- Email: [email protected]
Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence?
G Model
JINJ-5654; No. of Pages 5 Injury, Int. J. Care Injured xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Injury journal homepage: www.elsevier.com/locate/injury
Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Yu-Hua Huang a,d,*, Wei-Che Lin b, Cheng-Hsien Lu c, Wu-Fu Chen a a
Department of Neurosurgery, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan Department of Radiology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan c Department of Neurology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan d Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan b
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 16 February 2014
Background: Recurrence of chronic subdural haematoma (CSDH) is a significant issue in neurosurgical practice, and to distinguish individuals at high risk is important. In this study, we aim to clarify the relationship between quantitative haematoma volume and recurrence of CSDH. Methods: For this two-year retrospective study, 94 patients with CSDH were enrolled and all underwent burr-hole craniostomy with closed-system drainage. The volume of haematoma before surgery was quantitatively analysed by computed tomography (CT) of the brain. The patients were subdivided into 2 groups based on whether recurrence of CSDH was present or not. We investigated the intergroup differences in the volume of haematoma and other radiographic parameters. Results: Recurrence of CSDH was identified in 13 of 94 patients (14%). Univariable analysis of CT features revealed significant differences in the volume of haematoma, bilateral cerebral convexity, and layering of the haematoma. To adjust for the confounding effect, these 3 parameters were entered into multivariable logistic regression analysis. Ultimately, neither the volume of haematoma (p = 0.449) or bilateral cerebral convexity (p = 0.123) was relevant in this model. Only the presence of layering of the haematoma was independently associated with recurrence of CSDH (p = 0.009). Conclusion: The volume of CSDH is not related to recurrence in patients undergoing burr-hole craniostomy with closed-system drainage. Layering of the haematoma was the only independent risk factor on CT images for recurrence of CSDH in our series. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Chronic subdural haematoma Volume Burr hole Computed tomography Recurrence
Introduction Chronic subdural haematoma (CSDH) is a common form of intracranial haemorrhage that is often preceded by minor head trauma, resulting in a collection of subdural blood. Treatment for this condition is generally surgical evacuation, for which, burr-hole craniostomy with closed-system drainage is the most commonly used technique worldwide [1–3]. Improvement in the prognosis of CSDH can be achieved after surgery, and this surgical condition is considered to be a relatively benign entity of neurotrauma. However, a significant recurrence rate, ranging from 10% to 20%, is
* Corresponding author at: Department of Neurosurgery, Kaohsiung Chang Gung Memorial Hospital, 123, Ta Pei Road, Niao Sung District, Kaohsiung City, Taiwan. Tel.: +886 7 7317123x8011; fax: +886 7 7354309. E-mail address: [email protected] (Y.-H. Huang).
still reported [3–5]. Thus, the ability to distinguish individuals at risk of recurrence is important for informing further follow-up and management. Computed tomography (CT) of the brain, as the first choice of examination in patients with CSDH, provides essential diagnostic details with therapeutic implications. Several radiographic factors associated with recurrence of CSDH have been documented [5–7]. Quantitative analysis of intracranial haematoma volume can be accomplished using current imaging methods. This raises the issue of whether the volume of CSDH is relevant to recurrence following surgical drainage. In this study, we retrospectively collected the clinical and radiographic parameters of patients undergoing burr-hole evacuation with closed-system drainage for CSDH. Our goals were to characterise the relationship between volume of CSDH and recurrence, and also identify other CT factors that carry a potential risk of recurrence.
http://dx.doi.org/10.1016/j.injury.2014.02.023 0020–1383/ß 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
2
Materials and Methods
Statistical analysis
Data collection
Data were analysed using SPSS version 20.0 (IBM SPSS Statistics). Descriptive statistics were presented as frequencies (percentages) or as mean and standard deviation (SD). Categorical variables were compared using the chi-square test or Fisher’s exact test. Continuous variables were assessed using the Student’s t-test or Mann–Whitney U-test. Multivariable logistic regression was performed to adjust for independent risk factors of recurrence of CSDH, and the results were expressed as odds ratios with 95% confidence intervals. A p value of less than 0.05 was considered statistically significant.
This retrospective cohort study was carried out at Kaohsiung Chang Gung Memorial Hospital, a medical centre in Taiwan. After obtaining consent from the institutional review board, we reviewed the records of patients that had undergone burr-hole craniostomy with closed-system drainage for CSDH from January 2005 to December 2006. Inclusion criteria for CSDH were as follows: CT scan showed isodense to hypodense haematomas with respect to the adjacent brain; and when the haematoma was fluid identified at the time of surgery [8]. Ninety-four patients were enrolled for analysis. Trained research staff collected detailed clinical data, including the patients’ demographic information, underlying medical diseases, Glasgow Coma Score (GCS), and Markwalder Subdural Haematoma Grade [9]. CT studies and features The patients received a CT scan of the brain at admission. We measured the volumes of haematoma from the CT scans; all of these measurements were performed using the PACS imaging display software (Centricity RA1000, GE Healthcare, Taipei, Taiwan). The volume measurement was hand-traced by the radiologist on each axial image, and then these areas were added together and multiplied by the slice thickness. Other CT features that were evaluated included: the site of the haematoma (unilateral or bilateral cerebral convexity); midline shift identified as deviation of the septum pellucidum by more than 1 cm from the central position; layering of the haematoma, defined as containing 2 components of different densities with a clear boundary between them; and multiplicity of haematoma cavities, defined as a haematoma with inhomogeneous content and a high-density septum running between the inner and outer membranes [10]. Brain atrophy was classified into 3 stages: no or mild atrophy, definite atrophy such as dilated sulci, and severe atrophy such as widely dilated sulci and subdural space [11]. We also measured the Hounsfield units (HU) of the haematomas at the sites of highest density.
Results The 94 patients who underwent burr-hole craniostomy for CSDH included 79 (84%) males and 15 (16%) females. The mean age was 69.4 (SD 12.9) years (range, 29–93 years). Seventy (75%) patients had a history of head injury. With regard to underlying medical diseases 27 (29%) of the patients had diabetes mellitus, 47 (50%) had hypertension, 2 (2%), end stage renal disease, 8 (9%), coronary artery disease, 16 (17%), stroke, 7 (7%), dementia, and 14 (15%) patients had alcoholism. Twelve (13%) and 2 (2%) patients received antiplatelet and anticoagulant therapy, respectively. The presenting symptoms included 38 (40%) cases of headache, 23 (25%) of nausea or vomiting, 50 (53%) of haemiparesis, 45 (48%) of mental change, and 4 (4%) of seizure. At admission, neurological assessment before surgery showed 90 (96%) patients with a GCS of 9–15, 3 (3%) with a GCS of 6–8, and 1 (1%) with a GCS of 3–5. The number of patients with Markwalder Subdural Haematoma Grade 0, 1, 2, 3, and 4 was 5, 13, 71, 4, and 1, respectively. Fig. 1 shows the distribution of the volume of CSDH for the 94 patients. The mean volume of CSDH was 119.6 (SD 62.2) ml (range, 19.5–343.8 ml). The mean density of the haematoma was 35.2 (SD 11.3) HU (range, 11.0–57.0 HU). The individual CT scan characteristics included 24 (26%) bilateral CSDH, 39 (42%) midline shifts, 20 (21%) layering of the haematoma, and 35 (37%) multiplicity of haematoma cavities. The status of brain atrophy was no or mild, definite, and severe in 31 (33%), 42 (45%), and 21 (22%) patients, respectively. The feature-specific number and frequency of CT scans are summarised in Table 1.
Surgical techniques The surgical procedure was performed using 1 or 2 burr holes at each affected side of the CSDH for irrigation of the haematoma. All the patients underwent closed-system drainage. The drains were removed once drainage had stopped or the patients showed improvement in initial symptoms. Craniotomy was reserved for patients in whom the subdural haematoma was recurrent and the underlying membranes prevented adequate re-expansion of the brain. Recurrence of CSDH The patients were followed up at the outpatient department after discharge. The clinical and radiological criteria were integrated to evaluate CSDH recurrence. Reappearance of symptoms such as haemiparesis, headache, or change in consciousness indicated the accumulation of subdural haematoma. The radiological criteria consisted of an increase in the thickness of the haematoma and a change in the density of the haematoma on the treated side in follow-up CT scans within 3 months postoperatively [12]. Neurological outcome was assessed at the end of the follow-up period using the Glasgow Outcome Scale (GOS).
Fig. 1. Distribution of volume of chronic subdural haematoma.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
3
Table 1 Radiographic features of 94 patients with chronic subdural haematoma. Radiographic features
Volume of haematoma (ml) Density of haematoma (HU) Bilateral cerebral convexity Midline shift Layering of haematoma Multiplicity of haematoma cavities Brain atrophy No or mild Definite Severe
All cases
Recurrence
No recurrence
N = 94
N = 13
N = 81
119.6 (SD 62.2) 35.2 (SD 11.3) 24 (26%) 39 (42%) 20 (21%) 35 (37%)
157.5 (SD 90.4) 35.2 (SD 11.6) 7 (54%) 4 (31%) 7 (54%) 5 (39%)
113.6 (SD 54.7) 35.2 (SD 11.3) 17 (21%) 35 (43%) 13 (16%) 30 (37%)
31 (33%) 42 (45%) 21 (22%)
3 (23%) 7 (54%) 3 (23%)
28 (35%) 35 (43%) 18 (22%)
HU: Hounsfield unit.
The mean hospital stay was 13.4 (SD 13.1) days (range, 3–69 days). The patients were followed up at the clinics for a mean duration 10.5 (SD 10.0) months (range, 1–36 months). Two of the 94 patients with CSDH died from pneumonia complicated with respiratory failure, and 1 died due to non-Hodgkin lymphoma after discharge. The mean GOS at the end of follow-up was 4.6 (SD 0.9). The number of patients with GOS Grade 1, 2, 3, 4, and 5 was 3, 2, 1, 18, and 70, respectively. Within 3 months after the operation, recurrence of CSDH was found in 13 of the 94 patients, and the overall incidence was 14%. The baseline characteristics of the cases with or without recurrence of CSDH were compared, and there was no significant difference in any of the clinical variables as showed in Table 2. The univariable and multivariable logistic regression models for
radiographic variables that were probably risk factors for recurrence of CSDH were given in Table 3. Univariable analysis identified the following significant parameters: volume of the haematoma, bilateral cerebral convexity, and layering of the haematoma. To adjust for the confounding effect, these 3 parameters were entered into multivariable analysis. The result showed that volume of haematoma (odds ratio, 95% confidence interval = 1.004, 0.99–1.02; p = 0.449) and bilateral cerebral convexity (odds ratio, 95% confidence interval = 3.43, 0.72– 16.43; p = 0.123) were not significantly relevant in this model. Only the presence of layering of the haematoma was independently associated with recurrence of CSDH after burr-hole craniostomy with closed-system drainage (odds ratio, 95% confidence interval = 5.93, 1.55–22.61; p = 0.009).
Table 2 Comparisons of clinical characteristics of patients with or without recurrence of chronic subdural haematoma.
Mean age (year) Gender Male Female Head injury history Underlying medical condition Diabetes mellitus Hypertension End-stage renal disease Coronary arterial disease Stroke Dementia Alcoholism Antiplatelet therapy Anticoagulant therapy Presenting symptom/sign Headache Nausea or vomiting Haemiparesis Mental change Seizure GCS score at admission 9–15 6–8 3–5 Markwalder SDH Grade 0 1 2 3 4 Mean hospital stay (day) Mean GOS at the end of follow-up Mortality at the end of follow-up
Recurrence
No recurrence
N = 13
N = 81
68.5 (SD 12.6)
69.6 (SD 13.0)
11 (85%) 2 (15%) 7 (54%)
68 (84%) 13 (26%) 63 (78%)
0.088
p value
0.774 1.000
3 4 1 1 3 0 3 2 0
(23%) (31%) (8%) (8%) (23%) (0%) (23%) (15%) (0%)
24 43 1 7 13 7 11 10 2
(30%) (53%) (1%) (9%) (16%) (9%) (14%) (12%) (3%)
0.751 0.135 0.518 1.000 0.690 0.588 0.403 0.670 1.000
5 2 7 8 2
(39%) (15%) (54%) (62%) (15%)
33 21 43 37 2
(41%) (26%) (53%) (46%) (3%)
0.876 0.510 0.959 0.288 0.182 0.566
12 (92%) 1 (8%) 0 (0%)
78 (96%) 2 (3%) 1 (1%)
0 (0%) 1 (8%) 11 (85%) 1 (8%) 0 (0%) 15.5 (SD 15.0) 4.8 (SD 0.4) 0 (0%)
5 (6%) 12 (15%) 60 (74%) 3 (4%) 1 (1%) 13.0 (SD 12.9) 4.6 (SD 0.9) 3 (4%)
0.744
0.522 0.328 1.000
GCS: Glasgow Coma Scale; SDH: subdural haematoma; GOS: Glasgow Outcome Scale.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
4
Table 3 Univariable and multivariable analysis of potential risk factors on images for recurrence of chronic subdural haematoma. Multivariate
Univariate
Volume of haematoma Bilateral cerebral convexity Midline shift Layering of haematoma Density of haematoma (HU) Multiplicity of haematoma cavities Brain atrophy No or mild Definite Severe
Odds ratio (95% CI)
p value
Odds ratio (95% CI)
p value
1.01 4.39 0.58 6.10 1.00 1.06
0.025 0.017 0.402 0.004 0.999 0.921
1.004 (0.99–1.02) 3.43 (0.72–16.43)
0.449 0.123
5.93 (1.55–22.61)
0.009
(1.001–1.02) (1.30–14.80) (0.17–2.05) (1.76–21.12) (0.95–1.05) (0.32–3.55)
Reference 1.87 (0.44–7.89) 1.56 (0.28–8.57)
– 0.396 0.612
HU: Hounsfield unit.
Discussion Burr hole craniostomy for CSDH has the best cure-tocomplication ratio, and the use of post-operative closed-system drainage reduces the risk of recurrence without additional risk of morbidity [4]. Despite the wide acceptance of these optimum methods for treating CSDH, the incidence of recurrence remains significantly high. In the randomised controlled trial conducted by Santarius et al., 10 of 108 (9%) patients had recurrence following burr-hole drainage for CSDH [3]. Torihashi et al. reviewed 343 consecutive surgical cases and reported that 61 (18%) patients experienced recurrence of CSDH [6]. The rate of recurrence was even up to 22% in a series of 420 CSDH cases [5]. In this study, the incidence of recurrent CSDH was 14%, which is close to the percentage reported in previous studies. Recurrence is always a focus of CSDH research, and an increased understanding of the risks offers an opportunity to improve the therapeutic results. Numerous clinical risk factors for CSDH, such as anticoagulant therapy, DM, preoperative seizure, surgical techniques, postoperative posture, presence of intracranial air, and inflammatory cytokines, have been documented [4,5,13–15]. CT scan of the brain is the major study used with CSDH, and can provide objective information for clinicians. Thus, CT features associated with recurrence of CSDH are extensively discussed in the literature [5–7,12]. Some risk factors seen on CT imaging, including bilateral site of haematoma, width of haematoma, and preoperative midline displacement, raise concerns, because all of these risk factors seem to be closely related to haematoma volume. However, the use of volumetric analysis of CSDH is not generally reported, and the direct relationship between quantitative haematoma volume and recurrence following surgical drainage is uncertain so far. In this series, more than half of the patients had a CSDH volume of more than 100 ml. Since CSDH develops over a period, haematoma fluid is buffered by the cranial reserve capacity without a detrimental rise in intracranial pressure [16]. CSDH may induce neurological dysfunction primarily through mechanical distortion of the central brain regions, with an influence on the remote regions owing to transneural depression [17]. Patients with voluminous haematoma theoretically tend to have previous brain atrophy, which leads to poor brain expansion after surgery and creates the potential for reaccumulation of the haematoma [18]. However, our data show that the volume of the haematoma is not an independent parameter for recurrence of CSDH. One explanation is that a considerable amount of the haematoma occupies more intracranial volume in patients with bilateral CSDH, which is one of the recurrent factors in the literature [6,19]. Therefore, both the volume of the haematoma and the bilateral sites of CSDH are confounded by each other in the multivariate model. Kung et al. have quantitatively analysed the brain re-expansion rate after evacuation of CSDH, and provide evidence for a lower rate in
bilateral than in unilateral haematoma [18]. This, in conjunction with our results, reveals that the impairment of postoperative brain expansion may be more directly responsible for recurrence of CSDH than pre-operative haematoma volume. The layering of the haematoma on CT scans is the only independent risk factor for recurrence of CSDH in our study. In the investigation conducted by Kao et al., it was hypothesised that the sedimentation level (or layering) occurred as a result of rebleeding into a CSDH that was sufficiently old to result in its contents being homogenous prior to the rebleed [20]. In addition, a sufficient period of bed confinement in the brow-up position before CT examination allows the development of gravitational sedimentation in the haematoma. Some authors classify the internal architecture of CSDH, and report the incidence of recurrence is significantly high in the separated type of haematoma (synonymous with layering of the haematoma) [5,12], which is compatible with the result in this series. As a result, we suggest regular CT scanning after evacuation of CSDH is crucial for early detection of recurrence in patients with layering of the haematoma. This study has several potential limitations. It was a retrospective review of preexisting data and suffers from the inherent limitations of such studies. Data collection through chart and imaging reviews is less complete and accurate than is planned research. Variations in the assessment of clinical status may account for the observed differences in results. The period of evaluation of recurrent symptoms or signs varies, and follow-up information is difficult to obtain without scheduled returns to the clinic. From a statistical standpoint, the number of patients was still relatively small, and the study may be underpowered to detect the significance of some risk factors. In addition, the findings in this study reflect the experience of a single medical centre; hence, the results cannot be representative of patients in other institutes. Even with these issues in the preliminary analysis, we consider that these data provide valuable information to clarify the relationship between CT factors and recurrence and to identify the patients that require follow-up on their condition. Conclusions The volume of the CSDH is not related to recurrence in patients undergoing burr-hole craniostomy with closed-system drainage. Layering of the haematoma was the only independent risk factor on CT images for recurrence of CSDH in our series. Conflict of interest statement The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
Ethics statement The work has been approved by the ethical committees related to Kaohsiung Chang Gung Memorial Hospital in which it was performed and that subjects gave informed consent to the work. References [1] 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;99:44–6. [2] Santarius T, Lawton R, Kirkpatrick PJ, Hutchinson PJ. The management of primary chronic subdural haematoma: a questionnaire survey of practice in the United Kingdom and the Republic of Ireland. Br J Neurosurg 2008;22: 529–34. [3] Santarius T, Kirkpatrick PJ, Ganesan D, Chia HL, Jalloh I, Smielewski P, et al. Use of drains versus no drains after burr-hole evacuation of chronic subdural haematoma: a randomised controlled trial. Lancet 2009;374:1067–73. [4] Weigel R, Schmiedek P, Krauss JK. Outcome of contemporary surgery for chronic subdural haematoma: evidence based review. J Neurol Neurosurg Psychiatry 2003;74:937–43. [5] Chon KH, Lee JM, Koh EJ, Choi HY. Independent predictors for recurrence of chronic subdural hematoma. Acta Neurochir (Wien) 2012;154:1541–8. [6] Torihashi K, Sadamasa N, Yoshida K, Narumi O, Chin M, Yamagata S. Independent predictors for recurrence of chronic subdural hematoma: a review of 343 consecutive surgical cases. Neurosurgery 2008;63:1125–9. discussion 1129. [7] Yamamoto H, Hirashima Y, Hamada H, Hayashi N, Origasa H, Endo S. Independent predictors of recurrence of chronic subdural hematoma: results of multivariate analysis performed using a logistic regression model. J Neurosurg 2003;98:1217–21. [8] Scotti G, Terbrugge K, Melancon D, Belanger G. Evaluation of the age of subdural hematomas by computerized tomography. J Neurosurg 1977;47: 311–5.
5
[9] Markwalder TM, Steinsiepe KF, Rohner M, Reichenbach W, Markwalder H. The course of chronic subdural hematomas after burr-hole craniostomy and closed-system drainage. J Neurosurg 1981;55:390–6. [10] Amirjamshidi A, Eftekhar B, Abouzari M, Rashidi A. The relationship between Glasgow coma/outcome scores and abnormal CT scan findings in chronic subdural hematoma. Clin Neurol Neurosurg 2007;109:152–7. [11] Oishi M, Toyama M, Tamatani S, Kitazawa T, Saito M. Clinical factors of recurrent chronic subdural hematoma. Neurol Med Chir (Tokyo) 2001;41:382–6. [12] Nakaguchi H, Tanishima T, Yoshimasu N. Factors in the natural history of chronic subdural hematomas that influence their postoperative recurrence. J Neurosurg 2001;95:256–62. [13] Abouzari M, Rashidi A, Rezaii J, Esfandiari K, Asadollahi M, Aleali H, et al. The role of postoperative patient posture in the recurrence of traumatic chronic subdural hematoma after burr-hole surgery. Neurosurgery 2007;61:794–7. discussion 797. [14] Amirjamshidi A, Abouzari M, Eftekhar B, Rashidi A, Rezaii J, Esfandiari K, et al. Outcomes and recurrence rates in chronic subdural haematoma. Br J Neurosurg 2007;21:272–5. [15] Frati A, Salvati M, Mainiero F, Ippoliti F, Rocchi G, Raco A, et al. Inflammation markers and risk factors for recurrence in 35 patients with a posttraumatic chronic subdural hematoma: a prospective study. J Neurosurg 2004;100: 24–32. [16] Kawakami Y, Chikama M, Tamiya T, Shimamura Y. Coagulation and fibrinolysis in chronic subdural hematoma. Neurosurgery 1989;25:25–9. [17] Tanaka A, Nakayama Y, Yoshinaga S. Cerebral blood flow and intracranial pressure in chronic subdural hematomas. Surg Neurol 1997;47:346–51. [18] Kung WM, Hung KS, Chiu WT, Tsai SH, Lin JW, Wang YC, et al. Quantitative assessment of impaired postevacuation brain re-expansion in bilateral chronic subdural haematoma: possible mechanism of the higher recurrence rate. Injury 2012;43:598–602. [19] Huang YH, Yang KY, Lee TC, Liao CC. Bilateral chronic subdural hematoma: what is the clinical significance? Int J Surg 2013;11:544–8. [20] Kao MC. Sedimentation level in chronic subdural hematoma visible on computerized tomography. J Neurosurg 1983;58:246–51.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
JINJ-5654; No. of Pages 5 Injury, Int. J. Care Injured xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Injury journal homepage: www.elsevier.com/locate/injury
Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Yu-Hua Huang a,d,*, Wei-Che Lin b, Cheng-Hsien Lu c, Wu-Fu Chen a a
Department of Neurosurgery, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan Department of Radiology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan c Department of Neurology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan d Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan b
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 16 February 2014
Background: Recurrence of chronic subdural haematoma (CSDH) is a significant issue in neurosurgical practice, and to distinguish individuals at high risk is important. In this study, we aim to clarify the relationship between quantitative haematoma volume and recurrence of CSDH. Methods: For this two-year retrospective study, 94 patients with CSDH were enrolled and all underwent burr-hole craniostomy with closed-system drainage. The volume of haematoma before surgery was quantitatively analysed by computed tomography (CT) of the brain. The patients were subdivided into 2 groups based on whether recurrence of CSDH was present or not. We investigated the intergroup differences in the volume of haematoma and other radiographic parameters. Results: Recurrence of CSDH was identified in 13 of 94 patients (14%). Univariable analysis of CT features revealed significant differences in the volume of haematoma, bilateral cerebral convexity, and layering of the haematoma. To adjust for the confounding effect, these 3 parameters were entered into multivariable logistic regression analysis. Ultimately, neither the volume of haematoma (p = 0.449) or bilateral cerebral convexity (p = 0.123) was relevant in this model. Only the presence of layering of the haematoma was independently associated with recurrence of CSDH (p = 0.009). Conclusion: The volume of CSDH is not related to recurrence in patients undergoing burr-hole craniostomy with closed-system drainage. Layering of the haematoma was the only independent risk factor on CT images for recurrence of CSDH in our series. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Chronic subdural haematoma Volume Burr hole Computed tomography Recurrence
Introduction Chronic subdural haematoma (CSDH) is a common form of intracranial haemorrhage that is often preceded by minor head trauma, resulting in a collection of subdural blood. Treatment for this condition is generally surgical evacuation, for which, burr-hole craniostomy with closed-system drainage is the most commonly used technique worldwide [1–3]. Improvement in the prognosis of CSDH can be achieved after surgery, and this surgical condition is considered to be a relatively benign entity of neurotrauma. However, a significant recurrence rate, ranging from 10% to 20%, is
* Corresponding author at: Department of Neurosurgery, Kaohsiung Chang Gung Memorial Hospital, 123, Ta Pei Road, Niao Sung District, Kaohsiung City, Taiwan. Tel.: +886 7 7317123x8011; fax: +886 7 7354309. E-mail address: [email protected] (Y.-H. Huang).
still reported [3–5]. Thus, the ability to distinguish individuals at risk of recurrence is important for informing further follow-up and management. Computed tomography (CT) of the brain, as the first choice of examination in patients with CSDH, provides essential diagnostic details with therapeutic implications. Several radiographic factors associated with recurrence of CSDH have been documented [5–7]. Quantitative analysis of intracranial haematoma volume can be accomplished using current imaging methods. This raises the issue of whether the volume of CSDH is relevant to recurrence following surgical drainage. In this study, we retrospectively collected the clinical and radiographic parameters of patients undergoing burr-hole evacuation with closed-system drainage for CSDH. Our goals were to characterise the relationship between volume of CSDH and recurrence, and also identify other CT factors that carry a potential risk of recurrence.
http://dx.doi.org/10.1016/j.injury.2014.02.023 0020–1383/ß 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
2
Materials and Methods
Statistical analysis
Data collection
Data were analysed using SPSS version 20.0 (IBM SPSS Statistics). Descriptive statistics were presented as frequencies (percentages) or as mean and standard deviation (SD). Categorical variables were compared using the chi-square test or Fisher’s exact test. Continuous variables were assessed using the Student’s t-test or Mann–Whitney U-test. Multivariable logistic regression was performed to adjust for independent risk factors of recurrence of CSDH, and the results were expressed as odds ratios with 95% confidence intervals. A p value of less than 0.05 was considered statistically significant.
This retrospective cohort study was carried out at Kaohsiung Chang Gung Memorial Hospital, a medical centre in Taiwan. After obtaining consent from the institutional review board, we reviewed the records of patients that had undergone burr-hole craniostomy with closed-system drainage for CSDH from January 2005 to December 2006. Inclusion criteria for CSDH were as follows: CT scan showed isodense to hypodense haematomas with respect to the adjacent brain; and when the haematoma was fluid identified at the time of surgery [8]. Ninety-four patients were enrolled for analysis. Trained research staff collected detailed clinical data, including the patients’ demographic information, underlying medical diseases, Glasgow Coma Score (GCS), and Markwalder Subdural Haematoma Grade [9]. CT studies and features The patients received a CT scan of the brain at admission. We measured the volumes of haematoma from the CT scans; all of these measurements were performed using the PACS imaging display software (Centricity RA1000, GE Healthcare, Taipei, Taiwan). The volume measurement was hand-traced by the radiologist on each axial image, and then these areas were added together and multiplied by the slice thickness. Other CT features that were evaluated included: the site of the haematoma (unilateral or bilateral cerebral convexity); midline shift identified as deviation of the septum pellucidum by more than 1 cm from the central position; layering of the haematoma, defined as containing 2 components of different densities with a clear boundary between them; and multiplicity of haematoma cavities, defined as a haematoma with inhomogeneous content and a high-density septum running between the inner and outer membranes [10]. Brain atrophy was classified into 3 stages: no or mild atrophy, definite atrophy such as dilated sulci, and severe atrophy such as widely dilated sulci and subdural space [11]. We also measured the Hounsfield units (HU) of the haematomas at the sites of highest density.
Results The 94 patients who underwent burr-hole craniostomy for CSDH included 79 (84%) males and 15 (16%) females. The mean age was 69.4 (SD 12.9) years (range, 29–93 years). Seventy (75%) patients had a history of head injury. With regard to underlying medical diseases 27 (29%) of the patients had diabetes mellitus, 47 (50%) had hypertension, 2 (2%), end stage renal disease, 8 (9%), coronary artery disease, 16 (17%), stroke, 7 (7%), dementia, and 14 (15%) patients had alcoholism. Twelve (13%) and 2 (2%) patients received antiplatelet and anticoagulant therapy, respectively. The presenting symptoms included 38 (40%) cases of headache, 23 (25%) of nausea or vomiting, 50 (53%) of haemiparesis, 45 (48%) of mental change, and 4 (4%) of seizure. At admission, neurological assessment before surgery showed 90 (96%) patients with a GCS of 9–15, 3 (3%) with a GCS of 6–8, and 1 (1%) with a GCS of 3–5. The number of patients with Markwalder Subdural Haematoma Grade 0, 1, 2, 3, and 4 was 5, 13, 71, 4, and 1, respectively. Fig. 1 shows the distribution of the volume of CSDH for the 94 patients. The mean volume of CSDH was 119.6 (SD 62.2) ml (range, 19.5–343.8 ml). The mean density of the haematoma was 35.2 (SD 11.3) HU (range, 11.0–57.0 HU). The individual CT scan characteristics included 24 (26%) bilateral CSDH, 39 (42%) midline shifts, 20 (21%) layering of the haematoma, and 35 (37%) multiplicity of haematoma cavities. The status of brain atrophy was no or mild, definite, and severe in 31 (33%), 42 (45%), and 21 (22%) patients, respectively. The feature-specific number and frequency of CT scans are summarised in Table 1.
Surgical techniques The surgical procedure was performed using 1 or 2 burr holes at each affected side of the CSDH for irrigation of the haematoma. All the patients underwent closed-system drainage. The drains were removed once drainage had stopped or the patients showed improvement in initial symptoms. Craniotomy was reserved for patients in whom the subdural haematoma was recurrent and the underlying membranes prevented adequate re-expansion of the brain. Recurrence of CSDH The patients were followed up at the outpatient department after discharge. The clinical and radiological criteria were integrated to evaluate CSDH recurrence. Reappearance of symptoms such as haemiparesis, headache, or change in consciousness indicated the accumulation of subdural haematoma. The radiological criteria consisted of an increase in the thickness of the haematoma and a change in the density of the haematoma on the treated side in follow-up CT scans within 3 months postoperatively [12]. Neurological outcome was assessed at the end of the follow-up period using the Glasgow Outcome Scale (GOS).
Fig. 1. Distribution of volume of chronic subdural haematoma.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
3
Table 1 Radiographic features of 94 patients with chronic subdural haematoma. Radiographic features
Volume of haematoma (ml) Density of haematoma (HU) Bilateral cerebral convexity Midline shift Layering of haematoma Multiplicity of haematoma cavities Brain atrophy No or mild Definite Severe
All cases
Recurrence
No recurrence
N = 94
N = 13
N = 81
119.6 (SD 62.2) 35.2 (SD 11.3) 24 (26%) 39 (42%) 20 (21%) 35 (37%)
157.5 (SD 90.4) 35.2 (SD 11.6) 7 (54%) 4 (31%) 7 (54%) 5 (39%)
113.6 (SD 54.7) 35.2 (SD 11.3) 17 (21%) 35 (43%) 13 (16%) 30 (37%)
31 (33%) 42 (45%) 21 (22%)
3 (23%) 7 (54%) 3 (23%)
28 (35%) 35 (43%) 18 (22%)
HU: Hounsfield unit.
The mean hospital stay was 13.4 (SD 13.1) days (range, 3–69 days). The patients were followed up at the clinics for a mean duration 10.5 (SD 10.0) months (range, 1–36 months). Two of the 94 patients with CSDH died from pneumonia complicated with respiratory failure, and 1 died due to non-Hodgkin lymphoma after discharge. The mean GOS at the end of follow-up was 4.6 (SD 0.9). The number of patients with GOS Grade 1, 2, 3, 4, and 5 was 3, 2, 1, 18, and 70, respectively. Within 3 months after the operation, recurrence of CSDH was found in 13 of the 94 patients, and the overall incidence was 14%. The baseline characteristics of the cases with or without recurrence of CSDH were compared, and there was no significant difference in any of the clinical variables as showed in Table 2. The univariable and multivariable logistic regression models for
radiographic variables that were probably risk factors for recurrence of CSDH were given in Table 3. Univariable analysis identified the following significant parameters: volume of the haematoma, bilateral cerebral convexity, and layering of the haematoma. To adjust for the confounding effect, these 3 parameters were entered into multivariable analysis. The result showed that volume of haematoma (odds ratio, 95% confidence interval = 1.004, 0.99–1.02; p = 0.449) and bilateral cerebral convexity (odds ratio, 95% confidence interval = 3.43, 0.72– 16.43; p = 0.123) were not significantly relevant in this model. Only the presence of layering of the haematoma was independently associated with recurrence of CSDH after burr-hole craniostomy with closed-system drainage (odds ratio, 95% confidence interval = 5.93, 1.55–22.61; p = 0.009).
Table 2 Comparisons of clinical characteristics of patients with or without recurrence of chronic subdural haematoma.
Mean age (year) Gender Male Female Head injury history Underlying medical condition Diabetes mellitus Hypertension End-stage renal disease Coronary arterial disease Stroke Dementia Alcoholism Antiplatelet therapy Anticoagulant therapy Presenting symptom/sign Headache Nausea or vomiting Haemiparesis Mental change Seizure GCS score at admission 9–15 6–8 3–5 Markwalder SDH Grade 0 1 2 3 4 Mean hospital stay (day) Mean GOS at the end of follow-up Mortality at the end of follow-up
Recurrence
No recurrence
N = 13
N = 81
68.5 (SD 12.6)
69.6 (SD 13.0)
11 (85%) 2 (15%) 7 (54%)
68 (84%) 13 (26%) 63 (78%)
0.088
p value
0.774 1.000
3 4 1 1 3 0 3 2 0
(23%) (31%) (8%) (8%) (23%) (0%) (23%) (15%) (0%)
24 43 1 7 13 7 11 10 2
(30%) (53%) (1%) (9%) (16%) (9%) (14%) (12%) (3%)
0.751 0.135 0.518 1.000 0.690 0.588 0.403 0.670 1.000
5 2 7 8 2
(39%) (15%) (54%) (62%) (15%)
33 21 43 37 2
(41%) (26%) (53%) (46%) (3%)
0.876 0.510 0.959 0.288 0.182 0.566
12 (92%) 1 (8%) 0 (0%)
78 (96%) 2 (3%) 1 (1%)
0 (0%) 1 (8%) 11 (85%) 1 (8%) 0 (0%) 15.5 (SD 15.0) 4.8 (SD 0.4) 0 (0%)
5 (6%) 12 (15%) 60 (74%) 3 (4%) 1 (1%) 13.0 (SD 12.9) 4.6 (SD 0.9) 3 (4%)
0.744
0.522 0.328 1.000
GCS: Glasgow Coma Scale; SDH: subdural haematoma; GOS: Glasgow Outcome Scale.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
4
Table 3 Univariable and multivariable analysis of potential risk factors on images for recurrence of chronic subdural haematoma. Multivariate
Univariate
Volume of haematoma Bilateral cerebral convexity Midline shift Layering of haematoma Density of haematoma (HU) Multiplicity of haematoma cavities Brain atrophy No or mild Definite Severe
Odds ratio (95% CI)
p value
Odds ratio (95% CI)
p value
1.01 4.39 0.58 6.10 1.00 1.06
0.025 0.017 0.402 0.004 0.999 0.921
1.004 (0.99–1.02) 3.43 (0.72–16.43)
0.449 0.123
5.93 (1.55–22.61)
0.009
(1.001–1.02) (1.30–14.80) (0.17–2.05) (1.76–21.12) (0.95–1.05) (0.32–3.55)
Reference 1.87 (0.44–7.89) 1.56 (0.28–8.57)
– 0.396 0.612
HU: Hounsfield unit.
Discussion Burr hole craniostomy for CSDH has the best cure-tocomplication ratio, and the use of post-operative closed-system drainage reduces the risk of recurrence without additional risk of morbidity [4]. Despite the wide acceptance of these optimum methods for treating CSDH, the incidence of recurrence remains significantly high. In the randomised controlled trial conducted by Santarius et al., 10 of 108 (9%) patients had recurrence following burr-hole drainage for CSDH [3]. Torihashi et al. reviewed 343 consecutive surgical cases and reported that 61 (18%) patients experienced recurrence of CSDH [6]. The rate of recurrence was even up to 22% in a series of 420 CSDH cases [5]. In this study, the incidence of recurrent CSDH was 14%, which is close to the percentage reported in previous studies. Recurrence is always a focus of CSDH research, and an increased understanding of the risks offers an opportunity to improve the therapeutic results. Numerous clinical risk factors for CSDH, such as anticoagulant therapy, DM, preoperative seizure, surgical techniques, postoperative posture, presence of intracranial air, and inflammatory cytokines, have been documented [4,5,13–15]. CT scan of the brain is the major study used with CSDH, and can provide objective information for clinicians. Thus, CT features associated with recurrence of CSDH are extensively discussed in the literature [5–7,12]. Some risk factors seen on CT imaging, including bilateral site of haematoma, width of haematoma, and preoperative midline displacement, raise concerns, because all of these risk factors seem to be closely related to haematoma volume. However, the use of volumetric analysis of CSDH is not generally reported, and the direct relationship between quantitative haematoma volume and recurrence following surgical drainage is uncertain so far. In this series, more than half of the patients had a CSDH volume of more than 100 ml. Since CSDH develops over a period, haematoma fluid is buffered by the cranial reserve capacity without a detrimental rise in intracranial pressure [16]. CSDH may induce neurological dysfunction primarily through mechanical distortion of the central brain regions, with an influence on the remote regions owing to transneural depression [17]. Patients with voluminous haematoma theoretically tend to have previous brain atrophy, which leads to poor brain expansion after surgery and creates the potential for reaccumulation of the haematoma [18]. However, our data show that the volume of the haematoma is not an independent parameter for recurrence of CSDH. One explanation is that a considerable amount of the haematoma occupies more intracranial volume in patients with bilateral CSDH, which is one of the recurrent factors in the literature [6,19]. Therefore, both the volume of the haematoma and the bilateral sites of CSDH are confounded by each other in the multivariate model. Kung et al. have quantitatively analysed the brain re-expansion rate after evacuation of CSDH, and provide evidence for a lower rate in
bilateral than in unilateral haematoma [18]. This, in conjunction with our results, reveals that the impairment of postoperative brain expansion may be more directly responsible for recurrence of CSDH than pre-operative haematoma volume. The layering of the haematoma on CT scans is the only independent risk factor for recurrence of CSDH in our study. In the investigation conducted by Kao et al., it was hypothesised that the sedimentation level (or layering) occurred as a result of rebleeding into a CSDH that was sufficiently old to result in its contents being homogenous prior to the rebleed [20]. In addition, a sufficient period of bed confinement in the brow-up position before CT examination allows the development of gravitational sedimentation in the haematoma. Some authors classify the internal architecture of CSDH, and report the incidence of recurrence is significantly high in the separated type of haematoma (synonymous with layering of the haematoma) [5,12], which is compatible with the result in this series. As a result, we suggest regular CT scanning after evacuation of CSDH is crucial for early detection of recurrence in patients with layering of the haematoma. This study has several potential limitations. It was a retrospective review of preexisting data and suffers from the inherent limitations of such studies. Data collection through chart and imaging reviews is less complete and accurate than is planned research. Variations in the assessment of clinical status may account for the observed differences in results. The period of evaluation of recurrent symptoms or signs varies, and follow-up information is difficult to obtain without scheduled returns to the clinic. From a statistical standpoint, the number of patients was still relatively small, and the study may be underpowered to detect the significance of some risk factors. In addition, the findings in this study reflect the experience of a single medical centre; hence, the results cannot be representative of patients in other institutes. Even with these issues in the preliminary analysis, we consider that these data provide valuable information to clarify the relationship between CT factors and recurrence and to identify the patients that require follow-up on their condition. Conclusions The volume of the CSDH is not related to recurrence in patients undergoing burr-hole craniostomy with closed-system drainage. Layering of the haematoma was the only independent risk factor on CT images for recurrence of CSDH in our series. Conflict of interest statement The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023
G Model
JINJ-5654; No. of Pages 5 Y.-H. Huang et al. / Injury, Int. J. Care Injured xxx (2014) xxx–xxx
Ethics statement The work has been approved by the ethical committees related to Kaohsiung Chang Gung Memorial Hospital in which it was performed and that subjects gave informed consent to the work. References [1] 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;99:44–6. [2] Santarius T, Lawton R, Kirkpatrick PJ, Hutchinson PJ. The management of primary chronic subdural haematoma: a questionnaire survey of practice in the United Kingdom and the Republic of Ireland. Br J Neurosurg 2008;22: 529–34. [3] Santarius T, Kirkpatrick PJ, Ganesan D, Chia HL, Jalloh I, Smielewski P, et al. Use of drains versus no drains after burr-hole evacuation of chronic subdural haematoma: a randomised controlled trial. Lancet 2009;374:1067–73. [4] Weigel R, Schmiedek P, Krauss JK. Outcome of contemporary surgery for chronic subdural haematoma: evidence based review. J Neurol Neurosurg Psychiatry 2003;74:937–43. [5] Chon KH, Lee JM, Koh EJ, Choi HY. Independent predictors for recurrence of chronic subdural hematoma. Acta Neurochir (Wien) 2012;154:1541–8. [6] Torihashi K, Sadamasa N, Yoshida K, Narumi O, Chin M, Yamagata S. Independent predictors for recurrence of chronic subdural hematoma: a review of 343 consecutive surgical cases. Neurosurgery 2008;63:1125–9. discussion 1129. [7] Yamamoto H, Hirashima Y, Hamada H, Hayashi N, Origasa H, Endo S. Independent predictors of recurrence of chronic subdural hematoma: results of multivariate analysis performed using a logistic regression model. J Neurosurg 2003;98:1217–21. [8] Scotti G, Terbrugge K, Melancon D, Belanger G. Evaluation of the age of subdural hematomas by computerized tomography. J Neurosurg 1977;47: 311–5.
5
[9] Markwalder TM, Steinsiepe KF, Rohner M, Reichenbach W, Markwalder H. The course of chronic subdural hematomas after burr-hole craniostomy and closed-system drainage. J Neurosurg 1981;55:390–6. [10] Amirjamshidi A, Eftekhar B, Abouzari M, Rashidi A. The relationship between Glasgow coma/outcome scores and abnormal CT scan findings in chronic subdural hematoma. Clin Neurol Neurosurg 2007;109:152–7. [11] Oishi M, Toyama M, Tamatani S, Kitazawa T, Saito M. Clinical factors of recurrent chronic subdural hematoma. Neurol Med Chir (Tokyo) 2001;41:382–6. [12] Nakaguchi H, Tanishima T, Yoshimasu N. Factors in the natural history of chronic subdural hematomas that influence their postoperative recurrence. J Neurosurg 2001;95:256–62. [13] Abouzari M, Rashidi A, Rezaii J, Esfandiari K, Asadollahi M, Aleali H, et al. The role of postoperative patient posture in the recurrence of traumatic chronic subdural hematoma after burr-hole surgery. Neurosurgery 2007;61:794–7. discussion 797. [14] Amirjamshidi A, Abouzari M, Eftekhar B, Rashidi A, Rezaii J, Esfandiari K, et al. Outcomes and recurrence rates in chronic subdural haematoma. Br J Neurosurg 2007;21:272–5. [15] Frati A, Salvati M, Mainiero F, Ippoliti F, Rocchi G, Raco A, et al. Inflammation markers and risk factors for recurrence in 35 patients with a posttraumatic chronic subdural hematoma: a prospective study. J Neurosurg 2004;100: 24–32. [16] Kawakami Y, Chikama M, Tamiya T, Shimamura Y. Coagulation and fibrinolysis in chronic subdural hematoma. Neurosurgery 1989;25:25–9. [17] Tanaka A, Nakayama Y, Yoshinaga S. Cerebral blood flow and intracranial pressure in chronic subdural hematomas. Surg Neurol 1997;47:346–51. [18] Kung WM, Hung KS, Chiu WT, Tsai SH, Lin JW, Wang YC, et al. Quantitative assessment of impaired postevacuation brain re-expansion in bilateral chronic subdural haematoma: possible mechanism of the higher recurrence rate. Injury 2012;43:598–602. [19] Huang YH, Yang KY, Lee TC, Liao CC. Bilateral chronic subdural hematoma: what is the clinical significance? Int J Surg 2013;11:544–8. [20] Kao MC. Sedimentation level in chronic subdural hematoma visible on computerized tomography. J Neurosurg 1983;58:246–51.
Please cite this article in press as: Huang Y-H, et al. Volume of chronic subdural haematoma: Is it one of the radiographic factors related to recurrence? Injury (2014), http://dx.doi.org/10.1016/j.injury.2014.02.023