Endoscopically observed outer membrane of chronic subdural hematoma after endovascular embolization of middle meningeal artery
- Department of Neurosurgery, Yamaguchi University School of Medicine, Yamaguchi, Japan.
Sadahiro Nomura, Department of Neurosurgery, Yamaguchi University School of Medicine, Yamaguchi, Japan.
DOI:10.25259/SNI_886_2022Copyright: © 2022 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Sadahiro Nomura, Kohei Haji, Yuichi Fujiyama, Takuma Nishimoto, Fumiaki Oka, Hideyuki Ishihara. Endoscopically observed outer membrane of chronic subdural hematoma after endovascular embolization of middle meningeal artery. 11-Nov-2022;13:516
How to cite this URL: Sadahiro Nomura, Kohei Haji, Yuichi Fujiyama, Takuma Nishimoto, Fumiaki Oka, Hideyuki Ishihara. Endoscopically observed outer membrane of chronic subdural hematoma after endovascular embolization of middle meningeal artery. 11-Nov-2022;13:516. Available from: https://surgicalneurologyint.com/surgicalint-articles/12000/
Background: Embolization of the middle meningeal artery (MMA) has been established for chronic subdural hematoma (CSDH). Neuroendoscopic observation of the outer membrane of the hematoma was carried out after embolization. The treatment mechanism of embolization is discussed, focusing on the vasculature and inflammation of the membrane.
Methods: Four patients with recurrent CSDH were included in this study. The MMA was embolized using Embosphere® particles in three patients. The outer membrane was observed with normal and narrow band images (NBIs).
Results: The net-like vessels were not obstructed in the whole area of the outer membrane, but in a patchy fashion of embolized areas surrounded by nonembolized areas. In two patients, the nonembolized areas showed a hemorrhagic inflammatory red color. Histopathological examination confirmed hypertrophic dura with leukocyte infiltration. Dilated dural arteries and proliferated sinusoid arteries were located in the deep and superficial border cell layers. These arteries were visualized as green and brown on NBI, respectively. In the embolized area, the red membrane turned pink, indicating ischemia and subsiding inflammatory hyperemia. In the third patient, the outer membrane was white in both the nonembolized and embolized areas in endoscopic view, and the net-like vessels were sparse in both endoscopy and histology, indicating a scar inflammatory phase. The membrane transition was not observed in the patient that did not undergo embolization.
Conclusion: Endoscopic observation revealed that embolization of the MMA blocked both the dural and sinusoidal arteries. Ischemic transformation causing the suppression of inflammation of the outer membrane is a suggested mechanism of MMA embolization.
Keywords: Chronic subdural hematoma, Embolization, Inflammation, Neuroendoscope, Outer membrane
Chronic subdural hematoma (CSDH) is categorized as a traumatic brain disease; however, pathophysiologically, it may be included as an inflammatory disease.[
The active healing processes of CSDH are observed and staged by histopathology,[
The standard treatment of burr hole irrigation with drainage is symptomatic treatment for CSDH. An alternative treatment for embolization of the middle meningeal artery (MMA), the major blood supplier to the outer membrane, using endovascular intervention is a causal treatment. Angiographical hypervascularity of the MMA in CSDH and treatment with MMA embolization was first reported in 2000.[
The inhibition of local bleeding from the outer membrane by disturbance of the blood supply is a suspected mechanism of embolization;[
Patients with recurrent CSDH who required surgical decompression met the criteria for MMA embolization at our institute. Patients receiving initial treatment or those with recurrent asymptomatic small-sized hematoma, renal failure, or allergy to iodine contrast medium were not indicated for embolization. Urgent irrigation surgery without embolization was performed for patients with severe symptoms. Four patients with recurrent CSDH with and without embolization between December 2020 and June 2022 were included in the study. All the patients and their families were informed of the purposes, methods, and risks of MMA embolization, burr hole surgery, and endoscopic observation, and agreed with written permission. This retrospective study was approved by the Institutional Review Board of Yamaguchi University Hospital (approved number: H2021-042-2).
Superselective external carotid angiography was performed using a microcatheter. The MMA was embolized using Embosphere® (100–300 micrometers) particles. Surgery was performed 1–7 days after the embolization. The same burr hole made in the previous surgery was enlarged laterally by 5 mm to obtain a specimen of the dura mater. The CSDH was irrigated with artificial CSF, and an Olympus videoscope (VEF-V; Olympus Medical Systems, Tokyo, Japan) was inserted. The tip of the scope was angled outward to observe the outer membrane. Subdural drainage was performed until the day after surgery.
The severity of the clinical signs and symptoms before treatment was classified according to the neurological grade of CSDH.[
Three patients, all of whom were men (ages 62, 81, and 88 years), were treated with embolization and irrigation. A fourth patient, a 68-year-old woman, was treated with irrigation alone [
Net-like vessels were visualized on the outer membrane using an endoscope. These vessels were not obstructed in the whole area, but in a patchy fashion in the embolized areas surrounded by nonembolized areas. In Patients 1 and 2, the nonembolized areas showed a red hemorrhagic inflammatory color [
Normal and narrow band images (NBI) of the endoscope, and photomicrograph of the dural specimen. (a) Normal band endoscopic image of Patient 1 showing red-colored hypervasculature in the outer membrane where microsphere did not reach. (b) Normal band endoscopic image of the outer membrane of the right-sided CSDH of Patient 2. Red hypervasculature and pink avascular areas are shown in the lower and upper sides of the picture. (c) Photomicrograph of the dural specimen stained with hematoxylin-eosin (HE); original magnification, x40 in Patient 2. The upper part of the picture indicates the osteal side of the dura. The dural arteries are dilated, and inflammatory cells infiltrate the layer between the periosteal and meningeal dura (arrowhead). Hypertrophy of the dural border cell layer and development of sinusoid arteries (arrow). (d and e) NBI of the same area in (a and b). The hypervasculature are obvious in (d) and lower side in (e). The hypovasculature is seen in lower side in (e).
In Patient 3, the outer membrane, seen through a gap between the massive proliferated trabecula, was white in both the nonembolized and embolized areas [
Endoscopic and histological findings in Patient 3. (a and b) Normal band image (a) and NBI (b) of the outer membrane. White avascular (upper) and vascular (lower) areas are shown on the right side of the images. On the left side of the images, the membrane was hidden by the trabecula. (c) Photomicrograph of the dural specimen stained with HE; x40. Vessels and inflammatory cells are sparse between the periosteal and meningeal dura (arrowhead). No hypertrophy of the dural border cell layer or development of the sinusoid layer is observed (arrow).
In Patient 4, the outer membrane was a yellow color on NBI, which indicated inflammation [
Endoscopic observation of the outer membrane of the CSDH during burr hole irrigation after MMA embolization was performed in three patients. MMA embolization turned the red outer membrane to a pink color and obstructed the net-like vasculature in two patients. In the other patient, both the embolized and nonembolized areas were white. The transition of color or vessel obstruction was not observed in the patient previously treated with the irrigation surgery alone.
The effect of MMA embolization appeared primarily in sporadic ischemic changes in both the dural and sinusoid arteries. The dural arteries receive the embolus, whereas the sinusoid arteries are responsible for bleeding. The NBI showed the green dural arteries and brown sinusoid arteries together in one area and their obstruction of them together in other areas. None of the areas showed one of the remaining green or brown arteries. The results indicated that the sinusoid artery was supplied only from the adjacent dural artery. Therefore, embolization of the dural artery should be a reasonable approach for achieving hemostasis in the sinusoid artery. If further effectiveness is required, the materials and methods of embolization should be developed to cover a wider area, since the areas are distributed sporadically in the present findings.
The secondary effect of embolization is the enhancement of the healing process of inflammation. The pink color, not pale white, of the embolized outer membrane observed in Patients 1 and 2 indicates ischemia with residual inflammation. The white membrane of the scar, similar to that seen in Patient 3, appeared in subsequent stages. The inhibition of blood supply exerts anti-inflammatory effects by suppressing hyperemia, capillary permeability, and the secretion of chemical mediators. This method is also applied in other fields of treatment, such as vasoconstrictive nasal sprays for rhinitis[
MMA embolization may be helpful, especially in elderly patients. It is difficult to expect the atrophic brain to re-expand itself for clearance of the subdural space.[
Endoscopic observation would help a limited number of patients with CSDH in providing information for the treatment of choice. The staging of the outer membrane in combination with CT findings[
Endoscopic observation revealed that embolization of the MMA, the only blood supplier to the outer membrane, obstructed both the dural and sinusoid arteries, and changed the color of the outer membrane of CSDH. Ischemia and suppression of inflammation are suggested treatment mechanisms.
The authors certify that they have obtained all appropriate patient consent.
There are no conflicts of interest.
The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.
1. Adusumilli G, Ghozy S, Kallmes KM, Hardy N, Tarchand R, Zinn C. Common data elements reported on middle meningeal artery embolization in chronic subdural hematoma: An interactive systematic review of recent trials. J Neurointerv Surg. 2022. 14: 1027-32
2. Court J, Touchette CJ, Iorio-Morin C, Westwick HJ, Belzile F, Effendi K. Embolization of the Middle meningeal artery in chronic subdural hematoma-a systematic review. Clin Neurol Neurosurg. 2019. 186: 105464
3. Désir LL, D’Amico R, Link T, Silva D, Ellis JA, Doron O. Middle meningeal artery embolization and the treatment of a chronic subdural hematoma. Cureus. 2021. 13: e18868
4. Di Cristofori A, Remida P, Patassini M, Piergallini L, Buonanno R, Bruno R. Middle meningeal artery embolization for chronic subdural hematomas. A systematic review of the literature focused on indications technical aspects and future possible perspectives. Surg Neurol Int. 2022. 13: 94
5. Edlmann E, Giorgi-Coll S, Whitfield PC, Carpenter KL, Hutchinson PJ. Pathophysiology of chronic subdural haematoma: Inflammation, angiogenesis and implications for pharmacotherapy. J Neuroinflammation. 2017. 14: 108
6. Enriquez-Marulanda A, Gomez-Paz S, Salem MM, Mallick A, Motiei-Langroudi R, Arle JE. Middle meningeal artery embolization versus conventional treatment of chronic subdural hematomas. Neurosurgery. 2021. 89: 486-95
7. Frati A, Salvati M, Mainiero F, Ippoliti F, Rocchi G, Raco A. Inflammation markers and risk factors for recurrence in 35 patients with a posttraumatic chronic subdural hematoma: A prospective study. J Neurosurg. 2004. 100: 24-32
8. Fujisawa N, Oya S, Yoshida S, Tsuchiya T, Nakamura T, Indo M. A prospective randomized study on the preventive effect of Japanese herbal Kampo medicine Goreisan for recurrence of chronic subdural hematoma. Neurol Med Chir (Tokyo). 2021. 61: 12-20
9. Gandhoke GS, Kaif M, Choi L, Williamson RW, Nakaji P. Histopathological features of the outer membrane of chronic subdural hematoma and correlation with clinical and radiological features. J Clin Neurosci. 2013. 20: 1398-401
10. Haldrup M, Ketharanathan B, Debrabant B, Schwartz OS, Mikkelsen R, Fugleholm K. Embolization of the middle meningeal artery in patients with chronic subdural hematoma-a systematic review and meta-analysis. Acta Neurochir (Wien). 2020. 162: 777-84
11. Heller DB, Beggin AE, Lam AH, Kohi MP, Heller MB. Geniculate artery embolization: Role in knee hemarthrosis and osteoarthritis. Radiographics. 2022. 42: 289-301
12. Ironside N, Nguyen C, Do Q, Ugiliweneza B, Chen CJ, Sieg EP. Middle meningeal artery embolization for chronic subdural hematoma: A systematic review and meta-analysis. J Neurointerv Surg. 2021. 13: 951-7
13. Katsuki M, Kakizawa Y, Wada N, Yamamoto Y, Uchiyama T, Nakamura T. Endoscopically observed outer membrane color of chronic subdural hematoma and histopathological staging: White as a risk factor for recurrence. Neurol Med Chir (Tokyo). 2020. 60: 126-35
14. Kung WM, Lin MS. CT-based quantitative analysis for pathological features associated with postoperative recurrence and potential application upon artificial intelligence: A narrative review with a focus on chronic subdural hematomas. Mol Imaging. 2020. 19:
15. Majidi S, Matsoukas S, De Leacy RA, Morgenstern PF, Soni R, Shoirah H. Middle meningeal artery embolization for chronic subdural hematoma using n-butyl cyanoacrylate with D5W push technique. Neurosurgery. 2022. 90: 533-7
16. Mandai S, Sakurai M, Matsumoto Y. Middle meningeal artery embolization for refractory chronic subdural hematoma. Case report. J Neurosurg. 2000. 93: 686-8
17. Markwalder TM, Steinsiepe KF, Rohner M, Reichenbach W, Markwalder H. The course of chronic subdural hematomas after burr-hole craniostomy and closed-system drainage. J Neurosurg. 1981. 55: 390-6
18. Nagahori T, Nishijima M, Takaku A. Histological study of the outer membrane of chronic subdural hematoma: Possible mechanism for expansion of hematoma cavity. No Shinkei Geka. 1993. 21: 697-701
19. Nakaguchi H, Tanishima T, Yoshimasu N. Factors in the natural history of chronic subdural hematomas that influence their postoperative recurrence. J Neurosurg. 2001. 95: 256-62
20. Nakaguchi H, Yoshimasu N, Tanishima T. Relationship between the natural history of chronic subdural hematoma and enhancement of the inner membrane on post-contrast CT scan. No Shinkei Geka. 2003. 31: 157-64
21. Oka K. Introduction of the videoscope in neurosurgery. Neurosurgery. 2008. 62: S337-40
22. Sato-Boku A, Sento Y, Kamimura Y, Kako E, Okuda M, Tachi N. Comparison of hemostatic effect and safety between epinephrine and tramazoline during nasotracheal intubation: A double-blind randomized trial. BMC Anesthesiol. 2021. 21: 235
23. Shrestha DB, Budhathoki P, Sedhai YR, Jain S, Karki P, Jha P. Steroid in chronic subdural hematoma: An updated systematic review and meta-analysis post DEX-CSDH trial. World Neurosurg. 2022. 158: 84-99
24. Srivatsan A, Mohanty A, Nascimento FA, Hafeez MU, Srinivasan VM, Thomas A. Middle meningeal artery embolization for chronic subdural hematoma: Meta-analysis and systematic review. World Neurosurg. 2019. 122: 613-9
25. Takei J, Hirotsu T, Hatano K, Ishibashi T, Inomata T, Noda Y. Modified computed tomography classification for chronic subdural hematoma features good interrater agreement: A single-center retrospective cohort study. World Neurosurg. 2021. 151: e407-17
26. Wakuta N, Abe H, Nonaka M, Morishita T, Higashi T, Arima H. Analysis of endoscopic findings in the chronic subdural hematoma cavity: Bleeding factors in chronic subdural hematoma natural history and as predictors of recurrence. World Neurosurg. 2018. p. S1878-8750(18)32901-2
27. Waqas M, Vakhari K, Weimer PV, Hashmi E, Davies JM, Siddiqui AH. Safety and effectiveness of embolization for chronic subdural hematoma: Systematic review and case series. World Neurosurg. 2019. 126: 228-36