C. Time window for
clinical effectiveness of mass evacuation in a rat
balloon model mimicking an intra-
parenchymatous hematoma. J Neurol Sci. 2000;174:
1-2.
22. Chambers IR, Banister K, Mendelow AD. Intra-
cranial pressure within a developing intracerebral
haemorrhage. Br J Neurosurg. 2001;15:140-141.
23. Mendelow AD. Mechanisms of ischemic brain
damage with intracerebral hemorrhage. Stroke.
1993;24:118-119.
24. Xi G, Hua Y, Bhasin RR, Ennis SR, Keep RF,
Hoff JT. Mechanisms of edema formation after
intracerebral hemorrhage: effects of extravasated
www.journals.elsevier.com/world-neurosurgery
ORIGINAL ARTICLE
red blood cells on blood flow and blood-brain
barrier integrity. Stroke. 2001;32:2932-2938.
25. Mayer SA, Sacco RL, Shi T, Mohr JP. Neurologic
deterioration in noncomatose patients with
supratentorial intracerebral hemorrhage.
Neurology. 1994;44:1379-1384.
26. Alexander LD, Black SE, Gao F, Szilagyi G,
Danells CJ, McIlroy WE. Correlating lesion size
and location to deficits after ischemic stroke: the
influence of accounting for altered peri-necrotic
tissue and incidental silent infarcts. Behav Brain
Funct. 2010;6:6.
27. Morgenstern LB, Demchuk AM, Kim DH,
Frankowski RF, Grotta JC. Rebleeding leads to
poor outcome in ultra-early craniotomy for intra-
cerebral hemorrhage. Neurology. 2001;56:
1294-1299.
28. Donkin JJ, Vink R. Mechanisms of cerebral edema
in traumatic brain injury: therapeutic de-
velopments. Curr Opin Neurol. 2010;23:293-299.
29. Bareyre F, Wahl F, McIntosh TK, Stutzmann JM.
Time course of cerebral edema after traumatic
brain injury in rats: effects of riluzole and
mannitol. J Neurotrauma. 1997;14:839-849.
30. Staykov D, Wagner I, Volbers B, Hauer EM,
Doerfler A, Schwab S, et al. Natural course of
perihemorrhagic edema after intracerebral hem-
orrhage. Stroke. 2011;42:2625-2629.
31. Garibi J, Bilbao G, Pomposo I, Hostalot C. Prog-
nostic factors in a series of 185 consecutive
spontaneous supratentorial intracerebral haema-
tomas. Br J Neurosurg. 2002;16:355-361.
32. Beynon C, Schiebel P, Bösel J, Unterberg AW,
Orakcioglu B. Minimally invasive endoscopic sur-
gery for treatment of spontaneous intracerebral
haematomas. Neurosurg Rev. 2015;38:421-428 [dis-
cussion: 428].
Conflict of interest statement: The authors declare that the
article content was composed in the absence of any
commercial or financial relationships that could be construed
as a potential conflict of interest.
Received 17 August 2018; accepted 27 October 2018
Citation: World Neurosurg. (2019) 122:e995-e1001.
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