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Published in: European Radiology 8/2021

01-08-2021 | Stroke | Neuro

Quantitative susceptibility-weighted imaging may be an accurate method for determining stroke hypoperfusion and hypoxia of penumbra

Authors: Xiudi Lu, Linglei Meng, Yongmin Zhou, Shaoshi Wang, Miller Fawaz, Meiyun Wang, E. Mark Haacke, Chao Chai, Meizhu Zheng, Jinxia Zhu, Yu Luo, Shuang Xia

Published in: European Radiology | Issue 8/2021

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Abstract

Objectives

To quantitatively evaluate the volume of the ischemic penumbra using susceptibility-weighted imaging and mapping (SWIM) of asymmetrical prominent cortical veins (APCVs) in patients with acute ischemic stroke.

Methods

Eighty-five eligible patients with acute ischemic stroke on admission within 12 h from symptom onset were studied. The APCVs on SWIM were quantitatively (SWI-volume) and semi-quantitatively (SWI-Alberta Stroke Program Early CT Score, SWI-ASPECTS) evaluated to calculate mismatch. To assess the diagnostic efficacy of APCVs on SWIM, comparative analyses were performed between SWIvolume-DWI mismatch and SWIASPECTS-DWI mismatch, using PWI-DWI mismatch as a reference. Correlations were calculated between the mismatches, as well as between SWI-volume and time-to-maximum (Tmax) > 6 s volume. Additionally, each of these mismatches was correlated with the National Institute of Health Stroke Scale (NIHSS).

Results

The sensitivity, negative predictive value, and accuracy of SWIvolume-DWI mismatch were demonstrably higher than SWIASPECTS-DWI mismatch (100% vs. 53.7%, 100% vs. 9.5%, 97.7% vs. 54.5%, respectively). A significant positive correlation was found between SWIvolume-DWI and PWI-DWI mismatch (r = 0.691, p < 0.01), as well as between SWI-volume and Tmax > 6 s volume (r = 0.786, p < 0.001). A significant negative correlation was found between SWIvolume-DWI mismatch and NIHSS (r = − 0.360, p = 0.022), as well as between SWIASPECTS-DWI mismatch and NIHSS (r = − 0.499, p = 0.001).

Conclusions

SWIvolume-DWI mismatch had higher diagnostic efficacy than SWIASPECTS-DWI mismatch in defining the ischemic penumbra and showed good consistency with PWI-DWI mismatch in acute ischemic stroke. Quantitation of APCVs using SWIM provided an accurate method for determining hypoperfusion and provided a reliable method to reflect the hypoxia of penumbra.

Key Points

• SWI volume -DWI mismatch has higher diagnostic efficacy than SWI ASPECTS -DWI mismatch in defining the ischemic penumbra.
• SWI volume -DWI mismatch shows good consistency with PWI-DWI mismatch in managing penumbra in acute ischemic stroke.
• Quantitation of APCV volume using SWIM provided an accurate method for determining the hypoperfusion area and provided a reliable method to reflect the hypoxia of penumbra.
Appendix
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Literature
2.
go back to reference Wintermark M, Sanelli PC, Albers GW et al (2013) Imaging recommendations for acute stroke and transient ischemic attack patients: a joint statement by the American Society of Neuroradiology, the American College of Radiology, and the Society of NeuroInterventional Surgery. AJNR Am J Neuroradiol 34:E117–E127PubMedPubMedCentralCrossRef Wintermark M, Sanelli PC, Albers GW et al (2013) Imaging recommendations for acute stroke and transient ischemic attack patients: a joint statement by the American Society of Neuroradiology, the American College of Radiology, and the Society of NeuroInterventional Surgery. AJNR Am J Neuroradiol 34:E117–E127PubMedPubMedCentralCrossRef
3.
go back to reference Schlaug G, Benfield A, Baird AE et al (1999) The ischemic penumbra: operationally defined by diffusion and perfusion MRI. Neurology 53:1528–1537PubMedCrossRef Schlaug G, Benfield A, Baird AE et al (1999) The ischemic penumbra: operationally defined by diffusion and perfusion MRI. Neurology 53:1528–1537PubMedCrossRef
4.
go back to reference Albers GW, Thijs VN, Wechsler L et al (2006) Magnetic resonance imaging profiles predict clinical response to early reperfusion: the diffusion and perfusion imaging evaluation for understanding stroke evolution (DEFUSE) study. Ann Neurol 60:508–517PubMedCrossRef Albers GW, Thijs VN, Wechsler L et al (2006) Magnetic resonance imaging profiles predict clinical response to early reperfusion: the diffusion and perfusion imaging evaluation for understanding stroke evolution (DEFUSE) study. Ann Neurol 60:508–517PubMedCrossRef
5.
go back to reference Hjort N, Butcher K, Davis SM et al (2005) Magnetic resonance imaging criteria for thrombolysis in acute cerebral infarct. Stroke 36:388–397PubMedCrossRef Hjort N, Butcher K, Davis SM et al (2005) Magnetic resonance imaging criteria for thrombolysis in acute cerebral infarct. Stroke 36:388–397PubMedCrossRef
6.
go back to reference Davis SM, Donnan GA, Parsons MW et al (2008) Effects of alteplase beyond 3 h after stroke in the Echoplanar Imaging Thrombolytic Evaluation Trial (EPITHET): a placebo-controlled randomised trial. Lancet Neurol 7:299–309PubMedCrossRef Davis SM, Donnan GA, Parsons MW et al (2008) Effects of alteplase beyond 3 h after stroke in the Echoplanar Imaging Thrombolytic Evaluation Trial (EPITHET): a placebo-controlled randomised trial. Lancet Neurol 7:299–309PubMedCrossRef
7.
go back to reference Wang DJ, Alger JR, Qiao JX et al (2013) Multi-delay multi-parametric arterial spin-labeled perfusion MRI in acute ischemic stroke - comparison with dynamic susceptibility contrast enhanced perfusion imaging. Neuroimage Clin 3:1–7PubMedPubMedCentralCrossRef Wang DJ, Alger JR, Qiao JX et al (2013) Multi-delay multi-parametric arterial spin-labeled perfusion MRI in acute ischemic stroke - comparison with dynamic susceptibility contrast enhanced perfusion imaging. Neuroimage Clin 3:1–7PubMedPubMedCentralCrossRef
8.
go back to reference Wang DJ, Alger JR, Qiao JX et al (2012) The value of arterial spin-labeled perfusion imaging in acute ischemic stroke: comparison with dynamic susceptibility contrast-enhanced MRI. Stroke 43:1018–1024PubMedPubMedCentralCrossRef Wang DJ, Alger JR, Qiao JX et al (2012) The value of arterial spin-labeled perfusion imaging in acute ischemic stroke: comparison with dynamic susceptibility contrast-enhanced MRI. Stroke 43:1018–1024PubMedPubMedCentralCrossRef
9.
go back to reference Wang K, Shou Q, Ma SJ et al (2020) Deep learning detection of penumbral tissue on arterial spin labeling in stroke. Stroke 51:489–497PubMedCrossRef Wang K, Shou Q, Ma SJ et al (2020) Deep learning detection of penumbral tissue on arterial spin labeling in stroke. Stroke 51:489–497PubMedCrossRef
10.
go back to reference Chai C, Wang H, Liu S et al (2019) Increased iron deposition of deep cerebral gray matter structures in hemodialysis patients: a longitudinal study using quantitative susceptibility mapping. J Magn Reson Imaging 49:786–799PubMedCrossRef Chai C, Wang H, Liu S et al (2019) Increased iron deposition of deep cerebral gray matter structures in hemodialysis patients: a longitudinal study using quantitative susceptibility mapping. J Magn Reson Imaging 49:786–799PubMedCrossRef
11.
go back to reference Shahmaei V, Faeghi F, Mohammdbeigi A, Hashemi H, Ashrafi F (2019) Evaluation of iron deposition in brain basal ganglia of patients with Parkinson’s disease using quantitative susceptibility mapping. Eur J Radiol Open 6:169–174PubMedPubMedCentralCrossRef Shahmaei V, Faeghi F, Mohammdbeigi A, Hashemi H, Ashrafi F (2019) Evaluation of iron deposition in brain basal ganglia of patients with Parkinson’s disease using quantitative susceptibility mapping. Eur J Radiol Open 6:169–174PubMedPubMedCentralCrossRef
12.
go back to reference Li DTH, Hui ES, Chan Q et al (2018) Quantitative susceptibility mapping as an indicator of subcortical and limbic iron abnormality in Parkinson’s disease with dementia. Neuroimage Clin 20:365–373PubMedPubMedCentralCrossRef Li DTH, Hui ES, Chan Q et al (2018) Quantitative susceptibility mapping as an indicator of subcortical and limbic iron abnormality in Parkinson’s disease with dementia. Neuroimage Clin 20:365–373PubMedPubMedCentralCrossRef
13.
go back to reference Chai C, Guo R, Zuo C et al (2017) Decreased susceptibility of major veins in mild traumatic brain injury is correlated with post-concussive symptoms: a quantitative susceptibility mapping study. Neuroimage Clin 15:625–632PubMedPubMedCentralCrossRef Chai C, Guo R, Zuo C et al (2017) Decreased susceptibility of major veins in mild traumatic brain injury is correlated with post-concussive symptoms: a quantitative susceptibility mapping study. Neuroimage Clin 15:625–632PubMedPubMedCentralCrossRef
14.
go back to reference Tsivgoulis G, Zand R, Katsanos AH et al (2016) Risk of symptomatic intracerebral hemorrhage after intravenous thrombolysis in patients with acute ischemic stroke and high cerebral microbleed burden: a meta-analysis. JAMA Neurol 73:675–683PubMedCrossRef Tsivgoulis G, Zand R, Katsanos AH et al (2016) Risk of symptomatic intracerebral hemorrhage after intravenous thrombolysis in patients with acute ischemic stroke and high cerebral microbleed burden: a meta-analysis. JAMA Neurol 73:675–683PubMedCrossRef
15.
go back to reference Liu T, Surapaneni K, Lou M, Cheng L, Spincemaille P, Wang Y (2012) Cerebral microbleeds: burden assessment by using quantitative susceptibility mapping. Radiology 262:269–278PubMedPubMedCentralCrossRef Liu T, Surapaneni K, Lou M, Cheng L, Spincemaille P, Wang Y (2012) Cerebral microbleeds: burden assessment by using quantitative susceptibility mapping. Radiology 262:269–278PubMedPubMedCentralCrossRef
16.
go back to reference Hermier M, Nighoghossian N, Derex L et al (2001) MRI of acute post-ischemic cerebral hemorrhage in stroke patients: diagnosis with T2*-weighted gradient-echo sequences. Neuroradiology 43:809–815PubMedCrossRef Hermier M, Nighoghossian N, Derex L et al (2001) MRI of acute post-ischemic cerebral hemorrhage in stroke patients: diagnosis with T2*-weighted gradient-echo sequences. Neuroradiology 43:809–815PubMedCrossRef
17.
go back to reference Zhang Y, Wei H, Sun Y et al (2018) Quantitative susceptibility mapping (QSM) as a means to monitor cerebral hematoma treatment. J Magn Reson Imaging 48:907–915PubMedPubMedCentralCrossRef Zhang Y, Wei H, Sun Y et al (2018) Quantitative susceptibility mapping (QSM) as a means to monitor cerebral hematoma treatment. J Magn Reson Imaging 48:907–915PubMedPubMedCentralCrossRef
18.
go back to reference Sun H, Klahr AC, Kate M et al (2018) Quantitative susceptibility mapping for following intracranial hemorrhage. Radiology 288:830–839PubMedCrossRef Sun H, Klahr AC, Kate M et al (2018) Quantitative susceptibility mapping for following intracranial hemorrhage. Radiology 288:830–839PubMedCrossRef
19.
go back to reference Chang S, Zhang J, Liu T et al (2016) Quantitative susceptibility mapping of intracerebral hemorrhages at various stages. J Magn Reson Imaging 44:420–425PubMedCrossRef Chang S, Zhang J, Liu T et al (2016) Quantitative susceptibility mapping of intracerebral hemorrhages at various stages. J Magn Reson Imaging 44:420–425PubMedCrossRef
20.
go back to reference Xia S, Utriainen D, Tang J et al (2014) Decreased oxygen saturation in asymmetrically prominent cortical veins in patients with cerebral ischemic stroke. Magn Reson Imaging 32:1272–1276PubMedCrossRef Xia S, Utriainen D, Tang J et al (2014) Decreased oxygen saturation in asymmetrically prominent cortical veins in patients with cerebral ischemic stroke. Magn Reson Imaging 32:1272–1276PubMedCrossRef
21.
go back to reference Zhang J, Liu T, Gupta A, Spincemaille P, Nguyen TD, Wang Y (2015) Quantitative mapping of cerebral metabolic rate of oxygen (CMRO2 ) using quantitative susceptibility mapping (QSM). Magn Reson Med 74:945–952PubMedCrossRef Zhang J, Liu T, Gupta A, Spincemaille P, Nguyen TD, Wang Y (2015) Quantitative mapping of cerebral metabolic rate of oxygen (CMRO2 ) using quantitative susceptibility mapping (QSM). Magn Reson Med 74:945–952PubMedCrossRef
22.
go back to reference Li M, Hu J, Miao Y et al (2013) In vivo measurement of oxygenation changes after stroke using susceptibility weighted imaging filtered phase data. PLoS One 8:e63013PubMedPubMedCentralCrossRef Li M, Hu J, Miao Y et al (2013) In vivo measurement of oxygenation changes after stroke using susceptibility weighted imaging filtered phase data. PLoS One 8:e63013PubMedPubMedCentralCrossRef
23.
go back to reference Chai C, Liu S, Fan L et al (2018) Reduced deep regional cerebral venous oxygen saturation in hemodialysis patients using quantitative susceptibility mapping. Metab Brain Dis 33:313–323PubMedCrossRef Chai C, Liu S, Fan L et al (2018) Reduced deep regional cerebral venous oxygen saturation in hemodialysis patients using quantitative susceptibility mapping. Metab Brain Dis 33:313–323PubMedCrossRef
25.
go back to reference Mittal S, Wu Z, Neelavalli J, Haacke EM (2009) Susceptibility-weighted imaging: technical aspects and clinical applications, part 2. AJNR Am J Neuroradiol 30:232–252PubMedPubMedCentralCrossRef Mittal S, Wu Z, Neelavalli J, Haacke EM (2009) Susceptibility-weighted imaging: technical aspects and clinical applications, part 2. AJNR Am J Neuroradiol 30:232–252PubMedPubMedCentralCrossRef
26.
go back to reference Luo Y, Gong Z, Zhou Y et al (2017) Increased susceptibility of asymmetrically prominent cortical veins correlates with misery perfusion in patients with occlusion of the middle cerebral artery. Eur Radiol 27:2381–2390PubMedCrossRef Luo Y, Gong Z, Zhou Y et al (2017) Increased susceptibility of asymmetrically prominent cortical veins correlates with misery perfusion in patients with occlusion of the middle cerebral artery. Eur Radiol 27:2381–2390PubMedCrossRef
27.
go back to reference Kao HW, Tsai FY, Hasso AN (2012) Predicting stroke evolution: comparison of susceptibility-weighted MR imaging with MR perfusion. Eur Radiol 22:1397–1403PubMedCrossRef Kao HW, Tsai FY, Hasso AN (2012) Predicting stroke evolution: comparison of susceptibility-weighted MR imaging with MR perfusion. Eur Radiol 22:1397–1403PubMedCrossRef
28.
go back to reference Luo S, Yang L, Wang L (2015) Comparison of susceptibility-weighted and perfusion-weighted magnetic resonance imaging in the detection of penumbra in acute ischemic stroke. J Neuroradiol 42:255–260PubMedCrossRef Luo S, Yang L, Wang L (2015) Comparison of susceptibility-weighted and perfusion-weighted magnetic resonance imaging in the detection of penumbra in acute ischemic stroke. J Neuroradiol 42:255–260PubMedCrossRef
29.
go back to reference Dejobert M, Cazals X, Annan M, Debiais S, Lauvin MA, Cottier JP (2016) Susceptibility-diffusion mismatch in hyperacute stroke: correlation with perfusion-diffusion mismatch and clinical outcome. J Stroke Cerebrovasc Dis 25:1760–1766PubMedCrossRef Dejobert M, Cazals X, Annan M, Debiais S, Lauvin MA, Cottier JP (2016) Susceptibility-diffusion mismatch in hyperacute stroke: correlation with perfusion-diffusion mismatch and clinical outcome. J Stroke Cerebrovasc Dis 25:1760–1766PubMedCrossRef
30.
go back to reference Zhao G, Sun L, Wang Z et al (2017) Evaluation of the role of susceptibility-weighted imaging in thrombolytic therapy for acute ischemic stroke. J Clin Neurosci 40:175–179PubMedCrossRef Zhao G, Sun L, Wang Z et al (2017) Evaluation of the role of susceptibility-weighted imaging in thrombolytic therapy for acute ischemic stroke. J Clin Neurosci 40:175–179PubMedCrossRef
31.
go back to reference Jiang Q, Chen C-Y, Chen C-I, Tsai FY, Tsai P-H, Chan WP (2015) Prominent vessel sign on susceptibility-weighted imaging in acute stroke: prediction of infarct growth and clinical outcome. Plos One 10:e0131118CrossRef Jiang Q, Chen C-Y, Chen C-I, Tsai FY, Tsai P-H, Chan WP (2015) Prominent vessel sign on susceptibility-weighted imaging in acute stroke: prediction of infarct growth and clinical outcome. Plos One 10:e0131118CrossRef
34.
go back to reference Calamante F, Christensen S, Desmond PM, Ostergaard L, Davis SM, Connelly A (2010) The physiological significance of the time-to-maximum (Tmax) parameter in perfusion MRI. Stroke 41:1169–1174PubMedCrossRef Calamante F, Christensen S, Desmond PM, Ostergaard L, Davis SM, Connelly A (2010) The physiological significance of the time-to-maximum (Tmax) parameter in perfusion MRI. Stroke 41:1169–1174PubMedCrossRef
35.
go back to reference Olivot JM, Mlynash M, Thijs VN et al (2009) Optimal Tmax threshold for predicting penumbral tissue in acute stroke. Stroke 40:469–475PubMedCrossRef Olivot JM, Mlynash M, Thijs VN et al (2009) Optimal Tmax threshold for predicting penumbral tissue in acute stroke. Stroke 40:469–475PubMedCrossRef
36.
go back to reference Lansberg MG, Lee J, Christensen S et al (2011) RAPID automated patient selection for reperfusion therapy: a pooled analysis of the Echoplanar Imaging Thrombolytic Evaluation Trial (EPITHET) and the Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution (DEFUSE) Study. Stroke 42:1608–1614PubMedPubMedCentralCrossRef Lansberg MG, Lee J, Christensen S et al (2011) RAPID automated patient selection for reperfusion therapy: a pooled analysis of the Echoplanar Imaging Thrombolytic Evaluation Trial (EPITHET) and the Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution (DEFUSE) Study. Stroke 42:1608–1614PubMedPubMedCentralCrossRef
37.
go back to reference Tang J, Liu S, Neelavalli J, Cheng YC, Buch S, Haacke EM (2013) Improving susceptibility mapping using a threshold-based K-space/image domain iterative reconstruction approach. Magn Reson Med 69:1396–1407PubMedCrossRef Tang J, Liu S, Neelavalli J, Cheng YC, Buch S, Haacke EM (2013) Improving susceptibility mapping using a threshold-based K-space/image domain iterative reconstruction approach. Magn Reson Med 69:1396–1407PubMedCrossRef
38.
go back to reference Miyata M, Kakeda S, Kudo K et al (2019) Evaluation of oxygen extraction fraction in systemic lupus erythematosus patients using quantitative susceptibility mapping. J Cereb Blood Flow Metab 39:1648–1658PubMedCrossRef Miyata M, Kakeda S, Kudo K et al (2019) Evaluation of oxygen extraction fraction in systemic lupus erythematosus patients using quantitative susceptibility mapping. J Cereb Blood Flow Metab 39:1648–1658PubMedCrossRef
39.
go back to reference Aoki J, Kimura K, Shibazaki K, Sakamoto Y (2013) DWI-ASPECTS as a predictor of dramatic recovery after intravenous recombinant tissue plasminogen activator administration in patients with middle cerebral artery occlusion. Stroke 44:534–537PubMedCrossRef Aoki J, Kimura K, Shibazaki K, Sakamoto Y (2013) DWI-ASPECTS as a predictor of dramatic recovery after intravenous recombinant tissue plasminogen activator administration in patients with middle cerebral artery occlusion. Stroke 44:534–537PubMedCrossRef
40.
go back to reference Viallon M, Altrichter S, Pereira VM et al (2010) Combined use of pulsed arterial spin-labeling and susceptibility-weighted imaging in stroke at 3T. Eur Neurol 64:286–296PubMedCrossRef Viallon M, Altrichter S, Pereira VM et al (2010) Combined use of pulsed arterial spin-labeling and susceptibility-weighted imaging in stroke at 3T. Eur Neurol 64:286–296PubMedCrossRef
41.
go back to reference Wu X, Luo S, Wang Y et al (2017) Use of susceptibility-weighted imaging in assessing ischemic penumbra: a case report. Medicine (Baltimore) 96:e6091CrossRef Wu X, Luo S, Wang Y et al (2017) Use of susceptibility-weighted imaging in assessing ischemic penumbra: a case report. Medicine (Baltimore) 96:e6091CrossRef
42.
go back to reference Kesavadas C, Thomas B, Pendharakar H, Sylaja PN (2011) Susceptibility weighted imaging: does it give information similar to perfusion weighted imaging in acute stroke? J Neurol 258:932–934PubMedCrossRef Kesavadas C, Thomas B, Pendharakar H, Sylaja PN (2011) Susceptibility weighted imaging: does it give information similar to perfusion weighted imaging in acute stroke? J Neurol 258:932–934PubMedCrossRef
43.
go back to reference Huang P, Chen CH, Lin WC, Lin RT, Khor GT, Liu CK (2012) Clinical applications of susceptibility weighted imaging in patients with major stroke. J Neurol 259:1426–1432PubMedCrossRef Huang P, Chen CH, Lin WC, Lin RT, Khor GT, Liu CK (2012) Clinical applications of susceptibility weighted imaging in patients with major stroke. J Neurol 259:1426–1432PubMedCrossRef
44.
go back to reference Darwish EAF, Abdelhameed-El-Nouby M, Geneidy E (2020) Mapping the ischemic penumbra and predicting stroke progression in acute ischemic stroke: the overlooked role of susceptibility weighted imaging. Insights Imaging 11:6PubMedPubMedCentralCrossRef Darwish EAF, Abdelhameed-El-Nouby M, Geneidy E (2020) Mapping the ischemic penumbra and predicting stroke progression in acute ischemic stroke: the overlooked role of susceptibility weighted imaging. Insights Imaging 11:6PubMedPubMedCentralCrossRef
45.
go back to reference Tsui YK, Tsai FY, Hasso AN, Greensite F, Nguyen BV (2009) Susceptibility-weighted imaging for differential diagnosis of cerebral vascular pathology: a pictorial review. J Neurol Sci 287:7–16PubMedCrossRef Tsui YK, Tsai FY, Hasso AN, Greensite F, Nguyen BV (2009) Susceptibility-weighted imaging for differential diagnosis of cerebral vascular pathology: a pictorial review. J Neurol Sci 287:7–16PubMedCrossRef
46.
go back to reference Haacke EM, Tang J, Neelavalli J, Cheng YC (2010) Susceptibility mapping as a means to visualize veins and quantify oxygen saturation. J Magn Reson Imaging 32:663–676PubMedPubMedCentralCrossRef Haacke EM, Tang J, Neelavalli J, Cheng YC (2010) Susceptibility mapping as a means to visualize veins and quantify oxygen saturation. J Magn Reson Imaging 32:663–676PubMedPubMedCentralCrossRef
Metadata
Title
Quantitative susceptibility-weighted imaging may be an accurate method for determining stroke hypoperfusion and hypoxia of penumbra
Authors
Xiudi Lu
Linglei Meng
Yongmin Zhou
Shaoshi Wang
Miller Fawaz
Meiyun Wang
E. Mark Haacke
Chao Chai
Meizhu Zheng
Jinxia Zhu
Yu Luo
Shuang Xia
Publication date
01-08-2021
Publisher
Springer Berlin Heidelberg
Keyword
Stroke
Published in
European Radiology / Issue 8/2021
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-020-07485-2

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