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Comparison of Swirl Sign and Black Hole Sign in Predicting Early Hematoma Growth in Patients with Spontaneous Intracerebral Hemorrhage

Comparison of Swirl Sign and Black Hole Sign in Predicting Early Hematoma Growth in Patients with... CLINICAL RESEARCH e-ISSN 1643-3750 © Med Sci Monit, 2018; 24: 567-573 DOI: 10.12659/MSM.906708 Received: 2017.08.18 Comparison of Swirl Sign and Black Hole Sign in Accepted: 2017.09.18 Published: 2018.01.29 Predicting Early Hematoma Growth in Patients with Spontaneous Intracerebral Hemorrhage Authors’ Contrib ution: AE 1,2 Xin Xiong 1 Department of Neurology, The First Affiliated Hospital of Chongqing Medical Study Design A University, Chongqing, P.R. China ABG 1 Qi Li Data Collection B 2 Department of Neurology, Chongqing Traditional Chinese Medicine Hospital, BC 3 Wen-Song Yang Statistical Analysis C Chongqing, P.R. China Data Interpr etation D F 4 Xiao Wei 3 Department of Neurology, Yongchuan Hospital of Chongqing Medical University, Manuscript Preparation E Chongqing, P.R. China F 5 Xi Hu Literature Search F 4 Department of Medical Technology, Chongqing Medical and Pharmaceutical B 1 Xing-Chen Wang Funds Collection G College, Chongqing, P.R. China BD 1 Dan Zhu 5 Department of Neurosurgery, The Fourth People’s Hospital of Chongqing, Chongqing, P.R. China BC 1 Rui Li B 1 Du Cao ADG 1 Peng Xie Corresponding Authors: Peng Xie, e-mail: peng_xie@yahoo.com, Qi Li, e-mail: qili_md@126.com Source of support: This study was supported by the National Natural Science Foundation of China (Grant No. 81200899) and the National Key Research and Development Program of China (Grant No. 2017YFA0505700) Background: Early hematoma growth is associated with poor outcome in patients with spontaneous intracerebral hemor- rhage (ICH). The swirl sign (SS) and the black hole sign (BHS) are imaging markers in ICH patients. The aim of this study was to compare the predictive value of these 2 signs for early hematoma growth. Material/Methods: ICH patients were screened for the appearance of the 2 signs within 6 h after onset of symptoms. The sensi- tivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of the 2 signs in predict - ing early hematoma growth were assessed. The accuracy of the 2 signs in predicting early hematoma growth was analyzed by receiver-operator analysis. Results: A total of 200 patients were enrolled in this study. BHS was found in 30 (15%) patients, and SS was found in 70 (35%) patients. Of the 71 patients with early hematoma growth, BHS was found on initial computed to- mography scans in 24 (33.8%) and SS in 33 (46.5%). The sensitivity, specificity, PPV, and NPV of BHS for pre - dicting early hematoma growth were 33.8%, 95.3%, 80.0%, and 72.0%, respectively. The sensitivity, specificity, PPV, and NPV of SS were 46.5%, 71.3%, 47.0%, and 71.0%, respectively. The area under the curve was 0.646 for BHS and 0.589 for SS (P=0.08). Multivariate logistic regression showed that presence of BHS is an indepen- dent predictor of early hematoma growth. Conclusions: The Black hole sign seems to be good predictor for hematoma growth. The presence of swirl sign on admis- sion CT does not independently predict hematoma growth in patients with ICH. MeSH Keywords: Cerebral Hemorrhage • Hematoma • Multidetector Computed Tomography Full-text PDF: https://www.medscimonit.com/abstract/index/idArt/906708 1993 4 2 25 Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Background hematoma before the follow- up CT scan. The demographical data, previous medical history, cigarette smoking, alcohol con- Spontaneous intracerebral hemorrhage (ICH) is an acute neu- sumption, medication history, Glasgow coma scale, and blood rological emergency associated with high morbidity and mor- pressure were recorded. This study was approved by the Ethics tality [1,2]. It is estimated to account for approximately 10% Committee of the First Affiliated Hospital of Chongqing Medical to 20% of all strokes [3]. Early hematoma growth, which oc- University. Written informed consult was obtained from all par- curs in 1/3 of patients when scanned within 6 h, is one of the ticipants or their relatives. most important determinants of mortality and functional out- come [4,5]. The restricting early hematoma growth may be Imaging analysis useful [6]. The computed tomographic angiography (CTA) spot sign (and derived spot sign score) is a reliable sign for pred- The initial and follow-up CT scans were performed using stan- ication of early hematoma growth, early mortality, and poor dard clinical parameters with axial 5-mm section thickness. outcome [7,8]. However, early CTA examination is not avail- The images were obtained and stored for further evaluation. able in all clinical settings. In addition, several renal function Hematoma was assessed and classified as lobar, deep, and in - impairment and allergic reactions to contrast medium restrict fratentorial. According to previous definition, the swirl sign on the CTA examination. the NCCT was defined as follows: (1) a hypo- or iso-attenua - tion region (compared to the attenuation of brain parenchy- In recent years, noncontrast computed tomography (NCCT) im- ma) within the hyperattenuation hematoma; (2) shape may be aging markers, such as blend sign [9], black hole sign (BHS) [10], rounded, streak-like, or irregular [13]. The black hole sign on and hypodensities [11], have been identified as promising im - the NCCT was defined as follows: (1) a hypoattenuation area aging markers for predicting early hematoma growth. The swirl (black hole) encapsulated within the hyperattenuation hema- sign (SS), which was originally described as areas of low at- toma; (2) the black hole could be round, oval, or rodlike, but tenuation or radiolucency within hyperattenuated hematomas, was not connected to the adjacent brain tissue; (3) the black indicates active bleeding in epidural hematoma patient [12]. hole should have a clear border; (4) the hematoma should In a study of 203 patients with acute ICH, Selariu et al. doc- have at least a 28 Hounsfield unit (HU) difference between umented that SS is an independent predictor of death at 1 the 2 density regions [10].Two experienced readers who were month and functional outcome at 3 months [13]. However, blinded to all clinical data and follow-up CT images indepen- the ability of swirl sign to predict early hematoma growth re- dently evaluated the presence of SS and BHS on initial CT im- mains controversial. In 2016, Li et al. first proposed using the ages in all patients. Discrepancies in judging the occurrence of black hole sign to predict early hematoma growth [10]. More SS and BHS were settled by joint discussion of the 2 readers. recently, Yu et al. validated the predictive value of BHS in pre- Early hematoma growth was defined as an increase of hema - dicting early hematoma growth [14], but the predictive val- toma volume >33% or absolute hematoma growth >6 mL from ues of BHS and SS in predicting early hematoma growth have initial CT scan [15]. The hematoma volume was measured by never been compared. Therefore, we performed the present abc/2 formula [16]. Illustrative SS and BHS on initial CT imag- study to investigate the role of BHS and SS in predicting ear- es and follow-up images are shown in Figure 1. ly hematoma growth. Statistical analysis Material and Methods All statistical analyses were performed with commercially available software, SPSS version 19.0 (SPSS, Inc). Continuous Patients variables are expressed as mean (SD) values or median (inter- quartile range [IQR]) values, as appropriate, and discrete vari- We analyzed patients with spontaneous ICH aged >18 years ables are expressed as counts (percentages). Statistical sig- who were admitted to our hospital between July 2011 and nificance was determined by the c test, the Fisher exact test, October 2015 from our prospective ongoing database. The in- the t test, Z test, and the Mann-Whitney test, as appropriate. clusion criteria of this study were as follows: (1) ICH was con- Data with a P value of less than 0.05 were considered signifi - firmed on NCCT scan within 6 h after onset of symptoms; (2) cant. Multivariate logistic regression models were used to in- the follow-up CT scan was obtained within 24 h after the ini- vestigate factors that were independently associated with ear- tial CT scan. The exclusion criteria were as follows: (1) patients ly hematoma growth. Inter-rater reliability of SS and BHS were suffered from brain tumor, head trauma, or arteriovenous mal - estimated by k values. formation, rupture of an intracranial aneurysm, hemorrhag- ic infarction, or primary intraventricular hemorrhage; (2) an- ticoagulation-associated bleeding; (3) surgical evacuation of Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 A B C D Figure 1. Illustration of swirl sign, black hole sign, and follow-up CT images. (A) A 60-year-old man presented with sudden onset of left-sided paralysis. Admission CT image performed 1 h after onset of symptoms showing thalamic ICH with a swirl sign (arrow) and the hematoma volume was 16.57 ml. (B) Hematoma volume remains the same on follow-up CT scan performed 23 h after onset of symptoms. (C) A 75-year-old man with left deep ICH. Initial CT image performed 2 h after onset of symptoms shows black hole sign (arrow). (D) Follow-up CT image 4 h later shows significant hematoma growth. Results in cerebral lobes in 13%, and infratentorial in 7%. Hematoma growth was observed in 71 patients (35.5%) with ICH. There A total of 200 patients (135 men and 65 women) with sponta- were no statistically significant differences in age, sex, hyper - neous ICH fulfilled the inclusion criteria and were enrolled in our tension, diabetes mellitus, smoking, alcohol drinking, and in- study. The mean age of the patients was 60.5±12.4 years (age traventricular hemorrhage. The mean baseline hematoma vol- range, 27–90 years). The hematoma was located deep in 80%, ume was 18.5 ml (interquartile range, 10.3–35.4 ml) in patients Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Table 1. Baseline characteristics between patients with and without hematoma growth. Hematoma growth Hematoma growth Variables P value positive (n=71) negative (n=129) Demographic Mean age, y (SD) 61.5 (12.4) 60.0 (12.4) 0.411 Sex, male, n (%) 53 (74.6) 82 (63.6) 0.109 Medical history Alcohol consumption, n (%) 32 (45.7) 57 (44.5) 0.873 Smoking, n (%) 34 (48.6) 59 (46.1) 0.738 Hypertension, n (%) 48 (68.6) 94 (72.9) 0.522 Diabetes mellitus, n (%) 8 (11.4) 16 (12.4) 0.840 Clinical features Systolic blood pressure, mmHg (SD) 172.5 (29.2) 168.8 (28.2) 0.377 Diastolic blood pressure, mmHg SD) 99.5 (17.5) 97.0 (16.4) 0.320 Baseline hematoma volume, ml(IQR) 18.5 (10.3–35.4) 11.7 (6.7–16.6) <0.001 Onset-to-imaging time, h(IQR) 1 (1–3) 3 (1–4) <0.001 Baseline GCS score, median(IQR) 12 (8–14) 14 (12–15) <0.001 IVH at initial CT, n (%) 24 (33.8) 45 (34.9) 0.878 Black hole sign, n (%) 24 (33.8) 6 (4.7) <0.001 Swirl sign, n (%) 33 (46.5) 37 (28.7) 0.012 Lobar hemorrhage, n (%) 15 (21.1) 11 (8.5) 0.011 Deep hemorrhage, n (%) 52 (73.2) 108 (83.7) 0.076 Infratentorial hemorrhage, n (%) 4 (5.6) 10 (7.8) 0.574 CT – computed tomography; GCS – Glasgow Coma Scale; IVH – intraventricular hemorrhage; IQR – inter-quartile range; SD – standard deviation. with early hematoma growth when compared with 11.7 ml (in- The inter-rater agreement for identifying BHS and SS were 0.939 terquartile range, 6.7–16.6 ml) in patients without early hema- and 0.816, respectively, between the 2 readers. The sensitiv- toma growth (P<0.001). The onset-to-imaging time in patients ity, specificity, and positive and negative predictive value of with early hematoma growth was shorter than that in patients BHS for predicting early hematoma growth were 33.8%, 95.3%, without early hematoma growth (P<0.001). The mean baseline 80.0%, and 72.0%, respectively. The sensitivity, specificity, and Glasgow coma scale score in patients with early hematoma positive and negative predictive value of SS for predicting ear- growth was 12 (interquartile range, 8–14), while that in pa- ly hematoma growth were 46.5%, 71.3%, 47.0%, and 71%, re- tients without early hematoma growth was 14 (interquartile spectively. The receiver operating characteristic (ROC) of the 2 range, 12–15) (P<0.001). Detailed data comparing patients with signs for the prediction of early hematoma growth are shown and without early hematoma growth are displayed in Table 1. in Figure 2. The area under the curve (AUC) was 0.646 for BHS and 0.589 for SS (P=0.08). BHS was found in 30 (15%) of 200 patients with ICH, and SS was found in 70 (35%) of 200 patients with ICH at initial CT. Of In univariate logistic regression, admission Glasgow coma scale, the 71 patients with early hematoma growth, BHS was found on higher baseline hematoma volume, time to CT, and presence of initial CT scans in 24 (33.8%) and the SS in 33 (46.5%). Detailed BHS and SS on initial CT scan were associated with early he- baseline demographic, as well as clinical and radiological char- matoma growth (Table 3). In multivariate logistic regression, acteristics, between patient BHS and SS are displayed in Table 2. the presence of BHS on initial CT remained independently Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Table 2. Baseline characteristics of patients with black hole sign positive and swirl sign positive. Black hole sign Swirl sign Variables positive (n=30) positive (n=70) Demographic Mean age, y (SD) 62.5 (13.0) 61.1 (11.7) Sex, male, n (%) 20 (66.7) 46 (65.7) Medical history Alcohol consumption, n (%) 16 (53.3) 31 (44.3) Smoking, n (%) 16 (53.3) 32 (45.7) Hypertension, n (%) 20 (66.7) 53 (75.7) Diabetes mellitus, n (%) 3 (10) 8 (11.4) Clinical features Systolic blood pressure, mmHg (SD) 164.7 (27.6) 167.1 (26.1) Diastolic blood pressure, mmHg SD) 96.7 (14.5) 94.5 (14.2) Baseline hematoma volume, ml(IQR) 24.3 (14.9–50.8) 18.4 (13.4–29.0) Onset-to-imaging time, h(IQR) 2 (1–3.25) 2 (1–4) Baseline GCS score, median(IQR) 10 (7–14) 12 (8–14) IVH at initial CT, n (%) 11 (36.7) 31 (44.3) Lobar hemorrhage, n (%) 8 (26.7) 11 (15.7) Deep hemorrhage, n (%) 21 (70) 58 (82.9) Infratentorial hemorrhage, n (%) 1 (3.3) 1 (1.4) CT – computed tomography; GCS – Glasgow Coma Scale; IVH – intraventricular hemorrhage; IQR – inter-quartile range; SD – standard deviation. associated with early hematoma growth (odds ratio, 8.51 ROC curve 1.0 [95%CI, 2.55–28.40]; P <0.001). However, SS did not predict early hematoma growth in the multivariate logistic analysis (odds ratio, 0.61 [95%CI, 0.26–1.48]; P=0.276; Table 4). 0.8 0.6 Discussion 0.4 In this study, we found that BHS is more accurate than SS in prediction of early hematoma growth when comparing the 2 Black hole sign 0.2 signs in primary ICH patients. The AUC value of the BHS was Swirl sign Reference line 0.646, which was higher than that of SS (P=0.08). Controversy exists over whether SS is an independent predictor of early he- 0.0 0.0 0.2 0.4 0.6 0.8 1.0 matoma growth. In a study of 203 patients with ICH, Selariu et al. first defined SS as an imaging marker for predicting ear - 1-Specificity ly hematoma growth; the swirl sign was observed in 30% Figure 2. Receiver-operating characteristic (ROC) curve using a (61/203) of ICH patients in their study. However, the ability to binary definition of early hematoma growth. The AUC predict early hematoma growth was not investigated [13]. In value of the black hole sign=0.646 and the AUC value a study of 56 patients with ICH, Kim et al. found SS was ob- of the swirl sign=0.589; P=0.08. served in 13 of 56 (23%) patients with ICH, and SS was not Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Sensitivity Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Table 3. Univariate analyses for early hematoma growth. Variables Odds ratio 95% Confidence interval P value Age* 1.01 0.99–1.03 0.409 Baseline hematoma volume* 1.08 1.05–1.11 <0.001 Alcohol consumptiom 1.05 0.58–1.88 0.873 Smoking 1.11 0.62–1.98 0.738 Diabetes mellitus 0.91 0.37–2.25 0.840 Onset-to-imaging time* 0.69 0.57–0.84 <0.001 Baseline GCS score* 0.86 0.79–0.94 0.001 IVH at initial CT 0.95 0.52–1.76 0.878 Black hole sign 10.47 4.03–27.22 <0.001 Swirl sign 2.16 1.18–3.95 0.012 Lobar hemorrhage 2.87 1.24–6.66 0.014 Deep hemorrhage 0.53 0.26–1.08 0.079 Infratentorial hemorrhage 0.71 0.22–2.35 0.576 CT – computed tomography; GCS – Glasgow Coma Scale; IVH – intraventricular hemorrhage; IQR – inter-quartile range; SD – standard deviation. * Per unit change in regressor. Table 4. Multivariate analysis for early hematoma growth. Variables Odds ratio 95% Confidence interval P value Black hole sign 8.51 2.55–28.40 <0.001 Swirl sign 0.61 0.26–1.48 0.276 Baseline GCS score* 0.96 0.86–1.07 0.445 Onset-to-imaging time* 0.63 0.50–0.81 <0.001 Baseline hematoma volume* 1.08 1.04–1.12 <0.001 GCS – Glasgow Coma Scale. * Per unit change in regressor. independently predictive of hematoma growth [17]. In anoth- univariate analysis, but after multivariate analysis, SS could er study, Gökçe et al. reported that SS was observed in 36 of not predict early hematoma growth, which is in accordance 45 (80%) patients with ICH [18]. Interestingly, 46.6% (21/45) with most previous studies. In contrast, BHS, as proposed by of patients had anticoagulant-associated ICH, and the time of Li et al. [10], is a novel NCCT for early hematoma growth in pri- flow-up CT varied from 1.5 to 192 h, but they did not define he - mary ICH, with a high inter-rater agreement (0.939). This could matoma growth. In a retrospective study, Connor et al. studied be explained by the rigorous definition of BHS. 71 ICH patients presenting <24 h after onset of symptoms with baseline NCCT, and 24-h follow-up CT [19]. Their study showed BHS and SS are both imaging markers that reflect hemor - SS was observed in 46% (33/71) of patients. Multivariate anal- rhage density heterogeneity. Hematoma growth may occur in ysis demonstrated SS is independently associated with early a cascaded pattern, with initial bleeding causing secondary hematoma growth. Recently, Boulouis et al. [11] reported that peripheral vessels rupture for ongoing bleeding [20,21]. The 207 of 1029 (20%) ICH patients had SS. In univariate analy- CT attenuation of blood is dependent on the time course of sis, SS was associated with early hematoma growth, but in the bleeding [22], so the heterogeneity of the hematoma rep- the multivariable model, SS cannot independently predict he- resents blood of different ages. In addition, the hypoattenu - matoma growth. Strikingly, SS was reported in 20% to 80% ation area may indicate the fresh liquid blood bleeding [23]. of patients with ICH. In our study, SS was observed in 35% of However, the hypoattenuation region that connects to adjacent patients with ICH. SS can predict early hematoma growth in brain tissue may be a normal brain parenchyma, which may Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 be judged as SS according to Selariu’s definition [13], and this There are several limitations to the present study. Some NCCT might limit the ability to predict early hematoma growth. SS appearances can also predict early hematoma growth, but we has a vague definition, and the evaluation of SS is more sub - only compared SS and BHS because SS and BHS are more com- jective. In BHS, a clear border and a delta of ³28 HU between parable. This was a single-center study, and multicenter stud- the 2 density regions can improve the reliability and subjec- ies are needed to further valuate the predictive value. tivity. Therefore, the inter-rater reliability is higher than with SS. The rigorous definition of BHS results in a high specificity of BHS (95.3%) but a low sensitivity (33.8%). Conclusions Many studies have documented that the CTA spot sign is a To the best of our knowledge, there is no previous study com- good predictor of early hematoma growth [24]. Recent stud- paring SS and BHS in the prediction of early hematoma growth. ies have assessed the correction between CTA spot sign and Our study shows that BHS is be good predictor of hematoma NCCT markers. In a study of 115 patients with ICH, Zheng et growth, but baseline NCCT swirl sign does not independently al. reported that blend sign and CTA spot sign are good pre- predict hematoma growth in patients with ICH. dictors for early hematoma growth [25]. In a study of 129 pa- tients with ICH, Yu et al. demonstrated that the presence of Acknowledgements the BHS is associated with the spot sign, and BHS and CTA spot sign are both predictors of early hematoma growth [14]. We thank the patients who participated in this study and Interestingly, they also found early hematoma growth can oc- made it possible. cur in BHS-positive but CTA spot sign-negative patients. Conflict of interest None. References: 1. Qureshi AI, Tuhrim S, Broderick JP et al: Spontaneous intracerebral hemor- 13. Selariu E, Zia E, Brizzi M, Abul-Kasim K: Swirl sign in intracerebral haemor- rhage. N Engl J Med, 2001; 344(19): 1450–60 rhage: Definition, prevalence, reliability and prognostic value. 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Delgado AJE, Yoo AJ, Stone MJ et al: The spot sign score in primary intra- cerebral hemorrhage identifies patients at highest risk of in-hospital mor - 19. Connor D, Huynh TJ, Demchuk AM et al: Swirls and spots: Relationship be- tality and poor outcome among survivors. Stroke, 2010; 41: 54–60 tween qualitative and quantitative hematoma heterogeneity, hematoma expansion, and the spot sign. Neurovascular Imaging, 2015; 1: 1–8. 8. Huynh TJ, Demchuk AM, Dowlatshahi D et al: Spot sign number is the most important spot sign characteristic for predicting hematoma expansion using 20. Boulouis G, Dumas A, Betensky RA et al: Anatomic pattern of intracerebral first-pass computed tomography angiography: analysis from the PREDICT hemorrhage expansion: Relation to CT angiography spot sign and hema- study. Stroke, 2013; 44: 972–77 toma center. Stroke, 2014; 45: 1154–56 9. Li Q, Zhang G, Huang YJ et al: Blend sign on computed tomography: Novel 21. Dowlatshahi D, Wasserman JK, Momoli F et al: Evolution of computed to- and reliable predictor for early hematoma growth in patients with intrace- mography angiography spot sign is consistent with a site of active hemor- rebral hemorrhage. Stroke, 2015; 46: 2119–23 rhage in acute intracerebral hemorrhage. Stroke, 2014; 45: 277–80 10. Li Q, Zhang G, Xiong X et al: Black hole sign: Novel imaging marker that pre- 22. Parizel PM, Makkat S, Van Miert E et al: Intracranial hemorrhage: Principles dicts hematoma growth in patients with intracerebral hemorrhage. Stroke, of CT and MRI interpretation. Eur Radiol, 2001; 11: 1770–83 2016; 47: 1777–81 23. Schlunk F, Greenberg SM: The pathophysiology of intracerebral hemorrhage 11. Boulouis G, Morotti A, Brouwers HB et al: Association between hypoden- formation and expansion. Transl Stroke Res, 2015; 6: 257–63 sities detected by computed tomography and hematoma expansion in pa- 24. 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Med Sci Monit, 2018; 24: 2250–57 Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Medical Science Monitor : International Medical Journal of Experimental and Clinical Research Pubmed Central

Comparison of Swirl Sign and Black Hole Sign in Predicting Early Hematoma Growth in Patients with Spontaneous Intracerebral Hemorrhage

Medical Science Monitor : International Medical Journal of Experimental and Clinical Research , Volume 24 – Jan 29, 2018

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1234-1010
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1643-3750
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10.12659/MSM.906708
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Abstract

CLINICAL RESEARCH e-ISSN 1643-3750 © Med Sci Monit, 2018; 24: 567-573 DOI: 10.12659/MSM.906708 Received: 2017.08.18 Comparison of Swirl Sign and Black Hole Sign in Accepted: 2017.09.18 Published: 2018.01.29 Predicting Early Hematoma Growth in Patients with Spontaneous Intracerebral Hemorrhage Authors’ Contrib ution: AE 1,2 Xin Xiong 1 Department of Neurology, The First Affiliated Hospital of Chongqing Medical Study Design A University, Chongqing, P.R. China ABG 1 Qi Li Data Collection B 2 Department of Neurology, Chongqing Traditional Chinese Medicine Hospital, BC 3 Wen-Song Yang Statistical Analysis C Chongqing, P.R. China Data Interpr etation D F 4 Xiao Wei 3 Department of Neurology, Yongchuan Hospital of Chongqing Medical University, Manuscript Preparation E Chongqing, P.R. China F 5 Xi Hu Literature Search F 4 Department of Medical Technology, Chongqing Medical and Pharmaceutical B 1 Xing-Chen Wang Funds Collection G College, Chongqing, P.R. China BD 1 Dan Zhu 5 Department of Neurosurgery, The Fourth People’s Hospital of Chongqing, Chongqing, P.R. China BC 1 Rui Li B 1 Du Cao ADG 1 Peng Xie Corresponding Authors: Peng Xie, e-mail: peng_xie@yahoo.com, Qi Li, e-mail: qili_md@126.com Source of support: This study was supported by the National Natural Science Foundation of China (Grant No. 81200899) and the National Key Research and Development Program of China (Grant No. 2017YFA0505700) Background: Early hematoma growth is associated with poor outcome in patients with spontaneous intracerebral hemor- rhage (ICH). The swirl sign (SS) and the black hole sign (BHS) are imaging markers in ICH patients. The aim of this study was to compare the predictive value of these 2 signs for early hematoma growth. Material/Methods: ICH patients were screened for the appearance of the 2 signs within 6 h after onset of symptoms. The sensi- tivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of the 2 signs in predict - ing early hematoma growth were assessed. The accuracy of the 2 signs in predicting early hematoma growth was analyzed by receiver-operator analysis. Results: A total of 200 patients were enrolled in this study. BHS was found in 30 (15%) patients, and SS was found in 70 (35%) patients. Of the 71 patients with early hematoma growth, BHS was found on initial computed to- mography scans in 24 (33.8%) and SS in 33 (46.5%). The sensitivity, specificity, PPV, and NPV of BHS for pre - dicting early hematoma growth were 33.8%, 95.3%, 80.0%, and 72.0%, respectively. The sensitivity, specificity, PPV, and NPV of SS were 46.5%, 71.3%, 47.0%, and 71.0%, respectively. The area under the curve was 0.646 for BHS and 0.589 for SS (P=0.08). Multivariate logistic regression showed that presence of BHS is an indepen- dent predictor of early hematoma growth. Conclusions: The Black hole sign seems to be good predictor for hematoma growth. The presence of swirl sign on admis- sion CT does not independently predict hematoma growth in patients with ICH. MeSH Keywords: Cerebral Hemorrhage • Hematoma • Multidetector Computed Tomography Full-text PDF: https://www.medscimonit.com/abstract/index/idArt/906708 1993 4 2 25 Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Background hematoma before the follow- up CT scan. The demographical data, previous medical history, cigarette smoking, alcohol con- Spontaneous intracerebral hemorrhage (ICH) is an acute neu- sumption, medication history, Glasgow coma scale, and blood rological emergency associated with high morbidity and mor- pressure were recorded. This study was approved by the Ethics tality [1,2]. It is estimated to account for approximately 10% Committee of the First Affiliated Hospital of Chongqing Medical to 20% of all strokes [3]. Early hematoma growth, which oc- University. Written informed consult was obtained from all par- curs in 1/3 of patients when scanned within 6 h, is one of the ticipants or their relatives. most important determinants of mortality and functional out- come [4,5]. The restricting early hematoma growth may be Imaging analysis useful [6]. The computed tomographic angiography (CTA) spot sign (and derived spot sign score) is a reliable sign for pred- The initial and follow-up CT scans were performed using stan- ication of early hematoma growth, early mortality, and poor dard clinical parameters with axial 5-mm section thickness. outcome [7,8]. However, early CTA examination is not avail- The images were obtained and stored for further evaluation. able in all clinical settings. In addition, several renal function Hematoma was assessed and classified as lobar, deep, and in - impairment and allergic reactions to contrast medium restrict fratentorial. According to previous definition, the swirl sign on the CTA examination. the NCCT was defined as follows: (1) a hypo- or iso-attenua - tion region (compared to the attenuation of brain parenchy- In recent years, noncontrast computed tomography (NCCT) im- ma) within the hyperattenuation hematoma; (2) shape may be aging markers, such as blend sign [9], black hole sign (BHS) [10], rounded, streak-like, or irregular [13]. The black hole sign on and hypodensities [11], have been identified as promising im - the NCCT was defined as follows: (1) a hypoattenuation area aging markers for predicting early hematoma growth. The swirl (black hole) encapsulated within the hyperattenuation hema- sign (SS), which was originally described as areas of low at- toma; (2) the black hole could be round, oval, or rodlike, but tenuation or radiolucency within hyperattenuated hematomas, was not connected to the adjacent brain tissue; (3) the black indicates active bleeding in epidural hematoma patient [12]. hole should have a clear border; (4) the hematoma should In a study of 203 patients with acute ICH, Selariu et al. doc- have at least a 28 Hounsfield unit (HU) difference between umented that SS is an independent predictor of death at 1 the 2 density regions [10].Two experienced readers who were month and functional outcome at 3 months [13]. However, blinded to all clinical data and follow-up CT images indepen- the ability of swirl sign to predict early hematoma growth re- dently evaluated the presence of SS and BHS on initial CT im- mains controversial. In 2016, Li et al. first proposed using the ages in all patients. Discrepancies in judging the occurrence of black hole sign to predict early hematoma growth [10]. More SS and BHS were settled by joint discussion of the 2 readers. recently, Yu et al. validated the predictive value of BHS in pre- Early hematoma growth was defined as an increase of hema - dicting early hematoma growth [14], but the predictive val- toma volume >33% or absolute hematoma growth >6 mL from ues of BHS and SS in predicting early hematoma growth have initial CT scan [15]. The hematoma volume was measured by never been compared. Therefore, we performed the present abc/2 formula [16]. Illustrative SS and BHS on initial CT imag- study to investigate the role of BHS and SS in predicting ear- es and follow-up images are shown in Figure 1. ly hematoma growth. Statistical analysis Material and Methods All statistical analyses were performed with commercially available software, SPSS version 19.0 (SPSS, Inc). Continuous Patients variables are expressed as mean (SD) values or median (inter- quartile range [IQR]) values, as appropriate, and discrete vari- We analyzed patients with spontaneous ICH aged >18 years ables are expressed as counts (percentages). Statistical sig- who were admitted to our hospital between July 2011 and nificance was determined by the c test, the Fisher exact test, October 2015 from our prospective ongoing database. The in- the t test, Z test, and the Mann-Whitney test, as appropriate. clusion criteria of this study were as follows: (1) ICH was con- Data with a P value of less than 0.05 were considered signifi - firmed on NCCT scan within 6 h after onset of symptoms; (2) cant. Multivariate logistic regression models were used to in- the follow-up CT scan was obtained within 24 h after the ini- vestigate factors that were independently associated with ear- tial CT scan. The exclusion criteria were as follows: (1) patients ly hematoma growth. Inter-rater reliability of SS and BHS were suffered from brain tumor, head trauma, or arteriovenous mal - estimated by k values. formation, rupture of an intracranial aneurysm, hemorrhag- ic infarction, or primary intraventricular hemorrhage; (2) an- ticoagulation-associated bleeding; (3) surgical evacuation of Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 A B C D Figure 1. Illustration of swirl sign, black hole sign, and follow-up CT images. (A) A 60-year-old man presented with sudden onset of left-sided paralysis. Admission CT image performed 1 h after onset of symptoms showing thalamic ICH with a swirl sign (arrow) and the hematoma volume was 16.57 ml. (B) Hematoma volume remains the same on follow-up CT scan performed 23 h after onset of symptoms. (C) A 75-year-old man with left deep ICH. Initial CT image performed 2 h after onset of symptoms shows black hole sign (arrow). (D) Follow-up CT image 4 h later shows significant hematoma growth. Results in cerebral lobes in 13%, and infratentorial in 7%. Hematoma growth was observed in 71 patients (35.5%) with ICH. There A total of 200 patients (135 men and 65 women) with sponta- were no statistically significant differences in age, sex, hyper - neous ICH fulfilled the inclusion criteria and were enrolled in our tension, diabetes mellitus, smoking, alcohol drinking, and in- study. The mean age of the patients was 60.5±12.4 years (age traventricular hemorrhage. The mean baseline hematoma vol- range, 27–90 years). The hematoma was located deep in 80%, ume was 18.5 ml (interquartile range, 10.3–35.4 ml) in patients Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Table 1. Baseline characteristics between patients with and without hematoma growth. Hematoma growth Hematoma growth Variables P value positive (n=71) negative (n=129) Demographic Mean age, y (SD) 61.5 (12.4) 60.0 (12.4) 0.411 Sex, male, n (%) 53 (74.6) 82 (63.6) 0.109 Medical history Alcohol consumption, n (%) 32 (45.7) 57 (44.5) 0.873 Smoking, n (%) 34 (48.6) 59 (46.1) 0.738 Hypertension, n (%) 48 (68.6) 94 (72.9) 0.522 Diabetes mellitus, n (%) 8 (11.4) 16 (12.4) 0.840 Clinical features Systolic blood pressure, mmHg (SD) 172.5 (29.2) 168.8 (28.2) 0.377 Diastolic blood pressure, mmHg SD) 99.5 (17.5) 97.0 (16.4) 0.320 Baseline hematoma volume, ml(IQR) 18.5 (10.3–35.4) 11.7 (6.7–16.6) <0.001 Onset-to-imaging time, h(IQR) 1 (1–3) 3 (1–4) <0.001 Baseline GCS score, median(IQR) 12 (8–14) 14 (12–15) <0.001 IVH at initial CT, n (%) 24 (33.8) 45 (34.9) 0.878 Black hole sign, n (%) 24 (33.8) 6 (4.7) <0.001 Swirl sign, n (%) 33 (46.5) 37 (28.7) 0.012 Lobar hemorrhage, n (%) 15 (21.1) 11 (8.5) 0.011 Deep hemorrhage, n (%) 52 (73.2) 108 (83.7) 0.076 Infratentorial hemorrhage, n (%) 4 (5.6) 10 (7.8) 0.574 CT – computed tomography; GCS – Glasgow Coma Scale; IVH – intraventricular hemorrhage; IQR – inter-quartile range; SD – standard deviation. with early hematoma growth when compared with 11.7 ml (in- The inter-rater agreement for identifying BHS and SS were 0.939 terquartile range, 6.7–16.6 ml) in patients without early hema- and 0.816, respectively, between the 2 readers. The sensitiv- toma growth (P<0.001). The onset-to-imaging time in patients ity, specificity, and positive and negative predictive value of with early hematoma growth was shorter than that in patients BHS for predicting early hematoma growth were 33.8%, 95.3%, without early hematoma growth (P<0.001). The mean baseline 80.0%, and 72.0%, respectively. The sensitivity, specificity, and Glasgow coma scale score in patients with early hematoma positive and negative predictive value of SS for predicting ear- growth was 12 (interquartile range, 8–14), while that in pa- ly hematoma growth were 46.5%, 71.3%, 47.0%, and 71%, re- tients without early hematoma growth was 14 (interquartile spectively. The receiver operating characteristic (ROC) of the 2 range, 12–15) (P<0.001). Detailed data comparing patients with signs for the prediction of early hematoma growth are shown and without early hematoma growth are displayed in Table 1. in Figure 2. The area under the curve (AUC) was 0.646 for BHS and 0.589 for SS (P=0.08). BHS was found in 30 (15%) of 200 patients with ICH, and SS was found in 70 (35%) of 200 patients with ICH at initial CT. Of In univariate logistic regression, admission Glasgow coma scale, the 71 patients with early hematoma growth, BHS was found on higher baseline hematoma volume, time to CT, and presence of initial CT scans in 24 (33.8%) and the SS in 33 (46.5%). Detailed BHS and SS on initial CT scan were associated with early he- baseline demographic, as well as clinical and radiological char- matoma growth (Table 3). In multivariate logistic regression, acteristics, between patient BHS and SS are displayed in Table 2. the presence of BHS on initial CT remained independently Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Table 2. Baseline characteristics of patients with black hole sign positive and swirl sign positive. Black hole sign Swirl sign Variables positive (n=30) positive (n=70) Demographic Mean age, y (SD) 62.5 (13.0) 61.1 (11.7) Sex, male, n (%) 20 (66.7) 46 (65.7) Medical history Alcohol consumption, n (%) 16 (53.3) 31 (44.3) Smoking, n (%) 16 (53.3) 32 (45.7) Hypertension, n (%) 20 (66.7) 53 (75.7) Diabetes mellitus, n (%) 3 (10) 8 (11.4) Clinical features Systolic blood pressure, mmHg (SD) 164.7 (27.6) 167.1 (26.1) Diastolic blood pressure, mmHg SD) 96.7 (14.5) 94.5 (14.2) Baseline hematoma volume, ml(IQR) 24.3 (14.9–50.8) 18.4 (13.4–29.0) Onset-to-imaging time, h(IQR) 2 (1–3.25) 2 (1–4) Baseline GCS score, median(IQR) 10 (7–14) 12 (8–14) IVH at initial CT, n (%) 11 (36.7) 31 (44.3) Lobar hemorrhage, n (%) 8 (26.7) 11 (15.7) Deep hemorrhage, n (%) 21 (70) 58 (82.9) Infratentorial hemorrhage, n (%) 1 (3.3) 1 (1.4) CT – computed tomography; GCS – Glasgow Coma Scale; IVH – intraventricular hemorrhage; IQR – inter-quartile range; SD – standard deviation. associated with early hematoma growth (odds ratio, 8.51 ROC curve 1.0 [95%CI, 2.55–28.40]; P <0.001). However, SS did not predict early hematoma growth in the multivariate logistic analysis (odds ratio, 0.61 [95%CI, 0.26–1.48]; P=0.276; Table 4). 0.8 0.6 Discussion 0.4 In this study, we found that BHS is more accurate than SS in prediction of early hematoma growth when comparing the 2 Black hole sign 0.2 signs in primary ICH patients. The AUC value of the BHS was Swirl sign Reference line 0.646, which was higher than that of SS (P=0.08). Controversy exists over whether SS is an independent predictor of early he- 0.0 0.0 0.2 0.4 0.6 0.8 1.0 matoma growth. In a study of 203 patients with ICH, Selariu et al. first defined SS as an imaging marker for predicting ear - 1-Specificity ly hematoma growth; the swirl sign was observed in 30% Figure 2. Receiver-operating characteristic (ROC) curve using a (61/203) of ICH patients in their study. However, the ability to binary definition of early hematoma growth. The AUC predict early hematoma growth was not investigated [13]. In value of the black hole sign=0.646 and the AUC value a study of 56 patients with ICH, Kim et al. found SS was ob- of the swirl sign=0.589; P=0.08. served in 13 of 56 (23%) patients with ICH, and SS was not Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Sensitivity Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 Table 3. Univariate analyses for early hematoma growth. Variables Odds ratio 95% Confidence interval P value Age* 1.01 0.99–1.03 0.409 Baseline hematoma volume* 1.08 1.05–1.11 <0.001 Alcohol consumptiom 1.05 0.58–1.88 0.873 Smoking 1.11 0.62–1.98 0.738 Diabetes mellitus 0.91 0.37–2.25 0.840 Onset-to-imaging time* 0.69 0.57–0.84 <0.001 Baseline GCS score* 0.86 0.79–0.94 0.001 IVH at initial CT 0.95 0.52–1.76 0.878 Black hole sign 10.47 4.03–27.22 <0.001 Swirl sign 2.16 1.18–3.95 0.012 Lobar hemorrhage 2.87 1.24–6.66 0.014 Deep hemorrhage 0.53 0.26–1.08 0.079 Infratentorial hemorrhage 0.71 0.22–2.35 0.576 CT – computed tomography; GCS – Glasgow Coma Scale; IVH – intraventricular hemorrhage; IQR – inter-quartile range; SD – standard deviation. * Per unit change in regressor. Table 4. Multivariate analysis for early hematoma growth. Variables Odds ratio 95% Confidence interval P value Black hole sign 8.51 2.55–28.40 <0.001 Swirl sign 0.61 0.26–1.48 0.276 Baseline GCS score* 0.96 0.86–1.07 0.445 Onset-to-imaging time* 0.63 0.50–0.81 <0.001 Baseline hematoma volume* 1.08 1.04–1.12 <0.001 GCS – Glasgow Coma Scale. * Per unit change in regressor. independently predictive of hematoma growth [17]. In anoth- univariate analysis, but after multivariate analysis, SS could er study, Gökçe et al. reported that SS was observed in 36 of not predict early hematoma growth, which is in accordance 45 (80%) patients with ICH [18]. Interestingly, 46.6% (21/45) with most previous studies. In contrast, BHS, as proposed by of patients had anticoagulant-associated ICH, and the time of Li et al. [10], is a novel NCCT for early hematoma growth in pri- flow-up CT varied from 1.5 to 192 h, but they did not define he - mary ICH, with a high inter-rater agreement (0.939). This could matoma growth. In a retrospective study, Connor et al. studied be explained by the rigorous definition of BHS. 71 ICH patients presenting <24 h after onset of symptoms with baseline NCCT, and 24-h follow-up CT [19]. Their study showed BHS and SS are both imaging markers that reflect hemor - SS was observed in 46% (33/71) of patients. Multivariate anal- rhage density heterogeneity. Hematoma growth may occur in ysis demonstrated SS is independently associated with early a cascaded pattern, with initial bleeding causing secondary hematoma growth. Recently, Boulouis et al. [11] reported that peripheral vessels rupture for ongoing bleeding [20,21]. The 207 of 1029 (20%) ICH patients had SS. In univariate analy- CT attenuation of blood is dependent on the time course of sis, SS was associated with early hematoma growth, but in the bleeding [22], so the heterogeneity of the hematoma rep- the multivariable model, SS cannot independently predict he- resents blood of different ages. In addition, the hypoattenu - matoma growth. Strikingly, SS was reported in 20% to 80% ation area may indicate the fresh liquid blood bleeding [23]. of patients with ICH. In our study, SS was observed in 35% of However, the hypoattenuation region that connects to adjacent patients with ICH. SS can predict early hematoma growth in brain tissue may be a normal brain parenchyma, which may Indexed in: [Current Contents/Clinical Medicine] [SCI Expanded] [ISI Alerting System] This work is licensed under Creative Common Attribution- [ISI Journals Master List] [Index Medicus/MEDLINE] [EMBASE/Excerpta Medica] NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) [Chemical Abstracts/CAS] Xiong X et al.: Comparison of swirl sign and black hole sign… CLINICAL RESEARCH © Med Sci Monit, 2018; 24: 567-573 be judged as SS according to Selariu’s definition [13], and this There are several limitations to the present study. Some NCCT might limit the ability to predict early hematoma growth. SS appearances can also predict early hematoma growth, but we has a vague definition, and the evaluation of SS is more sub - only compared SS and BHS because SS and BHS are more com- jective. In BHS, a clear border and a delta of ³28 HU between parable. This was a single-center study, and multicenter stud- the 2 density regions can improve the reliability and subjec- ies are needed to further valuate the predictive value. tivity. Therefore, the inter-rater reliability is higher than with SS. The rigorous definition of BHS results in a high specificity of BHS (95.3%) but a low sensitivity (33.8%). Conclusions Many studies have documented that the CTA spot sign is a To the best of our knowledge, there is no previous study com- good predictor of early hematoma growth [24]. Recent stud- paring SS and BHS in the prediction of early hematoma growth. ies have assessed the correction between CTA spot sign and Our study shows that BHS is be good predictor of hematoma NCCT markers. In a study of 115 patients with ICH, Zheng et growth, but baseline NCCT swirl sign does not independently al. reported that blend sign and CTA spot sign are good pre- predict hematoma growth in patients with ICH. dictors for early hematoma growth [25]. In a study of 129 pa- tients with ICH, Yu et al. demonstrated that the presence of Acknowledgements the BHS is associated with the spot sign, and BHS and CTA spot sign are both predictors of early hematoma growth [14]. We thank the patients who participated in this study and Interestingly, they also found early hematoma growth can oc- made it possible. cur in BHS-positive but CTA spot sign-negative patients. Conflict of interest None. References: 1. Qureshi AI, Tuhrim S, Broderick JP et al: Spontaneous intracerebral hemor- 13. Selariu E, Zia E, Brizzi M, Abul-Kasim K: Swirl sign in intracerebral haemor- rhage. N Engl J Med, 2001; 344(19): 1450–60 rhage: Definition, prevalence, reliability and prognostic value. 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Published: Jan 29, 2018

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