Skip to main content
Top
Published in: International Journal of Computer Assisted Radiology and Surgery 9/2020

01-09-2020 | Stroke | Original Article

Automatic collateral circulation scoring in ischemic stroke using 4D CT angiography with low-rank and sparse matrix decomposition

Authors: Mumu Aktar, Donatella Tampieri, Hassan Rivaz, Marta Kersten-Oertel, Yiming Xiao

Published in: International Journal of Computer Assisted Radiology and Surgery | Issue 9/2020

Login to get access

Abstract

Purpose

Sufficient collateral blood supply is crucial for favorable outcomes with endovascular treatment. The current practice of collateral scoring relies on visual inspection and thus can suffer from inter and intra-rater inconsistency. We present a robust and automatic method to score cerebral collateral blood supply to aid ischemic stroke treatment decision making. The developed method is based on 4D dynamic CT angiography (CTA) and the ASPECTS scoring protocol.

Methods

The proposed method, ACCESS (Automatic Collateral Circulation Evaluation in iSchemic Stroke), estimates a target patient’s unfilled cerebrovasculature in contrast-enhanced CTA using the lack of contrast agent due to clotting. To do so, the fast robust matrix completion algorithm with in-face extended Frank–Wolfe optimization is applied on a cohort of healthy subjects and a target patient, to model the patient’s unfilled vessels and the estimated full vasculature as sparse and low-rank components, respectively. The collateral score is computed as the ratio of the unfilled vessels to the full vasculature, mimicking existing clinical protocols.

Results

ACCESS was tested with 46 stroke patients and obtained an overall accuracy of 84.78%. The optimal threshold selection was evaluated using a receiver operating characteristics curve with the leave-one-out approach, and a mean area under the curve of 85.39% was obtained.

Conclusion

ACCESS automates collateral scoring to mitigate the shortcomings of the standard clinical practice. It is a robust approach, which resembles how radiologists score clinical scans, and can be used to help radiologists in clinical decisions of stroke treatment.
Literature
1.
go back to reference Ashikuzzaman M, Belasso C, Kibria MG, Bergdahl A, Gauthier CJ, Rivaz H (2019) Low rank and sparse decomposition of ultrasound color flow images for suppressing clutter in real-time. IEEE Trans Med Imaging. 39(4):1073–1084PubMed Ashikuzzaman M, Belasso C, Kibria MG, Bergdahl A, Gauthier CJ, Rivaz H (2019) Low rank and sparse decomposition of ultrasound color flow images for suppressing clutter in real-time. IEEE Trans Med Imaging. 39(4):1073–1084PubMed
2.
go back to reference Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12(1):26–41PubMed Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12(1):26–41PubMed
3.
go back to reference Boers A, Barros RS, Jansen I, Berkhemer O, Beenen L, Menon BK, Dippel D, van der Lugt A, van Zwam W, Roos Y, van Oostenbrugge RJ (2018) Value of quantitative collateral scoring on CT angiography in patients with acute ischemic stroke. Am J Neuroradiol 39(6):1074–1082PubMedPubMedCentral Boers A, Barros RS, Jansen I, Berkhemer O, Beenen L, Menon BK, Dippel D, van der Lugt A, van Zwam W, Roos Y, van Oostenbrugge RJ (2018) Value of quantitative collateral scoring on CT angiography in patients with acute ischemic stroke. Am J Neuroradiol 39(6):1074–1082PubMedPubMedCentral
4.
go back to reference Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20(1):37–46 Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20(1):37–46
5.
go back to reference Coutts SB, Hill MD, Demchuk AM, Barber PA, Pexman J, Buchan A, Mak H, Yau K, Chan B (2003) ASPECTS reading requires training and experience. Stroke 34(10):e179PubMed Coutts SB, Hill MD, Demchuk AM, Barber PA, Pexman J, Buchan A, Mak H, Yau K, Chan B (2003) ASPECTS reading requires training and experience. Stroke 34(10):e179PubMed
7.
go back to reference Fawcett T (2006) An introduction to ROC analysis. Pattern Recognit Lett 27(8):861–874 Fawcett T (2006) An introduction to ROC analysis. Pattern Recognit Lett 27(8):861–874
8.
go back to reference Fleiss JL (1971) Measuring nominal scale agreement among many raters. Psychol Bull 76(5):378 Fleiss JL (1971) Measuring nominal scale agreement among many raters. Psychol Bull 76(5):378
9.
go back to reference Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL, Group BDC (2011) Unbiased average age-appropriate atlases for pediatric studies. Neuroimage 54(1):313–327PubMed Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL, Group BDC (2011) Unbiased average age-appropriate atlases for pediatric studies. Neuroimage 54(1):313–327PubMed
10.
go back to reference Freund RM, Grigas P, Mazumder R (2017) An extended Frank–Wolfe method with “in-face” directions, and its application to low-rank matrix completion. SIAM J Optim 27(1):319–346 Freund RM, Grigas P, Mazumder R (2017) An extended Frank–Wolfe method with “in-face” directions, and its application to low-rank matrix completion. SIAM J Optim 27(1):319–346
11.
go back to reference Frolich AM, Wolff SL, Psychogios MN, Klotz E, Schramm R, Wasser K, Knauth M, Schramm P (2014) Time-resolved assessment of collateral flow using 4D CT angiography in large-vessel occlusion stroke. Eur Radiol 24(2):390–396PubMed Frolich AM, Wolff SL, Psychogios MN, Klotz E, Schramm R, Wasser K, Knauth M, Schramm P (2014) Time-resolved assessment of collateral flow using 4D CT angiography in large-vessel occlusion stroke. Eur Radiol 24(2):390–396PubMed
12.
go back to reference Grotta JC, Chiu D, Lu M, Patel S, Levine SR, Tilley BC, Brott TG, HaleyJr EC, Lyden PD, Kothari R, Franke M, Lewandowski CA, Libman R, Kwiatkowski T, Broderick JP, Marler JR, Corrigan J, Huff S, Mitsias P, Talati S, Tanne D (1999) Agreement and variability in the interpretation of early CT changes in stroke patients qualifying for intravenous rtPA therapy. Stroke 30(8):1528–1533PubMed Grotta JC, Chiu D, Lu M, Patel S, Levine SR, Tilley BC, Brott TG, HaleyJr EC, Lyden PD, Kothari R, Franke M, Lewandowski CA, Libman R, Kwiatkowski T, Broderick JP, Marler JR, Corrigan J, Huff S, Mitsias P, Talati S, Tanne D (1999) Agreement and variability in the interpretation of early CT changes in stroke patients qualifying for intravenous rtPA therapy. Stroke 30(8):1528–1533PubMed
13.
go back to reference Grunwald IQ, Kulikovski J, Reith W, Gerry S, Namias R, Politi M, Papanagiotou P, Essig M, Mathur S, Joly O, Hussain K, Wagner V, Shah S, Harston G, Vlahovic J, Walter S, Podlasek A, Fassbenderh K (2019) Collateral automation for triage in stroke: evaluating automated scoring of collaterals in acute stroke on computed tomography scans. Cerebrovasc Dis 47(5–6):217–222PubMed Grunwald IQ, Kulikovski J, Reith W, Gerry S, Namias R, Politi M, Papanagiotou P, Essig M, Mathur S, Joly O, Hussain K, Wagner V, Shah S, Harston G, Vlahovic J, Walter S, Podlasek A, Fassbenderh K (2019) Collateral automation for triage in stroke: evaluating automated scoring of collaterals in acute stroke on computed tomography scans. Cerebrovasc Dis 47(5–6):217–222PubMed
14.
go back to reference Huck J, Wanner Y, Fan AP, Jäger AT, Grahl S, Schneider U, Villringer A, Steele CJ, Tardif CL, Bazin PL, Gauthier CJ (2019) High resolution atlas of the venous brain vasculature from 7 T quantitative susceptibility maps. Brain Struct Funct 224(7):2467–2485PubMed Huck J, Wanner Y, Fan AP, Jäger AT, Grahl S, Schneider U, Villringer A, Steele CJ, Tardif CL, Bazin PL, Gauthier CJ (2019) High resolution atlas of the venous brain vasculature from 7 T quantitative susceptibility maps. Brain Struct Funct 224(7):2467–2485PubMed
15.
go back to reference Jerman T, Pernuš F, Likar B, Špiclin Ž (2016) Enhancement of vascular structures in 3D and 2D angiographic images. IEEE Trans Med Imaging 35(9):2107–2118PubMed Jerman T, Pernuš F, Likar B, Špiclin Ž (2016) Enhancement of vascular structures in 3D and 2D angiographic images. IEEE Trans Med Imaging 35(9):2107–2118PubMed
16.
go back to reference Jin M, Hao D, Ding S, Qin B (2018) Low-rank and sparse decomposition with spatially adaptive filtering for sequential segmentation of 2D+t vessels. Phys Med Biol 63(17):17LT01PubMed Jin M, Hao D, Ding S, Qin B (2018) Low-rank and sparse decomposition with spatially adaptive filtering for sequential segmentation of 2D+t vessels. Phys Med Biol 63(17):17LT01PubMed
17.
go back to reference Kersten-Oertel M, Alamer A, Fonov V, Lo B, Tampieri D, Collins L (2016) Towards a computed collateral circulation score in ischemic stroke. arXiv preprint arXiv:2001.07169 Kersten-Oertel M, Alamer A, Fonov V, Lo B, Tampieri D, Collins L (2016) Towards a computed collateral circulation score in ischemic stroke. arXiv preprint arXiv:​2001.​07169
19.
go back to reference Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174PubMed Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174PubMed
20.
go back to reference Lin Z, Chen M, Ma Y (2010) The augmented lagrange multiplier method for exact recovery of corrupted low-rank matrices. arXiv preprint arXiv:1009.5055 Lin Z, Chen M, Ma Y (2010) The augmented lagrange multiplier method for exact recovery of corrupted low-rank matrices. arXiv preprint arXiv:​1009.​5055
21.
go back to reference Meijs M, Patel A, van de Leemput SC, Prokop M, van Dijk EJ, de Leeuw FE, Meijer FJ, van Ginneken B, Manniesing R (2017) Robust segmentation of the full cerebral vasculature in 4D CT of suspected stroke patients. Sci Rep 7(1):1–12 Meijs M, Patel A, van de Leemput SC, Prokop M, van Dijk EJ, de Leeuw FE, Meijer FJ, van Ginneken B, Manniesing R (2017) Robust segmentation of the full cerebral vasculature in 4D CT of suspected stroke patients. Sci Rep 7(1):1–12
22.
go back to reference Moccia S, De Momi E, El Hadji S, Mattos LS (2018) Blood vessel segmentation algorithms-review of methods, datasets and evaluation metrics. Comput Methods Programs Biomed 158:71–91PubMed Moccia S, De Momi E, El Hadji S, Mattos LS (2018) Blood vessel segmentation algorithms-review of methods, datasets and evaluation metrics. Comput Methods Programs Biomed 158:71–91PubMed
23.
go back to reference Pexman JW, Barber PA, Hill MD, Sevick RJ, Demchuk AM, Hudon ME, Hu WY, Buchan AM (2001) Use of the Alberta stroke program early CT score (ASPECTS) for assessing CT scans in patients with acute stroke. Am J Neuroradiol 22(8):1534–1542PubMedPubMedCentral Pexman JW, Barber PA, Hill MD, Sevick RJ, Demchuk AM, Hudon ME, Hu WY, Buchan AM (2001) Use of the Alberta stroke program early CT score (ASPECTS) for assessing CT scans in patients with acute stroke. Am J Neuroradiol 22(8):1534–1542PubMedPubMedCentral
24.
go back to reference Piedade GS, Schirmer CM, Goren O, Zhang H, Aghajanian A, Faber JE, Griessenauer CJ (2019) Cerebral collateral circulation: a review in the context of ischemic stroke and mechanical thrombectomy. World Neurosurg 122:33–42PubMed Piedade GS, Schirmer CM, Goren O, Zhang H, Aghajanian A, Faber JE, Griessenauer CJ (2019) Cerebral collateral circulation: a review in the context of ischemic stroke and mechanical thrombectomy. World Neurosurg 122:33–42PubMed
25.
go back to reference Rezaei B, Ostadabbas S (2017) Background subtraction via fast robust matrix completion. In: Proceedings of the IEEE international conference on computer vision, pp 1871–1879 Rezaei B, Ostadabbas S (2017) Background subtraction via fast robust matrix completion. In: Proceedings of the IEEE international conference on computer vision, pp 1871–1879
26.
go back to reference Shieh Y, Chang CH, Shieh M, Lee TH, Chang YJ, Wong HF, Chin SC, Goodwin S (2014) Computer-aided diagnosis of hyperacute stroke with thrombolysis decision support using a contralateral comparative method of CT image analysis. J Digit Imaging 27(3):392–406PubMedPubMedCentral Shieh Y, Chang CH, Shieh M, Lee TH, Chang YJ, Wong HF, Chin SC, Goodwin S (2014) Computer-aided diagnosis of hyperacute stroke with thrombolysis decision support using a contralateral comparative method of CT image analysis. J Digit Imaging 27(3):392–406PubMedPubMedCentral
27.
go back to reference Tan I, Demchuk A, Hopyan J, Zhang L, Gladstone D, Wong K, Martin M, Symons S, Fox A, Aviv R (2009) CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. Am J Neuroradiol 30(3):525–531PubMedPubMedCentral Tan I, Demchuk A, Hopyan J, Zhang L, Gladstone D, Wong K, Martin M, Symons S, Fox A, Aviv R (2009) CT angiography clot burden score and collateral score: correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. Am J Neuroradiol 30(3):525–531PubMedPubMedCentral
28.
go back to reference von Kummer R, Holle R, Gizyska U, Hofmann E, Jansen O, Petersen D, Schumacher M, Sartor K (1996) Interobserver agreement in assessing early CT signs of middle cerebral artery infarction. Am J Neuroradiol 17(9):1743–1748 von Kummer R, Holle R, Gizyska U, Hofmann E, Jansen O, Petersen D, Schumacher M, Sartor K (1996) Interobserver agreement in assessing early CT signs of middle cerebral artery infarction. Am J Neuroradiol 17(9):1743–1748
29.
go back to reference Xiao Y, Alamer A, Fonov V, Lo BW, Tampieri D, Collins DL, Rivaz H, Kersten-Oertel M (2017) Towards automatic collateral circulation score evaluation in ischemic stroke using image decompositions and support vector machines. In: Molecular imaging, reconstruction and analysis of moving body organs, and stroke imaging and treatment. Lecture Notes in Computer Science, vol 10555. Springer, Cham Xiao Y, Alamer A, Fonov V, Lo BW, Tampieri D, Collins DL, Rivaz H, Kersten-Oertel M (2017) Towards automatic collateral circulation score evaluation in ischemic stroke using image decompositions and support vector machines. In: Molecular imaging, reconstruction and analysis of moving body organs, and stroke imaging and treatment. Lecture Notes in Computer Science, vol 10555. Springer, Cham
30.
go back to reference Yang X, Liu C, Le Minh H, Wang Z, Chien A, Cheng KTT (2017) An automated method for accurate vessel segmentation. Phys Med Biol 62(9):3757PubMed Yang X, Liu C, Le Minh H, Wang Z, Chien A, Cheng KTT (2017) An automated method for accurate vessel segmentation. Phys Med Biol 62(9):3757PubMed
31.
go back to reference Zhang S, Chen W, Tang H, Han Q, Yan S, Zhang X, Chen Q, Parsons M, Wang S, Lou M (2016) The prognostic value of a four-dimensional CT angiography-based collateral grading scale for reperfusion therapy in acute ischemic stroke patients. PLoS ONE 11(8):e0160502PubMedPubMedCentral Zhang S, Chen W, Tang H, Han Q, Yan S, Zhang X, Chen Q, Parsons M, Wang S, Lou M (2016) The prognostic value of a four-dimensional CT angiography-based collateral grading scale for reperfusion therapy in acute ischemic stroke patients. PLoS ONE 11(8):e0160502PubMedPubMedCentral
Metadata
Title
Automatic collateral circulation scoring in ischemic stroke using 4D CT angiography with low-rank and sparse matrix decomposition
Authors
Mumu Aktar
Donatella Tampieri
Hassan Rivaz
Marta Kersten-Oertel
Yiming Xiao
Publication date
01-09-2020
Publisher
Springer International Publishing
Published in
International Journal of Computer Assisted Radiology and Surgery / Issue 9/2020
Print ISSN: 1861-6410
Electronic ISSN: 1861-6429
DOI
https://doi.org/10.1007/s11548-020-02216-w

Other articles of this Issue 9/2020

International Journal of Computer Assisted Radiology and Surgery 9/2020 Go to the issue