Formosan Journal of Surgery

: 2018  |  Volume : 51  |  Issue : 6  |  Page : 228--233

Statistical relevance of mean hematoma density and it's internal architecture: Potential clinical application in chronic subdural hematomas

Tzu-Yung Chen1, Sue-Ting Chang2, Muh-Shi Lin3,  
1 Department of Surgery, Division of Neurosurgery, Kuang Tien General Hospital; Department of Nursing, College of Nursing, Hung Kuang University, Taichung, Taiwan
2 Department of Technology Application and Human Resource Development, National Taiwan Normal University, Taipei; Department of Administration, Kuang-Tien General Hospital, Taichung, Taiwan
3 Department of Surgery, Division of Neurosurgery, Kuang Tien General Hospital, Taichung; Department of Biotechnology and Animal Science, College of Bioresources, National Ilan University, Yilan; Department of Biotechnology, College of Medical and Health Care, Hung Kuang University, Taichung, Taiwan

Correspondence Address:
Dr. Muh-Shi Lin
Department of Surgery, Division of Neurosurgery, Kuang Tien General Hospital, No. 117, Shatian Road, Shalu, Taichung 433


Background: The postoperative recurrence rate of chronic subdural hematomas (CSDHs) ranges from 9% to 20%, which is a serious concern for neurosurgeons. Both qualitative and quantitative assessment methods have been developed to identify the mechanisms involved in postoperative recurrence. These methods include Nakaguchi's clinical classification scheme and the quantification of mean hematoma density (MHD). This is the first study to examine the correlations between the quantification of MHD and Nakaguchi's clinical classification of patients with CSDHs. Materials and Methods: This study investigated 35 consecutive cases of CSDH between July 2010 and July 2013. In accordance with Nakaguchi's clinical classification, CSDH cases were separated into four groups: homogenous, laminar, separated, and trabecular. In addition, we quantified the area of the hematoma according to MHD using a computer-based image analysis of preoperative brain computed tomography scans. Results: The mean age of patients was 72.2 ± 8.05 years (range: 55–86). Mean MHD values were as follows: trabecular (12.45 ± 0.72 HU), homogenous (14.46 ± 4.51 HU), laminar (25.99 ± 0.93 HU), and separated (36.32 ± 3.04 HU). Differences in MHD were statistically significant for all CSDH types (P < 0.001, ANOVA with Student–Newman–Keuls post hoc test), and we observed a significant linear relationship between MHD and the priority order of clinical CSDH types determined according to postoperative recurrence (Spearman's rank correlation coefficient = 0.842, P < 0.001). Conclusions: This study provides statistical evidence that MHD is significantly correlated with Nakaguchi's clinical classification of CSDH. The applications of MHD quantification and hematoma's internal architecture helped to gain better understanding of possible mechanisms underlying CSDH recurrence.

How to cite this article:
Chen TY, Chang ST, Lin MS. Statistical relevance of mean hematoma density and it's internal architecture: Potential clinical application in chronic subdural hematomas.Formos J Surg 2018;51:228-233

How to cite this URL:
Chen TY, Chang ST, Lin MS. Statistical relevance of mean hematoma density and it's internal architecture: Potential clinical application in chronic subdural hematomas. Formos J Surg [serial online] 2018 [cited 2019 Feb 16 ];51:228-233
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Full Text


Chronic subdural hematoma (CSDH) commonly affects older individuals who have suffered a mild head injury, typically a few weeks following the occurrence of trauma. Patients showing symptoms of CSDH are generally treated by creating one or more burr holes in the skull to evacuate the hematoma. Despite the simplicity of this surgical technique, the reported postoperative recurrence rate is between 0.35% and 23%.[1],[2],[3],[4] This high relapse rate following surgery is a serious concern for neurosurgeons.

Risk factors associated with postoperative recurrence of CSDHs include advanced age, concomitant disease, bilateral CSDH, and coagulopathy, as in individuals suffering from leukemia, liver disease, or chronic renal failure.[5],[6],[7],[8],[9] A number of evaluation methods based on qualitative analysis of preoperative brain computed tomography (CT) scans have been developed to investigate the postoperative recurrence of CSDHs. These methods have indicated that CSDHs with high or mixed density are significantly more likely to recur.[5],[10],[11] Specifically, CSDHs with mixed density are the most likely to present rebleeding and hyperfibrinolytic activity.[10] Nakaguchi presented a practical classification system that uses CT observations to classify CSDHs according to internal architecture: homogenous, laminar, separated, and trabecular. The four classifications in Nakaguchi scheme represent the respective stages in the pathogenesis of CSDH.[12] Specifically, the four CSDH classes represent the initial formation (homogenous), development (laminar), maturity (separated), and absorption (trabecular) stages, respectively. Upon the initiation of CSDH, the tendency toward rebleeding depends on the balance between fibrinolysis and coagulation. The laminar stage presents greater vascularity than does the homogenous stage, as evidenced by brain CT scans showing a high-density layer along the inner membrane. The maturation of a hematoma is associated with an increase in the tendency to rebleed from the neomembrane of the outer membrane as well as the separation of blood components by gravity (i.e., separated type). In the hematoma-resolved stage (trabecular type), the tendency for bleeding is relatively low due to the fact that the outer membrane undergoes fibrosis. These observed trends in hematoma recurrence rates have proven useful and been widely cited.[5],[13]

Unfortunately, the aforementioned neuroimaging method does not provide quantitative evidence regarding the postoperative recurrence of CSDHs. In a previous study, we reported a simple, computer-based analytical method which uses pre-operative CT images to quantify mean hematoma density (MHD) in CSDHs.[14] Statistical evidence demonstrated that MHD is a significant and independent prognostic factor related to the postoperative recurrence of CSDH; specifically, MHD level increases with the risk of postoperative recurrence.[14] Thus, consideration of MHD could aid in the postoperative prognosis of CSDH.

No previous research has investigated the correlation between qualitative and quantitative methods used to assess the postoperative recurrence of CSDH. In this study, we sought to obtain evidence to support a correlation between MHD quantification and Nakaguchi's clinical classification. Our aim was to enhance the believability of quantitative methods based on MHD.

 Materials and Methods


This study reviewed brain CT scans and medical reports of 35 consecutive patients who underwent surgery for CSDH at our institute between July 2010 and July 2013.

To prevent confounding factors that might affect postoperative recurrence, all 35 patients receive the same treatment strategy as follows. The patients underwent burr hole craniostomy drainage on one side (unilateral CSDH, n = 27) or both sides (bilateral CSDHs, n = 8). Only one burr hole with a closed-drainage system was made on each symptomatic side. Postoperative bed rest in the supine position for 36 h was applied, and the steroid was not postoperatively used in our patients.

To control the variations of surgical techniques, we excluded patients who had undergone craniotomy or two-burr-hole technique each symptomatic side. Patients with bilateral CSDHs that included different Nakaguchi types or presented with coagulopathy due to liver disease or chronic renal failure were excluded from the present study. Moreover, patients with an isodensity hematoma were excluded from this study due to difficulties in distinguishing the contours of the hematomas from the brain parenchyma using CT scans.[9]

As previously reported,[14] intervals for follow-up CT scans were 24 h after surgery and at monthly intervals for at least 6 months until the recovery to neurologically and radiologically stable status. If persistent neurological deterioration occurred, CT scanning was performed earlier.

Recurrence of CSDH was defined as an increase in the volume of the SDH on the operated side and compression of the brain surface observed on CT scans obtained within 3 months postoperatively, when compared with findings on the first postoperative day.[15] A second operation was suggested due to persistent neurological symptoms and an increase in subdural collection with cerebral compression on the operated side, compared to CT findings obtained 24 h after surgery.[14] This study was approved by the Ethics Committee of our institute.

Clinical classification of chronic subdural hematoma

Cranial CT studies were performed on all 35 CSDH patients. Cases were classified into Nakaguchi types (i.e., homogenous, laminar, separated, or trabecular) according to the internal architecture of CSDHs.[12]

Computer-assisted quantitative analysis of chronic subdural hematomas

The procedures used to trace the margins of the hematoma on brain CT scans are outlined in [Figure 1] of a previous report.[9] Briefly, the boundary of the hematoma was traced and defined using image analysis software (GE PACS Web System). The density of the traced hematoma was calculated and presented in Hounsfield units (HU) for each axial slice. The above-mentioned measurement of hematomas was shown in [Figure 1].{Figure 1}

Assessment of chronic subdural hematomas in terms of mean hematoma density

This study defined MHD[14] as the average density expressed in HUs throughout the entire volume of the CSDH. MHDs of unilateral CSDHs were calculated using the following equation: the mean of Ai, where Ai = HU of the traced hematoma for each axial CT slice (i = serial CT slice number). MHDs of bilateral CSDHs were calculated using the equation: the mean of Bi, where Bi = the average HU of the traced hematoma on both sides of each axial CT slice (i = serial CT slice number).

Data analysis

For continuous data, we recorded the mean ± standard deviation as well as the median and interquartile range (the range between the 25th and 75th percentile). Differences in MHD among groups were detected using one-way ANOVA and the Student–Newman–Keuls (SNK) post hoc test. The relationship between MHD and the type of CSDH was assessed using Spearman's rank correlation test, with correlation strengths interpreted according to the following scale: very weak (0–0.19), weak (0.20–0.39), moderate (0.40–0.59), strong (0.60–0.79), and very strong (0.80–1.00). SAS software version 9.2 (SAS Institute Inc., Cary, NC) and MedCalc 11.5 (MedCalc Software, Ostend, Belgium) were used for all statistical analyses. A two-tailed P < 0.05 was considered to be statistically significant.


Thirty-five patients, 27 males (77%) and 8 females (23%), with a mean age of 72.2 ± 8.05 years (range: 55–86 years) were included in the study between July 2010 and July 2013. None of them lost to follow-up and they all had regular outpatient department follow-up return to the hospital until October 2016. The duration of follow-up ranged from 36 to 72 months.

The 35 cases were classified as follows: trabecular (n = 7), homogenous (n = 13), laminar (n = 7), and separated (n = 8). Representative CT images of our patients for each category of Nakaguchi classification were shown in [Figure 2]. The mean MHD for each CSDH type was: trabecular (12.45 ± 0.72 HU), homogenous (14.46 ± 4.51 HU), laminar (25.99 ± 0.93 HU), and separated (36.32 ± 3.04 HU) [Table 1]. Differences in MHD were statistically significant between all types [Table 1] and [Figure 3], P < 0.001, ANOVA with SNK post hoc test]. We postulate that four types of CSDHs exerted different tendency for postoperative recurrence and their respective MHD quantitations were, therefore, distinguished.{Figure 2}{Table 1}{Figure 3}

Since we previously observed higher MHD values in cases of postoperative recurrence,[14] we sought to determine whether there is a correlation between MHD levels and priority order of postoperative recurrence rate in Nakaguchi's clinical four types. Spearman's rank correlation was assembled to examine the two variants (MHD and four clinical types). We sorted the ranked variable – clinical types – in ascending order of postoperative recurrence rate as follows: trabecular, homogenous, laminar, and separate.[12] For each clinical type, we also ranked the measurement variable, MHD, in ascending order. A statistically significant correlation was observed between MHD values and the ranking of Nakaguchi's classifications determined according to postoperative recurrence [Spearman's rank correlation coefficient = 0.842, 95% confidence interval = 0.707–0.918; P < 0.001, [Figure 4]. In other words, clinical types that presented a higher risk of postoperative recurrence corresponded with higher MHD values.{Figure 4}

Among the 35 patients, two patients presented postoperative recurrence in the presence of neurological deficit and CT scan findings. They were separated type on preoperative CT.


The high rate of postoperative CSDH recurrence is a critical issue, and the underlying mechanisms are complex and controversial. We assert that these factors can be divided into two categories: anatomical and physiological. Anatomical factors tend to delay the obliteration of subdural spaces. A subdural space created by the occurrence of CSDH can be exacerbated when the dura and brain cortex do not adhere to each other. Unlike the epidural space, the subdural space cannot be surgically obliterated; however, it may be obliterated through the passive, postoperative expansion of the brain following the evacuation of the CSDH.

Anatomical factors associated with CSDH recurrence include brain aging and hematomas with bilateral or skull-based involvement. Atrophic brains in elderly individuals tend to be inelastic, such that subdural space (post-CSDH evacuation) is likely to delay obliteration.[16],[17],[18] CSDHs are more likely to be bilateral if the brain is relatively atrophic, and such a brain is less likely to re-expand following the evacuation of the CSDH.[7] Moreover, a large, extended postoperative subdural space is likely to delay brain expansion after surgery in cases that involve CSDH with skull base extension. Impairing brain re-expansion often results in the brain shifting within the fluid collection or within cerebrospinal fluid. Persistent shifting of the brain can lead to tears in bridging veins, which lack outer reinforcement.[19] This can, in turn, cause a higher recurrence of CSDHs.[16],[20]

Physiological factors which can increase the potential for rebleeding and accumulation of the hematoma in patients undergoing CSDH evacuation include susceptibility to bleeding and the presence of preoperative stage CSDHs. CSDH patients with susceptibility to bleeding or coagulopathy such as those with leukemia, liver disease, chronic renal failure sepsis, and other medical conditions (e.g., sepsis and disseminated intravascular coagulation) are more likely to suffer postoperative recurrence.[5],[6],[7],[8],[9] However, the presence of preoperative stage CSDHs is the physiological factor most commonly associated with postoperative recurrence. In stages with high postoperative recurrence, we postulate that a burr hole-based craniotomy could achieve partial removal of tissue affected by hyperfibrinolysis (e.g., the outer membrane). Nonetheless, even residual tissue has the potential for rebleeding.

In preoperative CT imaging, CSDHs are represented by both hyperdense and hypodense components of hematomas of various volumes. High-density components of CSDHs are not fully matured where repeated microhemorrhages from the neocapillary network in the outer membrane took place. Excessive growth of blood vessels into the CSDH membrane appears to be proportional to the amount of rebleeding in the hematoma cavity, which can result in higher density CSDHs. Our research team previously reported a quantitative method by which to determine the MHD of an entire subdural hematoma, and in so doing provide an overall average HU value for use as a standard.[14] We found that a one-unit increase in the MHD of CSDH increased the odds of postoperative recurrence by a factor of 1.243.[14] We interpret this to mean that a hematoma comprised primarily of hyperdense components is more likely to present postoperative recurrence, as this type of hematoma tends to have a higher MHD.

To obtain thorough interpretation and broad application of MHD in evaluation of outcomes in CSDH patients, we attempt to provide statistical evidence in support of a close correlation with the clinical observations of Nakaguchi. We provide statistical evidence to support the following: (1) MHD levels are significantly different between clinical types of CSDHs; (2) The sequence of MHD levels matches the priority order of clinical CSDH types determined according to postoperative recurrence. Moreover, our findings demonstrate that clinical CSDH types associated with a higher rate of recurrence, such as the separated type,[5],[10],[12] tend to have correspondingly high MHD level. Our data revealed that the separated CSDH type (36.32 ± 3.04 [HU]), which presents the highest risk of recurrence, also has the greatest mean MHD value. We postulate that compared to the other types, separated-type hematomas present a higher ratio of hyperdense to hypodense components, as their respective MHD level is also higher. Our findings support the supposition that MHD quantification improves the prediction accuracy of postoperative recurrence[14] and correlates very well with the clinical stages of CSDH. Furthermore, it has been reported that the incidence of CSDH recurrence in high-density types is significantly greater than that observed in low and isodensity types.[5],[6] Based on MHD calculations,[14] high-density homogenous CSDHs tend to have higher MHD levels and subsequently pose a higher risk of postoperative recurrence. Consideration low- and high-density homogenous hematomas as a one category is likely to underscore the risk of recurrence. Further longitudinal studies are warranted to examine this putative clinical observation.

It was evidenced that more than half of recurrent CSDHs recur within 30 days, and 70% of them recur within 3 months.[15],[18] In the present study, follow-up of our patients was for at least 3 years (range: 36–72 months). We consider that duration of follow-up in our study is enough to check recurrence. Furthermore, two patients suffered from the recurrence after surgery. They were separated type on preoperative CT. Because of too small number of recurrent patients, the current statistics thus made inconclusive in the correlations between recurrence and Nakaguchi classification. We believe the current study, as a preliminary research, aimed to investigate the correlations between the quantification of MHD and Nakaguchi's clinical classification of patients with CSDHs. We found that MHD is statistically correlated with Nakaguchi's clinical classification of CSDHs. Further quantitative studies are warranted to investigate the underlying mechanisms of in CSDHs.


This study provided statistical evidence related to the correlations between MHD and different types of CSDH as well as outcomes associated with each type. Our results revealed a close correlation between MHD levels and priority order of postoperative recurrence rate in Nakaguchi's clinical four types. MHD quantification is recommended as a means of assessing the likelihood of postoperative CSDH recurrence.

Ethical approval

The study was conducted in accordance with the Declaration of Helsinki and was approved by the local ethics committee of the institute. Informed written consent was obtained from all patients prior to their enrollment in this study.


This work was supported by grants from Kuang Tien General Hospital, Taiwan (Kuang Tien 105-07).

Financial support and sponsorship

This work was supported by grants from Kuang Tien General Hospital, Taiwan (Kuang Tien 105-07).

Conflicts of interest

There are no conflicts of interest.


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