- Email: [email protected]
Risk Factors for Recurrence of Chronic Subdural Hematoma: A Single Center Experience
Original Article
Risk Factors for Recurrence of Chronic Subdural Hematoma: A Single Center Experience Lun-Xin Liu1, Xu-Dong Cao2, Yan-Ming Ren1, Liang-Xue Zhou1, Chao-Hua Yang1
OBJECTIVE: Chronic subdural hematoma (CSDH) is a common form of intracranial hemorrhage with a substantial recurrence rate. We aimed to investigate the predictive factors for the postsurgical recurrence of CSDH.
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METHODS: We retrospectively reviewed the medical records of patients with CSDH who underwent surgery in West China Hospital between January 2012 and June 2018. Univariate and multivariate analyses were performed to identify the relationships between recurrence of CSDH and factors such as age, sex, history of injury, Markwalder grading, computed tomography findings, surgical methods, and outcomes.
thick inner neomembrane might be the primary cause of CSDH recurrence.
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RESULTS: A total of 328 patients (281 men and 47 women) aged 22e93 years (mean age, 65.14 13.76 years) were included. Computed tomography findings at admission showed mixed density hematoma in 136 patients, isodensity hematoma in 140, high-density hematoma in 34, and low-density hematoma in 18. The mortality and recurrence rate were 0.30% (1 of 328) and 2.44% (8 of 328), respectively. Six months postoperatively, 327 patients had Markwalder grade 0. Hematoma recurred in 8 patients of which 7 were mixed density hematoma and 1 was isodensity hematoma. Six patients who underwent craniotomy had thickened inner neomembrane that was resected. Univariate and multivariate analyses found mixed density hematoma to be an independent risk factor for the recurrence of CSDH.
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CONCLUSIONS: Burr hole craniostomy with irrigation and closed-system drainage is effective for the surgical treatment of CSDH. Mixed density hematoma is an independent predictor for the recurrence of CSDH. Presence of
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Key words - Burr hole - Chronic subdural hematoma - Membrane - Mixed density hematoma - Recurrence Abbreviations and Acronyms CI: Confidence interval CSDH: Chronic subdural hematoma CT: Computed tomography HU: Hounsfield unit OR: Odds ratio
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INTRODUCTION
C
hronic subdural hematoma (CSDH) is the abnormal collection of subdural liquefied blood that may lead to compression of the brain tissue and subsequent neurologic sequelae.1,2 The total incidence of CSDH is reportedly 1. 72e20.6 per 100,000 people per year, and the incidence rate is significantly higher in elderly individuals.1,3-9 Although some reports state that CSDH could be treated with pharmacotherapeutics, such as corticosteroids and atorvastatin, surgical intervention is the mainstay of treatment of CSDH especially in cases that manifest mass effect.10,11 Currently, twist-drill craniostomy, burr hole craniostomy, and craniotomy are the principal surgical techniques used to treat CSDH.12 Although most cases of CSDH resolve after simple skull drilling, its recurrence remains a problem. The recurrence rate of postsurgical CSDH have been reported to be 5% to 33%.13-15 Previous studies have focused on important factors indicative of postoperative clinical outcomes; however, only few studies have examined the postoperative clinical and radiologic factors and surgical findings predictive of the postoperative recurrence of CSDH.16,17 This study aimed to investigate the predictive factors for the recurrence of CSDH, and to summarize our surgical experience on how to reduce the incidence of recurrence of CSDH. METHODS Participants We retrospectively reviewed medical records of all patients who underwent surgery for CSDH at the West China Hospital from
From the 1Department of Neurosurgery, West China Hospital, Sichuan University, Chengdu, Sichuan; and 2Department of Neurosurgery, The People’s Hospital of Tibet Autonomous Region, Lhasa, Tibet, People’s Republic of China To whom correspondence should be addressed: Chao-Hua Yang, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019) 132:e506-e513. https://doi.org/10.1016/j.wneu.2019.08.089 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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RISK FACTORS FOR RECURRENCE OF CSDH
Table 1. Markwalder Grading Scale18 Grade 0
Neurologically normal
Grade 1
Alert and orientated: absence of mild symptoms such as headache, or mild neurologic deficit such as reflex asymmetry
Grade 2
Drowsy or disorientated, or variable neurologic deficit such as hemiparesis
Grade 3
Stuporous but responding appropriately to noxious stimuli, several focal signs such as hemiplegia
Grade 4
Comatose with absent motor responses to painful stimuli, decerebrate or decorticate posturing
Figure 1. Hematomas of different densities as visualized on computed tomography images. (A) Isodensity hematoma; (B) Low-density hematoma; (C)
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Hyperdensity hematoma; (D) Mixed density hematoma.
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Figure 2. A man aged 61 years with mixed density hematoma in whom the surgical procedure was revised to craniotomy on intraoperative finding of organized hematoma during burr hole craniostomy. (A) The white arrow indicates the organized hematoma. (B) The forceps show the thickened
January 2012 to June 2018. A diagnosis of CSDH was confirmed by computed tomography (CT). Patients with CSDH who underwent surgery with subsequent postsurgical confirmation of the CSDH were eventually included. The study was approved by the ethics committee of West China Hospital. Information regarding patients' age, sex, duration from symptoms to operation, location of CSDH (unilateral or bilateral), hypertension, diabetes, antiplatelet therapy, anticoagulant therapy, Markwalder grading scale (Table 1),18 distance of midline shift (mm), cisterna ambiens compression, initial maximal thickness of the subdural hematoma (mm), and presence of organized hematoma were assessed herein. Density of the subdural hematomas were classified into the 4 following groups based on CT findings17: low-density (<25 Hounsfield units [HU]), isodensity (25e35 HU), hyperdensity (>35 HU), and mixed density (Figure 1). The maximal thickness of the postoperative gas (mm) and liquid (mm) were measured on CT images (Figure 1). All included patients had been scheduled to undergo a single burr hole craniostomy with irrigation and closed-system drainage under general or local anesthesia. However, a craniotomy had been performed in cases in which organized hematoma was found during burr hole craniostomy (Figure 2). Selection of the procedure was based on surgical findings. A closed drainage was performed for all patients using a drain tube for 48 hours. CT scans were generally performed 1 day, 1 month, and 6 months postoperatively. However, CT was performed immediately
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inner neomembrane. (C) The white arrow indicates the partially resected inner neomembrane and the removed hematoma. (D) Preoperative computed tomography (CT) image. (E) CT image on postoperative day 1. (F) CT image at 2-month follow-up.
in patients who had presented symptoms such as headache, vomiting, weakness, et cetera. We defined the recurrence of CSDH as a case indicative of repeat surgery based on increase in the volume of ipsilateral subdural hematoma on CT scan, along with signs of neurologic deficit due to CSDH at 6-month follow-up. Statistical Analyses Univariate analysis was performed with the Pearson c2 test or the Fisher exact test. The ManneWhitney U test was used for analyzing noncategorical variables (age, midline shift; thickness of hematoma, postoperative gas, and postoperative liquid). Multivariate analysis with logistic regression model was used to determine independent associations among the various probable factors indicative of recurrence. The relationship between each predictive factor and recurrence of CSDH is expressed as odds ratio (OR) and 95% confidence interval (CI). A P value <0.05 was considered statistically significant. Statistical analysis was performed using the SPSS statistics software for Mac (SPSS Version 25.0, IBM Corporation, Armonk, New York, USA). RESULTS A total of 328 patients (281 men and 47 women; age range, 22e93 years; mean age, 65.14 13.76 years) with CSDH were included in the study. Among them, 170 patients had experienced apparent head trauma; the interval between trauma and first operation was
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Figure 3. A man aged 62 years with chronic subdural hematoma (CSDH). (A) Computed tomography (CT) image shows mixed density hematoma. (B) Postoperative day 1 CT image shows decrease in CSDH after burr hole drainage. (C) The patient experienced the recurrence of CSDH 10 days after the procedure. (D) Magnetic resonance image shows the inner neomembrane (red pointed arrow). (E) Intraoperative image shows
58.80 31.09 days. Nine patients consumed aspirin, and 8 patients consumed warfarin. The early symptoms of CSDH were headache, dizziness, weakness, disturbance of consciousness, and gait disturbance. According to Markwalder grading, 311 patients were grade 1, 14 patients were grade 2, 1 patient was grade 3, and 2 patients were grade 4. CT findings on admission identified 140 patients with isodensity hematoma (42.2%), 18 patients with lowdensity hematoma (5.5%), 34 patients with hyperdensity hematoma (10.4%), and 136 patients with mixed density hematoma (41.5%). The CSDH was left-sided in 147 patients, right-sided in 120 patients, and bilateral in 61 patients. Basal cisterns were compressed in 186 patients. Midline shift ranged from 0e15 mm (4.75 3.39 mm). Thickness of hematoma ranged from 7e40 mm (18.19 6.88 mm). Three hundred and twenty-one patients underwent single burr hole craniostomy with drainage; 7 patients were revised to craniotomy after organized hematoma was found during burr hole craniostomy, and additionally, they showed thickened inner neomembranes that were partially resected. After burr hole drainage, surgical site hemorrhage had developed in 3 patients. One patient with small epidural hematoma received conservative therapy; 1 patient with epidural mass/hematoma underwent craniotomy; a man aged 80 years with subdural mass/
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thickened inner neomembrane (green pointed arrow). The top left corner of the image shows the incision of the inner neomembrane, just above the arachnoid membrane. (F) CT image 1 day after craniotomy shows recurrence of CSDH has been removed. (G) Postoperative 1-month CT image shows disappearance of the patient’s CSDH.
hematoma died because his family members refused consent for repeat surgery. Eight patients (2.4%, 8 of 328) experienced recurrence of CSDH during the study period of which 7 patients presented mixed density hematoma and 1 patient had isodensity hematoma. Among them, 6 patients underwent craniotomy and their inner neomembrane were found to be thickened, and subsequently underwent partial resection (Figure 3). Two patients underwent a repeat burr hole craniostomy with drainage. The demographic information of the patients who experienced recurrence is listed in Table 2. All patients were followed-up. Three hundred and twenty-seven patients were Markwalder grade 0 at postoperative 6-month follow-up. The surgery in 7 patients was revised to craniotomy and 6 patients who experienced recurrence underwent craniotomy; none of these patients experienced hemorrhage, seizure, or postoperative recurrence of hematoma. Univariate analysis showed that recurrence of CSDH was significantly associated with cisterna ambiens compression (P ¼ 0.011) and mixed density hematoma (P ¼ 0.01). Multivariate logistic regression analysis identified mixed density hematoma (OR, 17.845; 95% CI, 1.473e216.207; P ¼ 0.024) as the only independent risk factors for the recurrence of CSDH. The results of
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5
5
10
5
10
10
5
10
2 25 Mixed density Yes 5 Left 1 None None
Male
Male
Male
71
62
66
None
2
15 20
20 Mixed density
Mixed density Yes
Yes 5
15 Left
Left 1
1 61
67 None
None
Male 49
None
Male 83
None
2 12 Mixed density Yes 10 Left 2 None None
Male 80
None
10
2 15
40 Mixed density
Mixed density Yes
Yes 3
8 Right
Right 1
1 26
65 None
Antiplatelet
Male 65
None
Male 50
Hypertension
5 30
15 Mixed density
Isodensity Yes
Yes 7
10 Right
Left 1
1 None
None None
Sex
None
None
10
DISCUSSION
None
Hemorrhage Side Markwalder Grading Scale Traumatic History (days) Antiplatelet and Anticoagulant Therapy Hypertension and Diabetes
univariate and multivariate analyses for the identification of factors predictive of CSDH recurrence are shown in Table 3.
Age (years)
Table 2. Demographic Information of Recurrence of Chronic Subdural Hematoma
Midline Shift (mm)
Cisterna Ambiens Compression
Hematoma Density
Thickness of Hematoma (mm)
Thickness of Postoperative Gas (mm)
Thickness of Postoperative Liquid (mm)
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Many risk factors for CSDH recurrence have been reported, including hemorrhage, advanced age, intracranial hypotension, bilateral CSDH, brain atrophy, hematoma density, postoperative posture, type of hematoma, diabetes, surgical technique, postoperative subdural accumulation of gas, inflammatory cytokines, alcohol consumption, and diversity in hematoma cavity.19-29 CSDH begins with the subdural accumulation of cerebrospinal fluid and blood cells, which occurs because of rupture of the arachnoid membrane following brain contusion or mild hemorrhage from a bridging vein. The next step involves the formation of a primary neomembrane with rich vasculature that develops following an inflammatory response caused by a continuous and mild hematogenous accumulation of subdural fluid. The neomembrane exhibits gradual bleeding with exudation of various cytokines and activating substances, and the unclotted hematoma grows in size as a wrapped hematoma with thick outer neomembrane and a thin inner neomembrane, above the arachnoid membrane, although some of the hematomas subside spontaneously.30 The neomembrane, especially the inner neomembrane, may prevent the brain tissue from expanding and forms a subdural hematoma cavity that cannot be eliminated. Although many risk factors have been included in our logistic regression model, only mixed density hematoma (OR, 17.845; 95% CI, 1.473e216.207; P ¼ 0.024) were found to be associated with the recurrence of CSDH. In consensus, other studies have reported similar findings.31,32 In 7 patients who had mixed density hematoma on CT, the surgery was revised to craniotomy because of intraoperative findings of organized hematoma and thick inner neomembrane. On the contrary, 8 patients experienced recurrence of CSDH, among which 7 were cases of mixed density hematoma. Organized hematoma and thick inner neomembranes were identified in 6 patients during craniotomy. No recurrence was reported in these patients after partial removal of the thickened inner neomembrane during craniotomy. Therefore, we speculate that patients indicated with mixed density hematoma may have thick inner neomembrane and organized hematoma. Furthermore, we believe that a thick inner neomembrane is an important factor contributing to the recurrence of CSDH. If cases with thin inner neomembrane of CSDH, the brain tissue expansion may occur and the residual liquid and gas from the craniotomy may be slowly absorbed, eventually leading to complete expansion of the brain tissue. On the contrary, a thick inner neomembrane of CSDH restricts the expansion of the brain tissue, increasing the probability of recurrence of CSDH. This observation may explain why the presence of residual liquid and gas did not affect the recurrence of CSDH in the present study, contrary to the results of other studies.33,34 Various types of surgery have been proposed for CSDH. The 3 most commonly used surgical techniques are the twist-drill craniostomy, burr hole craniostomy, and craniotomy.12 Burr hole craniostomy with closed drainage is presently the most popular surgical technique with a balanced risk and efficacy profiles.35-37 Reports indicate the postsurgical recurrence rate
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Table 3. Factors Related to Recurrence of Chronic Subdural Hematoma: Univariate Analysis and Multivariable Analysis Number of Patients (%) Factor
No Recurrence
Recurrence
320
8
Total Sex Male
P Value, Uni and Bivariable Analysis
P Value, Multivariable Analysis
OR (95% CI), Multivariable Analysis
0.242
0.997
NA
273 (97.2%)
47 (100%)
Female
8 (2.8%)
0 (0%)
Age (years)
65.13 13.81
65.75 12.37
0.900
0.270
0.96 (0.896e1.031)
61 (19.1%)
0 (0%)
0.360
0.997
NA
72（22.5%）
2 (25%)
1.00
0.584
1.838 (0.207e16.290)
Bilateral hematoma Hypertension Diabetes
19 (5.9%)
0 (0%)
1.00
0.998
NA
Antiplatelet therapy
8 (2.5%)
1 (12.5%)
0.202
0.263
5.911 (0.264e132.494)
Anticoagulant therapy Traumatic history (days)
8 (2.5%)
0 (0%)
1.00
0.999
NA
30.55 37.11
27.38 31.88
0.811
0.774
0.996 (0.970e1.023)
0.317
0.891
NA
0.08
0.546
1.098 (0.811e1.485)
Markwalder grading scale 1
304 (95.0%)
7（87.5%）
2
13 (4.1%)
1（12.5%）
3
1 (0.3%)
0 (0%)
4
2（0.6%）
0 (0%)
4.67 3.35
7.88 3.78
Midline shift (mm) Cisterna ambiens compression*
178 (95.7%)
8 (100%)
0.011
0.995
NA
Isodensity hematoma
139 (43.4%)
1 (12.5%)
0.145
NA
NA
18 (6.6%)
0 (0%)
1.00
NA
NA
Low-density hematoma High-density hematoma
34 (10.6%)
0 (0%)
1.00
NA
NA
Mixed density hematoma*
129 (40.3%)
7 (87.5%)
0.01
0.024
17.845 (1.473e216.207)
Thickness of hematoma (mm)
18.09 6.80
22.13 9.28
0.101
0.084
1.135 (0.983e1.31)
7 (2.2%)
0 (0%)
1.00
0.999
NA
Thickness of postoperative gas (mm)
8.23 5.87
8.17 5.36
0.972
0.452
1.080 (0.884e1.319)
Thickness of postoperative liquid (mm)
5.13 3.53
4.17 2.33
0.347
0.320
0.854 (0.627e1.165)
Organized hematoma
OR, odds ratio; CI, confidence interval; NA, not available. *Significant difference.
of CSDH to be about 5% to 33%.13-15 However, the recurrence rate was only 2.4% at our center, which is lower than that reported by previous studies. In our center, the single burr hole craniostomy with the closed drainage is the main technique preferred for CSDH. Two reasons may explain the low recurrence rate of CSDH at our center: 1) the burr hole (approximately 1.2 cm) is always larger than the diameter of the drainage tube, and helps to efficiently evacuate the hematoma, especially large hematomas, from the subdural cavity; and 2) the subdural cavity is irrigated with normal saline solution until the irrigational saline solution appears colorless and free of other materials (blood clot and floccule).38 Some reports have presumed that patients with parietal or occipital drainage have a higher recurrence rate and considerably
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greater subdural accumulation of air than those with frontal drainage; moreover, subdural accumulation of air was associated with the recurrence of CSDH.39 However, the brain tissue may expand because of gradual absorption of gas after removal of the hematoma. Moreover, logistic regression analysis showed no difference between the volume of the accumulated air. At our center, as part of routine practice, the drainage tube is inserted deep into the hematoma cavity and the whole cavity is irrigated with normal saline solution. Large hematoma clots and floccules are washed out, especially in patients with mixed density hematoma. Insufficient irrigation may lead to the retention of residual hematoma clot and floccule and contribute to the formation of thick inner neomembrane and organized hematoma.
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Based on our experience, craniotomy is the optimal method used at our center to manage the recurrence of CSDH and to remove inner neomembranes. In this study, 8 patients experienced recurrence over the course of follow-up. The recurrent CSDH was managed by craniotomy in 6 patients. However, 2 patients with symptoms of recurrence refused to undergo craniotomy. We performed burr hole craniostomy in these 2 patients with the presumption that the inner neomembrane was not thick. Removal of the inner membrane of CSDH remains a controversial issue. Lee et al.40 reported on the futility of procedures aimed to decrease the recurrence rate of CSDH after membranectomy. Nevertheless, Kim et al.41 reported a decrease in the recurrence rate of CSDH after membranectomy. Moreover, a meta-analysis study reported that the mortality and postoperative complications after craniotomy with membrane resection were similar to those of burr hole drainage, however, with reduced recurrence rate.42 The surgical procedure was revised to craniotomy in 7 patients, and 6 patients with recurrent CSDH underwent
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craniotomy; none of these patients experienced postoperative hemorrhage, seizure, or recurrence of hematoma. Our aim was to decompress the tension caused by the inner membrane; therefore, we performed a partial resection of the thick inner membrane that was loosely adhered to the brain. If the inner membrane is closely adhered to the brain, performing a craniostomy will only tear the inner neomembrane to avoid brain injury. Therefore, craniotomy was performed to partially resect the inner neomembrane, above the arachnoid membrane, in patients with recurrence of CSDH to avoid further recurrence. CONCLUSIONS Burr hole craniostomy with irrigation and closed-system drainage is an effective method for the surgical treatment of CSDH. Mixed density hematoma is an independent predictor of recurrence of CSDH. Moreover, the presence of thick inner neomembranes might be the main etiology for the recurrence of CSDH.
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39. Nakaguchi H, Tanishima T, Yoshimasu N. Relationship between drainage catheter location and postoperative recurrence of chronic subdural hematoma after burr-hole irrigation and closedsystem drainage. J Neurosurg. 2000;93:791-795.
35. Lind CR, Lind CJ, Mee EW. Reduction in the number of repeated operations for the treatment of subacute and chronic subdural hematomas by placement of subdural drains. J Neurosurg. 2003;99: 44-46.
40. Lee JY, Ebel H, Ernestus RI, Klug N. Various surgical treatments of chronic subdural hematoma and outcome in 172 patients: is membranectomy necessary? Surg Neurol. 2004;61: 523-527.
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41. Kim JH, Kang DS, Kim JH, Kong MH, Song KY. Chronic subdural hematoma treated by small or large craniotomy with membranectomy as the initial treatment. J Korean Neurosurg Soc. 2011;50: 103-108. 42. Sahyouni R, Mahboubi H, Tran P, Roufail JS, Chen JW. Membranectomy in chronic subdural hematoma: meta-analysis. World Neurosurg. 2017; 104:418-429.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 24 April 2019; accepted 14 August 2019 Citation: World Neurosurg. (2019) 132:e506-e513. https://doi.org/10.1016/j.wneu.2019.08.089 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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Risk Factors for Recurrence of Chronic Subdural Hematoma: A Single Center Experience Lun-Xin Liu1, Xu-Dong Cao2, Yan-Ming Ren1, Liang-Xue Zhou1, Chao-Hua Yang1
OBJECTIVE: Chronic subdural hematoma (CSDH) is a common form of intracranial hemorrhage with a substantial recurrence rate. We aimed to investigate the predictive factors for the postsurgical recurrence of CSDH.
-
METHODS: We retrospectively reviewed the medical records of patients with CSDH who underwent surgery in West China Hospital between January 2012 and June 2018. Univariate and multivariate analyses were performed to identify the relationships between recurrence of CSDH and factors such as age, sex, history of injury, Markwalder grading, computed tomography findings, surgical methods, and outcomes.
thick inner neomembrane might be the primary cause of CSDH recurrence.
-
RESULTS: A total of 328 patients (281 men and 47 women) aged 22e93 years (mean age, 65.14 13.76 years) were included. Computed tomography findings at admission showed mixed density hematoma in 136 patients, isodensity hematoma in 140, high-density hematoma in 34, and low-density hematoma in 18. The mortality and recurrence rate were 0.30% (1 of 328) and 2.44% (8 of 328), respectively. Six months postoperatively, 327 patients had Markwalder grade 0. Hematoma recurred in 8 patients of which 7 were mixed density hematoma and 1 was isodensity hematoma. Six patients who underwent craniotomy had thickened inner neomembrane that was resected. Univariate and multivariate analyses found mixed density hematoma to be an independent risk factor for the recurrence of CSDH.
-
CONCLUSIONS: Burr hole craniostomy with irrigation and closed-system drainage is effective for the surgical treatment of CSDH. Mixed density hematoma is an independent predictor for the recurrence of CSDH. Presence of
-
Key words - Burr hole - Chronic subdural hematoma - Membrane - Mixed density hematoma - Recurrence Abbreviations and Acronyms CI: Confidence interval CSDH: Chronic subdural hematoma CT: Computed tomography HU: Hounsfield unit OR: Odds ratio
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INTRODUCTION
C
hronic subdural hematoma (CSDH) is the abnormal collection of subdural liquefied blood that may lead to compression of the brain tissue and subsequent neurologic sequelae.1,2 The total incidence of CSDH is reportedly 1. 72e20.6 per 100,000 people per year, and the incidence rate is significantly higher in elderly individuals.1,3-9 Although some reports state that CSDH could be treated with pharmacotherapeutics, such as corticosteroids and atorvastatin, surgical intervention is the mainstay of treatment of CSDH especially in cases that manifest mass effect.10,11 Currently, twist-drill craniostomy, burr hole craniostomy, and craniotomy are the principal surgical techniques used to treat CSDH.12 Although most cases of CSDH resolve after simple skull drilling, its recurrence remains a problem. The recurrence rate of postsurgical CSDH have been reported to be 5% to 33%.13-15 Previous studies have focused on important factors indicative of postoperative clinical outcomes; however, only few studies have examined the postoperative clinical and radiologic factors and surgical findings predictive of the postoperative recurrence of CSDH.16,17 This study aimed to investigate the predictive factors for the recurrence of CSDH, and to summarize our surgical experience on how to reduce the incidence of recurrence of CSDH. METHODS Participants We retrospectively reviewed medical records of all patients who underwent surgery for CSDH at the West China Hospital from
From the 1Department of Neurosurgery, West China Hospital, Sichuan University, Chengdu, Sichuan; and 2Department of Neurosurgery, The People’s Hospital of Tibet Autonomous Region, Lhasa, Tibet, People’s Republic of China To whom correspondence should be addressed: Chao-Hua Yang, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019) 132:e506-e513. https://doi.org/10.1016/j.wneu.2019.08.089 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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RISK FACTORS FOR RECURRENCE OF CSDH
Table 1. Markwalder Grading Scale18 Grade 0
Neurologically normal
Grade 1
Alert and orientated: absence of mild symptoms such as headache, or mild neurologic deficit such as reflex asymmetry
Grade 2
Drowsy or disorientated, or variable neurologic deficit such as hemiparesis
Grade 3
Stuporous but responding appropriately to noxious stimuli, several focal signs such as hemiplegia
Grade 4
Comatose with absent motor responses to painful stimuli, decerebrate or decorticate posturing
Figure 1. Hematomas of different densities as visualized on computed tomography images. (A) Isodensity hematoma; (B) Low-density hematoma; (C)
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Hyperdensity hematoma; (D) Mixed density hematoma.
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Figure 2. A man aged 61 years with mixed density hematoma in whom the surgical procedure was revised to craniotomy on intraoperative finding of organized hematoma during burr hole craniostomy. (A) The white arrow indicates the organized hematoma. (B) The forceps show the thickened
January 2012 to June 2018. A diagnosis of CSDH was confirmed by computed tomography (CT). Patients with CSDH who underwent surgery with subsequent postsurgical confirmation of the CSDH were eventually included. The study was approved by the ethics committee of West China Hospital. Information regarding patients' age, sex, duration from symptoms to operation, location of CSDH (unilateral or bilateral), hypertension, diabetes, antiplatelet therapy, anticoagulant therapy, Markwalder grading scale (Table 1),18 distance of midline shift (mm), cisterna ambiens compression, initial maximal thickness of the subdural hematoma (mm), and presence of organized hematoma were assessed herein. Density of the subdural hematomas were classified into the 4 following groups based on CT findings17: low-density (<25 Hounsfield units [HU]), isodensity (25e35 HU), hyperdensity (>35 HU), and mixed density (Figure 1). The maximal thickness of the postoperative gas (mm) and liquid (mm) were measured on CT images (Figure 1). All included patients had been scheduled to undergo a single burr hole craniostomy with irrigation and closed-system drainage under general or local anesthesia. However, a craniotomy had been performed in cases in which organized hematoma was found during burr hole craniostomy (Figure 2). Selection of the procedure was based on surgical findings. A closed drainage was performed for all patients using a drain tube for 48 hours. CT scans were generally performed 1 day, 1 month, and 6 months postoperatively. However, CT was performed immediately
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inner neomembrane. (C) The white arrow indicates the partially resected inner neomembrane and the removed hematoma. (D) Preoperative computed tomography (CT) image. (E) CT image on postoperative day 1. (F) CT image at 2-month follow-up.
in patients who had presented symptoms such as headache, vomiting, weakness, et cetera. We defined the recurrence of CSDH as a case indicative of repeat surgery based on increase in the volume of ipsilateral subdural hematoma on CT scan, along with signs of neurologic deficit due to CSDH at 6-month follow-up. Statistical Analyses Univariate analysis was performed with the Pearson c2 test or the Fisher exact test. The ManneWhitney U test was used for analyzing noncategorical variables (age, midline shift; thickness of hematoma, postoperative gas, and postoperative liquid). Multivariate analysis with logistic regression model was used to determine independent associations among the various probable factors indicative of recurrence. The relationship between each predictive factor and recurrence of CSDH is expressed as odds ratio (OR) and 95% confidence interval (CI). A P value <0.05 was considered statistically significant. Statistical analysis was performed using the SPSS statistics software for Mac (SPSS Version 25.0, IBM Corporation, Armonk, New York, USA). RESULTS A total of 328 patients (281 men and 47 women; age range, 22e93 years; mean age, 65.14 13.76 years) with CSDH were included in the study. Among them, 170 patients had experienced apparent head trauma; the interval between trauma and first operation was
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ORIGINAL ARTICLE LUN-XIN LIU ET AL.
Figure 3. A man aged 62 years with chronic subdural hematoma (CSDH). (A) Computed tomography (CT) image shows mixed density hematoma. (B) Postoperative day 1 CT image shows decrease in CSDH after burr hole drainage. (C) The patient experienced the recurrence of CSDH 10 days after the procedure. (D) Magnetic resonance image shows the inner neomembrane (red pointed arrow). (E) Intraoperative image shows
58.80 31.09 days. Nine patients consumed aspirin, and 8 patients consumed warfarin. The early symptoms of CSDH were headache, dizziness, weakness, disturbance of consciousness, and gait disturbance. According to Markwalder grading, 311 patients were grade 1, 14 patients were grade 2, 1 patient was grade 3, and 2 patients were grade 4. CT findings on admission identified 140 patients with isodensity hematoma (42.2%), 18 patients with lowdensity hematoma (5.5%), 34 patients with hyperdensity hematoma (10.4%), and 136 patients with mixed density hematoma (41.5%). The CSDH was left-sided in 147 patients, right-sided in 120 patients, and bilateral in 61 patients. Basal cisterns were compressed in 186 patients. Midline shift ranged from 0e15 mm (4.75 3.39 mm). Thickness of hematoma ranged from 7e40 mm (18.19 6.88 mm). Three hundred and twenty-one patients underwent single burr hole craniostomy with drainage; 7 patients were revised to craniotomy after organized hematoma was found during burr hole craniostomy, and additionally, they showed thickened inner neomembranes that were partially resected. After burr hole drainage, surgical site hemorrhage had developed in 3 patients. One patient with small epidural hematoma received conservative therapy; 1 patient with epidural mass/hematoma underwent craniotomy; a man aged 80 years with subdural mass/
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RISK FACTORS FOR RECURRENCE OF CSDH
thickened inner neomembrane (green pointed arrow). The top left corner of the image shows the incision of the inner neomembrane, just above the arachnoid membrane. (F) CT image 1 day after craniotomy shows recurrence of CSDH has been removed. (G) Postoperative 1-month CT image shows disappearance of the patient’s CSDH.
hematoma died because his family members refused consent for repeat surgery. Eight patients (2.4%, 8 of 328) experienced recurrence of CSDH during the study period of which 7 patients presented mixed density hematoma and 1 patient had isodensity hematoma. Among them, 6 patients underwent craniotomy and their inner neomembrane were found to be thickened, and subsequently underwent partial resection (Figure 3). Two patients underwent a repeat burr hole craniostomy with drainage. The demographic information of the patients who experienced recurrence is listed in Table 2. All patients were followed-up. Three hundred and twenty-seven patients were Markwalder grade 0 at postoperative 6-month follow-up. The surgery in 7 patients was revised to craniotomy and 6 patients who experienced recurrence underwent craniotomy; none of these patients experienced hemorrhage, seizure, or postoperative recurrence of hematoma. Univariate analysis showed that recurrence of CSDH was significantly associated with cisterna ambiens compression (P ¼ 0.011) and mixed density hematoma (P ¼ 0.01). Multivariate logistic regression analysis identified mixed density hematoma (OR, 17.845; 95% CI, 1.473e216.207; P ¼ 0.024) as the only independent risk factors for the recurrence of CSDH. The results of
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5
5
10
5
10
10
5
10
2 25 Mixed density Yes 5 Left 1 None None
Male
Male
Male
71
62
66
None
2
15 20
20 Mixed density
Mixed density Yes
Yes 5
15 Left
Left 1
1 61
67 None
None
Male 49
None
Male 83
None
2 12 Mixed density Yes 10 Left 2 None None
Male 80
None
10
2 15
40 Mixed density
Mixed density Yes
Yes 3
8 Right
Right 1
1 26
65 None
Antiplatelet
Male 65
None
Male 50
Hypertension
5 30
15 Mixed density
Isodensity Yes
Yes 7
10 Right
Left 1
1 None
None None
Sex
None
None
10
DISCUSSION
None
Hemorrhage Side Markwalder Grading Scale Traumatic History (days) Antiplatelet and Anticoagulant Therapy Hypertension and Diabetes
univariate and multivariate analyses for the identification of factors predictive of CSDH recurrence are shown in Table 3.
Age (years)
Table 2. Demographic Information of Recurrence of Chronic Subdural Hematoma
Midline Shift (mm)
Cisterna Ambiens Compression
Hematoma Density
Thickness of Hematoma (mm)
Thickness of Postoperative Gas (mm)
Thickness of Postoperative Liquid (mm)
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Many risk factors for CSDH recurrence have been reported, including hemorrhage, advanced age, intracranial hypotension, bilateral CSDH, brain atrophy, hematoma density, postoperative posture, type of hematoma, diabetes, surgical technique, postoperative subdural accumulation of gas, inflammatory cytokines, alcohol consumption, and diversity in hematoma cavity.19-29 CSDH begins with the subdural accumulation of cerebrospinal fluid and blood cells, which occurs because of rupture of the arachnoid membrane following brain contusion or mild hemorrhage from a bridging vein. The next step involves the formation of a primary neomembrane with rich vasculature that develops following an inflammatory response caused by a continuous and mild hematogenous accumulation of subdural fluid. The neomembrane exhibits gradual bleeding with exudation of various cytokines and activating substances, and the unclotted hematoma grows in size as a wrapped hematoma with thick outer neomembrane and a thin inner neomembrane, above the arachnoid membrane, although some of the hematomas subside spontaneously.30 The neomembrane, especially the inner neomembrane, may prevent the brain tissue from expanding and forms a subdural hematoma cavity that cannot be eliminated. Although many risk factors have been included in our logistic regression model, only mixed density hematoma (OR, 17.845; 95% CI, 1.473e216.207; P ¼ 0.024) were found to be associated with the recurrence of CSDH. In consensus, other studies have reported similar findings.31,32 In 7 patients who had mixed density hematoma on CT, the surgery was revised to craniotomy because of intraoperative findings of organized hematoma and thick inner neomembrane. On the contrary, 8 patients experienced recurrence of CSDH, among which 7 were cases of mixed density hematoma. Organized hematoma and thick inner neomembranes were identified in 6 patients during craniotomy. No recurrence was reported in these patients after partial removal of the thickened inner neomembrane during craniotomy. Therefore, we speculate that patients indicated with mixed density hematoma may have thick inner neomembrane and organized hematoma. Furthermore, we believe that a thick inner neomembrane is an important factor contributing to the recurrence of CSDH. If cases with thin inner neomembrane of CSDH, the brain tissue expansion may occur and the residual liquid and gas from the craniotomy may be slowly absorbed, eventually leading to complete expansion of the brain tissue. On the contrary, a thick inner neomembrane of CSDH restricts the expansion of the brain tissue, increasing the probability of recurrence of CSDH. This observation may explain why the presence of residual liquid and gas did not affect the recurrence of CSDH in the present study, contrary to the results of other studies.33,34 Various types of surgery have been proposed for CSDH. The 3 most commonly used surgical techniques are the twist-drill craniostomy, burr hole craniostomy, and craniotomy.12 Burr hole craniostomy with closed drainage is presently the most popular surgical technique with a balanced risk and efficacy profiles.35-37 Reports indicate the postsurgical recurrence rate
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RISK FACTORS FOR RECURRENCE OF CSDH
Table 3. Factors Related to Recurrence of Chronic Subdural Hematoma: Univariate Analysis and Multivariable Analysis Number of Patients (%) Factor
No Recurrence
Recurrence
320
8
Total Sex Male
P Value, Uni and Bivariable Analysis
P Value, Multivariable Analysis
OR (95% CI), Multivariable Analysis
0.242
0.997
NA
273 (97.2%)
47 (100%)
Female
8 (2.8%)
0 (0%)
Age (years)
65.13 13.81
65.75 12.37
0.900
0.270
0.96 (0.896e1.031)
61 (19.1%)
0 (0%)
0.360
0.997
NA
72（22.5%）
2 (25%)
1.00
0.584
1.838 (0.207e16.290)
Bilateral hematoma Hypertension Diabetes
19 (5.9%)
0 (0%)
1.00
0.998
NA
Antiplatelet therapy
8 (2.5%)
1 (12.5%)
0.202
0.263
5.911 (0.264e132.494)
Anticoagulant therapy Traumatic history (days)
8 (2.5%)
0 (0%)
1.00
0.999
NA
30.55 37.11
27.38 31.88
0.811
0.774
0.996 (0.970e1.023)
0.317
0.891
NA
0.08
0.546
1.098 (0.811e1.485)
Markwalder grading scale 1
304 (95.0%)
7（87.5%）
2
13 (4.1%)
1（12.5%）
3
1 (0.3%)
0 (0%)
4
2（0.6%）
0 (0%)
4.67 3.35
7.88 3.78
Midline shift (mm) Cisterna ambiens compression*
178 (95.7%)
8 (100%)
0.011
0.995
NA
Isodensity hematoma
139 (43.4%)
1 (12.5%)
0.145
NA
NA
18 (6.6%)
0 (0%)
1.00
NA
NA
Low-density hematoma High-density hematoma
34 (10.6%)
0 (0%)
1.00
NA
NA
Mixed density hematoma*
129 (40.3%)
7 (87.5%)
0.01
0.024
17.845 (1.473e216.207)
Thickness of hematoma (mm)
18.09 6.80
22.13 9.28
0.101
0.084
1.135 (0.983e1.31)
7 (2.2%)
0 (0%)
1.00
0.999
NA
Thickness of postoperative gas (mm)
8.23 5.87
8.17 5.36
0.972
0.452
1.080 (0.884e1.319)
Thickness of postoperative liquid (mm)
5.13 3.53
4.17 2.33
0.347
0.320
0.854 (0.627e1.165)
Organized hematoma
OR, odds ratio; CI, confidence interval; NA, not available. *Significant difference.
of CSDH to be about 5% to 33%.13-15 However, the recurrence rate was only 2.4% at our center, which is lower than that reported by previous studies. In our center, the single burr hole craniostomy with the closed drainage is the main technique preferred for CSDH. Two reasons may explain the low recurrence rate of CSDH at our center: 1) the burr hole (approximately 1.2 cm) is always larger than the diameter of the drainage tube, and helps to efficiently evacuate the hematoma, especially large hematomas, from the subdural cavity; and 2) the subdural cavity is irrigated with normal saline solution until the irrigational saline solution appears colorless and free of other materials (blood clot and floccule).38 Some reports have presumed that patients with parietal or occipital drainage have a higher recurrence rate and considerably
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greater subdural accumulation of air than those with frontal drainage; moreover, subdural accumulation of air was associated with the recurrence of CSDH.39 However, the brain tissue may expand because of gradual absorption of gas after removal of the hematoma. Moreover, logistic regression analysis showed no difference between the volume of the accumulated air. At our center, as part of routine practice, the drainage tube is inserted deep into the hematoma cavity and the whole cavity is irrigated with normal saline solution. Large hematoma clots and floccules are washed out, especially in patients with mixed density hematoma. Insufficient irrigation may lead to the retention of residual hematoma clot and floccule and contribute to the formation of thick inner neomembrane and organized hematoma.
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Based on our experience, craniotomy is the optimal method used at our center to manage the recurrence of CSDH and to remove inner neomembranes. In this study, 8 patients experienced recurrence over the course of follow-up. The recurrent CSDH was managed by craniotomy in 6 patients. However, 2 patients with symptoms of recurrence refused to undergo craniotomy. We performed burr hole craniostomy in these 2 patients with the presumption that the inner neomembrane was not thick. Removal of the inner membrane of CSDH remains a controversial issue. Lee et al.40 reported on the futility of procedures aimed to decrease the recurrence rate of CSDH after membranectomy. Nevertheless, Kim et al.41 reported a decrease in the recurrence rate of CSDH after membranectomy. Moreover, a meta-analysis study reported that the mortality and postoperative complications after craniotomy with membrane resection were similar to those of burr hole drainage, however, with reduced recurrence rate.42 The surgical procedure was revised to craniotomy in 7 patients, and 6 patients with recurrent CSDH underwent
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 24 April 2019; accepted 14 August 2019 Citation: World Neurosurg. (2019) 132:e506-e513. https://doi.org/10.1016/j.wneu.2019.08.089 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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