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Bilateral basal ganglia hemorrhage: a systematic review of etiologies,


management strategies, and clinical outcomes

Article  in  Neurosurgical Review · June 2023


DOI: 10.1007/s10143-023-02044-x

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Neurosurgical Review (2023) 46:135
https://doi.org/10.1007/s10143-023-02044-x

REVIEW

Bilateral basal ganglia hemorrhage: a systematic review of etiologies,


management strategies, and clinical outcomes
Gina Watanabe1 · Andie Conching1 · Christian Ogasawara2 · Vishal Chavda3 · Othman Bin‑Alamer4 · Ali S. Haider5 ·
Stefano M. Priola6 · Mayur Sharma7 · Samer S. Hoz8 · Bipin Chaurasia9 · Giuseppe E. Umana10 · Paolo Palmisciano8

Received: 25 January 2023 / Revised: 6 May 2023 / Accepted: 27 May 2023


© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023

Abstract
Bilateral basal ganglia hemorrhages (BBGHs) represent rare accidents, with no clear standard of care currently defined. We
reviewed the literature on BBGHs and analyzed the available conservative and surgical strategies. PubMed, Scopus, Web of
Science, and Cochrane were searched following the PRISMA guidelines to include studies reporting patients with BBGHs.
Clinical characteristics, management, and outcomes were analyzed. We included 64 studies comprising 75 patients, 25 (33%)
traumatic and 50 (67%) non-traumatic. Traumatic cases affected younger patients (mean age 35 vs. 46 years, p=0.014) and
males (84% vs. 71%, p=0.27) and were characterized by higher proportion of normal blood pressures at admission (66% vs.
13%, p=0.0016) compared to non-traumatic cases. Most patients were comatose at admission (56%), with a mean Glasgow
Coma Scale (GCS) score of 7 and a higher proportion of comatose patients in the traumatic than in the non-traumatic group
(64% vs. 52%, p=0.28). Among the traumatic group, motor vehicle accidents and falls accounted for 79% of cases. In the
non-traumatic group, hemorrhage was most associated with hypertensive or ischemic (54%) and chemical (28%) etiologies.
Management was predominantly conservative (83%). Outcomes were poor in 56% of patients with mean follow-up of 8
months. Good recovery was significantly higher in the traumatic than in the non-traumatic group (48% vs. 17%, p=0.019).
BBGHs are rare occurrences with dismal prognoses. Standard management follows that of current intracerebral hemorrhage
guidelines with supportive care and early blood pressure management. Minimally invasive surgery is promising, though
substantial evidence is required to outweigh the potentially increased risks of bilateral hematoma evacuation.

Keywords  Basal ganglia · Head trauma · Hematoma evacuation · Intracerebral hemorrhage · Neurointensive care
management

Giuseppe E. Umana and Paolo Palmisciano contributed equally and


share the senior authorship.

6
* Paolo Palmisciano Department of Neurosurgery, Health Sciences North,
paolo.palmisciano94@gmail.com Northern Ontario School of Medicine, Sudbury, Ontario,
Canada
1
John A. Burns School of Medicine, University of Hawai’i, 7
Department of Neurosurgery, University of Minnesota,
Honolulu, HI, USA
Minneapolis, MN, USA
2
Department of Neurosurgery, University of Texas Medical 8
Department of Neurosurgery, University of Cincinnati, 231
Branch, Galveston, TX, USA
Albert Sabin Way, Cincinnati, OH 45229, USA
3
Department of Pathology, Stanford of School of Medicine, 9
Department of Neurosurgery, Neurosurgery Clinic, Birgunj,
Stanford University Medical Centre, Stanford, Palo Alto, CA,
Nepal
USA
10
4 Department of Neurosurgery, Trauma Center, Gamma Knife
Department of Neurosurgery, University of Pittsburgh
Center, Cannizzaro Hospital, Catania, Italy
Medical Center, Pittsburg, PA, USA
5
Department of Neurosurgery, The University of Texas
M.D. Anderson Cancer Center, Houston, TX, USA

13
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135   Page 2 of 24 Neurosurgical Review (2023) 46:135

Introduction Web of Science, and Cochrane were searched from data-


base inception to March 27, 2022, using the combination
Intracerebral hemorrhage (ICH) is the second most com- of the Boolean operators “OR” and “AND” and the follow-
mon cause of stroke, accounting for 10–15% of worldwide ing search terms: “bilateral,” “basal ganglia,” and “hemor-
cases and leading to major morbidity and mortality [1, 2]. rhage.” Studies were uploaded to Mendeley, and duplicates
Basal ganglia (BG) hemorrhages represent singular entities, were removed.
mostly occurring in spontaneous ICH and less frequently in
traumatic ICH [3, 4]. Bilateral basal ganglia hemorrhages Study selection
(BBGHs) are extremely rare and poorly studied. In view
of the BG’s deep location and highly metabolic nature, A priori inclusion and exclusion criteria were defined. Studies
BBGHs may arise from coup-contrecoup contusions after were included if they (1) included patients with radiologically
closed-head injury, hypertensive crises, cerebral venous confirmed intracranial hematomas/hemorrhages involving the
thrombosis, viral infections, or chemical poisoning [5–9]. bilateral BG; (2) reported available data on clinical features,
Clinical presentation is severe and prognosis dismal, charac- treatment strategies, and post-treatment outcomes; and (3) were
terized by early neurological deterioration from hematoma written in English. Studies were excluded if they were (1) litera-
expansion and corticospinal tract compression, secondary ture reviews, autopsy reports, or animal studies; (2) studies with
injury from perihematomal brain swelling with intracranial unclear distinction between patients with BBGH and patients
hypertension, and late hemotoxicity from blood degradation with other types of intracranial hemorrhages; and (3) studies
products [10, 11]. lacking 2 or more of patients’ demographics, clinical presenta-
Several trials investigated and compared the role of con- tion, management strategies, or post-treatment outcomes.
servative medical care, open surgical hematoma evacua- Two independent reviewers (G.W. and P.P.) screened
tion, minimally invasive/endoscopic hematoma aspiration, titles and abstracts of all retrieved studies, and then assessed
and thrombolysis in the treatment of traumatic and non- full texts of articles that met inclusion criteria. Disagree-
traumatic ICHs [12–15]. Although surgical intervention ments were solved by a third reviewer (G.E.U.). Eligible
was generally not associated with significant improve- studies were included based on the predefined criteria, and
ments in outcome over standard conservative therapies, references were screened for additional relevant articles.
evidence suggests benefit for certain subgroups, particu-
larly those with larger hemorrhage volumes and higher Data extraction
baseline Glasgow Coma Scale (GCS) scores [16, 17].
Endoscopic and minimally invasive surgical approaches Data were extracted by two authors (A.C. and C.O.), and then
appear to be more favorable in patients with deep-seated confirmed independently by one additional author (G.W.).
hematomas involving the BG and the thalami [18, 19]. Missing data were either not reported or not differentiable from
Still, the surgical-related risks should be considered, with other non-relevant data. Extracted data included authors, year,
a particular focus on complex cases such as BBGHs. age, gender, etiology, past medical history, level of conscious-
Although operative and non-operative management strat- ness, location of hemorrhage, dominant hemisphere, presence
egies have been widely studied for unilateral BG ICHs, only of concurrent intracranial hemorrhage, blood pressure, glucose
few reports on BBGHs are currently available, heterogene- level, GCS at admission and discharge, radiological exam and
ous in clinical characteristics and treatments. In this system- findings, hemorrhage volume, management type and details,
atic review, we comprehensively summarized demograph- complications, follow-up duration, overall survival, prognosis,
ics, etiologies, clinical features, and management strategies and vital status. The prognosis was categorized based on the
of BBGHs, further analyzing the impact of current treat- descriptions provided in the texts using the Glasgow Outcome
ments on patient functional outcomes and survival. Scale (GOS). Good recovery was defined as lack of symptoms
or minor deficits not affecting activities of daily living (e.g.,
“No focal neurological deficits,” “GCS 15,” “Able to work as
before”). Moderate disability was defined as having some dis-
Methods ability interfering with the ability to resume work, school, or
other previous activities, but the individual remains independ-
Literature search ent (e.g., “Deaf,” “Some motor weakness”). Severe disability
was defined as needing partial or full assistance of activities of
A systematic review was conducted following the Pre- daily living (e.g., “Hemiparesis,” “Bilateral optic atrophy”). A
ferred Reporting Items for Systematic Reviews and Meta- vegetative state was defined as an absence of awareness of self
Analyses (PRISMA) guidelines [20]. PubMed, Scopus, and the environment (e.g., “Comatose”). Based on etiologies,
BBGHs were divided into traumatic and non-traumatic groups.

13

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Neurosurgical Review (2023) 46:135 Page 3 of 24  135

Data synthesis and quality assessment with a mean age of 42 years (range 0.006–89 years). When
grouped by traumatic versus non-traumatic hemorrhage,
Primary outcomes of interest were patient demographics (age, cases of hemorrhage associated with trauma had a sig-
gender, past medical history), clinical characteristics (signs nificantly younger mean age (35 vs. 46 years, p=0.014), a
and symptoms, vitals, labs, GCS), hemorrhage characteristics higher proportion of males (84% vs. 71%, p=0.27), and a
(postulated etiology, location, concurrent hemorrhage, hemor- significantly higher proportion of unremarkable past medi-
rhage volume), management (conservative vs. surgical), and cal history (88% vs. 37%, p=0.0016). A minority of patients
outcomes (length of stay, follow-up, improvement in symp- (9%) were on anticoagulant or antiplatelet medications or
toms, clinical status, overall survival, prognosis). The level of were reported to have coagulation factor deficiencies. The
evidence of each article was evaluated upon the 2011 Oxford most common comorbidities were hypertension (41%) or
Centre For Evidence-Based Medicine guidelines [21]. Meta- diabetes (16%). Clinical characteristics are reported in
analysis was precluded because all included studies were level Table 3. Overall, the most common presentation involved
IV or V of evidence, and hazard ratios could not be deducted. motor symptoms (26%), such as weakness, and headaches
The risk of bias of each article was independently assessed by (11%). Among the 14 cases that described the laterality of
two authors (A.C. and G.W.) using the Joanna Briggs Institute weakness, most patients experienced unilateral weakness
checklists for case series [22]. (79%), with a nearly equal distribution of right- (47%) and
left-sided hemiplegia or hemiparesis. The non-traumatic
group had a slightly higher proportion of constitutional and
neurologic abnormalities though this was not statistically
Statistical analysis significant. Blood pressure at admission was within normal
limits in 36% of patients, with a significantly higher pro-
Descriptive analyses were performed using SPSS V.25 (IBM portion of normal readings reflected in the traumatic versus
Corp, Armonk, NY). Continuous variables are summarized non-traumatic group (66% vs. 13%, p=0.0016). Most of the
as means with standard deviation and range. Categorical reported glucose levels were within normal limits (70–110
variables were reported as frequencies and percentages. mg/dL) (64%), with a higher proportion of normal glucose
Comparisons between the traumatic and non-traumatic levels in the traumatic versus non-traumatic group (77% vs.
groups were conducted using chi-square tests for categorical 50%, p=0.16). Most patients were comatose at admission
variables or Fisher’s exact test for categories with less than (56%), with a mean GCS of 7. The traumatic group had a
five observations, and t-test for continuous variables only for significantly higher GCS mean at admission when compared
the features reliably and consistently reported among each to the non-traumatic group (8 vs. 6, p = 0.046). A higher
category type. proportion of patients in the traumatic group were comatose
at admission (64% vs. 52%, p = 0.28).
BBGHs were mostly associated with hypertension
(21%), motor vehicle accidents (20%), and methanol tox-
Results icity (10%) (Table 4). Among the traumatic group, motor
vehicle accidents and falls accounted for 79% of cases. In the
Study selection non-traumatic group, hemorrhage was most associated with
vascular or ischemic (55%) and chemical (28%) etiologies.
Figure 1 illustrates the study selection process. The initial The putamen was the most denoted location (39%), followed
search yielded 684 citations (PubMed: 197; Scopus: 321; by BG not otherwise specified (37%) and globus pallidus
Web of Science: 155; Cochrane: 11), of which 64 studies (20%). When analyzing by traumatic versus non-traumatic
were finally included upon the pre-determined criteria: 4 hemorrhage groups, traumatic cases had a higher propor-
case series (involving 9 patients) and 60 case reports (involv- tion of globus pallidus locations (37% vs. 16%, p=0.073)
ing 66 patients), categorized as level IV and V of evidence, and a lower proportion of BG not otherwise specified (16%
respectively (Table 1). Quality assessment resulted in low vs. 38%, p=0.098). Most articles referred to the BBGH
risk of bias for all included studies (Supplementary File 1). lesions as ICH (76%), while others referred to them as hem-
orrhagic infarction (21%) or hemorrhagic necrosis (3%).
Demographics and clinical characteristics Concurrent intracranial hemorrhage (e.g., subarachnoid,
epidural, or subdural hemorrhage) was present in a minority
There were 75 patients with BBGHs that met our inclusion of cases overall (24%), with a significantly higher presence
criteria, 25 (33%) traumatic and 50 (67%) non-traumatic in the traumatic versus non-traumatic group (44% vs. 13%,
hemorrhages (Table 2). Patients were mostly male (76%) p=0.0074). In the 10 cases that reported hemorrhage vol-
ume, there was an average estimate of 22 mL on each side.

13

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135   Page 4 of 24 Neurosurgical Review (2023) 46:135

Fig. 1  PRISMA 2020 flow


diagram Identification of new studies via databases

Records identified from:


Records removed before
PubMED (n = 197) screening:
Scopus (n = 321)
Web of Science (n = 155) Duplicate records (n = 274)
Cochrane (n = 11)

Records screened Records excluded


(n = 410) (n = 314)

Reports sought for Records not retrieved


retrieval (n = 96) (n = 0)

Full text assessed for


eligibility Records excluded (n = 32):
(n = 96)
No bilateral basal ganglia
hemorrhage (n = 15)

No hemorrhage (n = 10)

Autopsy (n = 7)
New studies included in
review
(n = 64)

A larger average combined hematoma volume was observed drainage (including external ventricular drainage) was the
for the non-traumatic group than for the traumatic group, but predominant procedure overall (55%), followed by decom-
this was not statistically significant (27 vs. 15 mL, p=0.18). pressive craniectomy (27%), third ventriculostomy (9%), and
intracranial pressure (ICP) monitor placement (9%). The
Management and outcomes most frequently performed surgical procedure was hema-
toma evacuation in the non-traumatic group (67%) compared
Management strategies are reported in Table 5. Patients were to decompressive craniectomy in the traumatic group (40%).
mostly managed conservatively (83%). Among studies that Among cases of surgical intervention, none reported
reported medical treatment, mannitol (26%) and pheny- which hemisphere was dominant nor mentioned considera-
toin (for seizure prophylaxis) (19%) were the most often tion of cerebral dominance. Of cases with explicitly reported
employed agents in traumatic cases. Meanwhile, unspeci- coagulopathic status (n = 6), none was on anticoagulant or
fied hypertensive agents (12%) and heparin (for deep venous antiplatelet medications nor had any known bleeding disor-
thrombosis prophylaxis) (10%) were most often used in der. There were also no reports of chronic kidney disease
non-traumatic cases. A higher proportion of medications or other renal abnormalities in this surgical subgroup, and
involved antiepileptics in the traumatic group compared to no mention of postcritical management. One case referred
the non-traumatic group (26% vs. 6%, p=0.081), all of which to the lesion as a hemorrhagic infarction. In all cases of
were used prophylactically without mention of seizures dur- BG hematoma evacuation reporting details of the procedure
ing admission nor history of seizures. In the eleven studies (n = 3), drainage was performed bilaterally. Hemorrhage
that reported surgical treatment, hematoma evacuation or volume was slightly asymmetric with an average of 10 mL

13

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Table 1  Overview of all included studies
No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)
LOE

Traumatic
Neurosurgical Review

1 Nagano Case report M 3 Penetrat- - - - Surgical - - - - - - A


et al. – –V ing head
1980 [23] injury
2 Lodder & Case report F 75 - - DS - Conserva- - Yes - - Arm Moderate A
Baard – –V tive rigidity, disability
1981 [24] decreased
(2023) 46:135

facial
expression
3 Ozgun & Case report M 32 Lightning 140/90 LN - Conserva- 5 Yes - 8 Deaf Moderate A
Castillo – –V strike tive disability
1995 [25]
4 Jang et al. – Case report M 50 Fall WNL - 15 Conserva- 14 - - 0.47 No FND Good A
2007 [26] –V tive recovery
5 Ishihara Case report M 0.92 Fall WNL CS - Conserva- 9 Yes - 25 No FND Good A
et al. – –V tive recovery
2009 [27]
6 Kaushal Case report M 42 MVA 136/88 LN, EC 5 Conserva- 14 Yes 15 - Some motor Moderate A
et al. – –V tive weakness disability
2011 [28]
7 Aygun et al. Case report M 35 Blast injury WNL - - Conserva- 7 Yes 15 - No FND Good A
– 2012 –V tive recovery
[29]
8 Bhargava Case report M 25 MVA WNL BG 4 Conserva- 35 Yes - - Dysphasia, Severe dis- A
et al. – –V tive R spastic ability
2012 [30] hemipa-
resis
Case report M 50 MVA WNL BG 4 Conserva- - Yes - - Motor - A
–V tive improve-
ment
9 Jain et al. – Case report M 38 Fall WNL - 15 Conserva- 5 - 15 2 No FND Good A
2013 [31] –V tive recovery
10 Calderon- Case report M 28 MVA WNL - 6 Conserva- 7 No - 0.1 Dead - D
Miranda –V tive

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et al. –
2014 [32]
11 Pandey et al. Case report M 37 MVA WNL CG 6 Surgical 28 No 6 - Coma Vegetative A
Page 5 of 24 

– 2014 –V state
[33]
135

13
Table 1  (continued)
135  

No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)

13
LOE

12 Vega et al. – Case report M 57 Assault - LN 8 Conserva- 17 Yes 15 18 Memory Severe dis- A
Page 6 of 24

2015 [34] –V tive deficits, ability


temporal
disorienta-
tion, dys-
calculia
13 Baek et al. – Case report M 6 MVA - - 6 Surgical 39 No - - Vegetative Vegetative A
2016 [35] –V state state
14 Bathla et al. Case report M 16 MVA WNL - 4 Surgical 6 No - 0.2 Dead - D
– 2016 [5] –V
Case report M 22 MVA - LN 3 Surgical 6 No - 0.2 Dead - D
–V
15 Kankane Case report M 20 MVA WNL BG 9 Conserva- 3 Yes 15 3 No FND Good A
et al. – –V tive recovery
2016 [36] Case report M 45 MVA WNL CG 10 Conserva- 5 Yes 15 3 No FND Good A
–V tive recovery
16 Zhang et al. Case report F 45 Fall 160/100 - 8 Conserva- 29 Yes 15 1 L hemipa- Severe dis- A
– 2016 [9] –V tive resis ability
17 Reddy et al. Case report M 34 MVA WNL - 5 Conserva- - No - 0.1 Dead - D
– 2019 –V tive
[37] Case report M 40 MVA - - 7 Conserva- - Yes 14 - - Good A
–V tive recovery
Case report F 40 Fall - - 10 Conserva- 20 Yes 15 - - Good A
–V tive recovery
18 Lee et al. – Case report M 33 Assault 100/60 GP 15 Conserva- 28 - 15 7 No FND Good A
2020 [38] –V tive recovery
19 Mughis Case report M 30 MVA 230/118 - 12 Conserva- 5 Yes 15 - No FND Good A
et al. – –V tive recovery
2020 [39]
20 Anh et al. – Case report F 63 MVA 150/90 LN 9 Conserva- 31 Yes 15 2 Initial Good A
2022 [40] –V tive quadriple- recovery
Neurosurgical Review

gia and
aphasia,

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normal
strength
and
speech
(2023) 46:135

recovered
2 mo later
Table 1  (continued)
No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)
LOE

Non-traumatic
Neurosurgical Review

21 Finelli et al. Case report M 57 - 104/60 GP - Conserva- - Yes - - Quadriple- Severe dis- A
– 1984 –V tive gic, mute ability
[41]
22 Naheedy Case report F 30 Preeclamp- - BG - - - - - - - - A
et al. – –V sia
1985 [42]
(2023) 46:135

23 Sato et al. – Case report M 45 Anticoagu- - P - Conserva- 30 Yes - 1 Walking Severe dis- A
1986 [43] –V lants tive with cane, ability
motor
dysphasia,
dysphagia,
dysarthria,
L hemipa-
resis
24 Erbguth Case series F 48 VT - BG - Conserva- 73.5 Yes - - Choreatic Moderate A
et al. – – IV tive movement disability
1991 [44] of R hand
25 Fujioka Case report M 69 CA - CS - - 40 No - 1.33 Vegetative Vegetative A
et al. – –V state state
1994 [45]
26 Kabuto et al. Case report M 65 HTN - P, ventri- - Conserva- - No - 0.13 Dead - D
– 1995 –V cles, IC tive
[46]
27 Nagatomo Case report F 50 VT - BG - Conserva- 21 Yes 4 0.7 No FND Good A
et al. – –V tive recovery
1995 [8]
28 Wang & Case report M 40 VT - BG - Conserva- 20 - - 1 No FND Good A
Shen – –V tive recovery
1995 [47]

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Page 7 of 24 
135

13
Table 1  (continued)
135  

No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)

13
LOE

29 Ertl-Wagner Case report F 59 DKA - BG - Conserva- 7 Yes - - Paraparesis, Moderate A


Page 8 of 24

– 1999 –V tive bilateral disability


[48] facial
palsy,
dysdia-
dochoki-
nesis,
impaired
coordina-
tion and
fine motor
function
30 Pidcock Case report F 8 - 140/100 P - Conserva- 30 Yes 6 - Decreased Severe dis- A
et al. – –V tive drooling, ability
1999 [49] improved
language
produc-
tion, use
of com-
munica-
tion board
31 Raabe & Case report M 46 HTN, HA 135/75 BG - Conserva- - Yes - - Severely Severe dis- A
Krug – –V tive disabled ability
1999 [50]
32 Kohshi et al. Case report F 76 HTN 196/90 Thal, P, IC - Conserva- 28 Yes - - Slight hemi- Moderate A
– 2000 –V tive paresis disability
[51]
33 Cho et al. – Case report M 40 HHS - P - Conserva- - No - 24 Vegetative Vegetative A
2002 [52] –V tive state state
34 Silliman Case report M 35 HTN 180/104 P - Conserva- 10 No - - Dead - D
et al. – –V tive
2003 [53]
35 Caparros- Case report M 50 EG - GP - Conserva- 30 Yes 14 6 No FND Good A
Neurosurgical Review

Lefebvre –V tive recovery


et al. –

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2005 [54]
36 Sarkar et al. Case report M 40 JE 180/90 BG - Conserva- - Yes - 2 Mild Good A
– 2005 –V tive emotional recovery
(2023) 46:135

[55] lability
Table 1  (continued)
No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)
LOE

37 Yen et al. – Case series M 55 HTN - P 3 Conserva- - - - - - - -


Neurosurgical Review

2005 [56] – IV tive


M 64 HTN - P 6 Surgical - No - - Dead - D
M 49 HTN - P 3 Conserva- - - - - - - -
tive
38 Ari et al. – Case report M 25 Methanol 130/90 P - Conserva- - Yes - 2 Bilateral Severe dis- A
(2023) 46:135

2007 [57] –V tive optic ability


atrophy
39 Asimi et al. Case report M 65 HTN 190/110 P 11 Conserva- 1 - - 0.03 Dead - D
– 2007 –V tive
[58]
40 Sefidbakht Case series M 27 Methanol - LN - Conserva- - - - - - - A
et al. – – IV tive
2007 [59] M 26 Methanol - LN - Conserva- - - - - - - A
tive
41 Nishina Case report F 74 HTN 220/90 P 4 Conserva- - No - 0.2 Dead - D
et al. – –V tive
2010 [60]
42 Terzi et al. – Case report M 63 HTN 190/110 BG - Conserva- - - - - No FND Good A
2010 [61] –V tive recovery
43 Amin et al. Case report F 28 Stroke 140/70 LN 3 Conserva- 35 Yes - 2 Dysphagia, Severe dis- A
– 2011 –V tive moderate ability
[62] hypoki-
nesia,
rigidity
44 Takeuchi Case series M 57 HTN 183/120 P 7 Surgical - - - - Severely Severe dis- A
et al. – – IV disabled ability
2011 [63] M 59 HTN 198/140 P 3 Surgical - No - - Vegetative Vegetative A
state state
M 89 HTN 150/78 P 3 Conserva- - No - - Dead - D
tive
45 Westover & Case report F 58 SSRI, - BG - Conserva- 30 Yes - 1 Minimal Good A

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Cohen. – –V RCVS tive receptive recovery
2011 [64] aphasia
46 Cha et al. – Case report M 55 CA 69/43 BG 3 Conserva- 15 No - 0.5 Dead - D
2012 [65] –V tive
Page 9 of 24 
135

13
Table 1  (continued)
135  

No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)

13
LOE

47 Permpalung Case report M 56 Methanol - BG - Conserva- - Yes - - - - A


et al. – –V tive
Page 10 of 24

2013 [66]
48 Srivastava & Case report M 35 Methanol - P - Conserva- - Yes - - - - A
Kadam – –V tive
2013 [67]
49 Thiruna- Case report M 30 Methanol - BG 8 Conserva- - Yes - - - - A
vukkarasu –V tive
et al. –
2013 [68]
50 Heck et al. – Case report M 29 Aneurysm - BG - Conserva- 11 - - 18 Minor Moderate A
2014 [69] –V tive speech disability
difficul-
ties, could
not use R
hand for
precise
manipula-
tions
51 Baldawa Case report M 60 HTN 220/110 BG - Conserva- 30 No - - Vegetative Vegetative A
et al. – –V tive state state
2015 [70]
52 Lee et al. – Case report M 32 Methanol - BG 3 Conserva- 21 - - 0.75 Dead - D
2015 [7] –V tive
53 Mahale et al. Case report M 5 JE 98/72 BG - Conserva- - Yes - - Akinetic- Severe dis- A
– 2015 –V tive mute state ability
[71]
54 Zhao et al. – Case report M 57 HTN 192/102 BG 5 Surgical - Yes - 10 Motor Moderate A
2016 [72] –V weakness disability
55 Boukobza Case report F 54 CA - CS 3 Conserva- 6 No - - Dead - D
& Baud – –V tive
2017 [73] Case report M 64 CA - CS 3 Conserva- 7 No - - Dead - A
Neurosurgical Review

–V tive
56 Gupta et al. Case report - 0.0055 GBS menin- - CS - Surgical - - - 6 Develop- Severe dis- A

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– 2018 –V gitis mental ability
[74] delay,
cerebral
palsy,
(2023) 46:135

hypsar-
rhythmia
Table 1  (continued)
No. Authors - Study Sex Age Etiology* BP Locations GCS1 Manage- LOS (days) Improved? GCS2 OS** Outcomes Prognosis Status
Year design – ment (mon)
LOE

57 Mahavar Case report M 25 Toluene 120/80 BG 3 Conserva- - No - - Dead - D


Neurosurgical Review

et al. – –V tive
2018 [75]
58 Daci et al. – Case report F 60 COVID WNL BG - - 11 - - 0.36 Dead - D
2020 [6] –V
59 Guo et al. – Case report M 0.083 Methyl- - C - Conserva- 14 - 14 - No FND - A
2020 [76] –V malonic tive
(2023) 46:135

acidemia
60 Haddadi Case report F 54 COVID 150/100 BG 10 Conserva- 7 Yes 5 - No FND Good A
et al. – –V tive recovery
2020 [77]
61 Schweyer Case report F 51 Olanzapine WNL BG - Surgical - Yes - 2 Vegetative Vegetative A
et al. – –V state state
2020 [78]
62 Shaheed Case report M 62 - WNL LN 14 Conserva- - - - - - - A
et al. – –V tive
2020 [79]
63 Zhang et al. Case report F 52 HTN 180/100 BG 6 Surgical - Yes 2 24 Mild motor Moderate A
– 2020 –V disorder, disability
[80] speech did
not return
to normal
64 Kayastha Case report M 39 - 200/100 BG 12 Conserva- 9 Yes - - No FND Moderate A
et al. – –V tive disability
2022 [81]

Abbreviations: BG, basal ganglia; CA, cardiac arrest; CG, capsuloganglionic; CS, corpus striatum; DKA, diabetic ketoacidosis; DS, dorsal striatum; FND, focal neurological deficits; EC, exter-
nal capsule; EG, ethylene glycol; GBS, group B Streptococcus; GCS, Glasgow Coma Scale; GCS1, admission GCS; GCS2, discharge or last known GCS; GP, globus pallidus; HA, headache;
HHS, hyperglycemic hyperosmolar syndrome; HTN, hypertension; IC, internal capsule; JE, Japanese encephalitis; LOE, level of evidence; LOS, length of stay; LN, lentiform nuclei; MVA, motor
vehicle accident; OS, overall survival; P, putamen; RCVS, reversible cerebral vasoconstriction syndrome; SSRI, selective serotonin reuptake inhibitor; Thal, thalamus; Tx, treatment; VT, venous
thrombosis; WNL, within normal limits
*Postulated etiology
**If patient alive, this refers to months of follow-up

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Page 11 of 24 
135

13
135   Page 12 of 24 Neurosurgical Review (2023) 46:135

Table 2  Summary of patient Characteristics Overall Non-traumatic Traumatic p-value


demographics. The number
of patients for which values Cohort size 75 50 25
are reported for traumatic and
Age (n = 75)
non-traumatic cases is denoted
in parenthesis. Analyses   Mean ± SD, range (years) 42 ± 20, 0.006–89 46 ± 19, 0.006–89 35 ± 18, 0.9–75 0.014
performed using the chi-square Gender (n = 75)
test for categorical values or   Female (%) 18 (24%) 14 (29%) 4 (16%) 0.27
Fisher’s exact test for categories
PMH
with less than five observations,
or t-test for numerical values   Unremarkable (n = 55) 29 (53%) 15 (37%) 14 (88%) 0.0016
with alpha < 0.05 being   Coagulopathy* (n = 46) 4 (9%) 3 (12%) 1 (5%) 0.62
statistically significant (denoted PMH conditions (n = 26)
in bold)
 Cardiovascular 27 (61%) 24 (62%) 3 (60%) 1.0
  HTN 18 (41%) 17 (44%) 1 (20%)
  Stroke 2 (5%) 2 (5%) -
  DVT 1 (2%) 1 (3%) -
  Thalassemia minor 1 (2%) 1 (3%) -
   Venous stasis ulcers 1 (2%) 1 (3%) -
  CHF 2 (5%) 1 (3%) 1 (20%)
  Atrial fibrillation 2 (5%) 1 (3%) 1 (20%)
 Endocrinologic
  DM 7 (16%) 6 (15%) 1 (20%) 1.0
 Cancer
  Rectal adenocarcinoma 1 (2%) 1 (3%) - 1.0
 Other 9 (20%) 8 (21%) 1 (20%) 1.0
   Hepatitis B/C virus 2 (5%) 1 (3%) 1 (20%)
  OSA 1 (2%) 1 (3%) -
  PE 1 (2%) 1 (3%) -
  Asthma 1 (2%) 1 (3%) -
  Depression 1 (2%) 1 (3%) -
  GERD 1 (2%) 1 (3%) -
  Migraine 1 (2%) 1 (3%) -
  Quadriparesis 1 (2%) 1 (3%) -

Abbreviations: CHF, congestive heart failure; DM, diabetes mellitus; DVT, deep venous thrombosis;
ESRD, end-stage renal disease; HTN, hypertension; GERD, gastroesophageal reflux disease; MI, myocar-
dial infarction; OSA, obstructive sleep apnea; PE, pulmonary embolism; PMH, past medical history; SD,
standard deviation
*Yes, if patient was reported to be on anticoagulant or antiplatelet agents, or had a known bleeding disorder

difference, and total volume ranged from 16.2 to 30 mL per intracranial hypertension were observed 1.5 h after clamping
side. In all three patients, draining catheters were left in the catheter following the initial urokinase infusion (20,000
place on both sides with subsequent thrombolysis and clot IU in 3 mL normal saline), which was relieved upon opening
aspiration. BG hemorrhage was larger on the left side in one the catheter valve. This prompted a change in administration
case and the right side in two cases. The patient with the schedule to urokinase infusion every 12 h for up to 4 doses
greater hemorrhage on the left side was left with non-fluent (presumably 5000 IU each). In the second pediatric case,
aphasia post-operatively. severe brain swelling developed 2 days following hematoma
Urokinase dissolved in normal saline was used in two evacuation and 1 day after the administration of 8000 IU of
patients with associated intraventricular hemorrhage. In an urokinase in 3 mL of normal saline every 8 h. This prompted
older adult (57 year old female), 5000 IU urokinase in 3 mL a decompressive huge craniectomy and duroplasty with ven-
normal saline was administered every 12 h for up to 4 doses, triculoperitoneal shunting and cranioplasty at post-operative
whereas in a child (6 year old male), 8000 IU urokinase day 39.
in 3 mL normal saline was administered every 8 h over 2 Patients stayed in the hospital for a mean of 19 days
days. In both cases of urokinase irrigation, complications overall (Table 6). This was shorter in the traumatic group
related to the procedure arose. In the first adult case, signs of than in the non-traumatic group (16 vs. 21 days, p=0.21).

13

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Neurosurgical Review (2023) 46:135 Page 13 of 24  135

Table 3  Clinical characteristics. The number of patients for which square test for categorical values or Fisher’s exact test for categories
values are reported for traumatic and non-traumatic cases is denoted with less than five observations, or t-test for numerical values with
in parenthesis (n = no. of cases). Analyses performed using the chi- alpha < 0.05 being statistically significant (denoted in bold)
Categories Overall Non-traumatic Traumatic p-value

Signs and symptoms (n = 54)


 Constitutional 17 (15%) 16 (16%) 1 (6%) 0.70
  N/V 8 (7%) 7 (7%) 1 (6%)
  Fever 4 (3%) 4 (4%) -
  Cough 2 (2%) 2 (2%) -
  Malaise 2 (2%) 2 (2%) -
  Dyspnea 1 (1%) 1 (1%) -
 Neurologic 19 (16%) 17 (17%) 2 (13%) 1.0
  Headache 13 (11%) 11 (11%) 2 (13%)
  Seizures 4 (3%) 4 (4%) -
  Dizziness 1 (1%) 1 (1%) -
  Urinary incontinence 1 (1%) 1 (1%) -
  System deficits 55 (47%) 49 (49%) 6 (38%) 0.60
   Visual 6 (5%) 6 (6%) -
   Speech, language, swallowing 8 (7%) 8 (8%) -
   Sensory 5 (4%) 5 (5%) -
   Motor 30 (26%) 26 (26%) 4 (25%)
    Weakness 12 (10%) 10 (10%) 2 (13%)
    Hypertonia 6 (5%) 6 (6%) -
    Hypotonia 3 (3%) 3 (3%) -
    Tremors 1 (1%) - 1 (6%)
    Other* 2 (2%) 1 (1%) 1 (6%)
   Coordination 2 (2%) 2 (2%) -
   Gait 3 (3%) 1 (1%) 2 (13%)
   Reflexes 30 (26%) 24 (24%) 6 (38%) 0.22
    Positive Babinski 13 (11%) 10 (10%) 3 (19%)
    Impaired PLR 8 (7%) 6 (6%) 2 (13%)
    Hyperreflexia 4 (3%) 3 (3%) 1 (6%)
    Hyporeflexia 3 (3%) 3 (3%) -
    Absent brainstem reflexes 2 (2%) 2 (2%) -
 Other 2 (2%) 1 (1%) 1 (6%) 0.24
  Abdominal pain 1 (1%) 1 (1%) -
  Hypersalivation 1 (1%) - 1 (6%)
  Vitals and labs
  BP (n = 41)
  WNL 15 (36%) 3 (13%) 12 (66%) 0.0016
   Systolic mean ± SD, range 160 ± 41, 69–230 162 ± 41, 69–220 153 ± 43, 100–230 0.63
   Diastolic mean ± SD, range 92 ± 20, 43–140 93 ± 21, 43–140 91 ± 19, 60–118 0.88
  Glucose (mg/dl) (n = 25)
  WNL 16 (64%) 6 (50%) 10 (77%) 0.16
   Mean ± SD, range 170 ± 122, 25–404 199 ± 145, 25–404 115 ± 14, 106–132 0.37
GCS (n = 40)
  At admission 7 ± 4, 3–15 6 ± 4, 3–14 8 ± 4, 3–15 0.046
LOC at admission (n = 75)
 Awake 13 (17%) 9 (18%) 4 (16%)
 Confused 3 (4%) 3 (6%) -
 Disoriented 1 (1%) 1 (2%) -
 Lethargic 8 (11%) 5 (10%) 3 (12%)
 Stuporous 3 (4%) 2 (4%) 1 (4%)
 Comatose 42 (56%) 26 (52%) 16 (64%) 0.28
  Altered, NOS 5 (7%) 4 (8%) 1 (4%)

*Includes 1 limb ballism in the traumatic group, and 1 bradykinesia in the non-traumatic group
Abbreviations: GCS, Glasgow Coma Scale; LOC, level of consciousness; NOS, not otherwise specified; N/V, nausea/vomiting; PLR, pupillary
light reflex; WNL, within normal limits; SD, standard deviation

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135   Page 14 of 24 Neurosurgical Review (2023) 46:135

Follow-up duration was a mean of 8 months. Most patients Understanding the etiology and mechanism of injury
were alive (78%). Of patients who were deceased, the overall in BG hemorrhage is important to evaluate the benefit, if
survival was a mean of 0.2 months (6 days). Among cases any, of surgical intervention, where the principal effects
that reported prognosis, most patients had a poor outcome are related to the dissipation of mass effect and removal of
(dead, vegetative state, or severe disability) (56%). A signifi- extravasated blood products. It is perhaps even more crucial
cantly higher proportion of good recovery was observed in in cases of bilateral hemorrhage, as surgical intervention
the traumatic group (48% vs. 17%, p=0.019). Among cases presents additional potential risks such as contralateral clot
of surgical intervention with reported outcomes (n = 10), destabilization or herniation if only one side is aspirated or
patients were dead (20%), remained in a vegetative state increased cortical injury if both sides are targeted. During
(40%), or were severely (20%) or moderately (20%) disabled. primary injury, an expanding hematoma can compress sur-
rounding tissues, including vasculature, potentially altering
blood flow if sufficiently large. However, the extent to which
Discussion this occurs in BBGH may be minimized by a stanching effect
of the contralateral hematoma and relative theoretical laxity
The BG is the most commonly reported location for non- of gray matter in this region in comparison to white mat-
traumatic ICH, with the putamen being implicated in nearly ter and the cerebral cortex [90, 91], which may contain the
a third of cases on imaging series [82]. However, BBGH bleed and limit significant tissue displacement. This remains
is a rare occurrence limited to case reports and brief case speculative as studies on viscoelastic properties of the brain
series. Based on the presence of trauma, BBGH has been cannot simulate all aspects of a BBGH in humans [92].
categorized as traumatic or “non-traumatic” in etiology, Secondary injury is attributed to the proinflammatory and
with the latter being associated with a variety of vascular, neurotoxic effects of thrombin and red blood cell contents
chemical, infectious, and endocrinologic triggers. The deep- such as hemoglobin, hemin, and iron following cell lysis,
seated nature of these lesions and often acute presentation which then can lead to edema with subsequent increased
of loss of consciousness raise questions as to whether neu- intracranial pressure and herniation [93, 94].
rosurgical intervention can bring any meaningful change Traumatic BG hemorrhage is thought to be caused by
to outcomes. The bilateral nature of the bleed also presents tears in branches of the anterior choroidal or lenticulostriate
unique factors that should be taken into consideration dur- arteries due to sudden acceleration-deceleration and shear-
ing management. In this systematic review, we assess the ing forces. This was first observed histologically by Mosberg
literature on BBGH and discuss the etiologies, management and Lindenberg upon discovering a ruptured arterial twig
strategies, and clinical outcomes. of the anterior choroidal artery in a patient with traumatic
hemorrhage of the left pallidum [95]. Mechanisms by which
Etiology bilateral traumatic tears occur are likely due to the same
shearing forces, with anatomical variations in the symme-
The BG are a collection of deep subcortical gray matter try or proximity of vasculature and trajectory of the exter-
structures that typically consist of the caudate nucleus, puta- nal force perhaps predisposing individuals to simultaneous
men, nucleus accumbens, globus pallidus, substantia nigra, rupture of arteries on both sides. Alternatively, hemorrhage
and subthalamic nucleus. Blood supply arises from anterior occurring initially on one side with subsequent hematoma
circulation via the lenticulostriate arteries of primarily the expansion [96, 97] may alter local hemodynamics and cause
middle and sometimes anterior cerebral arteries, with slight mass effect leading to rupture of contralateral arteries lack-
variations from person to person. The anterior choroidal ing normal wall integrity due to damage sustained from the
artery of the internal carotid artery provides further vascu- initial traumatic event. This latter view may be supported
lar supply to BG [83–85]. Selective BG hemorrhage is likely by the appearance of asymmetric hemorrhage volumes and
possible due to anatomic and metabolic factors rendering unilateral symptoms noted in most of our included cases.
this region particularly vulnerable to hypoxic and chemical Compared to the traumatic unilateral BG hemorrhage series
injury. Specifically, terminal blood supply with a lack of presented by Boto et al. in 2001 [98], our dataset included a
anastomoses between parenteral vessels [85] and high exci- lower proportion of motor vehicle accident cases (58% vs.
totoxic and oxidative stress [86] predisposes the BG to dam- 94%). This is likely due to their selection of severe cases
age following ischemic or toxic insult. Certain individuals through inclusion of only patients with a GCS score of 8
may have an increased risk for hemorrhage due to geometric or less. Our traumatic cases also included etiologies of dif-
feature variations of the middle cerebral artery that promote fuse nature, such as lightning strike and blast injury, which
wall stress and injury [87], and the presence of other comor- to our knowledge has not yet been reported as manifest-
bid conditions such as hypertension, heart disease, diabetes, ing with unilateral BG hemorrhage. Thus, traumatic BBGH
excessive alcohol consumption, and smoking [88, 89]. will likely share etiologic similarities with unilateral BG

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Neurosurgical Review (2023) 46:135 Page 15 of 24  135

Table 4  Hemorrhage Categories Overall Non-traumatic Traumatic p-value


characteristics. The number
of patients for which values Etiology (n = 70)
are reported for traumatic and
 Traumatic
non-traumatic cases is denoted
in parenthesis (n = no. of   MVA 14 (20%) - 14 (58%) -
cases). Analyses performed   Fall 5 (7%) - 5 (21%) -
using the chi-square test for   Assault 2 (3%) - 2 (8%) -
categorical values or Fisher’s
  Blast injury 1 (1%) - 1 (4%) -
exact test for categories with
less than five observations, or   Lightning 1 (1%) - 1 (4%) -
t-test for numerical values with    Penetrating head injury 1 (1%) - 1 (4%) -
alpha < 0.05 being statistically    Spontaneous
significant (denoted in bold)
  Vascular
   HTN 15 (21%) 15 (33%) - -
   Cardiac arrest 4 (6%) 4 (9%) - -
   Venous thrombosis 3 (4%) 3 (7%) - -
   Aneurysm 1 (1%) 1 (2%) - -
   Preeclampsia 1 (1%) 1 (2%) - -
   Migraine 1 (1%) 1 (2%) - -
  Chemical
   Methanol 7 (10%) 7 (16%) - -
   Ethylene glycol 1 (1%) 1 (2%) - -
   Methylmalonic acidemia 1 (1%) 1 (2%) - -
   Olanzapine 1 (1%) 1 (2%) - -
   Toluene 1 (1%) 1 (2%) - -
   Anticoagulants 1 (1%) 1 (2%) - -
   SSRI 1 (1%) 1 (2%) - -
  Infectious
   COVID 2 (3%) 2 (4%) - -
   Japanese encephalitis 2 (3%) 2 (4%) - -
   GBS meningitis 1 (1%) 1 (2%) - -
  Endocrinologic
   DKA 1 (1%) 1 (2%) - -
   HHS 1 (1%) 1 (2%) - -
  Unknown 1 (1%) - 1 (4%) -
Location (n = 75)
  Basal ganglia
 Putamen 32 (39%) 25 (39%) 7 (37%) 1.00
  Globus pallidus 17 (20%) 10 (16%) 7 (37%) 0.073
  Caudate nucleus 7 (8%) 5 (8%) 2 (11%) 0.65
  Basal ganglia, NOS 27 (33%) 24 (38%) 3 (16%) 0.098
Lesion referred As (n = 75)
  ICH (%) 57 (76%) 34 (68%) 23 (92%) 0.023
  Hemorrhagic infarction (%) 16 (21%) 14 (28%) 2 (8%) 0.072
  Hemorrhagic necrosis (%) 2 (3%) 2 (4%) - 1.0
Concurrent hemorrhage (n = 71)
  Yes (%) 17 (24%) 6 (13%) 11 (44%) 0.0074
Hemorrhage volume* (n = 10)
  Mean volume ± SD, range (mL) 22 ± 19, 1–74 27 ± 20, 1–74 15 ± 15, 3–42 0.18

*Volume for one side


Abbreviations: DKA, diabetic ketoacidosis; DM, diabetes mellitus; GBS, group B Streptococcus; HHS,
hyperosmolar hyperglycemic state; HTN, hypertension; MVA, motor vehicle accident; NOS, not otherwise
specified; SSRI, selective serotonin reuptake inhibitor

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135   Page 16 of 24 Neurosurgical Review (2023) 46:135

Table 5  Management. The Categories Overall Non-traumatic Traumatic p-value


number of patients for which
values are reported for traumatic Management type (n = 72)
and non-traumatic cases is  Conservative 60 (83%) 40 (85%) 20 (80%) 0.82
denoted in parenthesis (n = no. Medical treatment* (n = 39)
of cases). Analyses performed   Pressure management 34 (55%) 18 (58%) 16 (52%) 0.61
using the chi-square test for
ACE inhibitor
categorical values or Fisher’s
exact test for categories with    Enalapril 1 (2%) 1 (3%) -
less than five observations, or   Vasodilator
t-test for numerical values with    Hydralazine 1 (2%) 1 (3%) -
alpha < 0.05 being statistically   Inopressor
significant (denoted in bold)    Dopamine 1 (2%) 1 (3%) -
  DHP CCB
   Amlodipine 1 (2%) 1 (3%) -
   Nimodipine 1 (2%) 1 (3%) -
  Loop diuretic
  Furosemide 5 (8%) 1 (3%) 4 (13%)
  Beta-blocker
  Labetalol 1 (2%) - 1 (3%)
  Combination antihypertensives
  Perindopril/amlodipine 1 (2%) - 1 (3%)
   Irbesartan/hydrochlorothiazide 1 (2%) 1 (3%) -
  Antihypertensives, NOS 4 (6%) 4 (13%) -
  Osmotic agents
  Glycerin 1 (2%) 1 (3%) -
   Hypertonic saline 2 (3%) - 2 (6%)
   Human albumin 1 (2%) 1 (3%) -
   Mannitol 9 (15%) 1 (3%) 8 (26%)
   Osmotic diuretic, NOS 2 (3%) 2 (6%) -
   Antiedema, NOS 2 (3%) 2 (6%) -
 Pain
  Naproxen 1 (2%) 1 (3%) -
 Antiepileptics 10 (16%) 2 (6%) 8 (26%) 0.081
  Phenytoin 7 (11%) 1 (3%) 6 (19%)
  Antiepileptic, NOS 3 (5%) 1 (3%) 2 (6%)
  Thrombolytics
  Urokinase 3 (5%) 2 (6%) 1 (3%) 1.0
  Anticoagulant 4 (6%) 4 (13%) -
  Nafamostat mesilate 1 (2%) 1 (3%) -
  Heparin 3 (5%) 3 (10%) -
Other 10 (16%) 4 (13%) 6 (19%) 0.73
  Haloperidol 1 (2%) - 1 (3%)
  Statin 2 (3%) 2 (6%) -
  Steroid 2 (3%) 2 (6%) -
  Benzodiazepine 4 (6%) - 4 (13%)
  Phenobarbital 1 (2%) - 1 (3%)
Surgical treatment (n = 11)
  Hematoma evacuation** 6 (55%) 4 (67%) 2 (40%) 1.0
  Decompressive craniectomy*** 3 (27%) 1 (17%) 2 (40%) 0.30
  Third ventriculostomy 1 (9%) 1 (17%) - -
  ICP monitor 1 (9%) - 1 (20%) -

*Does not report detoxification agents (e.g., dialysis, fomepizole), vitamins (e.g., folate), or specific treatments for etiologies asso-
ciated with the onset of BBGH (e.g., antibiotics for infection) other than vascular or pressure management
**Includes 2 EVDs (1 traumatic, 1 non-traumatic)
***Includes 1 case of external decompression with debridement of cerebral contusion and removal of bone fragments
(traumatic)
Abbreviations: ACE, angiotensin-converting enzyme; CCB, calcium channel blocker; DHP, dihydropyridine; ICP, intrac-
ranial pressure; NOS, not otherwise specified

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Neurosurgical Review (2023) 46:135 Page 17 of 24  135

Table 6  Outcomes. The number Categories Overall Non-traumatic Traumatic p-value


of patients for which values
are reported for traumatic and Length of stay (n = 43)
non-traumatic cases is denoted
  Mean days ± SD, range 19 ± 14, 1–73.5 21 ± 16, 1–73.5 16 ± 12, 3–39 0.21
in parenthesis (n = no. of
cases). Analyses performed Follow-up (n = 29)
using the chi-square test for   Mean months ± SD, range 8 ± 8, 0.2–25 9 ± 8, 0.2–24 7 ± 8, 0.5–25 0.49
categorical values or Fisher’s Status (n = 73)
exact test for categories with
  Alive (%) 57 (78%) 36 (75%) 21 (84%) 0.56
less than five observations, or
t-test for numerical values with Overall survival (n = 11)
alpha < 0.05 being statistically   Mean months ± SD, range 0.2 ± 0.2, 0–0.8 0.3 ± 0.3, 0–0.8 0.2 ± 0.06, 0.1–0.2 0.38
significant (denoted in bold) Prognosis (n = 64)
  Good recovery 18 (28%) 7 (17%) 11 (48%) 0.019
  Moderate disability 10 (16%) 7 (17%) 3 (13%) 1.0
  Severe disability 13 (20%) 10 (24%) 3 (13%) 0.35
  Vegetative state 7 (11%) 5 (12%) 2 (9%) 1.0
 Dead 16 (25%) 12 (29%) 4 (17%) 0.37

Abbreviations: SD, standard deviation

hemorrhage, but may include events where trauma is sudden, Management


diffuse, and more uniform.
Non-traumatic BG hemorrhage is associated with a Management of BBGH was predominantly conservative,
variety of etiologies. Hypertension is the predominant resembling current themes of management in ICH and uni-
cause with persistent elevations in arterial pressure asso- lateral BGH cases. Options for management of BG hem-
ciated with lipohyalinosis and weakening of small vessel orrhage include medical therapies or surgical intervention
walls, which may lead to occlusion and ischemia (lacunar with the goal of removing the hematoma, limiting hematoma
stroke) or breach and hemorrhage [99]. Some cases are expansion, ICP monitoring, or minimizing consequences
hypothesized to occur from a sudden rise in blood pressure of secondary injury though the role of surgery remains
causing rupture of microaneurysms or tears in the len- controversial [103–105]. Several clinical trials have been
ticulostriate artery branches [100]. Other potential causes conducted to explore each of these therapeutic approaches
include toxic metabolites of alcohols and glycols, antico- predominantly in the setting of non-traumatic ICH. None
agulation therapy, vessel wall abnormalities (“no-reflow have demonstrated a clear benefit of surgery, though several
phenomenon”) or focal necrosis following ischemia, cer- limitations must be taken into consideration when apply-
ebral venous thrombosis in the great cerebral vein, and ing these findings to cases of deep-seated BG hemorrhage.
migraine-induced vascular changes. In our dataset, vas- In 2005, the Surgical Trial in Intracerebral Haemorrhage
cular and ischemic etiologies accounted for most cases (STICH) [14] evaluated the impact of early surgery (within
(53%), though chemical, infectious, and endocrinologic 72 h) versus conservative treatment in patients with non-
factors were implicated in nearly half of the other cases traumatic supratentorial ICH. One of the major limitations
and underscore the importance of inquiring about suicidal of this trial was in the inclusion of both lobar (39%) and
ideation, COVID-19 vaccination status and exposure, and BG (42%) hemorrhage within the same group and analysis.
glucose control in the setting of diabetes mellitus from Lobar and BG hemorrhage differ markedly, with BG hemor-
reliable historians. The role of COVID-19 infection in rhage causing permanent damage to critical gray matter in
BBGH may be related to hypercoagulopathy [101] or the immediate vicinity of the bleed. Additionally, compared
neurotropism [102] though future studies will be needed to lobar locations, hemorrhages of the BG are at higher risk
to explore this association further. Etiologies among uni- for intraventricular extension and are associated with greater
lateral and bilateral BGH are likely similar, though it is morbidity and mortality [106]. The lack of clear surgical
unclear if BBGH has higher proportions of certain etiolo- benefit noted in the STICH trial may be attributed to the
gies as epidemiological studies of specific BGH causes are permanence of deficits upon BG hemorrhage as surgical
difficult to perform. intervention cannot restore what was lost. Most surgeons in

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135   Page 18 of 24 Neurosurgical Review (2023) 46:135

the trial employed a craniotomy (75%), despite nearly 42% Minimally Invasive Removal of Intracerebral Hemorrhage
of hematoma originating within the BG or thalamus, raising (ENRICH) sponsored by the NICO corporation, and Mini-
questions as to whether a more minimally invasive surgical mally Invasive Endoscopic Surgical Treatment with Apollo/
approach would lead to better outcomes [107]. Early surgery Artemis in Patients with Brain Hemorrhage (INVEST) spon-
was associated with a slightly favorable outcome when the sored by Penumbra, will add to the minimally invasive surgi-
hematoma was located within 1 cm from the cortical surface, cal literature. Meanwhile, the Swiss Trial of Decompressive
which may have been a reflection of the advantages of crani- Craniectomy Versus Best Medical Treatment of Spontane-
otomy for superficial resection, though when this subgroup ous Supratentorial Intracerebral Hemorrhage (SWITCH)
was explored in a follow-up trial (STICH II) in 2013 [15], will provide information on the importance of strict control
the findings remained neutral. of intracranial hypertension with prophylactic decompres-
Minimally invasive strategies for evacuating hemorrhages sive craniectomy in patients with non-traumatic ICH in the
in deep locations such as the BG would be preferred over a BG and/or thalamus.
craniotomy. This approach was assessed in the MISTIE trials Evidence for surgical intervention in cases of traumatic
(Minimally Invasive Surgery with Thrombolysis in Intrac- ICH remains scarce, with only one randomized controlled
erebral Hemorrhage) [108], which provided a protocol for trial published to date that was terminated prematurely due
image-guided aspiration followed by thrombolysis of the clot to recruitment and funding issues. The Surgical Trial in
with alteplase administration every 8 h for up to nine doses. Traumatic Intracerebral Hemorrhage (STITCH) [12] was
In 2019, MISTIE III [13] evaluated the impact of MISTIE the first to investigate the impact of surgery in traumatic
treatment versus standard medical care on functional out- cases. Most surgeons opted to use craniotomy (97%) and the
comes based on the modified Rankin Scale score at 1 year. largest areas of hemorrhage were in the frontal or temporal
MISTIE treatment was not associated with improvements in lobes (92%). Although there were significantly more deaths
functional outcome; however, only 58% of cases met the clot in the first 6 months in the conservative treatment group
reduction goal of less than 15 mL. Subsequent analysis of (33% vs. 15%), sample sizes were low (n = 170). Since most
subjects that received adequate hematoma removal accord- cases involved lobar regions, it is difficult to translate these
ing to the surgical target of less than 15 mL demonstrated findings to traumatic BG hemorrhage. Surgical management
slight positive benefit in outcome compared to controls, and of traumatic BG hemorrhage will likely depend on stud-
further studies with more consistent surgical results are war- ies evaluating the role of minimally invasive approaches for
ranted. Several smaller studies have evaluated the role of non-traumatic ICH located in deep regions.
other minimally invasive surgical techniques, with mixed Taken together, these studies support conservative man-
results on the benefit of such interventions on overall out- agement for ICH especially when the hematoma resides
comes [18, 109–113]. in deep areas such as the BG, though timely minimally
Although studies on the impact of surgical evacuation of invasive surgery between 4 [116] and 72 h after the incit-
non-traumatic ICH are generally neutral, a 2018 meta-analy- ing event may be beneficial in cases where hematoma
sis with 15 published randomized controlled trials investigat- volume is moderate (20–50 mL) and GCS is above 9, and
ing minimally invasive surgery [114] found that it improved decompressive craniectomy may be considered for cases of
morbidity and mortality significantly more than medical impending herniation or neurologic worsening attributed
management or craniotomy, nearly doubling the chance of to mass effect. Another factor to take into consideration
independence and survival and follow-up. Though this does is the laterality of the bleed in relation to the dominant
not include recent results from MISTIE III, minimally inva- cerebral hemisphere. Surgical evacuation on the dominant
sive strategies show promise, especially when surgery can be side may cause new post-operative aphasia, making less
performed within 72 h of symptom onset in certain patient invasive approaches such as a decompressive craniectomy
subgroups such as those with moderate hematoma volume more favorable. Unfortunately, our dataset was severely lim-
20–50 mL and GCS ≥ 9 [17]. The 2022 American Heart ited in the number of surgical cases and surgical detail and
Association/American Stroke Association (AHA/ASA) determining whether the cause of post-operative aphasia is
guidelines for management of patients with spontaneous surgical intervention, or the inciting event may be challeng-
ICH reflect this with a moderate strength recommendation ing due to altered level of consciousness at admission, pre-
in regard to minimally invasive hematoma evacuation for venting an accurate assessment of speech and hemispheric
patients with supratentorial ICH of > 20–30 mL with GCS dominance. Future studies reporting laterality of the surgi-
scores of 5–12 [115]. However, the guidelines do not spec- cal approach and post-operative deficits are needed. Limited
ify etiology or location, and it will be difficult to ascertain evidence is thus available to determine whether surgical
benefit for BBGH until future studies investigate minimally intervention on one or both sides of a BBGH confers any
invasive strategies for unilateral BGH. In the coming years, benefit on outcome. Medical management, particularly the
two industry-sponsored randomized controlled trials, Early use of antihypertensives for early blood pressure lowering

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Neurosurgical Review (2023) 46:135 Page 19 of 24  135

(systolic blood pressure 130–150 mmHg) as described in also be a prognostic factor, as differences in outcomes have
the American Heart Association/American Stroke Associa- been observed based on which arterial territory is affected
tion guidelines [115], will likely remain the mainstay of [126] and certain sites such as the putamen have been associ-
treatment for most BBGH cases. ated with a higher frequency and volume of early hemorrhage
expansion [96, 97]. The bilateral nature of hemorrhage raises
Outcomes questions as to whether the contralateral hematoma in BBGH
assists in stabilizing the clot due to a stanching effect on the
Outcomes of BBGH were dismal. More than half of patients surrounding vessels, though this remains speculative.
experienced vegetative state, severe disability, or death
(56%), while only 28% experienced what was deemed good Limitations
recovery though follow-up was limited with an average
time of 8 months. Overall mortality rates were 25% and all This review is limited by the retrospective nature of case
occurred within the first month. Although this appears to be reports and case series, lack of consistent and comprehensive
lower than ICH mortality rates of 40% at 1 month and 54% at reporting of relevant clinical and surgical details, and differ-
1 year [1, 88], BBGH appears to have higher mortality rates ences in time periods of study which may have introduced
than unilateral basal ganglia hemorrhage cases in general confounding practice and technical factors. The assessment
(25% vs. 16%) [19]. Compared to literature reports of mostly of prognosis was subjective and scored by the authors based
unilateral cases, BBGHs have higher mortality rates among on the information provided in the text, which ranged from
non-traumatic BGH (29% vs. 13–19% [117, 118]) even in being a minimal general statement of the patient’s well-being
cases complicated with severe intraventricular hemorrhage to a more detailed explanation of exact daily functioning
(29% vs. 24–28% [119]). However, BBGH cases appear to with examples. Due to the retrospective nature of this review
have lower mortality rates among traumatic BGH (17% vs. and differences in granularity from study to study, we could
35–52% [120–123]) cases. One possibility for these differ- not evaluate the efficacy of any interventions. The severely
ences in outcomes between bilateral and unilateral disease limited number of cases with surgical management and dif-
is that in non-traumatic cases, BBGH correlates with greater ferences in surgical detail prevent us from offering indica-
burden of disease. However, in traumatic cases, BBGH may tions and insight into when surgical approaches would be
relate more to the direction or nature (e.g., diffuse, uniform) beneficial and what postcritical management should entail.
of external force rather than the intensity of impact. Assum- While most cases referred to the lesion as an ICH, a minor-
ing that patients with vegetative state, severe disability, or ity of cases referred to the lesion as a hemorrhagic infarct
death correspond to a modified Rankin Scale (mRS) of at or hemorrhagic necrosis though the criteria for naming was
least greater than 3, spontaneous BBGH cases also appear not explicitly mentioned. Due to different implications on
to be associated with worse functional outcomes than spon- prognosis, clarity regarding the nature of the hemorrhage
taneous unilateral cases (65% vs. 30–50% [118, 124]). is important for future studies. This heterogeneity of the
The traumatic BBGH group tended to do better than the literature highlights the importance of standardizing the
non-traumatic group in terms of shorter average length of collection and reporting of data across different institutions
stay, higher proportion of patients alive, and significantly worldwide. Case reports and series may also carry report-
higher proportion of patients experiencing good recovery at ing biases, where authors may be more inclined to report
follow-up. This echoes findings from other studies comparing cases if they are interesting, and thus, data reported from
traumatic and non-traumatic ICH. In 2002, Siddique et al. our cohort may not completely reflect the traumatic or non-
found that traumatic ICH cases were associated with better traumatic BBGH population. Although the comparative
outcomes (good recovery and moderate disability) than those analyses detected some significant differences between the
with non-traumatic ICH (67% vs. 24%) [125]. It should be two groups, the limited number of patients with available
noted that traumatic hematomas were often more superficial data within each group should be taken into account when
and lobar (91%) than in the non-traumatic group (56%) which considering the clinical power of such findings.
may have contributed to the starker difference in outcomes
than in our dataset of exclusively deep BG hemorrhages.
Cases of traumatic ICH may have more favorable prognosis Conclusions
than non-traumatic cases due to the often younger age of
patients which was also reflected in our study (35 vs. 47), and BBGH is a rare occurrence that can be associated with a
since the etiology is related to external factors (trauma) rather wide variety of traumatic, vascular, chemical, infectious,
than intrinsic factors (e.g., impaired vasculature) that may and endocrinologic factors. The differential should be kept
also hamper recovery. Specific location within the BG may wide, and management generally follows that of current

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135   Page 20 of 24 Neurosurgical Review (2023) 46:135

ICH guidelines with supportive care and early blood pres- 4. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H,
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unilateral cases of hemorrhage require stronger evidence in matic basal ganglia hemorrhage associated with diffuse axonal
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ture. Indian Neurotrauma 13:50–54. https://​doi.​org/​10.​1055/s-​
cially in cases of deep-seated lesions. The present review 0036-​15807​16
confirms that BG hemorrhages are associated with a poor 6. Daci R, Kennelly M, Ferris A, Azeem MU, Johnson MD,
prognosis and highlights the gaps in current scores and Hamzei-Sichani F, Jun-O’Connell AH, Natarajan SK (2020)
guidelines. There is an urgent need for improved assess- Bilateral basal ganglia hemorrhage in a patient with confirmed
COVID-19. AJNR Am J Neuroradiol 41:1797–1799. https://​
ment tools and recommendations regarding BGH. Future doi.​org/​10.​3174/​ajnr.​A6712
scores and trials in this field should take into consideration 7. Lee SM, Moon JM, Chun BJ, Song KH (2015) Unusual
the specific location of hemorrhage and dominance of the intracranial hemorrhage in severe methanol intoxication. Am
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Supplementary Information  The online version contains supplemen- 8. Nagatomo Y, Yanaka K, Kamezaki T, Kobayashi E, Matsumura
tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 10143-0​ 23-0​ 2044-x. A, Nose T (1995) Recovery from primary deep cerebral venous
sinus thrombosis with recanalisation. Neuroradiology 37:645–
Availability of data and material  The datasets generated and/or ana- 648. https://​doi.​org/​10.​1007/​BF005​93380
lyzed during the current study are available from the corresponding 9. Zhang Y-X, Wei S-Q, Xing Y-Y, Liu Q, He W-J (2016) Bilat-
author on reasonable request. eral traumatic hemorrhage of the basal ganglia. Chin J Trau-
matol 19:247–248. https://​doi.​org/​10.​1016/j.​cjtee.​2015.​11.​022
Author contributions  All authors contributed to the study conception 10. Li J, Wei XH, Liu YK, Chen LS, Zhu ZQ, Hou SY, Fang XK,
and design. The study was conceptualized and supervised by G.E.U. Wang ZQ (2020) Evidence of motor injury due to damaged
and P.P. Material preparation, data collection, and analysis were per- corticospinal tract following acute hemorrhage in the basal
formed by G.W., A.C., and C.O. The first draft of the manuscript was ganglia region. Sci Rep 10:16346. https://​d oi.​o rg/​1 0.​1 038/​
written by G.W. and V.C., O.B., A.S.H., S.M.P., M.S., S.S.H., B.C., s41598-​020-​73305-8
G.E.U., and P.P. commented on previous versions of the manuscript. 11. Pérez de la Ossa N, Sobrino T, Silva Y, Blanco M, Millán M,
All authors read and approved the final manuscript. Gomis M, Agulla J, Araya P, Reverté S, Serena J, Dávalos
A (2010) Iron-related brain damage in patients with intracer-
ebral hemorrhage. Stroke 41:810–813. https://​doi.​org/​10.​1161/​
Declarations  STROK​EAHA.​109.​570168
12. Gregson BA, Rowan EN, Francis R, McNamee P, Boyers D,
Ethics approval  As this is a literature review, ethics approval is not Mitchell P, McColl E, Chambers IR, Unterberg A, Mendelow
applicable. AD, STITCH(TRAUMA) investigators (2015) Surgical Trial
In Traumatic intraCerebral Haemorrhage (STITCH): a ran-
Consent to participate  As this is a literature review and no original domised controlled trial of early surgery compared with ini-
data from new patients were collected, consent to participate is not tial conservative treatment. Health Technol Assess 19:1–138.
applicable. https://​doi.​org/​10.​3310/​hta19​700
13. Hanley DF, Thompson RE, Rosenblum M, Yenokyan G, Lane
Consent for publication  As this is a literature review and no original K, McBee N, Mayo SW, Bistran-Hall AJ, Gandhi D, Mould
data from new patients were collected, consent for publication is not WA, Ullman N, Ali H, Carhuapoma JR, Kase CS, Lees KR,
applicable. Dawson J, Wilson A, Betz JF, Sugar EA et al (2019) Efficacy
and safety of minimally invasive surgery with thromboly-
Competing interests  The authors declare no competing interests. sis in intracerebral haemorrhage evacuation (MISTIE III): a
randomised, controlled, open-label, blinded endpoint phase
3 trial. The Lancet 393:1021–1032. https://​doi.​org/​10.​1016/​
S0140-​6736(19)​30195-3
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