Acta Neurochirurgica

https://doi.org/10.1007/s00701-019-04161-3

REVIEW ARTICLE - VASCULAR NEUROSURGERY - OTHER

Efficacy and safety of middle meningeal artery embolization

in the management of refractory or chronic subdural hematomas:
a systematic review and meta-analysis
Fareed Jumah 1 & Muhammad Osama 2 & Abdurrahman I. Islim 3,4 & Ammar Jumah 1 & Devi Prasad Patra 5 &
Jennifer Kosty 5 & Vinayak Narayan 1 & Anil Nanda 1 & Gaurav Gupta 1 & Rimal Hanif Dossani 5

Received: 18 September 2019 / Accepted: 30 November 2019

# Springer-Verlag GmbH Austria, part of Springer Nature 2020

Abstract
Introduction Refractory or chronic subdural hematomas (cSDH) constitute a challenging entity that neurosurgeons face fre-
quently nowadays. Middle meningeal artery embolization (MMAE) has emerged in the recent years as a promising treatment
option. However, solid evidence that can dictate management guidelines is still lacking.
Methods We conducted a systematic review and meta-analysis (MA) in compliance with the PRISMA guidelines to evaluate the
efficacy and safety of MMAE compared with conventional treatments for refractory or cSDH. Databases were searched up to
March 2019. Using a random-effects model, meta-analyses of proportions and risk difference were conducted recurrence, need
for surgical rescue, and complications.
Results Eleven studies (177 patients) were included. Majority (116, 69%) were males with a weighted mean age of
71 + −19.5 years. Meta-analysis of proportions showed treatment failure to be 2.8%, need for surgical rescue 2.7%, and
embolization-related complications 1.2%. Meta-analysis of risk-difference between embolized and non-embolized pa-
tients showed a 26% (p < 0.001, 95% CI 21%–31%, I2 = 0) lower risk of hematoma recurrence in MMAE. Similarly,
in the embolized group, the need for surgical rescue was 20% less (p < 0.001, 95% CI = 12%–27%, I2 = 12.4), and
complications were 3.6% less (p = 0.008, 95% CI 1%–6%, I2 = 0) compared to conventional groups.
Conclusions Although MMAE appears to be a promising treatment for refractory or cSDH, drawing definitive conclusions
remains limited by paucity of data and small sample sizes. Multicenter, randomized, prospective trials are needed to compare
embolization to conventional treatments like watchful waiting, medical management, or surgical evacuation. More extensive
research on MMAE could begin a new era in the minimally invasive management of cSDH.

Keywords Neurosurgery . Endovascular procedures . Embolization, therapeutic . Hematoma, subdural, intracranial

This article is part of the Topical Collection on Vascular Neurosurgery -

Other
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00701-019-04161-3) contains supplementary
material, which is available to authorized users.

* Rimal Hanif Dossani 3

Institute of Translational Medicine, University of Liverpool,
rimalh@gmail.com Liverpool, UK
4
1
Department of Neurosurgery, The Walton Centre NHS Foundation
Department of Neurosurgery, Rutgers- Robert Wood Johnson Trust, Liverpool, UK
Medical School & University Hospital, New Brunswick, NJ, USA 5
2
Department of Neurosurgery, Louisiana State University Health
Department of Surgery, Dr. Ruth KM Pfau Hospital, Dow University Sciences Center, Shreveport, LA, USA
of Health Sciences, Karachi, Pakistan

Introduction
Chronic subdural hematoma (cSDH) is one of the most
common conditions that neurosurgeons face nowadays.
Surgical evacuation and drainage by burr hole remains
the gold standard for treatment. However, the growing
elderly population, increasing comorbidity burden, use
of antithrombotic medications, and high failure rates that
plague surgical treatments (2%–37%) all have made sur-
gical decision-making more challenging. [1, 10, 17, 24,
53] A number of nonsurgical options including steroids,
statins, and ACE inhibitors have been investigated, with
unsatisfactory outcomes [5, 33, 34, 41, 45]. Other surgi-
cal procedures for the management of refractory cSDH
include placement of Ommaya reservoir [3, 37], subdural
shunt [2, 29, 49], hematoma drainage and membranecto-
my through craniotomy [48], and endoscopic-assisted
evacuation of septated or organized cSDH [13, 35].
Middle meningeal artery embolization has emerged as a
promising treatment modality after the first successful report
in 2000 [25]. Thanks to histopathologic and radiologic studies
[21, 30, 38, 43, 51], we have gained a deeper understanding of
the true pathophysiology underlying the refractoriness and
chronicity of subdural hematomas. Dural feeders from the
middle meningeal artery (MMA) supplying the hematoma
capsule play a major role in re-bleeding after surgical evacu-
ation, thus should be obliterated. Herein, we systematically
review the literature regarding the efficacy and safety of this
procedure in treating refractory or chronic subdural
hematomas.
Methods
We performed this systematic review in line with the Preferred
Reporting Items for Systematic Reviews and Meta-analyses
(PRISMA) guidelines to carry out literature search, to deter-
mine inclusion and exclusion criteria, and to select appropriate
statistical methods (Fig. 1) [20]. No ethical approval or patient
consent was needed for this study.
Literature search
A detailed search of the literature, last updated on
March 5, 2019, was performed in Medline (Ovid),
EMBASE (Ovid), the Cochrane Library, and CINAHL
Plus (EBSCO) using various combinations of the key-
words “embolization,” “middle meningeal artery”,
“chronic subdural hematoma”, and “refractory subdural
hematoma.” The search strategy implemented in
Medline, EMBASE, and CINAHL Plus is outlined in
Supplementary Material 1. Furthermore, a detailed
Acta Neurochir
inspection of the reference lists of relevant publications
was performed.
Study selection
After removing duplicates, two authors (FJ, OM) indepen-
dently carried out title and abstract screening based on the
population, intervention, comparison, outcome, and study de-
sign (PICOS) shown in Supplementary Material 2. Next, the
same authors ran a thorough full-text inspection of the resul-
tant articles to ensure final eligibility for data extraction.
Conflicts were resolved after discussion with the senior author
(RHD). Due to scarcity of data, we included studies with small
sample sizes < 5 patients—but not case reports—as well as
studies with of patients undergoing MMAE without a com-
parator arm.
Data extraction and outcome measures
From eligible studies, two authors (FJ and OM) indepen-
dently extracted data on patient characteristics, treatment
parameters, outcomes, and complications. Patient demo-
graphics and characteristics included sex, age, history of
chronic alcoholism, cerebral atrophy, use of antiplatelets
and anticoagulants, hypertension, diabetes, previous cere-
brovascular accidents, cardiovascular disease, and head
trauma. We also looked at laterality and mean thickness
of hematomas on imaging, as well as the percentage of
symptomatic hematomas. In the management of subdural
hematomas, we recorded the embolization materials used,
adjunct surgical drainage following embolization, and the
follow-up duration of patients. The main outcome of in-
terest was the failure rate of embolization, defined as per-
centage of patients who had hematoma recurrence after
embolization. Secondary outcomes included the need for
surgical rescue, defined as surgical drainage of hematoma
after failed embolization. Finally, complications—
including mortality—related to embolization procedure
were recorded. Extracted data was organized into a
Microsoft Excel spreadsheet before importing into statis-
tical software.
Statistical analysis
Data was collected from individual studies and presented as
percentages, means, or medians. The pooled rates (95% con-
fidence interval [95% CI]) of primary outcome measures were
calculated and a cutoff of P < 0.05 denoted statistical signifi-
cance. Given the assumption of heterogeneity within study-
specific patient populations and research methodologies, all
meta-analyses were conducted using a random-effects model
(DerSirmonian-Laird method). In the risk-difference meta-
analysis, results are deemed statistically insignificant when
Acta Neurochir
Fig. 1 PRISMA flowchart
demonstrating the study selection
process
the 95% CI crosses zero. Study heterogeneity was assessed
using the I2 and Cochran’s Q tests. Based on I2 values, het-
erogeneity was considered low (≤ 25%), moderate (~ 50%), or
high (≥ 75%).
Simple pooled analysis
We combined patient characteristics and treatment parameters
(except hematoma thickness) in embolized patients across all
studies, which we reported as percentages. A comparison of
patient characteristics between embolized and conventional
treatment groups was assessed using Chi-squared and
Student’s t-test for categorical and continuous variables,
respectively. Descriptive statistics were performed using
Microsoft Excel 2019.
Meta-analysis
Meta-analyses were used to assess outcomes of MMA embo-
lization. First, we ran a meta-analysis of proportions to com-
bine outcomes (failure rate, need for surgical rescue, and com-
plications) of embolized patients across all studies. On the
other hand, we compared outcomes between embolized and
non-embolized patients across double-armed cohort studies
using a meta-analysis of risk difference. Meta-analyses were
performed using OpenMeta-analyst v5.26.14.

Quality and Bias assessment
Using the National Heart, Lung, and Blood Institute (NHLBI)
Quality Assessment Tool, two authors (FJ and AI) indepen-
dently assessed the quality of selected studies using standard-
ized checklists [31]. Conflicts were resolved by discussion
with the senior author (RHD). This assessment tool evaluates
the internal validity of studies based on parameters like selec-
tion, measurement, and outcomes biases. Reporting bias was
assessed via the Harbord’s and Begg’s tests with correspond-
ing funnel plot generated in StatsDirect v3.0.
Results
Study and patient characteristics
After removal of duplicates, 1077 articles were identified; 85
were retrieved for further evaluation of which 11 met our
criteria for data extraction. Our selection process resulted in
177 patients across three cohort studies [4, 19, 26] and eight
case series [6, 12, 14, 15, 21, 22, 28, 44]. The three cohort
studies, one of which was prospective [4], were double-arm
studies and contributed to almost half of the aggregate sample
size (96 patients; 54%).
Most patients were male (116/169; 69%) with a weighted
mean age of 71 + −19.5 years. Rate of chronic alcoholism was
15% (15/98), cerebral atrophy 39% (41/104), use of
anticoagulants/antiplatelets 52% (87/165), and history of head
trauma 55% (64/116). The radiological appearance of SDH on
CT prior to MMA embolization was recorded in 9 studies.
About 73% of hematomas were unilateral (23%; 33/143 on
the right, and 50%; 71/143 on the left) while 28% (45/160)
were bilateral. Mean hematoma thickness was reported in 4
Fig. 2 Baseline comparison of patient characteristics. This histogram
shows the pooled samples from three cohort studies that compared
MMA embolization (n = 96) versus conventional treatment (n = 502)
groups. Parameters that achieved statistical significance are use of AP/
Acta Neurochir
studies [4, 19, 21, 22], with a weighted mean of 17.9 +
−13.3 mm. Majority of patients had symptomatic hematomas
(82%; 118/144), despite having received at least one attempt
of surgical drainage (72%; 123/170) using burr hole or
craniotomy.
Comparison of baseline characteristics between the
embolized and non-embolized groups (Fig. 2) revealed statis-
tically significant differences in use of AC and/or AP (X2 =
9.7, p = 0.002), hematoma thickness on CT (t-test = 3.3, p =
0.001), cerebral atrophy (X2 = 9.5, p = 0.002), hypertension
(X2 = 8.8, p = 0.003), and CVD (X2 = 4.2, p = 0.04). Detailed
patient characteristics are shown in Supplementary Material 3.
Treatment characteristics
The type of embolic material used was polyvinyl alcohol
(91%; 160/177), occasionally supplemented with coils (4%;
7/161) and NCBA in 9% (16/177). Almost a third of patients
received adjunct surgical drainage of hematoma immediately
following embolization (36%; 62/170). Mean follow-up dura-
tion was 20 weeks (range = 6–60). Details of treatment param-
eters are shown in Supplementary Material 4.
Outcomes and complications
In embolized patients across 11 studies, proportion MA
showed rate of treatment failure to be 2.8% (95% CI =
0.5%–5.2%, I2 = 0%), need for surgical rescue 2.7% (95%
CI = 0.4%–5%, I2 = 0%), and embolization-related complica-
tions 1.2% (95% CI 0.4%–2.7%, I2 = 0%). See
Supplementary Material 5 for detailed outcomes in individual
studies. Meta-analysis of risk-difference (Fig. 3) between
embolized and non-embolized patients in three double-
armed cohort studies showed a 26% lower risk of failure in
AC, presence of bilateral hematomas. *Age in years, **Hematoma
thickness in millimeters. AP, antiplatelet; AC, anticoagulation; BL,
bilateral; HTN, hypertension; DM, diabetes mellitus; CVA,
cerebrovascular accidents; CVD, cardiovascular disease
Acta Neurochir
Fig. 3 Forest plots of studies comparing (a) treatment failure, (b) the need
for surgical rescue, and (c) complications in embolized versus
conventional treatment groups. The black squares indicate the incidence
of event from each study, with square sizes reflecting the statistical weight
of the study. The blue diamonds indicate the summary effect size. The
horizontal lines indicate 95% confidence intervals. The vertical solid line
MMAE (95% CI 21%–31%, I2 = 0, Cochran Q = 0.64) that
was statistically significant (p < 0.001). Similarly, the need for
surgical rescue in MMAE group was 20% less than conven-
tional group (95% CI = 12%–27%, I2 = 12.4, Cochran Q =
2.28) with p < 0.001. Complication rate was 3.6% less in
embolized compared to conventional treatment groups (95%
CI 1%–6%, I2 = 0, Cochran Q = 0.31) that was statistically
significant (p = 0.008).
Quality and bias assessment results
The quality assessment for each in individual study is summa-
rized in Supplementary Material 6. Five studies were rated
“good,” four rated “fair,” and two “poor.” The generated fun-
nel plot for the single-arm MA of 11 studies was suspicious
indicates the line of no effect (risk difference = 0). These plots show that
all measures achieved statistically significant difference all to three
outcomes in favor of embolization over conventional treatment. Wide
confidence intervals are possibly due to small number and size of
analyzed studies
for possible reporting bias However, Harbord’s (bias = 0.001)
and Begg’s (0.393) tests (p > 0.05) failed to indicate a statisti-
cally significant bias (Supplementary Material 7).
Discussion
Summary of findings
We performed this systematic review to evaluate the role of
MMA embolization as an emerging treatment option for
chronic or refractory subdural hematomas. Eleven studies
comprising 177 patients were included. Our results show
MMAE to have high success rates in patient with refractory
or cSDH with minimal complications.

Rationale
The demographics of patients with cSDH have been changing
over the past 2 decades where they are becoming older, har-
boring more comorbidities and increasingly using antithrom-
botic medications [9, 46]. Despite this change, the manage-
ment of cSDH has relatively remained unchanged, and surgi-
cal evacuation remains the gold standard treatment. However,
repeated surgical drainage for recurrent hematomas is risky in
this fragile patient population. Therefore, we are in need, now
more than ever, of less invasive treatment strategies that obvi-
ate scalp incision, skull drilling, and general anesthesia. The
etiology of CSDH was historically thought to be due to frank
trauma; however, research has brought evidence to support a
more complex pathophysiology that involves cycles of angio-
genesis, fibrinolysis, and inflammation [8, 11, 16, 18, 32, 36,
40]. The process starts with traumatic damage to the arachnoid
membrane and bridging veins. Dural border cell layer sepa-
rates and CSF and blood extravasate into the subdural space,
and, by mixing with each other, elicit an inflammatory re-
sponse releasing chemokines that attract inflammatory cells,
including eosinophils, neutrophils, lymphocytes, and macro-
phages [11, 32, 36]. Afterwards, granulation tissue derived
from the dura mater forms the cavity’s outer membrane.
Angiogenesis follows, creating a network of fragile and leaky
neovasculature within the walls of the outer membrane that
penetrate the overlying dura and end up connecting to the
MMA [8, 11, 18, 32, 36, 40]. In this way, these penetrating
vessels act as an important source of bleeding and growth
mediators which further nourish the hematoma, hence the the-
orized benefit of MMA embolization which halts bleeding and
allows the brain to resorb hematoma over time. Takizawa et al.
showed that the MMA was significantly larger on the ipsilat-
eral side of the hematoma [42], further supporting the role of
MMA in the development of cSDH. Furthermore, D-dimers
and fibrinogen were found in the hematoma which suggests a
process of fibrinolysis that prevents formation of platelet plug
[16, 52]. The traditional view of SDH as an isolated venous
pathology has now thus shifted to involve the MMA as an
evident culprit in pathogenesis.
Clinical implications
Despite the growing interest in MMA embolization, data is
still scare and surgical evacuation of remains first-line treat-
ment. However, MMA embolization seems to be an attractive
alternative to surgical management in the treatment of recur-
rent cSDH. In asymptomatic patients or patients with tolerable
symptoms, studies have shown MMA to be an excellent treat-
ment option [4, 19, 22]. According to our review, failure rate
of this procedure was almost 3%, all of which were due to
hematoma recurrence on follow-up, while a complication rate
of only 1.12%. Some of the largest patient series up to date
Acta Neurochir
consisting 72 and 60 patients showed zero embolization-
related complications [4, 22]. Furthermore, our review shows
that rates of hematoma recurrence—and subsequent rescue
drainage—tend to be 26% and 20% lower, respectively, in
patients who underwent MMA embolization compared with
conventional treatment groups. Ban et al. [4] suggested that, in
asymptomatic cSDH, MMA embolization can be used as an
alternative to surgical evacuation. However, in those requiring
symptomatic relief, a combination of surgical drainage and
MMAE seems optimal. In our analysis, the big proportion of
symptomatic patients undergoing embolization (82%) com-
bined with the favorable outcomes suggest that MMA embo-
lization can be safely used in patients with symptoms given
they can tolerate it.
Taking it a step further, Link et al. [21] utilized the proce-
dure as upfront treatment for cSDH that has failed conserva-
tive medical management, reporting excellent outcomes.
However, intolerable symptoms, mass effect, neurologic dete-
rioration, or impending signs of herniation unquestionably
warrant surgical evacuation. More interestingly, as per our
analysis, patients who underwent embolization had signifi-
cantly better outcomes compared with the conventional treat-
ment group despite being more likely to have risk factors
compared to conventional groups such as use of antithrombot-
ic medications (p = 0.002) and cerebral atrophy (p = 0.002).
Embolization of the MMA requires excellent knowledge of
its structure. In most cases, the MMA usually branches off the
maxillary artery and enters through the foramen spinosum to
course laterally within the floor of the middle cranial fossa. It
branches into two main divisions, the frontal (anterior) and
parietal (posterior) branches which supply the dura mater
and periosteum of inner calvaria. Since these are the targets
of embolization, the tip of microcatheter should be placed
proximal to their origin in order to achieve maximal oblitera-
tion (Fig. 4) [23, 47]. Moreover, it is important to remember
that some regions of the dura receive blood supply from other
arteries: branches of the ophthalmic, occipital, and vertebral
arteries. These can become important sources of hematoma
recurrence following MMA embolization [47]. Given the
complex embryological origin of the MMA, many anatomic
variations exist, which calls for careful interpretation of angi-
ography when planning for embolization. For example, when
ophthalmic or petrosal branches are identified, the tip of
microcatheter must be meticulously advanced past these
branches in order to avoid blindness and injury to the facial
nerve, respectively. However, even if such branches cannot be
identified on angiography, it is recommended to advance the
microcatheter tip past the petrous part of temporal bone. [23].
Comparison with previous studies
Previous systematic reviews have assessed the role of MMA
embolization in cSDH refractory to conventional treatments
Acta Neurochir
Fig. 4 a Pre-embolization conventional angiogram showing the anterior
(short arrow) and posterior (long arrow) branches of the middle
meningeal artery distal to the bifurcation (circle). Note the mini
craniotomy (asterisk) previously employed to drain the subdural
[7, 39, 50]. However, no meta-analyses were conducted in two
of them as the authors felt they were unfeasible. They reported
recurrence in 3.6% [50] and 5.3% [7] of 193 procedures and
190 patients, respectively, compared to 2.8% in our analysis.
On the other hand, Srivatsan et al. performed a meta-analysis
of odds ratio on three studies revealing similar with regard to
reduction of risk of recurrence (26% vs. 25.6%) and compli-
cations (3.6% vs. 2.3%) in embolized patients [39]. Our meta-
analysis additionally reported a 20% reduction in the need for
surgical rescue in patients who underwent MMAE. Meta-
analyses of odds ratio tend to overestimate the difference
when arms have zero events. Thus, we felt a meta-analysis
of risk difference was more appropriate in comparing
embolized vs. non-embolized patients.
Study strengths and limitations
This study was conducted in strict compliance with the
PRISMA guidelines. We were able to carry out a meta-
analysis using a random-effects model and included a quality
analysis of the included studies (Supplementary Material 6).
However, this systematic review is not free of limitations. For
the most part, the analysis was mainly based on retrospective
studies, case series, and case reports which affect the power of
the results. The small sample sizes and marked heterogeneity
between the included studies further limit our ability to draw
definitive conclusions that can establish clearer management
guidelines. Due to wide confidence intervals (Fig. 3), caution
should be exercised in interpretation of pooled proportions.
hematoma in a patient with multiple hematoma recurrences. b
Postembolization angiogram showing the onyx filling the common
trunk (short arrow) and posterior branch (long arrow) thus achieving
maximal occlusion of the MMA blood supply to the dura
It is worth noting that the number of patients who received
MMAE as primary and secondary treatments was 123 (72%)
and 47 (28%), respectively, and analyzing outcomes in these
two populations is warranted. However, subgroup analysis
was not possible due to absence of individual patient data.
Furthermore, almost third of patients received surgical drain-
age following embolization. Inclusion of these patients makes
it hard to know whether treatment success occurred due to
embolization, drainage, or the combination. However, major-
ity of patients who underwent both are from the studies which
were included in the meta-analyses of risk difference [4, 19,
26] that compared them against standard of care, i.e., surgical
evacuation which highlights the utility of MMAE. Future
comparative studies of these two patient populations are war-
ranted to answer this question.
Conclusion—where do we stand on MMA
embolization?
Endovascular embolization of the middle meningeal artery
has gained increasing interest in the treatment of chronic or
refractory subdural hematomas. Despite a growing body of
evidence that points to its efficacy and safety, large, prospec-
tive controlled trials [27] are needed to compare embolization
to conventional treatments, like watchful waiting, medical
management, or surgical evacuation. Future studies should
also evaluate other important parameters like median Rankin
Scores pre- and post-embolization, time for brain re-

expansion, and possibly compare different embolic materials.
With more extensive research, MMA embolization could be-
gin a new era in minimally invasive management of chronic
subdural hematomas.
Author contributions The following authors have contributed to the
manuscript “Efficacy and Safety of Middle Meningeal Artery
Embolization in the Management of Refractory or Chronic Subdural
Hematomas: a Systematic Review and Meta-analysis” as follows:
• Conception and Design: Rimal Dossani, Fareed Jumah,
Abdurrahman Islim, Gaurav Gupta, and Anil Nanda
• Data Acquisition: Fareed Jumah, Muhammad Osama, Ammar
Jumah, and Vinayak Narayan
• Data Analysis: Fareed Jumah, Abdurrhaman Islim, Devi Patra,
Vinayak Narayan
• Interpretation of Data: Fareed Jumah, Abdurrahman Islim, Jennifer
Kosty, Devi Patra, and Vinayak Narayan
• Drafting Manuscript: Fareed Jumah, Muhammad Osama, Ammar
Jumah, Jennifer Kosty, Rimal Dossani, Vinayak Narayan, and Gaurav
Gupta
• Critical Revision of Manuscript: Rimal Dossani, Jennifer Kosty,
Devi Patra, Abdurrahman Islim, Gaurav Gupta, Anil Nanda, Vinayak
Narayan
• Final Approval of Manuscript: All authors
• Agreement to be accountable for all aspects of work: All authors
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval This article does not contain any studies with human
participants or animals performed by any of the authors.
Informed consent No informed consent was required for this study.
References
1. Almenawer SA, Farrokhyar F, Hong C, Alhazzani W, Manoranjan
B, Yarascavitch B, Arjmand P, Baronia B, Reddy K, Murty N,
Singh S (2014) Chronic subdural hematoma management: a sys-
tematic review and meta-analysis of 34,829 patients. Ann Surg 259:
449–457. https://doi.org/10.1097/SLA.0000000000000255
2. Aoki N (1990) Chronic subdural hematoma in infancy: clinical
analysis of 30 cases in the CT era. J Neurosurg 73:201–205
3. Arbit E, Patterson RH Jr, Fraser RA (1981) An implantable subdur-
al drain for treatment of chronic subdural hematoma. Surg Neurol
15:175–177
4. Ban SP, Hwang G, Byoun HS, Kim T, Lee SU, Bang JS, Han JH,
Kim C-Y, Kwon O-K, Oh CW (2017) Middle meningeal artery
embolization for chronic subdural hematoma. Radiology 286:
992–999
5. Berghauser Pont LM, Dirven CM, Dippel DW, Verweij BH,
Dammers R (2012) The role of corticosteroids in the management
of chronic subdural hematoma: a systematic review. Eur J Neurol
19:1397–1403. https://doi.org/10.1111/j.1468-1331.2012.03768.x
6. Chihara H, Imamura H, Ogura T, Adachi H, Imai Y, Sakai N (2014)
Recurrence of a refractory chronic subdural hematoma after middle
meningeal artery embolization that required craniotomy. NMC
Case Rep J 1:1–5
Acta Neurochir
7. Court J, Touchette CJ, Iorio-Morin C, Westwick HJ, Belzile F,
Effendi K (2019) Embolization of the middle meningeal artery in
chronic subdural hematoma–a systematic. Clin Neurol Neurosurg
105464
8. Frati A, Salvati M, Mainiero F, Ippoliti F, Rocchi G, Raco A, Caroli
E, Cantore G, Delfini R (2004) Inflammation markers and risk
factors for recurrence in 35 patients with a posttraumatic chronic
subdural hematoma: a prospective study. J Neurosurg 100:24–32
9. Gaist D, Rodríguez LAG, Hellfritzsch M, Poulsen FR, Halle B,
Hallas J, Pottegård A (2017) Association of antithrombotic drug
use with subdural hematoma risk. Jama 317:836–846
10. Gernsback J, Kolcun JP, Jagid J (2016) To drain or two drains:
recurrences in chronic subdural hematomas. World Neurosurg 95:
447–450. https://doi.org/10.1016/j.wneu.2016.08.069
11. Haines DE, Harkey HL, Al-Mefty O (1993) The “subdural” space:
a new look at an outdated concept. Neurosurgery 32:111–120
12. Hashimoto T, Ohashi T, Watanabe D, Koyama S, Namatame H,
Izawa H, Haraoka R, Okada H, Ichimasu N, Akimoto J (2013)
Usefulness of embolization of the middle meningeal artery for re-
fractory chronic subdural hematomas. Surg Neurol Int 4
13. Hellwig D, Kuhn TJ, Bauer BL, List-Hellwig E (1996) Endoscopic
treatment of septated chronic subdural hematoma. Surg Neurol 45:
272–277
14. Hirai S, Ono J, Odaki M, Serizawa T, Nagano O (2004)
Embolization of the middle meningeal artery for refractory chronic
subdural haematoma: usefulness for patients under anticoagulant
therapy. Interv Neuroradiol 10:101–104
15. Ishihara H, Ishihara S, Kohyama S, Yamane F, Ogawa M, Sato A,
Matsutani M (2007) Experience in endovascular treatment of recur-
rent chronic subdural hematoma. Interv Neuroradiol 13:141–144
16. Ito H, Yamamoto S, Komai T, Mizukoshi H (1976) Role of local
hyperfibrinolysis in the etiology of chronic subdural hematoma. J
Neurosurg 45:26–31
17. Ivamoto HS, Lemos HP Jr, Atallah AN (2016) Surgical treatments
for chronic subdural hematomas: a comprehensive systematic re-
view. World Neurosurg 86:399–418. https://doi.org/10.1016/j.
wneu.2015.10.025
18. Kalamatianos T, Stavrinou LC, Koutsarnakis C, Psachoulia C,
Sakas DE, Stranjalis G (2013) PlGF and sVEGFR-1 in chronic
subdural hematoma: implications for hematoma development. J
Neurosurg 118:353–357
19. Kim E (2017) Embolization therapy for refractory hemorrhage in pa-
tients with chronic subdural hematomas. World Neurosurg 101:520–527
20. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC,
Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D
(2009) The PRISMA statement for reporting systematic reviews
and meta-analyses of studies that evaluate health care interventions:
explanation and elaboration. PLoS Med 6:e1000100
21. Link TW, Boddu S, Marcus J, Rapoport BI, Lavi E, Knopman J
(2017) Middle meningeal artery embolization as treatment for
chronic subdural hematoma: a case series. Oper Neurosurg 14:
556–562
22. Link TW, Boddu S, Paine SM, Kamel H, Knopman J (2018)
Middle meningeal artery embolization for chronic subdural hema-
toma: a series of 60 cases. Neurosurgery. https://doi.org/10.1093/
neuros/nyy521
23. Link TW, Rapoport BI, Paine SM, Kamel H, Knopman J (2018)
Middle meningeal artery embolization for chronic subdural hema-
toma: endovascular technique and radiographic findings. Interv
Neuroradiol 24:455–462
24. Liu W, Bakker NA, Groen RJ (2014) Chronic subdural hematoma: a
systematic review and meta-analysis of surgical procedures. J
Neurosurg 121:665–673. https://doi.org/10.3171/2014.5.JNS132715
25. Mandai S, Sakurai M, Matsumoto Y (2000) Middle meningeal
artery embolization for refractory chronic subdural hematoma: case
report. J Neurosurg 93:686–688
Acta Neurochir
26. Matsumoto H, Hanayama H, Okada T, Sakurai Y, Minami H,
Masuda A, Tominaga S, Miyaji K, Yamaura I, Yoshida Y (2018)
Which surgical procedure is effective for refractory chronic subdur-
al hematoma? Analysis of our surgical procedures and literature
review. J Clin Neurosci 49:40–47
27. Middle Meningeal Artery Embolization for Treatment of Chronic
Subdural Hematoma (2019) Retrieved from https://ClinicalTrials.
gov/show/NCT03307395. (Identification No. NCT03307395).
Weill Cornell Medical College, New York
28. Mino M, Nishimura S, Hori E, Kohama M, Yonezawa S,
Midorikawa H, Kaimori M, Tanaka T, Nishijima M (2010)
Efficacy of middle meningeal artery embolization in the treatment
of refractory chronic subdural hematoma. Surg Neurol Int 1
29. Misra M, Salazar JL, Bloom DM (1996) Subdural-peritoneal shunt:
treatment for bilateral chronic subdural hematoma. Surg Neurol 46:
378–383
30. Nagahori T, Nishijima M, Takaku A (1993) Histological study of
the outer membrane of chronic subdural hematoma: possible mech-
anism for expansion of hematoma cavity. No shinkei geka Neurol
Surg 21:697–701
31. National Heart L, Institute B (2014) Quality assessment tool for ob-
servational cohort and cross-sectional studies. National Institutes of
Health, Department of Health and Human Services, Bethesda
32. Orlin JR, Osen KK, Hovig T (1991) Subdural compartment in pig:
a morphologic study with blood and horseradish peroxidase infused
subdurally. Anat Rec 230:22–37
33. Poulsen FR, Munthe S, Søe M, Halle B (2014) Perindopril and
residual chronic subdural hematoma volumes six weeks after burr
hole surgery: a randomized trial. Clin Neurol Neurosurg 123:4–8
34. Qiu S, Zhuo W, Sun C, Su Z, Yan A, Shen L (2017) Effects of
atorvastatin on chronic subdural hematoma: a systematic review.
Medicine 96
35. Rodziewicz G, Chuang W (1995) Endoscopic removal of organized
chronic subdural hematoma. Surg Neurol 43:569–573
36. Santarius T, Kirkpatrick PJ, Kolias AG, Hutchinson PJ (2010)
Working toward rational and evidence-based treatment of chronic
subdural hematoma. Clin Neurosurg 57:112–122
37. Sato M, Iwatsuki K, Akiyama C, Kumura E, Yoshimine T (2001)
Implantation of a reservoir for refractory chronic subdural hemato-
ma. Neurosurgery 48:1297–1301. https://doi.org/10.1097/
00006123-200106000-00023
38. Shono T, Inamura T, Morioka T, K-i M, Suzuki SO, Ikezaki K,
Iwaki T, Fukui M (2001) Vascular endothelial growth factor in
chronic subdural haematomas. J Clin Neurosci 8:411–415
39. Srivatsan A, Mohanty A, Nascimento FA, Hafeez MU, Srinivasan
VM, Thomas A, Chen SR, Johnson JN, Kan P (2018) Middle
meningeal artery embolization for chronic subdural hematoma:
meta-analysis and systematic review. World Neurosurg
40. Stanisic M, Aasen AO, Pripp AH, Lindegaard K-F, Ramm-
Pettersen J, Lyngstadaas SP, Ivanovic J, Konglund A, Ilstad E,
Sandell T (2012) Local and systemic pro-inflammatory and anti-
inflammatory cytokine patterns in patients with chronic subdural
hematoma: a prospective study. Inflamm Res 61:845–852
41. Sun T, Boet R, Poon W (2005) Non-surgical primary treatment of
chronic subdural haematoma: preliminary results of using dexa-
methasone. Br J Neurosurg 19:327–333
42. Takizawa K, Sorimachi T, Ishizaka H, Osada T, Srivatanakul K,
Momose H, Matsumae M (2016) Enlargement of the middle men-
ingeal artery on MR angiography in chronic subdural hematoma. J
Neurosurg 124:1679–1683
43. Tanaka T, Fujimoto S, Saito K, Kaimori M (1997) Histological
study of operated cases of chronic subdural hematoma in adults:
relationship between dura mater and outer membrane. No shinkei
geka Neurol Surg 25:701–705
44. Tempaku A, Yamauchi S, Ikeda H, Tsubota N, Furukawa H, Maeda
D, Kondo K, Nishio A (2015) Usefulness of interventional embo-
lization of the middle meningeal artery for recurrent chronic sub-
dural hematoma: five cases and a review of the literature. Interv
Neuroradiol 21:366–371
45. Thotakura AK, Marabathina NR (2015) Nonsurgical treatment of
chronic subdural hematoma with steroids. World Neurosurg 84:
1968–1972
46. Toi H, Kinoshita K, Hirai S, Takai H, Hara K, Matsushita N,
Matsubara S, Otani M, Muramatsu K, Matsuda S (2018) Present
epidemiology of chronic subdural hematoma in Japan: analysis of
63,358 cases recorded in a national administrative database. J
Neurosurg 128:222–228
47. Tunali S (2016) External carotid artery. In: Shoja MM, Loukas M
(eds) Tubbs RS. John Wiley & Sons, Bergman's Comprehensive
Encyclopedia of Human Anatomic Variation, pp 477–486. https://
doi.org/10.1002/9781118430309.ch47
48. Tyson G, Strachan WE, Newman P, Winn HR, Butler A, Jane J
(1980) The role of craniectomy in the treatment of chronic subdural
hematomas. J Neurosurg 52:776–781
49. Vinchon M, Noulé N, Soto-Ares G, Dhellemmes P (2001)
Subduroperitoneal drainage for subdural hematomas in infants: re-
sults in 244 cases. J Neurosurg 95:249–255
50. Waqas M, Vakharia K, Weimer PV, Hashmi E, Davies JM, Siddiqui
AH (2019) Safety and effectiveness of embolization for chronic sub-
dural hematoma: systematic review and case series. World Neurosurg
51. Weigel R, Hohenstein A, Schilling L (2014) Vascular endothelial
growth factor concentration in chronic subdural hematoma fluid is
related to computed tomography appearance and exudation rate. J
Neurotrauma 31:670–673
52. Weir B, Gordon P (1983) Factors affecting coagulation: fibrinolysis
in chronic subdural fluid collections. J Neurosurg 58:242–245.
https://doi.org/10.3171/jns.1983.58.2.0242
53. Xu CS, Lu M, Liu LY, Yao MY, Cheng GL, Tian XY, Xiao F, Wan
Q, Chen F (2017) Chronic subdural hematoma management: clar-
ifying the definitions of outcome measures to better understand
treatment efficacy - a systematic review and meta-analysis. Eur
Rev Med Pharmacol Sci 21:809–818
Publisher’s note Springer Nature remains neutral with regard to jurisdic-
tional claims in published maps and institutional affiliations.