Factors Affecting Chronic Subdural Hematoma Recurrence after Middle Meningeal Artery Embolization

Abstract

Objectives

Although the predictors of chronic subdural hematoma (SDH) recurrence after surgical evacuation are well known, there is limited evidence available on factors affecting its recurrence after middle meningeal artery (MMA) embolization. The objective of this study was to determine the factors influencing the risk of recurrence in patients with chronic SDH undergoing MMA embolization.

Materials and Methods

A prospective study was performed between September 2022 and October 2024 on patients with chronic SDH who underwent MMA embolization with or without surgical evacuation. The primary outcome was clinical recurrence of SDH within 90 days after the embolization, defined as new onset or worsening of existing neurological symptoms, associated with a residual or recurrent SDH with hyperdense contents on computed tomography (CT).

Statistical Analysis

The association of demographic, clinical, imaging, and angiographic parameters with SDH recurrence was analyzed. For variables that showed a significant association with recurrence, relative risks were ascertained. All statistical tests were two-sided, and a p-value of less than 0.05 was considered significant

Results

Seventy-four patients (mean age, 67.3 ± 11 [standard deviation] years; males, 66/74 [89.2%]) with 96 SDHs were included in the study. Clinical recurrence of chronic SDH was observed in 6 patients (8.1%). Membrane enhancement on pre-embolization CT was less common in hematomas that recurred than those that did not (2/8, 25% vs. 61/88, 69.3%; p = 0.018). The absence of membrane enhancement was a significant risk factor for clinical recurrence after MMA embolization (relative risk, 5.7 [95% confidence interval, 1.2–26.8], p = 0.01). Out of the 33 SDHs with no membrane enhancement, 6 recurred (18.2%).

Conclusion

The absence of enhancement on pre-embolization CT is a risk factor for SDH recurrence after MMA embolization. The high recurrence rate in hematomas without membrane enhancement indicates that MMA embolization may not reduce the risk of recurrence in these patients.

Keywords

chronic subdural hematoma - computed tomography - embolization - meningeal artery - risk factors

Introduction

Chronic subdural hematoma (SDH) occurs as a result of minor trauma that causes extravasation of blood into the subdural space, followed by inflammation and angiogenesis.[1] Following a variable latency period during which the hematoma slowly increases in size, the patients present with symptoms such as altered mental status, memory disturbances, headache, seizures, and focal neurological deficits due to compression of the adjoining brain parenchyma by the hematoma.[2] Although surgical evacuation is the primary treatment for SDH, it is associated with a high recurrence rate of 11.2 to 27.7%.[3] [4] Various factors contributing to recurrence are greater thickness of SDH, greater midline shift, hyperdense content, laminar and separated morphology, antiplatelet or anticoagulant use, bilaterality, and pneumocephalus.[5] [6] [7] [8] [9]

Middle meningeal artery (MMA) embolization reduces the incidence of chronic SDH recurrence after surgical evacuation by reducing the vascularity of the hypervascular membrane surrounding the SDH cavity.[10] Although the factors that influence the recurrence of SDH following surgical evacuation have been well studied, the factors affecting its recurrence after MMA embolization are yet to be studied in detail. SDH recurrence can occur due to vascular supply from the contralateral MMA.[11] Dural blood supply from arteries other than the ipsilateral MMA may be a cause of persistent hypervascularity in the dural membrane following MMA embolization.

Various angiographic findings seen during MMA embolization include cotton wool-like staining, contrast pooling around distal vessels, opacification of the membrane, and contrast pooling in the SDH cavity.[12] Extravasation of contrast into the SDH cavity indicates leakiness of the membrane. It needs to be studied whether these angiographic features can predict the clinical outcome after MMA embolization.

The objective of this study was to evaluate the factors that influence the risk of recurrence following MMA embolization in patients with chronic SDH.

Materials and Methods

A prospective observational study was conducted between September 2022 and October 2024 on patients with chronic SDH who underwent MMA embolization with or without surgical evacuation. The exclusion criteria were acute kidney injury, severe chronic kidney disease (estimated glomerular filtration rate < 30 mL/min/1.73 m²), history of severe contrast reaction to iodinated contrast agents, and follow-up duration < 90 days after the procedure. The study was initiated after obtaining approval from the Institute Ethics Committee, and written informed consent was obtained from all participants.

Preprocedure Imaging

All computed tomography (CT) scans were done on a SOMATOM Definition Flash dual-source 256-slice CT machine (Siemens Healthcare, Erlangen, Germany). Interpretation of the CT images was performed by a single observer with 10 years of experience in diagnostic radiology, before the MMA embolization. The imaging parameters that showed a significant association with SDH recurrence were reassessed by another independent observer with 7 years of experience in diagnostic radiology who was blinded to the treatment outcome, and the interrater agreement was ascertained. The parameters assessed on baseline CT were the maximum thickness of SDH, whether unilateral or bilateral, the degree of midline shift, and the morphology of SDH. The maximum thickness of SDH was measured on the axial section of CT above the level of the temporal bones and lateral ventricles.[13] The morphology of SDH was described as homogenous, laminated, separated, or trabecular according to the classification proposed by Nakaguchi et al.[14] In patients who underwent surgical evacuation, a noncontrast CT scan was repeated, and the thickness of the residual SDH cavity, degree of midline shift, and the presence of hyperdense contents within the cavity were noted. A multiphasic contrast-enhanced CT, with intravenous administration of 1.2 mL/kg of iohexol (Omnipaque 350, GE Healthcare, Shanghai, China), was performed before MMA embolization to ascertain the enhancement of the membrane covering the SDH cavity. Membrane enhancement was classified as involving only the outer membrane, and both outer and inner membranes ([Fig. 1]).[15] The morphology of enhancement was classified as thin, thick (≥ 2 mm in thickness), nodular, and septated ([Fig. 2]). Presence of the spandrel sign, defined as a triangular thick enhancement at the junction of the outer and the inner membranes of the SDH cavity, was ascertained ([Fig. 2B]).[16]

Fig. 1 Inner and outer membrane enhancement on preprocedure computed tomography (CT). (A, B) Noncontrast (A) and contrast-enhanced venous phase CT images showing enhancing outer membrane (arrow in B). (C, D) Noncontrast (C) and contrast-enhanced venous phase CT images showing enhancing inner (white arrow in D) and outer (black arrow in D) membranes.

Fig. 2 Patterns of membrane enhancement on preprocedure computed tomography (CT). (A–D) Contrast-enhanced venous phase CT images showing thin enhancement of the inner membrane (arrow in A), thick enhancement of the outer membrane (white arrow in B), spandrel sign (black arrow in B), nodular enhancement (arrow in C), and septated enhancement (arrow in D).

Middle Meningeal Artery Embolization

All cases were performed on an Artis Zee biplane digital subtraction angiography machine (Siemens Healthcare), with local anesthesia used for most cases and general anesthesia for uncooperative and intubated patients. The procedure was performed by one of the three interventional radiologists with at least 8 years' experience in neurovascular interventions. A 5-F 70-cm long sheath (Flexor Raabe, Cook Medical, Indiana, United States) was placed in the common carotid artery through the common femoral artery access. The external carotid artery was catheterized using a 4-F Berenstein catheter (Cordis, Florida, United States). After priming the external carotid artery with 0.5 mg nimodipine diluted in 25 mL normal saline to prevent vasospasm, the MMA was super selectively catheterized using a Merit Maestro 2.4 F microcatheter (Merit Medical, Utah, United States). The parameters observed on the MMA angiogram were the diameter of MMA just before it entered the foramen spinosum, branching pattern, anastomosis with the internal carotid artery, membrane blush, and collateral supply across the midline. Note that 0.5 mg of diluted nimodipine was injected into the MMA before the advancement of the microcatheter into the divisions to prevent vasospasm. Embolization was performed using 100 to 300 µm tris-acryl gelatin microspheres (Embospheres, Merit Medical, Utah, United States) until stasis within the MMA. MMA on the unaffected side was also embolized to reduce the risk of recurrence due to collateralization across the midline. A cone-beam CT was performed immediately after embolization to look for hyperdensity in the subdural space, suggesting contrast pooling.

Outcome Measures

The primary outcome was clinical recurrence of SDH within 90 days after the embolization, defined as new onset or worsening of existing neurological symptoms, associated with a residual or recurrent SDH with hyperdense contents on CT. Periprocedural adverse events occurring within 48 hours of the procedure were recorded as per the adverse event severity scale of the Society of Interventional Radiology.[17]

Statistical Analysis

The data were compiled and analyzed for their potential effects on the postprocedural outcome. Stata software, version 18 (StataCorp, Texas, United States), was used for statistical analysis. Fisher's exact test or chi-square test was used for categorical variables. Numerical variables were expressed as mean ± standard deviation (SD) or median with interquartile range (IQR) and analyzed using Student's t-test or Wilcoxon rank sum test. For variables that showed a significant association with recurrence, relative risks were ascertained. The kappa coefficient was used to determine the interrater agreement of variables that had a significant association with recurrence. All statistical tests were two-sided, and a p-value less of than 0.05 was considered significant.

Results

Demographics of the Study Population

MMA embolization was performed on 77 patients. After excluding 3 patients who were lost to follow-up, 74 patients were included in the final analysis. The mean age was 67.3 ± 11 (SD) years, and 89.2% of the patients (66/74) were males.

Clinical and Imaging Features

The mean duration of symptoms was 10.2 ± 14.2 (SD) days. Sixty-six patients (89.2%) had a history of antecedent head injury. Ninety-six SDHs were seen in the 74 patients. The mean thickness of SDH was 17.5 ± 7 (SD) mm, and bilateral SDH was seen in 22 patients (29.7%). Sixty-five patients (87.8%) had a midline shift in baseline CT with a mean shift of 8 ± 4.9 (SD) mm. A contrast-enhanced CT was performed after the surgical evacuation, on the day before MMA embolization in all patients. Membrane enhancement was best visualized in the venous phase of the scan. While only outer membrane enhancement was seen in 27/96 (28.1%) hematomas, both inner and outer membrane enhancement were seen in 36/96 (37.5%) hematomas. Surgical evacuation was performed before MMA embolization in 65 patients (87.8%) with 84 hematomas. The mean thickness of the residual SDH cavity on postoperative CT was 9.2 ± 4.7 (SD) mm. Hyperdense contents were seen on the postoperative CT in 53/84 (63.1%) hematomas, and residual midline shift was seen in 37/65 (56.9%) patients with a mean shift of 3 ± 3.3 (SD) mm.

MMA Embolization

MMA embolization was performed as an adjunct to surgery in 65 patients (87.8%) and as the primary treatment in 9 patients (12.2%). The findings observed in 147 MMAs during the angiography in 74 patients are depicted in [Table 1]. In one patient, MMA on the affected side could not be visualized on angiography as the internal maxillary artery was found to be occluded. Of the 147 MMAs, 95 were on the affected side and 52 were on the unaffected side. The MMA was significantly larger on the affected side (mean diameter ± SD, 1.15 ± 0.03 mm) than on the unaffected side (mean diameter ± SD, 1.03 ± 0.03 mm) (p = 0.003). Ophthalmic artery arising from the MMA and MMA arising from the ophthalmic artery were the most common variants. Cone-beam CT was performed in 68 patients with 82 SDHs immediately after MMA embolization.

Table 1 Angiographic findings observed during middle meningeal artery embolization

Variable	Number of patients (%)/Number of hematomas (%)/Number of arteries (%)/Mean ± SD
Origin
Internal maxillary artery	140/147 (95.2%)
OA	2/147 (1.4%)
Direct origin from ECA	1/147 (0.7%)
Variant anatomy
OA arising from MMA	3/147 (2%)
Anterior division arising from OA	2/147 (1.4%)
Absent posterior division	1/147 (0.7%)
ECA-ICA anastomosis
MMA to OA via lacrimal artery	1/147 (0.7%)
Dural supply from accessory meningeal artery	0
MMA supply across the midline	27/74 (36.5%)
Membrane blush during angiogram	54/95 (56.8%)
Contrast pooling on post-embolization cone-beam CT	74/82 (90.2%)

Abbreviations: CT, computed tomography; ECA, external carotid artery; ICA, internal carotid artery; MMA, middle meningeal artery; OA, ophthalmic artery; SD, standard deviation.

A total of 143 MMAs were embolized in 74 patients—93 MMAs on the affected side and 50 on the unaffected side. Only one of the MMAs could be embolized in three patients with bilateral SDH due to an occluded internal maxillary artery, MMA arising from the ophthalmic artery, and ophthalmic artery arising from MMA, with failure to advance the microcatheter distal to the ophthalmic artery origin. MMA on the unaffected side could not be embolized in two patients due to its origin from the ophthalmic artery, and a small caliber of MMA in one patient each. In two cases in which the ophthalmic artery arose from the MMA on the unaffected side, there was collateral supply from the MMA across the midline into the dura of the affected side. Embolization was therefore performed by advancing the microcatheter distal to the origin of the ophthalmic artery. Similarly, in one case in which there was anastomosis of the MMA with the ophthalmic artery, embolization was performed after advancing the microcatheter distal to the anastomosis. No procedure-related complications were observed in these cases.

Factors Affecting SDH Recurrence

The patients were followed up for a mean duration of 195.2 ± 137.6 (SD) days after MMA embolization, and eight recurrent SDHs were observed in six patients (6/74, 8.1%). The surgical rescue rate was 5.4% (4/74), and two patients with recurrence were managed conservatively. No recurrences were observed in patients in whom MMA embolization was performed as a standalone treatment. No procedure-related death or severe adverse events were observed. Minor adverse events were headache (26/74, 35.1%) and jaw pain (2/74, 2.7%), both lasting less than 24 hours.

The association of SDH recurrence following MMA embolization with the various clinical features, imaging findings, angiographic findings, and embolization parameters is depicted in [Table 2]. Membrane enhancement on the preprocedure CT was significantly less common in hematomas that recurred than those that did not (2/8, 25% vs. 61/88, 69.3%; p = 0.018). However, there was no significant association between the location or morphology of enhancement and recurrence ([Table 2]). None of the other parameters had a significant association with recurrence. The absence of membrane enhancement was a significant risk factor for clinical recurrence (relative risk, 5.7 [95% confidence interval [CI], 1.2–26.8], p = 0.01) ([Fig. 3]). Out of the 33 hematomas with no membrane enhancement, 6 recurred (18.2%). Membrane enhancement had an excellent interrater agreement between the two observers (kappa coefficient, 0.95; p-value < 0.001). In patients with recurrence, there was 100% agreement between the two observers.

Fig. 3 Recurrence of chronic subdural hematoma (SDH) after middle meningeal artery (MMA) embolization. (A) Coronal reformatted noncontrast computed tomography (CT) image of an elderly patient, on antiplatelet therapy for coronary artery disease, who presented with slurring of speech and giddiness, showing bilateral chronic SDHs. Bilateral burr-hole evacuation was done. (B) Coronal reformatted contrast-enhanced CT image showed no enhancing membrane around the SDH. (C, D) The right (C) and the left MMA (D) were superselectively catheterized and embolized using 100 to 300 µm tris-acryl gelatin microspheres. (E, F) Lateral projections of post-embolization angiograms of right (E) and left (F) MMAs showing stasis within. (G) The patient presented with paraparesis 40 days later, and noncontrast CT showed bilateral recurrent SDH.

Table 2 Association of clinical, imaging, angiographic, and embolization parameters with chronic subdural hematoma recurrence after middle meningeal artery embolization

Variable	Number of patients (%)/Number of hematomas (%)/Mean ± SD/Median (IQR)		p-Value
	No recurrence	Recurrence
Male sex	60/68 (88.2%)	6/6 (100%)	1.00
Age	67.2 ± 10.9	68.7 ± 13.4	0.76
Duration of symptoms before treatment (d)	7 (2.5–10)	6 (3–12)	0.84
Diabetes mellitus	34/68 (50%)	3/6 (50%)	1.00
Hypertension	34/68 (50%)	4/6 (66.7%)	0.68
History of trauma	44/68 (64.7%)	4/6 (66.7%)	1.00
Antiplatelet or anticoagulant use	26/68 (38.2%)	2/6 (33.3%)	1.00
Glasgow coma scale at presentation	15 (14.5–15)	15 (14–15)	0.60
Focal neurological deficit at presentation	26/68 (38.2%)	5/6 (83.3%)	0.08
Bilateral SDH	19/68 (27.9%)	3/6 (50%)	0.35
SDH thickness on baseline CT (mm)	17.4 ± 6.8	18.6 ± 9.2	0.64
Presence of midline shift on baseline CT	60/68 (88.2%)	5/6 (83.3%)	0.55
Morphology
Homogenous	19/88 (21.6%)	3/8 (37.5%)	0.51
Laminated	8/88 (9.1%)	0
Separated	33/88 (37.5%)	4/8 (50%)
Trabecular	28/88 (31.8%)	1/8 (12.5%)
SDH thickness on postoperative CT (mm)	9.1 ± 4.8	9.8 ± 4.0	0.71
Presence of midline shift on postoperative CT	33/59 (55.9%)	4/6 (66.7%)	0.69
Presence of hyperdense contents on postoperative CT	50/76 (65.8%)	3/8 (37.5%)	0.14
Membrane enhancement on pre-embolization CT	61/88 (69.3%)	2/8 (25%)	0.018
Location of membrane enhancement
Only outer membrane	25/61 (41%)	2/2 (100%)	0.18
Both outer and inner membranes	36/61 (59%)	0/2
Morphology of membrane enhancement
Thin	44/61 (72.1%)	1/2 (50%)	0.49
Thick	9/61 (14.8%)	1/2 (50%)
Nodular	1/61 (1.6%)	0/2
Septated	7/61 (11.5%)	0/2
Spandrel sign in hematomas with membrane enhancement	7/61 (11.5%)	0/2	1.00
Interval between last surgery and embolization (d)	4.7 ± 9.4	3 ± 1.8	0.66
Diameter of MMA on the affected side (mm)	1.16 ± 0.26	1.1 ± 0.15	0.53
Collateral supply from contralateral MMA	26/68 (38.2%)	1/6 (16.7%)	0.41
Membrane blush on angiogram	50/87 (57.5%)	4/8 (50%)	0.72
Bilateral MMA embolization	63/68 (92.7%)	6/6 (100%)	1.00
Microcatheter position during embolization of MMA on the affected side
Main trunk of MMA	52/85 (61.2%)	7/8 (87.5%)	0.25
Anterior and posterior divisions	33/85 (38.8%)	1/8 (12.5%)
Contrast pooling on post-embolization cone-beam CT	69/77 (89.6%)	5/5 (100%)	1.00
Postprocedure headache	24/68 (35.3%)	2/6 (33.3%)	1.00

Abbreviations: CT, computed tomography; IQR, interquartile range; MMA, middle meningeal artery; SD, standard deviation; SDH, subdural hematoma.

Discussion

MMA embolization is an effective treatment for chronic SDH, both as an adjunct to surgery and as a standalone treatment.[3] [18] [19] [20] [21] [22] In our study, we observed low clinical recurrence and surgical rescue rates of 8.1 and 5.4%, respectively, after MMA embolization. In the limited number of patients in whom MMA embolization was performed as a standalone procedure, no recurrences were observed. The low recurrence rate observed in our study is similar to that observed in prior studies.[3] [18] [19] [20] [21] [22] However, the recently published EMPROTECT trial failed to show a significant reduction in SDH recurrence after MMA embolization using tris-acryl gelatin microspheres compared with standard treatment (14.8% vs. 21%; odds ratio, 0.64 [95% CI, 0.36–1.14]; p = 0.13). The trial included only those patients who were at high risk of SDH recurrence after surgical evacuation, and the embolization was done using large 300 to 500 µm particles.[23] The use of smaller particles (100–300 µm) and the inclusion of all patients with chronic SDH, regardless of the risk of recurrence, may have contributed to the lower recurrence rate in our study.

We investigated the factors influencing the risk of SDH recurrence following MMA embolization. The absence of an enhancing membrane on the pre-embolization contrast-enhanced CT was identified as a risk factor for recurrence. Membrane formation in SDH occurs as a result of the proliferation of dural border cells, which differentiate into connective tissue.[24] The outer membrane of SDH contains pathological sinusoidal capillaries, which contribute to recurrent bleeding into the SDH cavity.[25] Membrane enhancement around the SDH cavity is associated with early recurrence after surgery, and such patients will benefit from MMA embolization as it reduces the hypervascularity of the membrane.[15] In contrast to our study results, a study by Weinberg et al did not find any difference in the recurrence rate in membranous and nonmembranous SDH. Notably, in their study, postoperative neurological improvement after MMA embolization was better in patients with membranous SDH.[26] However, MMA embolization was done as a standalone treatment in most of the patients in their study, indicating that the characteristics of their study population differ from ours. As MMA embolization was performed as a standalone procedure in only 12.2% of the patients in our study, a subgroup analysis on the impact of membrane enhancement on the outcome could not be performed in this subset. The recurrence rate for hematomas without membrane enhancement was high (18.2%), similar to that reported after surgical evacuation without MMA embolization (11.2–27.7%).[3] [4] Therefore, a routine pre-embolization contrast-enhanced CT would help identify patients with no membrane enhancement and high risk of recurrence after MMA embolization. The high rate of recurrence in these patients suggests that other factors may contribute to the recurrence. Increased levels of proinflammatory cytokines are observed in the SDH, indicating that inflammation and increased vascular permeability contribute to hematoma expansion.[27] Hyperfibrinolysis within the SDH cavity also plays a role in hematoma expansion by preventing stable clot formation and promoting continued bleeding.[24] Surgical techniques like membranectomy may help reduce the rate of recurrence in patients with nonenhancing membranes.[28]

Apart from the absence of membrane, none of the other variables had an association with SDH recurrence following MMA embolization in our study. There was no association of location or morphology of enhancement with recurrence. Notably, although the lack of membrane enhancement had an association with recurrence, the membrane blush observed on the MMA angiogram did not have a significant association with recurrence. This is likely because the membrane blush was influenced by the volume and rate of contrast injection into the microcatheter, which was not standardized in our study. A study by Salem et al found that the use of anticoagulant agents, midline shift, MMA diameter < 1.5 mm, and superselective embolization of the MMA without targeting the main trunk were significant predictors of treatment failure following the embolization.[29] Supportive evidence from a study by Fuentes et al also indicates that anticoagulant use is a predictor for recurrence following MMA embolization.[30] Evaluation of the factors affecting the resolution of SDH following embolization has led to the finding that mixed density and separated types, postoperative SDH thickness and midline shift, and antiplatelet or anticoagulant use are associated with delayed hematoma resolution.[31]

We observed that the MMA on the same side as that of the SDH was significantly larger than the MMA on the unaffected side (mean diameter, 1.17 ± 0.02 vs. 1.03 ± 0.03 mm, p < 0.001). Similar results were observed in a study by Pouvelle et al, who found that the MMA on the same side as that of the SDH was significantly larger than the contralateral MMA (median [IQR], 1.6 [1.4–1.8] vs. 1.4 [1.25–1.6]; p < 0.001).[32] Enlargement of the MMA has been reported to occur when SDH develops following trauma.[33] However, our study did not find a significant association between MMA diameter and SDH recurrence.

Apart from the normal origin of MMA from the internal maxillary artery, anatomical variants are rarely observed. Fantoni et al observed MMA originating from the ophthalmic artery in 13.8% of patients undergoing MMA embolization.[34] However, in our study, the MMA had a variant origin from the ophthalmic artery in only 1% of cases. MMA embolization is risky in such cases due to the potential risk of injury to the ophthalmic artery during superselective catheterization and nontarget embolization into the central retinal artery.

The MMA can have anastomoses with the branches of the internal carotid artery. We observed an anastomosis between the MMA and the ophthalmic artery through the recurrent meningeal branch of the lacrimal artery in one of the cases. Further, the ophthalmic artery originated from the MMA instead of the internal carotid artery in 2.5% of the cases. There is a potential risk of developing blindness following nontarget embolization into the ophthalmic artery in such cases. However, embolization can safely be performed by navigating the microcatheter distal to the dangerous anastomosis.[35] Selective catheterization of the anterior and posterior branches of MMA above the level of the anterior clinoid process is recommended to avoid nontarget embolization into the dangerous anastomoses.[13] No complications were observed in our patients in whom the embolization was performed by advancing the microcatheter distal to the origin of the ophthalmic artery.

Our study has various limitations. The sample size was small, and therefore, the number of patients with SDH recurrence after MMA embolization was small. The small number would have affected the assessment of factors influencing the recurrence. The assessment of membrane blush on the MMA angiogram was subjective and thus prone to errors. Follow-up CT was not performed for all patients, because of which asymptomatic recurrences could have been missed.

Conclusion

The absence of membrane enhancement on baseline CT is a risk factor for SDH recurrence after MMA embolization. The recurrence rate was high in hematomas without membrane enhancement, indicating that MMA embolization may not be useful in reducing the recurrence rate in this subset of patients.

Conflict of Interest

None declared.

• References

• 1 Holl DC, Volovici V, Dirven CMF. et al; Dutch Chronic Subdural Hematoma Research Group (DSHR). Pathophysiology and nonsurgical treatment of chronic subdural hematoma: from past to present to future. World Neurosurg 2018; 116: 402-411.e2
• 2 Iliescu IA, Constantinescu AI. Clinical evolutional aspects of chronic subdural haematomas - literature review. J Med Life 2015; 8 (Spec Issue): 26-33
• 3 Srivatsan A, Mohanty A, Nascimento FA. et al. Middle meningeal artery embolization for chronic subdural hematoma: meta-analysis and systematic review. World Neurosurg 2019; 122: 613-619
• 4 Bartek Jr J, Sjåvik K, Kristiansson H. et al. Predictors of recurrence and complications after chronic subdural hematoma surgery: a population-based study. World Neurosurg 2017; 106: 609-614
• 5 Miah IP, Tank Y, Rosendaal FR. et al; Dutch Chronic Subdural Hematoma Research Group. Radiological prognostic factors of chronic subdural hematoma recurrence: a systematic review and meta-analysis. Neuroradiology 2021; 63 (01) 27-40
• 6 Amoo M, O'Cearbhaill RM, McHugh P. et al. Derivation of a clinical score for prediction of recurrence following evacuation of chronic subdural hematoma: a retrospective cohort study at a national referral centre. World Neurosurg 2021; 154: e743-e753
• 7 Stanišic M, Pripp AH. A reliable grading system for prediction of chronic subdural hematoma recurrence requiring reoperation after initial burr-hole surgery. Neurosurgery 2017; 81 (05) 752-760
• 8 Chon KH, Lee JM, Koh EJ, Choi HY. Independent predictors for recurrence of chronic subdural hematoma. Acta Neurochir (Wien) 2012; 154 (09) 1541-1548
• 9 You CG, Zheng XS. Postoperative pneumocephalus increases the recurrence rate of chronic subdural hematoma. Clin Neurol Neurosurg 2018; 166: 56-60
• 10 Fiorella D, Arthur AS. Middle meningeal artery embolization for the management of chronic subdural hematoma. J Neurointerv Surg 2019; 11 (09) 912-915
• 11 Hubbard ZS, Al Kasab S, Porto GB, Spiotta A. Chronic subdural hematoma recurrence due to contralateral neovascularization following middle meningeal artery embolization. Interv Neuroradiol 2022; 28 (06) 639-643
• 12 Link TW, Boddu S, Marcus J, Rapoport BI, Lavi E, Knopman J. Middle meningeal artery embolization as treatment for chronic subdural hematoma: a case series. Oper Neurosurg (Hagerstown) 2018; 14 (05) 556-562
• 13 Kan P, Fiorella D, Dabus G. et al; ARISE I Academic Industry Roundtable. ARISE I consensus statement on the management of chronic subdural hematoma. Stroke 2024; 55 (05) 1438-1448
• 14 Nakaguchi H, Tanishima T, Yoshimasu N. Factors in the natural history of chronic subdural hematomas that influence their postoperative recurrence. J Neurosurg 2001; 95 (02) 256-262
• 15 Nakagawa I, Park HS, Kotsugi M. et al. Enhanced hematoma membrane on DynaCT images during middle meningeal artery embolization for persistently recurrent chronic subdural hematoma. World Neurosurg 2019; 126: e473-e479
• 16 Chen H, Colasurdo M, Malhotra A, Gandhi D, Bodanapally UK. Advances in chronic subdural hematoma and membrane imaging. Front Neurol 2024; 15: 1366238
• 17 Khalilzadeh O, Baerlocher MO, Shyn PB. et al. Proposal of a new adverse event classification by the Society of Interventional Radiology standards of practice committee. J Vasc Interv Radiol 2017; 28 (10) 1432-1437.e3
• 18 Davies JM, Knopman J, Mokin M. et al; EMBOLISE Investigators. Adjunctive middle meningeal artery embolization for subdural hematoma. N Engl J Med 2024; 391 (20) 1890-1900
• 19 Chen H, Colasurdo M, Kan PT. Middle meningeal artery embolization as standalone treatment versus combined with surgical evacuation for chronic subdural hematomas: systematic review and meta-analysis. J Neurosurg 2023; 140 (03) 819-825
• 20 Ironside N, Nguyen C, Do Q. et al. Middle meningeal artery embolization for chronic subdural hematoma: a systematic review and meta-analysis. J Neurointerv Surg 2021; 13 (10) 951-957
• 21 Jumah F, Osama M, Islim AI. et al. Efficacy and safety of middle meningeal artery embolization in the management of refractory or chronic subdural hematomas: a systematic review and meta-analysis. Acta Neurochir (Wien) 2020; 162 (03) 499-507
• 22 Onyinzo C, Berlis A, Abel M, Kudernatsch M, Maurer CJ. Efficacy and mid-term outcome of middle meningeal artery embolization with or without burr hole evacuation for chronic subdural hematoma compared with burr hole evacuation alone. J Neurointerv Surg 2022; 14 (03) 297-300
• 23 Shotar E, Mathon B, Salle H. et al. Meningeal embolization for preventing chronic subdural hematoma recurrence after surgery: the EMPROTECT randomized clinical trial. JAMA 2025 . Accessed June 15, 2025 at: https://jamanetwork.com/journals/jama/fullarticle/2834971
• 24 Edlmann E, Giorgi-Coll S, Whitfield PC, Carpenter KLH, Hutchinson PJ. Pathophysiology of chronic subdural haematoma: inflammation, angiogenesis and implications for pharmacotherapy. J Neuroinflammation 2017; 14 (01) 108
• 25 Kim H, Choi Y, Lee Y. et al. Neovascularization in outer membrane of chronic subdural hematoma: a rationale for middle meningeal artery embolization. J Korean Neurosurg Soc 2024; 67 (02) 146-157
• 26 Weinberg JH, Akhter A, Zakeri A. et al. Middle meningeal artery embolization for membranous versus nonmembranous subdural hematomas: a retrospective and multicenter cohort study. World Neurosurg 2023; 177: e680-e685
• 27 Stanisic M, Aasen AO, Pripp AH. et al. Local and systemic pro-inflammatory and anti-inflammatory cytokine patterns in patients with chronic subdural hematoma: a prospective study. Inflamm Res 2012; 61 (08) 845-852
• 28 Sahyouni R, Mahboubi H, Tran P, Roufail JS, Chen JW. Membranectomy in chronic subdural hematoma: a meta-analysis. World Neurosurg 2017; 104: 418-429
• 29 Salem MM, Kuybu O, Nguyen Hoang A. et al. Middle meningeal artery embolization for chronic subdural hematoma: predictors of clinical and radiographic failure from 636 embolizations. Radiology 2023; 307 (04) e222045
• 30 Fuentes AM, Khalid SI, Mehta AI. Predictors of subsequent intervention after middle meningeal artery embolization for treatment of subdural hematoma: a nationwide analysis. Neurosurgery 2023; 92 (01) 144-149
• 31 Liu Z, Wang Y, Tang T. et al. Time and influencing factors to chronic subdural hematoma resolution after middle meningeal artery embolization. World Neurosurg 2023; 179: e6-e14
• 32 Pouvelle A, Pouliquen G, Premat K. et al. Larger middle meningeal arteries on computed tomography angiography in patients with chronic subdural hematomas as compared with matched controls. J Neurotrauma 2020; 37 (24) 2703-2708
• 33 Xu H, Huang X, Xu J. et al. Enlargement of the middle meningeal artery may be an initiating factor of chronic subdural hematoma: three case reports and a literature review. Curr Med Imaging 2024; 10: e240323214952
• 34 Fantoni M, Eliezer M, Serrano F. et al. High frequency of ophthalmic origin of the middle meningeal artery in chronic subdural hematoma. Neuroradiology 2020; 62 (05) 639-644
• 35 Lee YM, Mattay RR, Haddad AF, Rinaldo L, Savastano L. Middle meningeal artery embolization with polyvinyl alcohol particles in a patient with ophthalmic artery origin from middle meningeal artery: case report and technical note. Interv Neuroradiol 2023; 15 910199231188862

Publication History

Article published online:
09 December 2025