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AbstractObjectiveTexture analysis is widely used in all walks of life, and also in medicine. This paper aims to discuss the value of texture analysis in postoperative recurrence of chronic subdural hematoma (CSDH).
MethodsA total of 173 patients with CSDH who were hospitalized in our hospital from January 2018 to August 2023 were selected . All the patients underwent magnetic resonance imaging (MRI) examinations before surgery. According to whether patients with CSDH have relapsed after surgery, the patients are divided into recurrence group and non-recurrence group. FireVoxel software (https://firevoxel.org) was used to manually delineate the region of interest on the largest level of the hematoma cavity during MRI plain scans and measure the texture parameters. The texture parameters with statistical difference were analyzed by receiver operating characteristic curve.
ResultsHeterogeneity and entropy texture parameters in the recurrence group were statistically different from those in the nonrecurrence group (p<0.05). When the cut-off point of the heterogeneity parameter was 0.284, the sensitivity, specificity, and accuracy of judging whether CSDH relapsed were 83.3%, 80.4%, and 80.7%, respectively.
INTRODUCTIONChronic subdural hematoma (CSDH) is a common disease in neurosurgery, which is more common in elderly patients. Although there are some reports on the treatment of CSDH with drugs, such as glucocorticoids and atorvastatin, surgical intervention is still the main method of treating CSDH, especially in the case of obvious compression symptoms. In the operation, one or multiple burr hole was used, followed by intraoperative irrigation and drainage. Most of the patients have good surgical results, but there is still a high recurrent rate which is 20-26% reported in different reports [1,4,9,14]. In recent years, with the rapid development of medical image digitization, using texture analysis to study medical images has become a hot spot. Texture analysis has the advantage of not relying on doctors’ subjective judgment, avoiding different doctors’ different interpretations of the same imaging data. Using texture analysis to determine whether CSDH relapse after surgery, achieving early prevention and reduction of recurrence can not only reduce the burden of future medical system, but also reduce the incidence rate and mortality related to recurrence.
MATERIALS AND METHODSThis study was approved by the Ethics Committee of The Second Affiliated Hospital of Jiaxing University (Institutional review board number : 2023-ZFYJ-037).
Clinical materialsFrom January 2018 to August 2023, 173 patients with CSDH who were examined by magnetic resonance imaging (MRI) before surgery in our hospital were collected. All patients underwent burr-hole craniotomy to treat CSDH. The clinical manifestations were walking instability, slurred speech, consciousness disorder, etc.
Inclusion and exclusion criteriaInclusion criteria : 1) age ≥18 years old; 2) CSDH was confirmed by imaging examination; 3) burr-hole craniotomy as a surgical intervention; and 4) follow-up for more than 2 months after surgery. Exclusion criteria : 1) patients with intracranial space-occupying lesions, inflammatory changes and other types of intracranial diseases; 2) patients receiving long-term anticoagulant or antiplatelet therapy; 3) patients with severe underlying diseases (such as thrombocytopenia, coagulation dysfunction, liver failure, etc.); 4) the patient underwent craniotomy; and 5) severe complications or death occurred during or after operation.
MRI examination methodPatients in the group were examined by MRI before surgery in our hospital. Using Signa EVCITE 1.5T MR scanner (GE HealthCare, Waukesha, WI, USA), the scan parameters were set as following : SE sequence T1WI (repetition time [TR], 2200.6 ms; echo time [TE], 9.8 ms), T2WI (TR, 3440 ms; TE, 106.8 ms), T1 fluid attenuated inversion recovery (FLAIR) (TR, 1867.8 ms; TE, 9.1 ms), T2 FLAIR (TR, 8002 ms; TE, 169.2 ms), diffusion weighted imaging (TR, 4000 ms; TE, 73.4 ms).
Treatment methodsBased on the patient’s preoperative imaging data, a burr-hole craniotomy was performed at the thickest part of the hematoma. During the operation, a large amount of physiological saline was used to flush the hematoma cavity until the drainage fluid was clarified, and a drainage tube was placed in the hematoma cavity. After the operation, the patients should be in the supine position, and the drainage tube should be continuously drained for 2-3 days. When there is no significant increase in drainage volume, the drainage tube can be removed. Moreover, patients should sit up and get out of bed as early as possible after extubation (Fig. 1).
Follow-up waysAll patients were followed up in the neurosurgery department of our hospital after surgery. The follow-up time was 2 months after surgery. The follow-up contents included medical history collection and imaging examination. Recurrence was defined as recurrence of hematoma at the original hematoma site requiring reoperation during follow-up [3]. These patients may be accompanied by neurological symptoms or signs. Most of these symptoms and signs are headache, some are accompanied by psychiatric symptoms such as dementia, apathy, and mental retardation, and a few are accompanied by neurological symptoms such as hemiplegia, aphasia, and focal epilepsy. These patients may also lack neurological symptoms or signs, and the recurrence of CSDH is only discovered during a follow-up computed tomography (CT) or MRI, indicating the volume has reached the criteria for reoperation.
Imaging data extraction and texture analysisMRI T2 FLAIR images were exported and stored at picture archiving and communication systems workstation in digital imaging and communications in medicine format. Using FireVoxel software (build 457; FireVoxel Software, New York, NY, USA) and referring to the methods used by scholar’s published article [16], we did the texture analysis. Briefly, the MRI T2 FLAIR images of each patient were loaded into the software FireVoxel, then, two doctors with many years of experience in neuroimaging readings, without knowing each other, manually delineated the largest CSDH region as the region of interest (ROI). If there was a significant difference in the results of parameters analyzed independently by two doctors, the final judgment was made by the clinically experienced department director. ROI contains all CSDH regions, except for brain parenchyma. The software automatically processed the ROI and output the following parameters : heterogeneity, skewness, kurtosis and entropy, and the average given by two doctors were analyzed (Fig. 2).
Statistical analysisSPSS ver. 20.0 (IBM Corporation, Armonk, NY, USA) statistical analysis software was applied. Chi-squared test or successive correction method was used for counting data. Measurement data were expressed as (mean±standard deviation), and the intergroup comparison of data was conducted using the independent sample t-test. Receiver operating characteristic (ROC) curve was used to analyze texture parameters with statistical differences. p<0.05 represented that the difference was statistically significant.
RESULTSGeneral data comparisonThe number of recurrences in 173 patients with CSDH was 31. Age (≥60 years), gender, history of trauma, hypertension, diabetes, and history of anticoagulant use were not risk factors for CSDH recurrence. There was no statistical difference between the recurrence group and the non-recurrence group (p>0.05, Table 1).
Texture analysis of CSDHThere was no statistical difference in the skewness and kurtosis between the recurrence group and the non-recurrence group. The recurrence group (0.313±0.056) was higher than the non-recurrence group (0.224±0.087) in the heterogeneity comparison, and the difference was statistically significant (p=0.017). In the entropy comparison, the recurrence group (3.993±0.219) was higher than the non-recurrence group (3.626±0.392), and the difference was statistically significant (p=0.029). Using ROC curve to analyze texture parameters with statistical differences, the area under the curve (AUC) of entropy parameter was significantly better than the heterogeneity parameter AUC. When we set the cut-off point of the heterogeneity parameter at 0.284, the sensitivity, specificity, and accuracy of judging whether CSDH relapsed by heterogeneity were 83.3%, 80.4%, 80.7%, respectively (Tables 2 and 3, Fig. 3).
DISCUSSIONCSDH is an enveloped hematoma located between the dura mater and the arachnoid membrane. It usually shows clinical symptoms and signs 3 weeks after the trauma. Burr-hole craniotomy is a common clinical treatment, which has good effect but high recurrence rate. Moreover, researches at home and abroad have different definitions of postoperative recurrence of CSDH. For example, a large multicenter cohort study in the UK defines CSDH recurrence as repeated surgical drainage within 60 days after surgery [15]. You et al. [24] thought if the patient has a hematoma accumulation again on the ipsilateral subdural space with neurological deficits, surgery is needed again, which was defined as CSDH recurrence. Therefore, in this study, recurrence was defined as recurrence of ipsilateral CSDH requiring reoperation within 2 months after the initial surgery.
Many non-surgical risk factors are thought to be related to the recurrence of CSDH, including age, patient status at admission, drinking, systemic diseases such as liver and kidney dysfunction, and bilateral CSDH [23]. Another multicenter retrospective study of 719 cases showed that age, gender, diabetes, hypertension, chronic renal failure, drinking, consciousness disorder on admission, and preoperative CT density were not related to CSDH recurrence, and antiplatelet therapy significantly affected the recurrence of CSDH [18]. A meta-analysis reported by Wang et al. [21] also showed that antithrombotic drugs are a risk factor for CSDH recurrence. Our study found that age (≥60 years), gender, history of trauma, hypertension, diabetes, and history of anticoagulant use were not risk factors for CSDH recurrence. Thus, this may be related to our small amount of data, and further research is needed to determine whether non-surgical risk factors are related to the recurrence of CSDH. But it also shows that it is difficult to judge the recurrence of CSDH only by general data.
In recent years, many literatures have found that the density, drainage, thickness, and typing of CSDHs are related to CSDH recurrence. The articles published by You et al. [24] show that homogeneous high-density hematomas can be used to predict whether recurrence after CSDH. Articles published by Liu et al. [13] showed that mixed density hematomas are independent predictors of CSDH recurrence. Ridwan et al. [15]’s study found that the separated stratified, separated, and trabecular Nakaguchi subtypes were independent predictors of CSDH relapse. However, there are certain limitations in predicting the recurrence of CSDH by imaging. There are differences in different doctors’ interpretation of the same imaging data, and even there will be greater differences. Therefore, the standardized interpretation of the imaging data of patients with CSDHs will eliminate the differences between different observers, which will help predict the recurrence of patients with CSDH in advance, formulate personalized treatments, reduce the recurrence rate and improve the quality of life.
The difference in the number of patients between the recurrence group and the non-recurrence group in this study is related to the recurrence rate of CSDH. Recurrence rates of CSDH have been reported to range from 9.2% to 26.5%, and recurrence rates also range from 5% to 33% [8,11]. The recurrence rate calculated from the number of patients in the two groups in our manuscript was 17.9%, which is consistent with the recurrence rate reported in the literature. We performed statistical analyses using previous literature, in which there were also differences in the number of patients between the two groups, to ensure the robustness of the analyses.
Texture analysis is a process of extracting texture feature parameters through image processing technology to obtain quantitative or qualitative description of texture [5]. At present, texture analysis is widely used in all walks of life, and also in medicine. For example, the application of texture analysis on cardiac MRI T1 and T2 maps provides quantitative imaging parameters for the diagnosis of acute and chronic heart failure-like myocarditis [2]; the texture analysis of susceptibility weighted imaging (SWI) can quantify Identifying patients with amyotrophic lateral sclerosis [10]; placental MRI texture analysis is helpful for prenatal diagnosis of implanted placental spectrum [4]; in the field of tumors, MRI-based texture analysis can be used for the differential diagnosis of pancreatic nonfunctional neuroendocrine tumors and solid pseudopapillary tumors [12]; predict the efficacy of neoadjuvant chemotherapy for cervical cancer [7]; predict bone metastases before prostate cancer treatment [20]; there is a review that texture analysis plays an important role in the evaluation of breast cancer diagnosis, prognosis and treatment response [6]. Moreover, texture analysis also has a good application prospect in neurosurgery, and many literatures have reported it. Texture analysis can identify different types of posterior cranial fossa tumors such as medulloblastoma, brain metastases, and hemangioblastoma [25]. Furthermore, texture analysis can identify glioblastoma and primary central nervous system lymphoma before surgery [22]. Meta-analysis shows that MRI texture analysis can accurately distinguish low-grade and high-grade gliomas [19].
According to literature reports [17], FLAIR sequence can more effectively distinguish subdural hematoma from cerebrospinal fluid than T2 sequence, and is an effective sequence for the detection of subdural hematoma. In this study, it was necessary to accurately delineate the boundary of CSDH and then perform texture analysis. Therefore, FLAIR sequence can effectively distinguish CSDH from cerebrospinal fluid, and is more suitable for this study than T2, SWI and other sequences. T2 FLAIR sequence was used for texture analysis in this study.
Therefore, this study is the first to report the texture analysis of CSDH by Firevoxel software, which avoids the deviation of analysis by different doctors. We found that the heterogeneity of the relapsed group (0.313±0.056) was greater than that of the non-relapsed group (0.224±0.087), and the difference was statistically significant (p=0.017). And when the cut-off point of heterogeneity is 0.820, the sensitivity, specificity, and accuracy of judging the recurrence of CSDH through heterogeneity were 83.3%, 80.4%, and 80.7%, respectively.
Entropy is obtained by computing the probability distribution of the gray values of pixels in the image. Specifically, entropy measures the randomness and uncertainty of the gray value in the image texture. Quantifying texture complexity: entropy can quantify the complexity of image texture. High entropy values indicate complex image texture and high information content, while low entropy values indicate simple image texture and low information content. This quantification facilitates a deeper understanding and analysis of the image. Texture classification and recognition : in texture classification and recognition tasks, entropy can be used as one of the features to help distinguish different textures. By calculating the entropy of different texture images, a classifier can be constructed to achieve automatic texture classification and recognition. Image quality evaluation : entropy can also be used to evaluate the quality of images. In the process of image compression and transmission, the change of entropy value can reflect the loss of image information. Therefore, entropy can be used as an important index for image quality evaluation.
This study confirms that texture analysis can be used to predict postoperative recurrence of CSDH. In addition, texture analysis is a non-invasive, economical, and easy-to-use technique. It is of great significance to predict the recurrence of CSDH after surgery, that is, it can not only provide a reference for the diagnosis and treatment program, ensure the safety of patients, but also appropriately reduce the medical expenses, and reduce the burden for families and society. However, the shortcoming of this study is that the amount of data included is small, and more institutions are needed to join the study, which further confirms the value of texture analysis in the postoperative recurrence of CSDH.
CONCLUSIONThe analysis of the texture of CSDH provides a new method for judging the recurrence of CSDH, which is helpful to achieve early prevention and reduction of recurrence. This will not only reduce the burden on the healthcare system in the future, but also reduce the morbidity and mortality associated with recurrence.
NotesInformed consent Informed consent was obtained from all individual participants included in this study. Fig. 1.An 84 years old, men, headache with walking instability for 2 weeks. A : Computed tomography (CT) image on admission. B : CT image on the first day after surgery. C : CT image after the drainage tube was pulled out on the third day after surgery. D : CT image on the 34th day after surgery when the patient was readmitted for reexamination due to unstable walking. ![]() Fig. 2.The results of delineating region of interest and analysis by the FireVoxel software (FireVoxel Software, New York, NY, USA). A : The delineating image of left chronic subdural hematoma. B : The FireVoxel software analysis of (A). C : The delineating image of right chronic subdural hematoma. D : The FireVoxel software analysis of (C). ![]() Fig. 3.Comparison of texture parameter heterogeneity and entropy receiver operating characteristic (ROC) curve. A : The area under the heterogeneity parameter curve (area under the curve, AUC) is 0.820. B : The entropy parameter AUC is 0.788. When the cut-off point of the heterogeneity parameter is 0.284, the sensitivity, specificity and accuracy are 83.3%, 80.4%, and 80.7%, respectively. ![]() Table 1.Relationship between general data and CSDH recurrence Table 2.Relationship between texture parameters and CSDH recurrence References1. Almenawer SA, Farrokhyar F, Hong C, Alhazzani W, Manoranjan B, Yarascavitch B, et al : Chronic subdural hematoma management: a systematic review and meta-analysis of 34829 patients. Ann Surg 259 : 449-457, 2014
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