Skip to main content
Download PDF

The length of susceptibility vessel sign predicts early neurological deterioration in minor acute ischemic stroke with large vessel occlusion

BMC Neurology volume 21, Article number: 421 (2021) Cite this article

Abstract

Background

Patients with acute large vessel occlusion (LVO) presenting with minor stroke are at risk of early neurological deterioration (END). The present study aimed to evaluate the frequency and potential predictors of END in patients with medical management and LVO presenting with minor stroke. The relationship between SVS length and END was also investigated.

Methods

This was a prospective multicenter study. Consecutive patients were collected with anterior circulation. LVO presented with minor stroke [National Institutes of Health Stroke Scale (NIHSS) ≤ 4] within 24 h following onset. END was defined as a deterioration of NIHSS ≥4 within 24 h, without parenchymal hemorrhage. The length of the susceptibility vessel sign (SVS) was measured using the T2* gradient echo imaging.

Results

A total of 134 consecutive patients with anterior circulation LVO presenting with minor stroke were included. A total of 27 (20.15%) patients experienced END following admission. Patients with END exhibited longer SVS and higher baseline glucose levels compared with subjects lacking END (P < 0.05). ROC curve analysis indicated that the optimal cutoff point SVS length for END was SVS ≥ 9.45 mm. Multivariable analysis indicated that longer SVS [adjusted odds ratio (aOR), 2.03; 95% confidence interval (CI), 1.45–2.84; P < 0.001] and higher baseline glucose (aOR,1.02; 95% CI, 1.01–1.03; P = 0.009) levels were associated with increased risk of END. When SVS ≥ 9.45 mm was used in the multivariate logistic regression, SVS ≥ 9.45 mm (aOR, 5.41; 95%CI, 1.00–29.27; P = 0.001) and higher baseline glucose [aOR1.01; 95%CI, 1.00–1.03; P = 0.021] were associated with increased risk of END.

Conclusions

END was frequent in the minor stroke patients with large vessel occlusion, whereas longer SVS and higher baseline glucose were associated with increased risk of END. SVS ≥ 9.45 mm was a powerful independent predictor of END.

Peer Review reports

Background

Patients with minor neurological symptoms of acute ischemic stroke (AIS) are frequent. Neurological symptoms account for approximately half of all patients with AIS [1, 2]. Although minor strokes are considered benign, nearly one-third of the subjects affected have a persistent disability [3,4,5]. Previous studies have shown that approximately 30% of minor strokes are caused by acute large vessel occlusion (LVO). The affected patients were at high risk of early neurological deterioration (END) [6, 7].

The susceptibility vessel sign (SVS) on gradient echo (GRE) imaging is defined as a hypointense signal exceeding the diameter of the contralateral artery at the site of the thrombus [8, 9]. The SVS is related to the presence of deoxyhemoglobin, which causes inhomogeneities in local magnetic fields and therefore signal loss on the T2* sequences. Certain studies have suggested that SVS is associated with cardioembolic (CE) subtype [10,11,12] and the characteristics of SVS, such as their diameter and length, may predict stroke subtypes [13].

Recent studies have shown that SVS is significantly associated with lower early [14] or 24-h [13, 15] recanalization rate in the AIS group with intravenous thrombolysis [13,14,15]. Longer thrombus size was independently associated with END in patients with minor stroke and LVO following intravenous thrombolysis [16].

Accurate prediction of END in patients with minor stroke and large vessel occlusion following medical treatment may aid clinicians to select appropriate treatment, such as thrombectomy.

However, the relationship between SVS length and END in patients with minor AIS and LVO receiving medical treatment has been studied to a lesser extent. Therefore, the current study aimed to evaluate the frequency and potential predictors of END in medically managed patients with LVO presenting with minor AIS. Moreover, the relationship between SVS length and END was investigated.

Methods

Study population

The present study was a multicenter prospective study conducted in the three following medical centers: The Second People’s Hospital of Chengdu, Yongchuan Hospital of Chongqing Medical University and the Nuclear Industry 416 Hospital. The patients with AIS were admitted within 24 h of the onset symptoms between May 2014 and September 2020, who were diagnosed as AIS according to the WHO diagnostic criteria and were confirmed with the brain computed tomography (CT) or diffusion-weighted imaging (DWI) using Siemens Magnetom Avan to 1.5 Tesla (Siemens Medical Solutions, Erlangen, Germany) on admission. LVO was confirmed with computed tomography angiography (CTA) or magnetic resonance angiography (MRA). The initial severity of stroke was assessed by the National Institutes of Health Stroke Scale (NIHSS).

Inclusion and exclusion criteria

The patients were enrolled only if they fulfilled the following criteria: 1. Age ≥ 18 years; 2. Admission for first-ever acute ischemic stroke within 24 h; 3. NIHSS≤4; 4.Evidence for ischemic lesions consistent with clinical presentation; 5. Acute LVO in the anterior circulation (defined by occlusion of the intracranial internal carotid artery, proximal segment of the middle cerebral artery [M1 or M2 trunk], or tandem occlusion). 6. All patients received standard therapy (including antiplatelet agents, statins, blood pressure control, or intravenous thrombolysis). The exclusion criteria were the following: 1. Ongoing infection at admission; 2. A history of previous stroke; 3. Moyamoya; 4. Treatment with endovascular therapy (EVT) prior to END; 5. Cerebral hemorrhage, hypoxia (arterial oxyhemoglobin saturation < 90%); 6. Contraindications for MRI examination.

Clinical assessment and definition of END

The characteristics and vascular risk factors of the patients were collected. Blood cell counts, lipid and glucose levels were obtained on admission.

END was defined as neurological symptoms with an increase in the total NIHSS ≥4 that was attributed to the underlying LVO (excluding the subjects related to hemorrhagic transformation or medical complications) within 24 h.

MR imaging was performed on a 1.5 T magnet (Siemens Medical Solutions, Erlangen, Germany) with a phased array head coil. The acquisition parameters for GRE T2* were the following: TR, 800 ms; TE, 30 ms; section thickness, 5 mm; intersection gap, 1 mm; FOV, 250 × 250 mm; flip angle, 20°. All patients were imaged on the same 1.5-T MRI system and the same parameters for GRE T2 were used in three medical centers.

SVS length was measured and its location was noted according to the predefined arterial segments. The in-plane length of the clot corresponded to the distance between the proximal and distal part of the SVS; the length of the clot perpendicular to the axial acquisition plane was obtained by multiplying the number of cross-sectional locations where the clot was visible by the slice thickness (Fig. 1).

Fig. 1
figure 1

Examples of long SVS and short SVS. MRI of 2 patients presenting with long SVS (A and B, white arrow) and short SVS (C and D, white arrow); A and C, axial views of T2*-GRE; B, MRA; D, CTA

Full size image

All generated images were stored on a CD-ROM with the visualization software (Siemens Germany). Two radiologists independently reviewed all MRI images without the clinical data and potential disagreements were resolved by discussion.

Statistical analysis

Firstly, patients were classified into no END and END groups. The data are presented as median values (interquartile range [IQR]), numbers (%), or mean values (±standard deviation). To identify the differences between subgroups, the Pearson χ2 test was used for categorical variables. The distributions of the continuous variables were determined by the Kolmogorov–Smirnov test, while the Mann–Whitney two sample test was applied in case of non-normal distributions. Secondly, receiver operating characteristic (ROC) curve analysis was used to evaluate sensitivity, specificity and to determine the optimal cutoff point of length of SVS for END. Thirdly, the variables associated with END in the univariate analyses with a P-value < 0.20 were included in the multivariate analysis. Subsequently logistic regressions analyses were performed to determine the association between specific factors and END. The results were expressed as adjusted odds ratios (aOR) with the corresponding 95% confidence interval (CI). The data were analyzed using SPSS software (SPASS 22.0). P < 0.05 was considered to indicate statistically significant differences.

Results

Characteristics of the study subjects

A total of 174 patients with acute LVO presenting with minor stroke were enrolled at the three centers. Among them, 2 patients demonstrated infection at admission, whereas 17 patients exhibited a history of previous stroke, 1 had Moyamoya disease and 3 had cerebral hemorrhage transformation. A total of 11 subjects had contraindications for MRI examination, while 6 patients were directly transferred for EVT. The remaining 134 patients were recruited. The mean age was 67.01 ± 10.15 years (45.8–96.8 years) and the sample size comprised 50% (67) men. In the study population, 111 patients had a history of hypertension, 51 presented with a history of diabetes, 90 exhibited a history of hyperlipidemia, 24 were current smokers and 33 were current alcohol drinkers. The occlusion sites were intracranial ICA in 34 patients (25.37%), MCA M1 in 65 patients (48.51%) and MCA M2 in 35 patients (26.12%). The median NIHSS score at admission was 2 (interquartile range, 1–3). A total of 35 (26.12%) patients underwent intravenous thrombolysis. Among them, 27 (20.15%) patients experienced END following admission.

Evaluation of the prognostic value of SVS for END

ROC curve analysis indicated high accuracy for SVS in order to predict END with AUC of 0.74 (95% CI 0.63 to 0.84) (Fig. 2). By using a cutoff value of SVS ≥ 9.45 mm, the sensitivity and specificity was 77.78 and 56.07%, respectively, which provided a positive predictive value (PPV) for END of 30.89% and a negative predictive value (NPV) of 90.91%.

Fig. 2
figure 2

Receiver operating characteristic curve analysis for SVS. The curve was used for determining the prognostic value of END

Full size image

Univariable models for predictors of END

A total of 27 (20.15%) patients experienced END following admission. Patients with SVS ≥ 9.45 mm experienced more END [30.88% (21/68) versus 9.09% (6/66), P = 0.002]. The baseline characteristics of patients in the no END and END groups were compared (Table 1). At baseline, patients with END indicated significantly higher baseline glucose levels (156.88 ± 43.67 vs. 128.75 ± 39.95, P < 0.001), and longer SVS [10.68(9.70–13.25) vs. 9.13(7.73–10.41), P < 0.001] than patients with no END. No significant differences were noted in the occlusion site between the groups with or without END (P > 0.05).

Table 1 Comparison of baseline characteristics between patients with no END and END
Full size table

Multivariable models on the association between SVS ≥ 9.45 mm and END

In the unadjusted models, an association between SVS ≥ 9.45 mm and END was noted (OR, 4.66; 95%CI, 3.24–6.72, P < 0.001). When the factors were associated with END in the univariate analyses (P < 0.20) they were used into the multivariate logistic regression analysis (adjustment for SVS value, baseline glucose, hypertension, current smoking, cardiac embolism, undetermined stroke). The results indicated that longer SVS [aOR, 2.03; 95%CI, 1.45–2.84; P < 0.001] and higher baseline glucose (aOR, 1.02; 95% CI, 1.01–1.03; P = 0.009) were associated with increased risk of END. When SVS ≥ 9.45 mm was used in the multivariate logistic regression, (aOR, 5.41; 95%CI, 1.00–29.27; P = 0.001), higher baseline glucose levels (aOR1.01; 95%CI, 1.00–1.03; P = 0.021] were associated with increased risk of END (Table 2).

Table 2 Multivariable models showing predictors of END
Full size table

Discussion

The present study indicated that 20.15% (27) of patients experienced END in minor stroke with LVO. The optimal length of SVS for predicting END was SVS ≥ 9.45 mm. Furthermore, we found that higher baseline glucose levels and longer SVS were associated with increased risk of END in patients with minor stroke and LVO.

Various acute AIS patients experience neurological deterioration during hospitalization. The common feature for neurological deterioration in these patients is the presence of an underlying LVO [17,18,19,20]. According to previous studies, END incidence ranged from 12 to 40% in patients with minor AIS and LVO [16, 21, 22]. A recent study indicated that the incidence of END in mild stroke patients (NIHSS≤5) with LVO was 19.7% [22], whereas another study reported that END occurred in 39.4% in minor stroke and LVO [21]. In a previous study conducted in France, the results indicated that END occurred in 12.1% patients with minor stroke and LVO was intended for intravenous thrombolysis alone [16]. These differences may reflect the clinical environment following stroke, including the inconsistent definitions of neurological deterioration, the medical conditions in the hospital, the differences in nursing conditions and the admission of the patients to the stroke unit. Our findings are in line with the results reported from previously published studies [16, 21,22,23].

A previous study indicated that the site of occlusion was the predictor of the risk of END, which was reported to be more frequent in the carotid terminus and in the tandem occlusions [23]. However, the applicability of these findings to LVO strokes is questionable since these studies included patients with no LVO stroke, patients with moderate to severe stroke, or exhibited small sample size and inconsistent definitions of END. No statistical differences were noted in the occlusion site between the groups with or without END. These differences may be due to the inclusion of patients with more proximal anterior circulation occlusions (intracranial internal carotid artery, middle cerebral artery M1/2, or tandem occlusion) in the current study. Based on magnetic resonance imaging (MRI) and T2*-gradient echo imaging sequence (T2*-gradient echo imaging), the thrombus with high red blood cell content exhibited low signals, which is termed susceptible vessel sign (SVS)+. SVS is related to the presence of deoxyhemoglobin, which leads to the inhomogeneity of local magnetic field and the loss of the T2* signal. Previous studies indicated that decreased SVS length was associated with increased recanalization rate [24,25,26]. In the present study, we aimed to investigate the association between SVS length and END in patients with minor stroke and LVO. The data demonstrated that longer SVS was associated with increased risk of END in patients with minor stroke and LVO. The END group exhibited a significantly higher SVS than that of the non-END group. The results were consistent with those reported in previous studies [16].

Although the exact mechanisms of END are unclear, one hypothesis is that the symptomatic ischemic tissue (i.e. infarct core and/or penumbra) is extended into the surrounding asymptomatic tissue [27,28,29]. Only emboli containing deoxyhemoglobin or hemosiderin can be identified as SVS. In other words, SVS is a predictor of older thrombosis. Longer SVS represent a higher clot burden, which is associated with decreased effectiveness of medical treatment and leads to secondary hemodynamic and metabolic disorders. It may be the mechanism of END in patients with minor stroke presented with LVO.

In a previous study, it was shown that thrombus length>9 mm was a powerful predictor of lack of early recanalization following intravenous thrombolysis [14]. In the present study, the optimal cutoff point of SVS length for END was SVS ≥ 9.45 mm. However, following adjustment for confounders, a significant association of SVS ≥ 9.45 mm was noted with risks of END in patients with minor stroke and LVO. Therefore, longer thrombus length (especially> 9 mm) was associated with poor prognosis [14, 16]. The results of the present study indicated that the length of SVS was a valuable marker of END in patients following minor stroke.

It has been shown that patients with hyperglycemia exhibit increased risk for stroke and notably ischemic stroke [30]. Elevated levels of blood glucose in the peri-infarct period are closely associated with poor outcome in patients with AIS [31,32,33,34]. In patients with END, blood glucose levels were significantly elevated and the possible mechanisms associated with this outcome included poor collateral flow and endothelial cell injury, oxidative stress and lactic acid increase, glucose and energy metabolism disorders. In the present study, higher baseline glucose levels were associated with increased risk of END, which was consistent with previous studies [31,32,33,34].

Given the correlation between END and SVS length in patients with mild stroke with LVO, restoration of perfusion is considered a potential treatment strategy for patients at high risk of END. EVT may be a treatment option for patients with long SVS. However, further clinical trials should be designed to demonstrate the benefit of immediate EVT in patients with minor stroke and LVO who are at high risk for END.

The present study contains certain limitations that merit consideration. Firstly, in the present study, data on stroke volume were not available. Secondly, we did not analyze the perfusion images, which may influence the results. Thirdly, SVS was detected using MRI, which required longer time than computed tomography in LVO. MRI was not available for certain stroke patients. However, despite these limitations, the present study was a multicenter clinical study, which required the collection of several important clinical data and the adjustment of data analyses for a wide variety of confounding factors. The results of this study were useful for clinical treatment.

Conclusions

In conclusion, the present study indicated that END was frequent in minor stroke patients with LVO. Longer SVS and that higher baseline glucose levels were associated with increased risk of END. Moreover, SVS ≥ 9.45 mm was a powerful independent predictor of END. The END prediction is very important, which can reduce mortality and improve the outcome. Length SVS may have potential predictive value in risk stratification of ischemic stroke, which may help to select high-risk patients to initiate intervention in time. The results of the present study imply that this method may be applicable in AIS management.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

CI:

Confidence Interval

M:

Mean

OR:

Odds Ratio

SD:

Standard Deviation

END:

Early neurological deterioration

LVO:

Large vessel occlusion

NIHSS:

National Institutes of Health Stroke Scale

SVS:

Susceptibility vessel sign (SVS)

IQR:

Interquartile range

LAA:

Large-artery atherothrombosis

TOAST:

Trial of Org 10,172 in Acute Stroke Treatment

EVT:

Endovascular therapy

IVT:

Intravenous thrombolysis

References

  1. Heldner MR, Zubler C, Mattle HP, Schroth G, Weck A, Mono ML, et al. National Institutes of Health stroke scale score and vessel occlusion in 2152 patients with acute ischemic stroke. Stroke. 2013;44(4):1153–7. https://doi.org/10.1161/STROKEAHA.111.000604.

    Article  PubMed  Google Scholar 

  2. Reeves M, Khoury J, Alwell K, Moomaw C, Flaherty M, Woo D, et al. Distribution of national institutes of health stroke scale in the Cincinnati/Northern Kentucky stroke study. Stroke. 2013;44(11):3211–3. https://doi.org/10.1161/STROKEAHA.113.002881.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Spokoyny I, Raman R, Ernstrom K, Khatri P, Meyer DM, Hemmen TM, et al. Defining mild stroke: outcomes analysis of treated and untreated mild stroke patients. J Stroke Cerebrovasc Dis. 2015;24(6):1276–81. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.01.037.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Khatri P, Conaway MR, Johnston KC. Acute stroke accurate prediction study (ASAP) investigators. Ninety-day outcome rates of a prospective cohort of consecutive patients with mild ischemic stroke. Stroke. 2012;43(2):560–2. https://doi.org/10.1161/STROKEAHA.110.593897.

    Article  PubMed  Google Scholar 

  5. Romano JG, Smith EE, Liang L, Gardener H, Camp S, Shuey L, et al. Outcomes in mild acute ischemic stroke treated with intravenous thrombolysis: a retrospective analysis of the get with the guidelines-stroke registry. JAMA Neurol. 2015;72(4):423–31. https://doi.org/10.1001/jamaneurol.2014.4354.

    Article  PubMed  Google Scholar 

  6. Rajajee V, Kidwell C, Starkman S, Ovbiagele B, Alger JR, Villablanca P, et al. Early MRI and outcomes of untreated patients with mild or improving ischemic stroke. Neurology. 2006;67(6):980–4. https://doi.org/10.1212/01.wnl.0000237520.88777.71.

    Article  CAS  PubMed  Google Scholar 

  7. Kim JT, Park MS, Chang J, Lee JS, Choi KH, Cho KH. Proximal arterial occlusion in acute ischemic stroke with low NIHSS scores should not be considered as mild stroke. PLoS One. 2013;8(8):e70996. https://doi.org/10.1371/journal.pone.0070996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Brinjikji W, Duffy S, Burrows A, Hacke W, Liebeskind D, Majoie CBLM, et al. Correlation of imaging and histopathology of thrombi in acute ischemic stroke with etiology and outcome: a systematic review. J Neurointerv Surg. 2017;9(6):529–34. https://doi.org/10.1136/neurintsurg-2016-012391.

    Article  PubMed  Google Scholar 

  9. Liebeskind DS, Sanossian N, Yong WH, Starkman S, Tsang MP, Moya AL, et al. CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke. 2011;42(5):1237–43. https://doi.org/10.1161/STROKEAHA.110.605576.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Horie N, Tateishi Y, Morikawa M, Morofuji Y, Hayashi K, Izumo T, et al. Acute stroke with major intracranial vessel occlusion:characteristics of cardioembolism and atherosclerosis-related in situ stenosis/occlusion. J Clin Neurosci. 2016;32:24–9. https://doi.org/10.1016/j.jocn.2015.12.043.

    Article  PubMed  Google Scholar 

  11. Kim SK, Yoon W, Kim TS, Kim HS, Heo TW, Park MS. Histologic analysis of retrieved clots in acute ischemic stroke: correlation with stroke etiology and gradient-echo MRI. AJNR Am J Neuroradiol. 2015;36(9):1756–62. https://doi.org/10.3174/ajnr.A4402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Liebeskind DS, Sanossian N, Yong WH, Starkman S, Tsang MP, Moya AL, et al. Saver JL.CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke. 2011;42(5):1237–43. https://doi.org/10.1161/STROKEAHA.110.605576.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Liu M, Li L, Li G. The different clinical value of susceptibility vessel sign in acute ischemic stroke patients under different interventional therapy: a systematic review and meta-analysis. J Clin Neurosci. 2019;62:72–9. https://doi.org/10.1016/j.jocn.2019.01.002.

    Article  PubMed  Google Scholar 

  14. Seners P, Delepierre J, Turc G, Henon H, Piotin M, Arquizan C, et al. Thrombus length predicts lack of post-thrombolysis early recanalization in minor stroke with large vessel occlusion. Stroke. 2019;50(3):761–4. https://doi.org/10.1161/STROKEAHA.118.023455.

    Article  PubMed  Google Scholar 

  15. Legrand L, Naggara O, Turc G, Mellerio C, Roca P, Calvet D, et al. Clot burden score on admission T2*-MRI predicts recanalization in acute stroke. Stroke. 2013;44(7):1878–84. https://doi.org/10.1161/STROKEAHA.113.001026.

    Article  CAS  PubMed  Google Scholar 

  16. Seners P, Ben Hassen W, Lapergue B, Arquizan C, Heldner MR, Henon H, et al. Prediction of early neurological deterioration in individuals with minor stroke and large vessel occlusion intended for intravenous thrombolysis alone. JAMA Neurol. 2021;78(3):321–8. https://doi.org/10.1001/jamaneurol.2020.4557.

    Article  PubMed  Google Scholar 

  17. Rajajee V, Kidwell C, Starkman S, Ovbiagele B, Alger JR, Villablanca P, et al. Early MRI and outcomes of untreated patients with mild or improving ischemic stroke. Neurology. 2006;67(2):980–4. https://doi.org/10.1212/01.wnl.0000237520.88777.71.

    Article  CAS  PubMed  Google Scholar 

  18. Kim JT, Park MS, Chang J, Lee JS, Choi KH, Cho KH. Proximal arterial occlusion in acute ischemic stroke with low NIHSS scores should not be considered as mild stroke. PLoS One. 2013;8:e70996. https://doi.org/10.1371/journal.pone.0070996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kim JT, Heo SH, Yoon W, Choi KH, Park MS, Saver JL, et al. Clinical outcomes of patients with acute minor stroke receiving rescue IA therapy following early neurological deterioration. J Neurointerv Surg. 2016;8(5):461–5. https://doi.org/10.1136/neurintsurg-2015-011690.

    Article  PubMed  Google Scholar 

  20. Griessenauer CJ, Medin C, Maingard J, Chandra RV, Ng W, Brooks DM, et al. Endovascular mechanical thrombectomy in large-vessel occlusion ischemic stroke presenting with low national institutes of health stroke scale: systematic review and meta-analysis. World Neurosurg. 2018;110:263–9. https://doi.org/10.1016/j.wneu.2017.11.076.

    Article  PubMed  Google Scholar 

  21. Gwak DS, Kwon JA, Shim DH, Kim YW, Hwang YH. Perfusion and diffusion variables predict early neurological deterioration in minor stroke and large vessel occlusion. J Stroke. 2021;23(1):61–8. https://doi.org/10.5853/jos.2020.01466.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Saleem Y, Nogueira RG, Rodrigues GM, Kim S, Sharashidze V, Frankel M, et al. Acute neurological deterioration in large vessel occlusions and mild symptoms managed medically. Stroke. 2020;51(5):1428–34. https://doi.org/10.1161/STROKEAHA.119.027011.

    Article  PubMed  Google Scholar 

  23. Mazya MV, Cooray C, Lees KR, Toni D, Ford GA, Bar M, et al. Minor stroke due to large artery occlusion. When is intravenous thrombolysis not enough? Results from the SITS International Stroke Thrombolysis Register. Eur Stroke J. 2018;3(1):29–38. https://doi.org/10.1177/2396987317746003.

    Article  PubMed  Google Scholar 

  24. Kimura K, Iguchi Y, Shibazaki K, Watanabe M, Iwanaga T, Aoki J. M1 susceptibility vessel sign on T2* as a strong predictor for no early recanalization after IV-t-PA in acute ischemic stroke. Stroke. 2009;40(9):3130–22. https://doi.org/10.1161/STROKEAHA.109.552588.

    Article  CAS  PubMed  Google Scholar 

  25. Aoki J, Kimura K, Shibazaki K, Sakamoto Y, Saji N, Uemura J. Location of the susceptibility vessel sign on T2*-weighted MRI and early recanalization within 1 hour after tissue plasminogen activator administration. Cerebrovasc Dis Extra. 2013;3(1):111–20. https://doi.org/10.1159/000354848.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cho KH, Kim JS, K won SU, Cho AH, Kang DW. Significance of susceptibility vessel sign on T2*-weighted gradient echo imaging for identification of stroke subtypes. Stroke. 2005;36(1):2379–83. https://doi.org/10.1161/01.STR.0000185932.73486.7a.

    Article  PubMed  Google Scholar 

  27. Alawneh JA, Moustafa RR, Baron JC. Hemodynamic factors and perfusion abnormalities in early neurological deterioration. Stroke. 2009;40(6):e443–50. https://doi.org/10.1161/STROKEAHA.108.532465.

    Article  PubMed  Google Scholar 

  28. Tisserand M, Seners P, Turc G, Legrand L, Labeyrie MA, Charron S, et al. Mechanisms of unexplained neurological deterioration after intravenous thrombolysis. Stroke. 2014;45(12):3527–34. https://doi.org/10.1161/STROKEAHA.114.006745.

    Article  CAS  PubMed  Google Scholar 

  29. Fu J, Zhou Y, Li Q, Zhong G, Zhang S, Zhang R, et al. Perfusion changes of unexplained early neurological deterioration after reperfusion therapy. Transl Stroke Res. 2020;11(2):195–203. https://doi.org/10.1007/s12975-019-00723-w.

    Article  PubMed  Google Scholar 

  30. Wang F, Jiang B, Kanesan L, Zhao Y, Yan B. Higher admission fasting plasma glucose levels are associated with a poorer short-term neurologic outcome in acute ischemic stroke patients with good collateral circulation. Acta Diabetol. 2018;55(7):703–14. https://doi.org/10.1007/s00592-018-1139-6.

    Article  CAS  PubMed  Google Scholar 

  31. Gordon WR, Salamo RM, Behera A, Chibnall J, Alshekhlee A, Callison RC, et al. Association of blood glucose and clinical outcome after mechanical thrombectomy for acute ischemic stroke. Interv Neurol. 2018;7(3–4):182–8. https://doi.org/10.1159/000486456.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Simonsen CZ, Schmitz ML, Madsen MH, Mikkelsen IK, Chandra RV, Leslie-Mazwi T, et al. Early neurological deterioration after thrombolysis: clinical and imaging predictors. Int J Stroke. 2016;11(7):776–82. https://doi.org/10.1177/1747493016650454.

    Article  PubMed  Google Scholar 

  33. Huang ZX, Huang Y, Zeng J, Hao H, Petroski GF, Lu H, et al. Admission glucose levels may increase the risk for early neurological deterioration in females with acute ischemic stroke. Front Neurol. 2020;11:548892. https://doi.org/10.3389/fneur.2020.548892.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yi X, Wang C, Liu P, Fu C, Lin J, Chen Y. Antiplatelet drug resistance is associated with early neurological deterioration in acute minor ischemic stroke in the Chinese population. J Neurol. 2016;263(8):1612–9. https://doi.org/10.1007/s00415-016-8181-5.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank all patients and their families for generously consenting to the use of human tissues in the current research.

Funding

This work was funded by the Health and Family Planning Commission of Chengdu (2015009), the Chengdu Medical College Natural Science Foundation (CYZ18-33, CYZ19-33), the Sichuan Provincial Education Department (17ZA0134), the Sichuan Medical Association (S18023), the Chengdu Science and Technology Bureau focuses on research and development support plan (2019-YF09-00097-SN), the popular scientific research project of Sichuan Health Commission (20PJ171) and Sichuan undergraduate innovation and startup program funding support (S201913705080, S201913705130, S201913705059, S202013705070, S202013705075, S202013705108). Yunnan Education Bureau (SYSX202036) was not involved in the database management (collection, analysis, interpretation of data) and had no access to patient information. The funding body did not participate in designing the study or writing the manuscript. The study protocol had undergone peer-review process by the funding body.

Author information

Authors and Affiliations

  1. Department of Neurology, The Second People’s Hospital of Chengdu, Chengdu, 610021, People’s Republic of China

    Lanying He, Jian Wang, Feng Wang & Lili Zhang

  2. Department of Neurology, The Second Affiliated Hospital of Chengdu College, Nuclear Industry 416 Hospital, Chengdu, 610021, People’s Republic of China

    Lijuan Zhang

  3. Department of Neurology, Yongchuan Hospital, Chongqing Medical University, Chongqing, 610020, People’s Republic of China

    Wang Zhao

  4. Beijing Institute of Basic Medical Sciences, Beijing, 100850, China

    Xiechuan Weng

  5. School of Public Health Chengdu Medical College, Chengdu, 610500, Sichuan, China

    Fan Xu

Authors
  1. Lanying He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Feng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lili Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lijuan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiechuan Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LYH was responsible for the concept and design of the study, data collection and analysis and the first draft of the paper and final manuscript. JW, XW, FX were responsible for the concept and design of the study, data analysis and interpretation. FW was responsible for overseeing the concept and design of the study, data analysis and interpretation and drafting the paper for important intellectual content. LLZ, LJZ and WZ were responsible for data collection. All authors read and approved the final version of the manuscript intended for publication.

Corresponding authors

Correspondence to Xiechuan Weng or Fan Xu.

Ethics declarations

Ethics approval and consent to participate

We obtained ethical approval for this study from the Medical and Health Research Ethics Committee of the Second People’s Hospital of Chengdu, Medical and Health Research Ethics Committee of the Yongchuan Hospital of Chongqing Medical University and Medical and Health Research Ethics Committee of Nuclear Industry 416 Hospital. The current study was carried out according to the Declaration of Helsinki. Prior to enrollment, all patients or their legal proxies provided detailed information regarding the aims, scope and possible consequences of the trial by a physician. No diagnostic or interventional procedures were required for the clinical trial. Written informed consent was obtained from all study participants or their legal proxies.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, L., Wang, J., Wang, F. et al. The length of susceptibility vessel sign predicts early neurological deterioration in minor acute ischemic stroke with large vessel occlusion. BMC Neurol 21, 421 (2021). https://doi.org/10.1186/s12883-021-02455-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12883-021-02455-7

Keywords

BMC Neurology

ISSN: 1471-2377

Contact us