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Embolization Therapy for Refractory Hemorrhage in Patients with Chronic Subdural Hematomas
Original Article
Embolization Therapy for Refractory Hemorrhage in Patients with Chronic Subdural Hematomas El Kim
OBJECTIVE: There is no definite operative procedure for patients with intractable chronic subdural hematoma (CSDH). We describe the safety and efficacy of embolization treatment of the middle meningeal artery (MMA) for such cases.
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METHODS: Patients were divided into an embolization group (n [ 20) and a conventional group (n [ 23) based on the therapeutic approach to their CSDHs. The targets of the endovascular treatment were 26 recollected hematomas with increased risk of recurrence. To eliminate the arterial supply of the external membrane of CSDHs, 2 branches of the MMA were selected and occluded by injection of polyvinyl alcohol particles.
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RESULTS: Older age and antiplatelet drug use were comparatively related to the embolization group (P < 0.05). Among imaging study variables, severe brain atrophy and hematoma bilaterality were the risk factors for necessity of MMA embolization (P < 0.05). The complication rate and functional outcome were not significantly different between the 2 groups (P > 0.05). After multivariate analysis, early brain re-expansion (P [ 0.003) and lesser hematoma recurrence (P [ 0.024) remained independently associated with patients who underwent embolization therapy.
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CONCLUSIONS: This pilot study indicated that perioperative MMA embolization could be offered as the least
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Key words Chronic subdural hematoma - Embolization - Middle meningeal artery - Recurrence -
Abbreviations and Acronyms CI: Confidence interval CSDH: Chronic subdural hematoma CT: Computed tomography MMA: Middle meningeal artery MRA: Magnetic resonance angiography mRS: modified Rankin Scale
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invasive and most effectual means of treatment for resistant patients of CSDHs with 1 or more recurrences.
INTRODUCTION
C
hronic subdural hematoma (CSDH) is an increasing clinical occurrence in modern neurosurgical practice. Trephination and drainage are the gold standard for patients with space-occupying CSDHs. Treatment outcomes are good in most patients, but recollection of blood requiring reoperation sometimes occurs. In the reports on CSDHs treated by burr-hole surgery, 11%e28% of operative cases developed a recurrent hematoma.1,2 Subdural drainage is the most widely accepted management for symptomatic recurrences; however, previous studies3,4 have found that revision surgery was unsuccessful in some cases. Furthermore, it is more difficult to treat patients with CSDHs in whom resolution cannot be achieved even after repeated craniostomy and irrigation procedures. This intractability is more commonly encountered in patients with coagulopathy, elderly patients with cerebral atrophy, and patients on antithrombotic drugs.5 Treatment for intractable CSDHs should concentrate on addressing the capillary feeders of hematomas that originate from the middle meningeal artery (MMA). However, only a few sporadic reports of achieving transarterial therapy for patients with recurrent CSDH have been published in the literature.6,7 In this study, the MMA embolization method was applied to patients
OR: Odds ratio SDH: Subdural hematoma Departments of Neurosurgery and Medical Imaging, Dongsan Medical Center, Keimyung University School of Medicine, Daegu, Republic of Korea To whom correspondence should be addressed: El Kim, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017) 101:520-527. http://dx.doi.org/10.1016/j.wneu.2017.02.070 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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with uncontrolled hemorrhage in refractory CSDHs and the potential role of this strategy for preventing further recurrence of hematomas was examined. METHODS Patient Selection A review was carried out of 372 patients who were hospitalized for burr-hole surgery to evacuate newly diagnosed unilateral or bilateral CSDHs from January 2007 to December 2015. These patients received 1 or 2 burr-hole trephinations for subdural irrigation under general or local anesthesia. A silicon tube was pulled out when drainage became negligible. The recurrence of CSDHs was shown by the reappearance of neurologic manifestations and an increase in hematoma volume on computed tomography (CT) or magnetic resonance imaging. In this series, the first-time recurrence of hematoma was observed in 43 patients (11.6%). Reopening the burr hole for hematoma drainage was the primary procedure for symptomatic recollections (Figure 1AeD). This retrospective study comprised 20 of 372 patients (5.4%) in whom the MMA was selected to devascularize the external membrane of the CSDHs. There were 6 women and 14 men, with a mean age of 72.4 years (median age, 74 years; range, 60e84 years). The Markwalder grading scale was used for patient classification and it ranged from 0 to 4.8 Seventeen patients (85.0%) had a good neurologic status (grade 0e2) at the initial
Figure 1. Computed tomography (CT) images in a 59-year-old man who had a refractory chronic subdural hematoma treated by embolization of the middle meningeal artery. CT scans before (A) and after (B) the initial drainage and irrigation. Brain scan at the recurrence shows massive hematoma (C), which requires an emergent evacuation. The recollection of
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preoperative visit. A history of head trauma was evident in 8 patients (40.0%). The medical evaluation showed that all patients had 1 or more concomitant disease. There were 6 patients with brain stroke, 4 with heart disease, 7 with diabetes mellitus, 4 with a malignancy, 3 with kidney dysfunction, 1 with dementia, 3 with liver disease, 13 with hypertension, and 2 with shunt-dependent hydrocephalus. Laboratory study showed impaired blood coagulation in 5 patients (25.0%). Nine patients (45.0%) had taken anticoagulant or antiplatelet medications (Table 1). Patients on platelet inhibition therapy had their medication discontinued immediately in an attempt to prevent hematoma expansion and facilitate the operative intervention. When rapid clinical deterioration occurred in these patients, platelet concentrate was routinely infused. Reversing anticoagulation before surgery was accomplished using fresh frozen plasma and vitamin K. Those with thrombocytopenia from hematologic disorder, renal failure, liver cirrhosis, and malignancy received platelet transfusion. Restarting the antiplatelet or anticoagulative agents was weighed with a focus on the history of embolism, reason for antithrombosis, hemostatic function, serial CT scans of CSDHs after burr-hole surgery, and neurologic evaluation. Radiographic Characteristics Bilateral blood collection was detected in 6 patients (30.0%). In the unilateral group, the CSDH was located over the left hemisphere in
hematoma is noted 2 weeks later after the second surgery (D). A contrast leakage into the hematoma is defined on CT immediately taken after the middle meningeal artery embolization (E). Follow-up CT scan obtained 20 days after intravascular therapy demonstrates complete resolution of chronic subdural hematoma in the left hemisphere (F).
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Table 1. Clinical Characteristics of Groups with Recurrent Chronic Subdural Hematomas Variables
Conventional (n [ 23)
Embolization (n [ 20)
Significance (P)
Age (years)
65.65 6.91
73.65 7.14
0.041
Male/female
16 (69.6)/7 (30.4)
14 (70.0)/6 (30.0)
0.975
Head trauma
17 (73.9)
8 (40.0)
0.033
Markwadler grade
0.421
0e2
22 (95.7)
18 (90.0)
3e4
1 (4.3)
2 (10.0)
Antiplatelets
1 (4.3)
6 (30.0)
0.038
Anticoagulants
1 (4.3)
3 (15.0)
0.323
Hypertension
5 (21.7)
13 (65.0)
0.469
Diabetes mellitus
4 (17.4)
7 (35.0)
0.721
Liver dysfunction
1 (4.3)
3 (15.0)
0.323
Renal failure
1 (4.3)
3 (15.0)
0.323
Heart disease
3 (13.0)
4 (20.0)
0.787
Malignancy
2 (8.7)
4 (20.0)
0.687
Medication use
Underlying diseases
Coagulopathy
1 (4.3)
5 (25.0)
0.065
Brain infarction
3 (13.0)
6 (30.0)
0.261
Values are number (%) except where indicated otherwise.
53.8% (14/26) and over the right hemisphere in 46.2% (12/26). Hematomas were divided into 4 types based on their internal architecture in CT findings: homogenous, laminar, separate, or trabecular.9 The numbers of each subtype were as follows: 11 (homogenous), 4 (laminar), 4 (separated), and 7 (trabecular), respectively. On the preoperative CT scans, the mean hematoma thickness was 15.6 3.6 mm (range, 2.9e29.4 mm) on the left side and 17.6 4.9 mm (range, 3.1e34.4 mm) on the right side. The CT grading of the brain atrophy was determined according to the widening of the sulci and subdural space.10 The numbers of cases classified as definite and severe grade were 4 (20.0%) and 15 (75.0%), respectively. The amount of subdural air found on immediate postoperative CT scans was categorized into the minimal and definite degrees.11 For cases of recently treated CSDHs, the maximum diameter of the MMA was measured and then compared with both sides on magnetic resonance angiography (MRA) (Figure 2A). Indication of MMA Embolization Angiography and embolization of the MMA were considered for 26 lesions in 20 patients with progressed hematoma collection after burr-hole and drainage surgery. This clinical study was approved by the institutional review board, and informed consent for the endovascular therapy was provided by the patients or their
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families. The decision of whether, when, and how to embolize the MMA should be tailored to the individual patient and their unique risk profile in the setting of recurrent hematoma formation. Generally, we favored this minimally invasive technique in an effort to reduce the hematoma recurrences and subsequent reoperations for the patients who are high-risk surgical candidates with recurrence of CSDHs. Angiography and embolization treatment for patients with recurrent CSDHs were determined by the following circumstances: 1) not requiring an emergent evacuation; 2) symptomatic recurrence within a short time after successful treatment; 3) elderly with brain atrophy; 4) enlarged ipsilateral MMA on MRA; 5) under antiplatelet and anticoagulant therapy; 6) advanced combined medical diseases; 7) bleeding tendency or coagulopathy; and 8) hematomas with multilocular collections. The timing of embolization differed for each patient at the surgeon’s discretion based on the operative finding and the clinical and radiologic presentations of patients with CSDHs that failed to resolve. In 16 patients, MMA embolization was performed at an early stage after surgery when signs of inadequate evacuation were observed on immediate postoperative CT, whereas another 4 patients more prone to bleeding because of underlying diseases or antithrombotic drugs preferentially underwent the intervention just before the burr-hole drainage. Endovascular Procedure Angiography and embolization of MMA were performed with the patient awake. Intravenous heparin was not administered. For intravascular surgery, a 5-F or 6-F guiding catheter was inserted into the femoral artery and placed near the origin of the external carotid artery on the hematoma side. A flow-guided type microcatheter (Prowler 10 [Cordis Neurovascular, Miami Lakes, Florida, USA]) was positioned in the main trunk of the MMA for superselective angiography. The angiographic feature was the arterial dilatation and visualization of abnormal vascular stains on the affected sides (Figure 2B and C). A neuroradiologist ensured that no collaterals to the orbit were present. Thereafter, the microcatheter was advanced through the frontal and parietal branches of the MMA, and then polyvinyl alcohol particles ranging from 150 to 250 mm in diameter were slowly injected under fluoroscopic control. This procedure was terminated when the cotton-woolelike blushing around the branches of the MMA was no longer seen (Figure 2D and E). A contrast leakage into the hematomas within the subdural space was clearly defined by postprocedure head CT scan (Figure 1E). There were no undesired effects from the angiography and embolization. Clinical and Radiographic Surveillance Every patient being treated for refractory CSDHs requires close follow-up for signs of recollected hematoma. Neurologic monitoring and serial CT scanning were frequently performed until detection of nearly total resolution of the CSDH and their improvement to a reasonable result (Figure 1F). Control CT was performed on the day after surgery to check for adequate drainage or any remarkable complication. The patient was discharged on the seventh postoperative day after confirming the absence of new hemorrhage. After the patients were discharged, they were regularly seen as outpatients at 2 weeks, 1 month, and 3 months after surgery, with additional visits up to
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Figure 2. Magnetic resonance angiography and selective arteriograms of middle meningeal artery (MMA) in patients with recurrent chronic subdural hematoma. The left MMA (arrowhead) that nourishes the hematoma is larger than the right MMA (arrow) (A). The hypertrophied MMA and cotton-wool staining are
6 months if there was a persistent subdural hematoma (SDH) on the 3-month scan. On follow-up CT scans, hematoma recurrence and cerebral re-expansion were defined as an increase in the hematoma density and width, and restoration of bilateral symmetry of the brain, respectively.12 Within the follow-up period, if new or progressive symptoms or signs developed, additional imaging was performed to diagnose the recurrence as soon as possible. The clinical status was based on a modified Rankin Scale (mRS) during the follow-up examinations, and a favorable outcome was defined as an mRS score of 0e2. Patients with an mRS score <3 at 3 months were not scheduled further, whereas patients with higher mRS scores were reassessed at 6 months after treatment. Statistical Analysis To assess the effect of intravascular treatment, the clinicalradiologic features and treatment results were statistically compared between the embolization group and the conventional group with 24 recurrent hematomas treated by craniostomy alone. A univariate analysis was performed with a Pearson c2 test, Fisher exact test, and Student t test. The statistical significance was set at P < 0.05. A multivariate analysis was performed using a logistic
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well visualized on lateral fluoroscopy image (B). Diffuse capillary networks are clearly delineated along the peripheral branches of MMA (C and D), which had completely disappeared at the end of particle embolization (E).
regression model. The relationship between the variables and treatment outcomes was presented based on a 95% confidence interval (CI) and the odds ratio (OR). RESULTS Demographic and clinical data are listed in Table 1. The embolization group was found to be associated with older age (P ¼ 0.041) and antiplatelet medication (P ¼ 0.038) but not with history of head trauma. On comparing the neurologic status on admission, no statistical difference was observed in either group. Hypertension, diabetes, and cerebral infarct were more frequently observed in the embolization group, but these factors did not reach statistical significance. Severe brain atrophy (P ¼ 0.041) and bilateral involvement of the hematomas (P ¼ 0.038) more frequently characterized the CT findings of the embolization therapy group (Table 2). The length of hospital stay and morbidity were statistically insignificant between the 2 groups (P > 0.05). Among 43 cases, 9 (20.9%) were affected by treatment-related complications, 2 had intracranial bleeding, 2 had wound hematoma, 1 had seizure, 2 had angina pectoris, 1 had urinary tract infection, 2 had pneumonia, and 1 had delirium. Postoperative hemorrhages were
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Figure 3. Pathologic examination of excised specimen in a patient of intractable chronic subdural hematoma (original magnification 100). Numerous blood vessels are observed in the interstitial space of the outer membrane of the hematoma. Fresh hemorrhages at the periphery are surrounded by many hemosiderin-laden macrophages on hematoxylin-eosin staining.
minor and managed with conservation. Times for restoring the bihemispheric symmetry in embolized CSDHs were significantly shorter than those of the control group (mean, 34.65 15.45 vs. 98.29 52.99 days; P < 0.001). A significant difference in the Table 2. Computed Tomography Data of Groups with Recurrent Chronic Subdural Hematomas Variables
Conventional (n [ 23)
Embolization (n [ 20)
Significance (P)
1 (4.3)
6 (30.0)
0.038
further recollection of hematoma was found between the 2 groups (P ¼ 0.008) (Table 3). In the conventional group, 8 of 24 lesions recurred (33.3%), and consequently, the hematomas were evacuated through an additional craniostomy (n ¼ 5) and craniotomy (n ¼ 3). In contrast, MMA embolization was curative in the study group, with the exception of 1 hematoma (3.8%), which spontaneously regressed. Regardless of agedness and concurrent illness, the functional outcomes of the embolization group were comparable with those of the conventional group (P > 0.05). Two patients (4.6%) in both groups died after discharge from causes not related to the operation. Logistic regression models showed that patients in the embolization group experienced a shortened brain re-expansion time (P ¼ 0.003; OR, 1.179; 95% CI, 1.059e1.313) and a higher rate of hematoma cure (P ¼ 0.024; OR, 1.029; 95% CI, 0.970e5.024) than did patients who were managed using a conventional approach (Table 3).
DISCUSSION Managing CSDH is a straightforward process, but an unremitting hemorrhage is sometimes difficult to treat. This factor was shown in the present study because the cohort had underlying medical diseases that complicated the clinical course of CSDHs. Revision surgery for drainage and irrigation is the first-line treatment for recollected hematomas. However, a few surgeons have performed complex procedures, such as craniotomy and membranectomy, subdural shunt, reservoir placement, hollow screw insertion, and craniectomy with duroplasty in patients with repeatedly relapsed CSDHs.13-17 An endoscope-assisted and sonogram-assisted evacuation is an emerging option for opening compartments and excising membranes in multiloculated hematomas.9,12 However, controversy remains regarding the best
Hematoma site Bilateral Unilateral Hematoma thickness (mm)
22 (95.7)
14 (70.0)
21.01 6.21
18.90 7.58
0.507 Variables
Brain atrophy None or mild
Table 3. Treatment Results of Two Groups with Recurrent Chronic Subdural Hematomas Conventional Embolization Significance Multivariate (n [ 23) (n [ 20) (P) (P)
Hospital stay 14.25 15.02 19.96 13.44 (days)
0.162
98.29 52.99 34.65 15.45
<0.001
12 (52.2)
3 (15.0)
0.021
Definite
8 (34.8)
4 (20.0)
0.281
Severe
3 (13.0)
13 (65.0)
0.041
17 (73.9)
11 (55.0)
Laminar
3 (13.0)
4 (20.0)
Separated
2 (8.7)
4 (20.0)
Trabecular
2 (8.7)
7 (35.0)
Minimal
16 (66.7)
16 (61.5)
0e2
20 (87.0)
17 (85.0)
Definite
8 (33.3)
10 (38.5)
3e6
3 (13.0)
3 (15.0)
Hematoma subtypes Homogenous
0.205
Subdural air collection
1.25
Values are number (%) except where indicated otherwise.
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Brain reexpansion time (days)
0.003
Complications Surgical
2 (8.7)
2 (10.0)
0.932
Medical
2 (8.7)
3 (15.0)
0.222
Hematoma recurrence
8 (33.3)
1 (3.8)
0.008
Modified Rankin Scale scores
0.024
1
Values are number (%) except where indicated otherwise.
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strategy because each tactic has associated operative risks and significant recurrence rates. Extensive research has identified that CSDH is an angiogenic and inflammatory disease. Blood products mixed with subdural fluid trigger a foreign body reaction, which is followed by formation of a neomembrane comprising immature vasculature on the interior of the pachymeninx. Continuous exudation and oozing from fragile neovessels in the membrane contribute to the generation and growth of CSDHs (Figure 3).10,18-20 Reports on the vascular anatomy of CSDHs21,22 have shown that numerous sinusoids penetrate the dura mater and connect to MMA branches. These sinusoids were seen as a giant capillary network and cotton-woolelike stains on the superselective angiography of the author’s embolization group. This finding was consistent with the results of investigations on MMA angiograms for refractory recurrent CSDHs in the literature.6,7,22 Contrast extravasation into the subdural space on postembolization CT of the illustrative case also indicated the communication between the hematoma cavity and the MMA. Intractability has commonly been found to lead to readmission and prolonged hospitalization and, because of effects from repeat surgery, may be life threatening for patients with rehemorrhagic CSDH. However, operative mortality in this series did not exceed that of ordinary CSDHs, which ranges from 1.2% to 3.8%.3,11,23 Recent analysis of MRA showed that the MMA ipsilateral to the hematoma becomes diffusely enlarged during the initiation period for the development of CSDHs.24 On the basis of this finding, we were supportive of an early intervention for refractory CSDHs, which contrasted with previous research that proposed the use of MMA embolization for hematomas with more than 2 or 3 recurrences.25,26 In this study, the embolization treatment proved to be a beneficial option for patients who had intractable CSDHs with 1 or more recurrences and reaccumulation within 1 month after satisfactory evacuation. Statistically, our embolization group was at an increased risk of recurrence and reoperation because they frequently involved variables, such as older age, marked brain atrophy, antiplatelet use, and bilateral hematomas. Despite unfavorable conditions in the patients, the higher resolution rate of hematomas was obtained by applying the MMA embolization at an early stage when signs of subdural recollection appeared. Furthermore, the extent of neurologic recovery in the group who underwent embolization was comparable with that of another series treated by various surgical methods.1,11,13,27 The occurrence of CSDHs associated with taking drugs that interfere with the coagulation system or platelet function is increasing in modern neurosurgery. Patients with antithrombotics-related CSDHs have been found to be more susceptible to surgical failure and recollection of hematomas after several operative attempts.28 To verify the clinical usefulness of embolization treatment for recurrent CSDHs, bleeding-prone patients with liver cirrhosis, antithrombosis, and hemodialysis were primarily enrolled for this preliminary study. Patients in our embolization group were more frequently affected by bilateral CSDHs that usually developed atraumatically and spontaneously. In theory, high-flow inputs into the capillary channel through the hypertrophied MMA result in repeated microhemorrhage from the neomembranes in patients under anticoagulation and antiplatelet therapy. Moreover, extensive electrocautery of the hematoma
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capsule is mostly impossible because of limited access and can cause fresh bleeding and acute SDH formation during burr-hole surgery. In our experience, the advantage of MMA embolization became apparent for the study population with coagulation disturbance, who required immediate cessation of bleeding from the outer membrane of CSDH. Nevertheless, in terms of the postoperative resumption of antiplatelets or anticoagulants, there are no data to address the clinical guideline regarding protocols for these patients on oral antithrombotics who underwent craniostomy plus embolization for related CSDHs. These medications were restarted after the operation wound was healed and when there was no significant recurrent or acute hemorrhage in the CT scan around the time of discharge. This author’s pharmacologic strategy did not need to be withheld for more than a week after the embolization treatment in those patients with a high thromboembolic risk receiving preoperative antithrombosis treatment. Refractory CSDH of elderly patients is an important indicator of MMA angiography and embolization treatment. In these cases, CSDHs have primarily been found to exert prolonged compression on the cerebral hemisphere, and consequently, a capacious room for hematomas 2e3 cm below the dura mater is created before any neurologic symptom arises.29 In addition, an aged brain of high elasticity invariably fails to re-expand, which leads to persistence of midline shifting after successful evacuation of CSDHs, with impaired adhesion between the inner and outer membranes, thus facilitating postoperative reaccumulation of the hematomas within the expansive subdural cavity.30 On the basis of these facts, it is reasonable to stop bleeding from the membrane and to promote resolution of the hematoma for patients with advanced brain atrophy in whom it is not easy to achieve better obliteration of the subdural space and then restore intracranial pressure dynamics. Theoretically, MMA embolization can play a major role in breaking the cycle of neomembrane formation, vascular hyperpermeability, inflammatory exudation, and repeated bleeding, thus allowing reabsorption of the clot over time without expansion.19,21,31 In this study, the primary merit of perioperative embolization was to enhance the cerebral re-expansion rate and to obviate additional operations for recurrent CSDHs in geriatric patients. This option might be used as a sole therapy for elderly patients who cannot tolerate anesthesia or sedation and for whom intracranial pressure is not relieved immediately. In addition, the presence of layering and mixed-density SDHs with partitioning membranes was more frequently observed in the patients in the embolization group. In managing patients with this status, the author also recommends MMA embolization treatment after burrhole drainage in preference to a more complicated craniotomy surgery.8,27 The procedure presented here that shut off the capillary flow to the intralesional septum appears to be safe and effective in the prevention of recurrence, with enhanced shrinkage of the hematoma remnant left after drainage and irrigation. The appropriate indication and timing for the use of MMA embolization to the recurrent CSDHs remain unclear. The decision protocol of embolization was left entirely to the treating surgeon’s discretion in accordance with the radiographic, neurologic, and operative features of the patients with CSDHs. Most patients in this series had the embolization treatment after revision burr-hole surgery for repeatedly collected hematomas. In previous
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research,7,22,25 although an embolization was performed after various instances of repeated CSDH formation in each patient, favorable results were obtained regardless of the timing. Commonly used materials for embolizing the MMA are N-butyl cyanoacrylate, polyvinyl alcohol particles, and coils, with almost the same therapeutic outcomes.6,7,22,25 When performing an embolization treatment, we must be cautious not to inject particles through the MMA branch involved in dangerous collateral to the orbit. In addition, the interventionist should keep in mind that the capillary feeders of CSDHs are easily missed when contrast media is infused at the main trunk of the external carotid artery. A disadvantage of MMA embolization was the lag time before the resolution of symptoms in some cases with recurrence of refractory CSDH. Hair loss and wound breakdown are also important issues to consider when planning embolization therapy in elderly patients or in poor surgical candidates with premorbidity. Recent advances in endovascular technology made the embolization procedure more precise for our patients, allowing for
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15. Sato M, Iwatsuki K, Akiyama C, Kumura E, Yoshimine T. Implantation of a reservoir for refractory chronic subdural hematoma. Neurosurgery. 2001;48:1297-1301.
7. Tsukamoto Y, Oishi M, Shinbo J, Fujii Y. Transarterial embolisation for refractory bilateral chronic subdural hematomas in a case with dentatorubral-pallidoluysian atrophy. Acta Neurochir (Wien). 2011;153:1145-1147.
16. Safain M, Roguski M, Antoniou A, Schirmer CS, Malek AM, Riesenburger R. A single center’s experience with the bedside subdural evacuating port system: a useful alternative to traditional methods for chronic subdural hematoma evacuation. J Neurosurg. 2013;118:694-700.
8. Mohamed EH. Chronic subdural haematoma treated by craniotomy, durectomy, outer membranectomy and subgaleal suction drainage. Personal experience in 39 patients. Br J Neurosurg. 2003;17:244-247.
17. Oku Y, Takimoto N, Yamamoto K. Trial of a new operative method for recurrent chronic subdural hematoma. J Neurosurg. 1984;61:269-272.
26. Ishihara H, Ishihara S, Kohyama S, Yamane F, Ogawa M, Sato A, et al. Experience in endovascular treatment of recurrent chronic subdural hematoma. Interv Neuroradiol. 2007;3:141-144.
18. Hong HJ, Kim YJ, Yi HJ, Ko Y, Oh SJ, Kim JM. Role of angiogenic growth factors and inflammatory cytokines on recurrence of subdural hematoma. Surg Neurol. 2009;71:161-165.
27. Mondorf Y, Abu-Owaimer M, Gaab MR, Oertel JM. Chronic subdural hematomacraniotomy versus burr hole trepanation. Br J Neurosurg. 2009;23:612-616.
9. Berhouma M, Jacquesson T, Jouanneau E. The minimally invasive endoscopic management of septated chronic subdural hematomas: surgical
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25. Tempaku A, Yamauchi S, Ikeda H, Tsubota N, Furukawa H, Maeda D, et al. Usefulness of interventional embolization of the middle meningeal artery for recurrent chronic subdural hematoma: five cases and a review of the literature. Interv Neuroradiol. 2015;21:366-371.
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28. Lindvall P, Koskinen LO. Anticoagulants and antiplatelet agents and the risk of development and recurrence of chronic subdural haematomas. J Clin Neurosci. 2009;16:1287-1290.
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with a posttraumatic chronic subdural hematoma: a prospective study. J Neurosurg. 2004;100: 24-32.
29. Fukuhara T, Gotoh M, Asari A, Ohmoto T, Akioka T. The relationship between brain surface elastance and brain reexpansion after evacuation of chronic subdural hematoma. Surg Neurol. 1996; 45:570-574.
31. Kuwahara S, Fukuoka M, Koan Y, Miyake H, Ono Y, Moriki A, et al. Subdural hyperintense band on diffusion-weighted imaging of chronic subdural hematoma indicates bleeding from the outer membrane. Neurol Med Chir (Tokyo). 2005;45: 125-131.
30. Frati A, Salvati M, Mainiero F, Ippoliti F, Rocchi G, Raco A, et al. Inflammation markers and risk factors for recurrence in 35 patients
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
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commercial or financial relationships that could be construed as a potential conflict of interest. Received 26 November 2016; accepted 15 February 2017 Citation: World Neurosurg. (2017) 101:520-527. http://dx.doi.org/10.1016/j.wneu.2017.02.070 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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Embolization Therapy for Refractory Hemorrhage in Patients with Chronic Subdural Hematomas El Kim
OBJECTIVE: There is no definite operative procedure for patients with intractable chronic subdural hematoma (CSDH). We describe the safety and efficacy of embolization treatment of the middle meningeal artery (MMA) for such cases.
-
METHODS: Patients were divided into an embolization group (n [ 20) and a conventional group (n [ 23) based on the therapeutic approach to their CSDHs. The targets of the endovascular treatment were 26 recollected hematomas with increased risk of recurrence. To eliminate the arterial supply of the external membrane of CSDHs, 2 branches of the MMA were selected and occluded by injection of polyvinyl alcohol particles.
-
RESULTS: Older age and antiplatelet drug use were comparatively related to the embolization group (P < 0.05). Among imaging study variables, severe brain atrophy and hematoma bilaterality were the risk factors for necessity of MMA embolization (P < 0.05). The complication rate and functional outcome were not significantly different between the 2 groups (P > 0.05). After multivariate analysis, early brain re-expansion (P [ 0.003) and lesser hematoma recurrence (P [ 0.024) remained independently associated with patients who underwent embolization therapy.
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CONCLUSIONS: This pilot study indicated that perioperative MMA embolization could be offered as the least
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Key words Chronic subdural hematoma - Embolization - Middle meningeal artery - Recurrence -
Abbreviations and Acronyms CI: Confidence interval CSDH: Chronic subdural hematoma CT: Computed tomography MMA: Middle meningeal artery MRA: Magnetic resonance angiography mRS: modified Rankin Scale
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invasive and most effectual means of treatment for resistant patients of CSDHs with 1 or more recurrences.
INTRODUCTION
C
hronic subdural hematoma (CSDH) is an increasing clinical occurrence in modern neurosurgical practice. Trephination and drainage are the gold standard for patients with space-occupying CSDHs. Treatment outcomes are good in most patients, but recollection of blood requiring reoperation sometimes occurs. In the reports on CSDHs treated by burr-hole surgery, 11%e28% of operative cases developed a recurrent hematoma.1,2 Subdural drainage is the most widely accepted management for symptomatic recurrences; however, previous studies3,4 have found that revision surgery was unsuccessful in some cases. Furthermore, it is more difficult to treat patients with CSDHs in whom resolution cannot be achieved even after repeated craniostomy and irrigation procedures. This intractability is more commonly encountered in patients with coagulopathy, elderly patients with cerebral atrophy, and patients on antithrombotic drugs.5 Treatment for intractable CSDHs should concentrate on addressing the capillary feeders of hematomas that originate from the middle meningeal artery (MMA). However, only a few sporadic reports of achieving transarterial therapy for patients with recurrent CSDH have been published in the literature.6,7 In this study, the MMA embolization method was applied to patients
OR: Odds ratio SDH: Subdural hematoma Departments of Neurosurgery and Medical Imaging, Dongsan Medical Center, Keimyung University School of Medicine, Daegu, Republic of Korea To whom correspondence should be addressed: El Kim, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017) 101:520-527. http://dx.doi.org/10.1016/j.wneu.2017.02.070 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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with uncontrolled hemorrhage in refractory CSDHs and the potential role of this strategy for preventing further recurrence of hematomas was examined. METHODS Patient Selection A review was carried out of 372 patients who were hospitalized for burr-hole surgery to evacuate newly diagnosed unilateral or bilateral CSDHs from January 2007 to December 2015. These patients received 1 or 2 burr-hole trephinations for subdural irrigation under general or local anesthesia. A silicon tube was pulled out when drainage became negligible. The recurrence of CSDHs was shown by the reappearance of neurologic manifestations and an increase in hematoma volume on computed tomography (CT) or magnetic resonance imaging. In this series, the first-time recurrence of hematoma was observed in 43 patients (11.6%). Reopening the burr hole for hematoma drainage was the primary procedure for symptomatic recollections (Figure 1AeD). This retrospective study comprised 20 of 372 patients (5.4%) in whom the MMA was selected to devascularize the external membrane of the CSDHs. There were 6 women and 14 men, with a mean age of 72.4 years (median age, 74 years; range, 60e84 years). The Markwalder grading scale was used for patient classification and it ranged from 0 to 4.8 Seventeen patients (85.0%) had a good neurologic status (grade 0e2) at the initial
Figure 1. Computed tomography (CT) images in a 59-year-old man who had a refractory chronic subdural hematoma treated by embolization of the middle meningeal artery. CT scans before (A) and after (B) the initial drainage and irrigation. Brain scan at the recurrence shows massive hematoma (C), which requires an emergent evacuation. The recollection of
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preoperative visit. A history of head trauma was evident in 8 patients (40.0%). The medical evaluation showed that all patients had 1 or more concomitant disease. There were 6 patients with brain stroke, 4 with heart disease, 7 with diabetes mellitus, 4 with a malignancy, 3 with kidney dysfunction, 1 with dementia, 3 with liver disease, 13 with hypertension, and 2 with shunt-dependent hydrocephalus. Laboratory study showed impaired blood coagulation in 5 patients (25.0%). Nine patients (45.0%) had taken anticoagulant or antiplatelet medications (Table 1). Patients on platelet inhibition therapy had their medication discontinued immediately in an attempt to prevent hematoma expansion and facilitate the operative intervention. When rapid clinical deterioration occurred in these patients, platelet concentrate was routinely infused. Reversing anticoagulation before surgery was accomplished using fresh frozen plasma and vitamin K. Those with thrombocytopenia from hematologic disorder, renal failure, liver cirrhosis, and malignancy received platelet transfusion. Restarting the antiplatelet or anticoagulative agents was weighed with a focus on the history of embolism, reason for antithrombosis, hemostatic function, serial CT scans of CSDHs after burr-hole surgery, and neurologic evaluation. Radiographic Characteristics Bilateral blood collection was detected in 6 patients (30.0%). In the unilateral group, the CSDH was located over the left hemisphere in
hematoma is noted 2 weeks later after the second surgery (D). A contrast leakage into the hematoma is defined on CT immediately taken after the middle meningeal artery embolization (E). Follow-up CT scan obtained 20 days after intravascular therapy demonstrates complete resolution of chronic subdural hematoma in the left hemisphere (F).
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Table 1. Clinical Characteristics of Groups with Recurrent Chronic Subdural Hematomas Variables
Conventional (n [ 23)
Embolization (n [ 20)
Significance (P)
Age (years)
65.65 6.91
73.65 7.14
0.041
Male/female
16 (69.6)/7 (30.4)
14 (70.0)/6 (30.0)
0.975
Head trauma
17 (73.9)
8 (40.0)
0.033
Markwadler grade
0.421
0e2
22 (95.7)
18 (90.0)
3e4
1 (4.3)
2 (10.0)
Antiplatelets
1 (4.3)
6 (30.0)
0.038
Anticoagulants
1 (4.3)
3 (15.0)
0.323
Hypertension
5 (21.7)
13 (65.0)
0.469
Diabetes mellitus
4 (17.4)
7 (35.0)
0.721
Liver dysfunction
1 (4.3)
3 (15.0)
0.323
Renal failure
1 (4.3)
3 (15.0)
0.323
Heart disease
3 (13.0)
4 (20.0)
0.787
Malignancy
2 (8.7)
4 (20.0)
0.687
Medication use
Underlying diseases
Coagulopathy
1 (4.3)
5 (25.0)
0.065
Brain infarction
3 (13.0)
6 (30.0)
0.261
Values are number (%) except where indicated otherwise.
53.8% (14/26) and over the right hemisphere in 46.2% (12/26). Hematomas were divided into 4 types based on their internal architecture in CT findings: homogenous, laminar, separate, or trabecular.9 The numbers of each subtype were as follows: 11 (homogenous), 4 (laminar), 4 (separated), and 7 (trabecular), respectively. On the preoperative CT scans, the mean hematoma thickness was 15.6 3.6 mm (range, 2.9e29.4 mm) on the left side and 17.6 4.9 mm (range, 3.1e34.4 mm) on the right side. The CT grading of the brain atrophy was determined according to the widening of the sulci and subdural space.10 The numbers of cases classified as definite and severe grade were 4 (20.0%) and 15 (75.0%), respectively. The amount of subdural air found on immediate postoperative CT scans was categorized into the minimal and definite degrees.11 For cases of recently treated CSDHs, the maximum diameter of the MMA was measured and then compared with both sides on magnetic resonance angiography (MRA) (Figure 2A). Indication of MMA Embolization Angiography and embolization of the MMA were considered for 26 lesions in 20 patients with progressed hematoma collection after burr-hole and drainage surgery. This clinical study was approved by the institutional review board, and informed consent for the endovascular therapy was provided by the patients or their
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families. The decision of whether, when, and how to embolize the MMA should be tailored to the individual patient and their unique risk profile in the setting of recurrent hematoma formation. Generally, we favored this minimally invasive technique in an effort to reduce the hematoma recurrences and subsequent reoperations for the patients who are high-risk surgical candidates with recurrence of CSDHs. Angiography and embolization treatment for patients with recurrent CSDHs were determined by the following circumstances: 1) not requiring an emergent evacuation; 2) symptomatic recurrence within a short time after successful treatment; 3) elderly with brain atrophy; 4) enlarged ipsilateral MMA on MRA; 5) under antiplatelet and anticoagulant therapy; 6) advanced combined medical diseases; 7) bleeding tendency or coagulopathy; and 8) hematomas with multilocular collections. The timing of embolization differed for each patient at the surgeon’s discretion based on the operative finding and the clinical and radiologic presentations of patients with CSDHs that failed to resolve. In 16 patients, MMA embolization was performed at an early stage after surgery when signs of inadequate evacuation were observed on immediate postoperative CT, whereas another 4 patients more prone to bleeding because of underlying diseases or antithrombotic drugs preferentially underwent the intervention just before the burr-hole drainage. Endovascular Procedure Angiography and embolization of MMA were performed with the patient awake. Intravenous heparin was not administered. For intravascular surgery, a 5-F or 6-F guiding catheter was inserted into the femoral artery and placed near the origin of the external carotid artery on the hematoma side. A flow-guided type microcatheter (Prowler 10 [Cordis Neurovascular, Miami Lakes, Florida, USA]) was positioned in the main trunk of the MMA for superselective angiography. The angiographic feature was the arterial dilatation and visualization of abnormal vascular stains on the affected sides (Figure 2B and C). A neuroradiologist ensured that no collaterals to the orbit were present. Thereafter, the microcatheter was advanced through the frontal and parietal branches of the MMA, and then polyvinyl alcohol particles ranging from 150 to 250 mm in diameter were slowly injected under fluoroscopic control. This procedure was terminated when the cotton-woolelike blushing around the branches of the MMA was no longer seen (Figure 2D and E). A contrast leakage into the hematomas within the subdural space was clearly defined by postprocedure head CT scan (Figure 1E). There were no undesired effects from the angiography and embolization. Clinical and Radiographic Surveillance Every patient being treated for refractory CSDHs requires close follow-up for signs of recollected hematoma. Neurologic monitoring and serial CT scanning were frequently performed until detection of nearly total resolution of the CSDH and their improvement to a reasonable result (Figure 1F). Control CT was performed on the day after surgery to check for adequate drainage or any remarkable complication. The patient was discharged on the seventh postoperative day after confirming the absence of new hemorrhage. After the patients were discharged, they were regularly seen as outpatients at 2 weeks, 1 month, and 3 months after surgery, with additional visits up to
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Figure 2. Magnetic resonance angiography and selective arteriograms of middle meningeal artery (MMA) in patients with recurrent chronic subdural hematoma. The left MMA (arrowhead) that nourishes the hematoma is larger than the right MMA (arrow) (A). The hypertrophied MMA and cotton-wool staining are
6 months if there was a persistent subdural hematoma (SDH) on the 3-month scan. On follow-up CT scans, hematoma recurrence and cerebral re-expansion were defined as an increase in the hematoma density and width, and restoration of bilateral symmetry of the brain, respectively.12 Within the follow-up period, if new or progressive symptoms or signs developed, additional imaging was performed to diagnose the recurrence as soon as possible. The clinical status was based on a modified Rankin Scale (mRS) during the follow-up examinations, and a favorable outcome was defined as an mRS score of 0e2. Patients with an mRS score <3 at 3 months were not scheduled further, whereas patients with higher mRS scores were reassessed at 6 months after treatment. Statistical Analysis To assess the effect of intravascular treatment, the clinicalradiologic features and treatment results were statistically compared between the embolization group and the conventional group with 24 recurrent hematomas treated by craniostomy alone. A univariate analysis was performed with a Pearson c2 test, Fisher exact test, and Student t test. The statistical significance was set at P < 0.05. A multivariate analysis was performed using a logistic
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well visualized on lateral fluoroscopy image (B). Diffuse capillary networks are clearly delineated along the peripheral branches of MMA (C and D), which had completely disappeared at the end of particle embolization (E).
regression model. The relationship between the variables and treatment outcomes was presented based on a 95% confidence interval (CI) and the odds ratio (OR). RESULTS Demographic and clinical data are listed in Table 1. The embolization group was found to be associated with older age (P ¼ 0.041) and antiplatelet medication (P ¼ 0.038) but not with history of head trauma. On comparing the neurologic status on admission, no statistical difference was observed in either group. Hypertension, diabetes, and cerebral infarct were more frequently observed in the embolization group, but these factors did not reach statistical significance. Severe brain atrophy (P ¼ 0.041) and bilateral involvement of the hematomas (P ¼ 0.038) more frequently characterized the CT findings of the embolization therapy group (Table 2). The length of hospital stay and morbidity were statistically insignificant between the 2 groups (P > 0.05). Among 43 cases, 9 (20.9%) were affected by treatment-related complications, 2 had intracranial bleeding, 2 had wound hematoma, 1 had seizure, 2 had angina pectoris, 1 had urinary tract infection, 2 had pneumonia, and 1 had delirium. Postoperative hemorrhages were
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Figure 3. Pathologic examination of excised specimen in a patient of intractable chronic subdural hematoma (original magnification 100). Numerous blood vessels are observed in the interstitial space of the outer membrane of the hematoma. Fresh hemorrhages at the periphery are surrounded by many hemosiderin-laden macrophages on hematoxylin-eosin staining.
minor and managed with conservation. Times for restoring the bihemispheric symmetry in embolized CSDHs were significantly shorter than those of the control group (mean, 34.65 15.45 vs. 98.29 52.99 days; P < 0.001). A significant difference in the Table 2. Computed Tomography Data of Groups with Recurrent Chronic Subdural Hematomas Variables
Conventional (n [ 23)
Embolization (n [ 20)
Significance (P)
1 (4.3)
6 (30.0)
0.038
further recollection of hematoma was found between the 2 groups (P ¼ 0.008) (Table 3). In the conventional group, 8 of 24 lesions recurred (33.3%), and consequently, the hematomas were evacuated through an additional craniostomy (n ¼ 5) and craniotomy (n ¼ 3). In contrast, MMA embolization was curative in the study group, with the exception of 1 hematoma (3.8%), which spontaneously regressed. Regardless of agedness and concurrent illness, the functional outcomes of the embolization group were comparable with those of the conventional group (P > 0.05). Two patients (4.6%) in both groups died after discharge from causes not related to the operation. Logistic regression models showed that patients in the embolization group experienced a shortened brain re-expansion time (P ¼ 0.003; OR, 1.179; 95% CI, 1.059e1.313) and a higher rate of hematoma cure (P ¼ 0.024; OR, 1.029; 95% CI, 0.970e5.024) than did patients who were managed using a conventional approach (Table 3).
DISCUSSION Managing CSDH is a straightforward process, but an unremitting hemorrhage is sometimes difficult to treat. This factor was shown in the present study because the cohort had underlying medical diseases that complicated the clinical course of CSDHs. Revision surgery for drainage and irrigation is the first-line treatment for recollected hematomas. However, a few surgeons have performed complex procedures, such as craniotomy and membranectomy, subdural shunt, reservoir placement, hollow screw insertion, and craniectomy with duroplasty in patients with repeatedly relapsed CSDHs.13-17 An endoscope-assisted and sonogram-assisted evacuation is an emerging option for opening compartments and excising membranes in multiloculated hematomas.9,12 However, controversy remains regarding the best
Hematoma site Bilateral Unilateral Hematoma thickness (mm)
22 (95.7)
14 (70.0)
21.01 6.21
18.90 7.58
0.507 Variables
Brain atrophy None or mild
Table 3. Treatment Results of Two Groups with Recurrent Chronic Subdural Hematomas Conventional Embolization Significance Multivariate (n [ 23) (n [ 20) (P) (P)
Hospital stay 14.25 15.02 19.96 13.44 (days)
0.162
98.29 52.99 34.65 15.45
<0.001
12 (52.2)
3 (15.0)
0.021
Definite
8 (34.8)
4 (20.0)
0.281
Severe
3 (13.0)
13 (65.0)
0.041
17 (73.9)
11 (55.0)
Laminar
3 (13.0)
4 (20.0)
Separated
2 (8.7)
4 (20.0)
Trabecular
2 (8.7)
7 (35.0)
Minimal
16 (66.7)
16 (61.5)
0e2
20 (87.0)
17 (85.0)
Definite
8 (33.3)
10 (38.5)
3e6
3 (13.0)
3 (15.0)
Hematoma subtypes Homogenous
0.205
Subdural air collection
1.25
Values are number (%) except where indicated otherwise.
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Brain reexpansion time (days)
0.003
Complications Surgical
2 (8.7)
2 (10.0)
0.932
Medical
2 (8.7)
3 (15.0)
0.222
Hematoma recurrence
8 (33.3)
1 (3.8)
0.008
Modified Rankin Scale scores
0.024
1
Values are number (%) except where indicated otherwise.
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strategy because each tactic has associated operative risks and significant recurrence rates. Extensive research has identified that CSDH is an angiogenic and inflammatory disease. Blood products mixed with subdural fluid trigger a foreign body reaction, which is followed by formation of a neomembrane comprising immature vasculature on the interior of the pachymeninx. Continuous exudation and oozing from fragile neovessels in the membrane contribute to the generation and growth of CSDHs (Figure 3).10,18-20 Reports on the vascular anatomy of CSDHs21,22 have shown that numerous sinusoids penetrate the dura mater and connect to MMA branches. These sinusoids were seen as a giant capillary network and cotton-woolelike stains on the superselective angiography of the author’s embolization group. This finding was consistent with the results of investigations on MMA angiograms for refractory recurrent CSDHs in the literature.6,7,22 Contrast extravasation into the subdural space on postembolization CT of the illustrative case also indicated the communication between the hematoma cavity and the MMA. Intractability has commonly been found to lead to readmission and prolonged hospitalization and, because of effects from repeat surgery, may be life threatening for patients with rehemorrhagic CSDH. However, operative mortality in this series did not exceed that of ordinary CSDHs, which ranges from 1.2% to 3.8%.3,11,23 Recent analysis of MRA showed that the MMA ipsilateral to the hematoma becomes diffusely enlarged during the initiation period for the development of CSDHs.24 On the basis of this finding, we were supportive of an early intervention for refractory CSDHs, which contrasted with previous research that proposed the use of MMA embolization for hematomas with more than 2 or 3 recurrences.25,26 In this study, the embolization treatment proved to be a beneficial option for patients who had intractable CSDHs with 1 or more recurrences and reaccumulation within 1 month after satisfactory evacuation. Statistically, our embolization group was at an increased risk of recurrence and reoperation because they frequently involved variables, such as older age, marked brain atrophy, antiplatelet use, and bilateral hematomas. Despite unfavorable conditions in the patients, the higher resolution rate of hematomas was obtained by applying the MMA embolization at an early stage when signs of subdural recollection appeared. Furthermore, the extent of neurologic recovery in the group who underwent embolization was comparable with that of another series treated by various surgical methods.1,11,13,27 The occurrence of CSDHs associated with taking drugs that interfere with the coagulation system or platelet function is increasing in modern neurosurgery. Patients with antithrombotics-related CSDHs have been found to be more susceptible to surgical failure and recollection of hematomas after several operative attempts.28 To verify the clinical usefulness of embolization treatment for recurrent CSDHs, bleeding-prone patients with liver cirrhosis, antithrombosis, and hemodialysis were primarily enrolled for this preliminary study. Patients in our embolization group were more frequently affected by bilateral CSDHs that usually developed atraumatically and spontaneously. In theory, high-flow inputs into the capillary channel through the hypertrophied MMA result in repeated microhemorrhage from the neomembranes in patients under anticoagulation and antiplatelet therapy. Moreover, extensive electrocautery of the hematoma
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capsule is mostly impossible because of limited access and can cause fresh bleeding and acute SDH formation during burr-hole surgery. In our experience, the advantage of MMA embolization became apparent for the study population with coagulation disturbance, who required immediate cessation of bleeding from the outer membrane of CSDH. Nevertheless, in terms of the postoperative resumption of antiplatelets or anticoagulants, there are no data to address the clinical guideline regarding protocols for these patients on oral antithrombotics who underwent craniostomy plus embolization for related CSDHs. These medications were restarted after the operation wound was healed and when there was no significant recurrent or acute hemorrhage in the CT scan around the time of discharge. This author’s pharmacologic strategy did not need to be withheld for more than a week after the embolization treatment in those patients with a high thromboembolic risk receiving preoperative antithrombosis treatment. Refractory CSDH of elderly patients is an important indicator of MMA angiography and embolization treatment. In these cases, CSDHs have primarily been found to exert prolonged compression on the cerebral hemisphere, and consequently, a capacious room for hematomas 2e3 cm below the dura mater is created before any neurologic symptom arises.29 In addition, an aged brain of high elasticity invariably fails to re-expand, which leads to persistence of midline shifting after successful evacuation of CSDHs, with impaired adhesion between the inner and outer membranes, thus facilitating postoperative reaccumulation of the hematomas within the expansive subdural cavity.30 On the basis of these facts, it is reasonable to stop bleeding from the membrane and to promote resolution of the hematoma for patients with advanced brain atrophy in whom it is not easy to achieve better obliteration of the subdural space and then restore intracranial pressure dynamics. Theoretically, MMA embolization can play a major role in breaking the cycle of neomembrane formation, vascular hyperpermeability, inflammatory exudation, and repeated bleeding, thus allowing reabsorption of the clot over time without expansion.19,21,31 In this study, the primary merit of perioperative embolization was to enhance the cerebral re-expansion rate and to obviate additional operations for recurrent CSDHs in geriatric patients. This option might be used as a sole therapy for elderly patients who cannot tolerate anesthesia or sedation and for whom intracranial pressure is not relieved immediately. In addition, the presence of layering and mixed-density SDHs with partitioning membranes was more frequently observed in the patients in the embolization group. In managing patients with this status, the author also recommends MMA embolization treatment after burrhole drainage in preference to a more complicated craniotomy surgery.8,27 The procedure presented here that shut off the capillary flow to the intralesional septum appears to be safe and effective in the prevention of recurrence, with enhanced shrinkage of the hematoma remnant left after drainage and irrigation. The appropriate indication and timing for the use of MMA embolization to the recurrent CSDHs remain unclear. The decision protocol of embolization was left entirely to the treating surgeon’s discretion in accordance with the radiographic, neurologic, and operative features of the patients with CSDHs. Most patients in this series had the embolization treatment after revision burr-hole surgery for repeatedly collected hematomas. In previous
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research,7,22,25 although an embolization was performed after various instances of repeated CSDH formation in each patient, favorable results were obtained regardless of the timing. Commonly used materials for embolizing the MMA are N-butyl cyanoacrylate, polyvinyl alcohol particles, and coils, with almost the same therapeutic outcomes.6,7,22,25 When performing an embolization treatment, we must be cautious not to inject particles through the MMA branch involved in dangerous collateral to the orbit. In addition, the interventionist should keep in mind that the capillary feeders of CSDHs are easily missed when contrast media is infused at the main trunk of the external carotid artery. A disadvantage of MMA embolization was the lag time before the resolution of symptoms in some cases with recurrence of refractory CSDH. Hair loss and wound breakdown are also important issues to consider when planning embolization therapy in elderly patients or in poor surgical candidates with premorbidity. Recent advances in endovascular technology made the embolization procedure more precise for our patients, allowing for
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