Skip to main content
Top
Published in: Journal of Cardiovascular Magnetic Resonance 1/2017

Open Access 01-12-2017 | Research

Experimental validation of contrast-enhanced SSFP cine CMR for quantification of myocardium at risk in acute myocardial infarction

Authors: David Nordlund, Mikael Kanski, Robert Jablonowski, Sasha Koul, David Erlinge, Marcus Carlsson, Henrik Engblom, Anthony H. Aletras, Håkan Arheden

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

Login to get access

Abstract

Background

Accurate assessment of myocardium at risk (MaR) after acute myocardial infarction (AMI) is necessary when assessing myocardial salvage. Contrast-enhanced steady-state free precession (CE-SSFP) is a recently developed cardiovascular magnetic resonance (CMR) method for assessment of MaR up to 1 week after AMI. Our aim was to validate CE-SSFP for determination of MaR in an experimental porcine model using myocardial perfusion single-photon emission computed tomography (MPS) as a reference standard and to test the stability of MaR-quantification over time after injecting gadolinium-based contrast.

Methods

Eleven pigs were subjected to either 35 or 40 min occlusion of the left anterior descending artery followed by six hours of reperfusion. A technetium-based perfusion tracer was administered intravenously ten minutes before reperfusion. In-vivo and ex-vivo CE-SSFP CMR was performed followed by ex-vivo MPS imaging. MaR was expressed as % of left ventricular mass (LVM).

Results

There was good agreement between MaR by ex-vivo CMR and MaR by MPS (bias: 1 ± 3% LVM, r 2 = 0.92, p < 0.001), between ex-vivo and in-vivo CMR (bias 0 ± 2% LVM, r 2 = 0.94, p < 0.001) and between in-vivo CMR and MPS (bias -2 ± 3% LVM, r 2 = 0.87, p < 0.001. No change in MaR was seen over the first 30 min after contrast injection (p = 0.95).

Conclusions

Contrast-enhanced SSFP cine CMR can be used to measure MaR, both in vivo and ex vivo, in a porcine model with good accuracy and precision over the first 30 min after contrast injection. This offers the option to use the less complex ex-vivo imaging when determining myocardial salvage in experimental studies.
Literature
1.
go back to reference Reimer KA, Jennings RB. The “wavefront phenomenon” of myocardial ischemic cell death. II. Transmural progression of necrosis within the framework of ischemic bed size (myocardium at risk) and collateral flow. Lab Invest. 1979;40:633–44.PubMed Reimer KA, Jennings RB. The “wavefront phenomenon” of myocardial ischemic cell death. II. Transmural progression of necrosis within the framework of ischemic bed size (myocardium at risk) and collateral flow. Lab Invest. 1979;40:633–44.PubMed
2.
go back to reference Kim RJ, Wu E, Rafael A, Chen E-L, Parker MA, Simonetti O, Klocke FJ, Bonow RO, Judd RM. The Use of Contrast-Enhanced Magnetic Resonance Imaging to Identify Reversible Myocardial Dysfunction. N Engl J Med. 2000;343:1445–53.CrossRefPubMed Kim RJ, Wu E, Rafael A, Chen E-L, Parker MA, Simonetti O, Klocke FJ, Bonow RO, Judd RM. The Use of Contrast-Enhanced Magnetic Resonance Imaging to Identify Reversible Myocardial Dysfunction. N Engl J Med. 2000;343:1445–53.CrossRefPubMed
3.
go back to reference Simonetti OP, Kim RJ, Fieno DS, Hillenbrand HB, Wu E, Bundy JM, Finn JP, Judd RM. An improved MR imaging technique for the visualization of myocardial infarction. Radiology. 2001;218:215–23.CrossRefPubMed Simonetti OP, Kim RJ, Fieno DS, Hillenbrand HB, Wu E, Bundy JM, Finn JP, Judd RM. An improved MR imaging technique for the visualization of myocardial infarction. Radiology. 2001;218:215–23.CrossRefPubMed
4.
go back to reference Aletras AH, Tilak GS, Natanzon A, Hsu L-Y, Gonzalez FM, Hoyt RFJ, Arai AE. Retrospective determination of the area at risk for reperfused acute myocardial infarction with T2-weighted cardiac magnetic resonance imaging: histopathological and displacement encoding with stimulated echoes (DENSE) functional validations. Circulation. 2006;113:1865–70.CrossRefPubMed Aletras AH, Tilak GS, Natanzon A, Hsu L-Y, Gonzalez FM, Hoyt RFJ, Arai AE. Retrospective determination of the area at risk for reperfused acute myocardial infarction with T2-weighted cardiac magnetic resonance imaging: histopathological and displacement encoding with stimulated echoes (DENSE) functional validations. Circulation. 2006;113:1865–70.CrossRefPubMed
5.
go back to reference Carlsson M, Ubachs JFA, Hedström E, Heiberg E, Jovinge S, Arheden H. Myocardium at Risk After Acute Infarction in Humans on Cardiac Magnetic Resonance. JACC Cardiovasc Imaging. 2009;2:569–76.CrossRefPubMed Carlsson M, Ubachs JFA, Hedström E, Heiberg E, Jovinge S, Arheden H. Myocardium at Risk After Acute Infarction in Humans on Cardiac Magnetic Resonance. JACC Cardiovasc Imaging. 2009;2:569–76.CrossRefPubMed
6.
go back to reference Nordlund D, Klug G, Heiberg E, Koul S, Larsen TH, Hoffmann P, Metzler B, Erlinge D, Atar D, Aletras AH, Carlsson M, Engblom H, Arheden H. Multi-vendor, multicentre comparison of contrast-enhanced SSFP and T2-STIR CMR for determining myocardium at risk in ST-elevation myocardial infarction. Eur Hear J – Cardiovasc Imaging. 2016;17:744–53.CrossRef Nordlund D, Klug G, Heiberg E, Koul S, Larsen TH, Hoffmann P, Metzler B, Erlinge D, Atar D, Aletras AH, Carlsson M, Engblom H, Arheden H. Multi-vendor, multicentre comparison of contrast-enhanced SSFP and T2-STIR CMR for determining myocardium at risk in ST-elevation myocardial infarction. Eur Hear J – Cardiovasc Imaging. 2016;17:744–53.CrossRef
7.
go back to reference Keegan J, Gatehouse PD, Prasad SK, Firmin DN. Improved turbo spin-echo imaging of the heart with motion-tracking. J Magn Reson Imaging. 2006;24:563–70.CrossRefPubMed Keegan J, Gatehouse PD, Prasad SK, Firmin DN. Improved turbo spin-echo imaging of the heart with motion-tracking. J Magn Reson Imaging. 2006;24:563–70.CrossRefPubMed
8.
go back to reference Kellman P, Aletras AH, Mancini C, McVeigh ER, Arai AE. T2-prepared SSFP improves diagnostic confidence in edema imaging in acute myocardial infarction compared to turbo spin echo. Magn Reson Med. 2007;57:891–7.CrossRefPubMedPubMedCentral Kellman P, Aletras AH, Mancini C, McVeigh ER, Arai AE. T2-prepared SSFP improves diagnostic confidence in edema imaging in acute myocardial infarction compared to turbo spin echo. Magn Reson Med. 2007;57:891–7.CrossRefPubMedPubMedCentral
9.
go back to reference Sörensson P, Heiberg E, Saleh N, Bouvier F, Caidahl K, Tornvall P, Rydén L, Pernow J, Arheden H. Assessment of myocardium at risk with contrast enhanced steady-state free precession cine cardiovascular magnetic resonance compared to single-photon emission computed tomography. J Cardiovasc Magn Reson. 2010;12:25.CrossRefPubMedPubMedCentral Sörensson P, Heiberg E, Saleh N, Bouvier F, Caidahl K, Tornvall P, Rydén L, Pernow J, Arheden H. Assessment of myocardium at risk with contrast enhanced steady-state free precession cine cardiovascular magnetic resonance compared to single-photon emission computed tomography. J Cardiovasc Magn Reson. 2010;12:25.CrossRefPubMedPubMedCentral
10.
go back to reference Ubachs JFA, Sorensson P, Engblom H, Carlsson M, Jovinge S, Pernow J, Arheden H. Myocardium at risk by magnetic resonance imaging: head-to-head comparison of T2-weighted imaging and contrast-enhanced steady-state free precession. Eur Hear J - Cardiovasc Imaging. 2012;13:1008–15.CrossRef Ubachs JFA, Sorensson P, Engblom H, Carlsson M, Jovinge S, Pernow J, Arheden H. Myocardium at risk by magnetic resonance imaging: head-to-head comparison of T2-weighted imaging and contrast-enhanced steady-state free precession. Eur Hear J - Cardiovasc Imaging. 2012;13:1008–15.CrossRef
11.
go back to reference Erlinge D, Götberg M, Lang I, Holzer M, Noc M, Clemmensen P, Jensen U, Metzler B, James S, Bötker HE, Omerovic E, Engblom H, Carlsson M, Arheden H, Östlund O, Wallentin L, Harnek J, Olivecrona GK. Rapid Endovascular Catheter Core Cooling Combined With Cold Saline as an Adjunct to Percutaneous Coronary Intervention for the Treatment of Acute Myocardial Infarction. J Am Coll Cardiol. 2014;63:1857–65.CrossRefPubMed Erlinge D, Götberg M, Lang I, Holzer M, Noc M, Clemmensen P, Jensen U, Metzler B, James S, Bötker HE, Omerovic E, Engblom H, Carlsson M, Arheden H, Östlund O, Wallentin L, Harnek J, Olivecrona GK. Rapid Endovascular Catheter Core Cooling Combined With Cold Saline as an Adjunct to Percutaneous Coronary Intervention for the Treatment of Acute Myocardial Infarction. J Am Coll Cardiol. 2014;63:1857–65.CrossRefPubMed
12.
go back to reference Atar D, Arheden H, Berdeaux A, Bonnet J-L, Carlsson M, Clemmensen P, Cuvier V, Danchin N, Dubois-Rande J-L, Engblom H, Erlinge D, Firat H, Halvorsen S, Hansen HS, Hauke W, Heiberg E, Koul S, Larsen A-I, Le Corvoisier P, Nordrehaug JE, Paganelli F, Pruss RM, Rousseau H, Schaller S, Sonou G, Tuseth V, Veys J, Vicaut E, Jensen SE. Effect of intravenous TRO40303 as an adjunct to primary percutaneous coronary intervention for acute ST-elevation myocardial infarction: MITOCARE study results. Eur Heart J. 2014;36:1–8. Atar D, Arheden H, Berdeaux A, Bonnet J-L, Carlsson M, Clemmensen P, Cuvier V, Danchin N, Dubois-Rande J-L, Engblom H, Erlinge D, Firat H, Halvorsen S, Hansen HS, Hauke W, Heiberg E, Koul S, Larsen A-I, Le Corvoisier P, Nordrehaug JE, Paganelli F, Pruss RM, Rousseau H, Schaller S, Sonou G, Tuseth V, Veys J, Vicaut E, Jensen SE. Effect of intravenous TRO40303 as an adjunct to primary percutaneous coronary intervention for acute ST-elevation myocardial infarction: MITOCARE study results. Eur Heart J. 2014;36:1–8.
13.
go back to reference Heiberg E, Sjögren J, Ugander M, Carlsson M, Engblom H, Arheden H. Design and validation of Segment--freely available software for cardiovascular image analysis. BMC Med Imaging. 2010;10:1.CrossRefPubMedPubMedCentral Heiberg E, Sjögren J, Ugander M, Carlsson M, Engblom H, Arheden H. Design and validation of Segment--freely available software for cardiovascular image analysis. BMC Med Imaging. 2010;10:1.CrossRefPubMedPubMedCentral
14.
go back to reference Engblom H, Tufvesson J, Jablonowski R, Carlsson M, Aletras AH, Hoffmann P, Jacquier A, Kober F, Metzler B, Erlinge D, Atar D, Arheden H, Heiberg E. A new automatic algorithm for quantification of myocardial infarction imaged by late gadolinium enhancement cardiovascular magnetic resonance: experimental validation and comparison to expert delineations in multi-center, multi-vendor patient data. J Cardiovasc Magn Reson. 2016;18:27.CrossRefPubMedPubMedCentral Engblom H, Tufvesson J, Jablonowski R, Carlsson M, Aletras AH, Hoffmann P, Jacquier A, Kober F, Metzler B, Erlinge D, Atar D, Arheden H, Heiberg E. A new automatic algorithm for quantification of myocardial infarction imaged by late gadolinium enhancement cardiovascular magnetic resonance: experimental validation and comparison to expert delineations in multi-center, multi-vendor patient data. J Cardiovasc Magn Reson. 2016;18:27.CrossRefPubMedPubMedCentral
15.
16.
go back to reference Heiberg E, Ugander M, Engblom H, Götberg M, Olivecrona GK, Erlinge D, Arheden H. Automated quantification of myocardial infarction from MR images by accounting for partial volume effects: animal, phantom, and human study. Radiology. 2008;246:581–8.CrossRefPubMed Heiberg E, Ugander M, Engblom H, Götberg M, Olivecrona GK, Erlinge D, Arheden H. Automated quantification of myocardial infarction from MR images by accounting for partial volume effects: animal, phantom, and human study. Radiology. 2008;246:581–8.CrossRefPubMed
17.
go back to reference Ugander M, Soneson H, Engblom H, van der Pals J, Erlinge D, Heiberg E, Arheden H. Quantification of myocardium at risk in myocardial perfusion SPECT by co-registration and fusion with delayed contrast-enhanced magnetic resonance imaging--an experimental ex vivo study. Clin Physiol Funct Imaging. 2012;32:33–8.CrossRefPubMed Ugander M, Soneson H, Engblom H, van der Pals J, Erlinge D, Heiberg E, Arheden H. Quantification of myocardium at risk in myocardial perfusion SPECT by co-registration and fusion with delayed contrast-enhanced magnetic resonance imaging--an experimental ex vivo study. Clin Physiol Funct Imaging. 2012;32:33–8.CrossRefPubMed
18.
go back to reference Altman DG, Bland JM. Measurement in Medicine: The Analysis of Method Comparison Studies. Stat. 1983;32:307. Altman DG, Bland JM. Measurement in Medicine: The Analysis of Method Comparison Studies. Stat. 1983;32:307.
19.
go back to reference Bieri O, Scheffler K. Fundamentals of balanced steady state free precession MRI. J Magn Res Imaging. 2013:38(1):2–11. Bieri O, Scheffler K. Fundamentals of balanced steady state free precession MRI. J Magn Res Imaging. 2013:38(1):2–11.
20.
go back to reference Ugander M, Bagi PS, Oki AJ, Chen B, Hsu L-Y, Aletras AH, Shah S, Greiser A, Kellman P, Arai AE. Myocardial Edema as Detected by Pre-Contrast T1 and T2 CMR Delineates Area at Risk Associated With Acute Myocardial Infarction. JACC Cardiovasc Imaging. 2012;5:596–603.CrossRefPubMedPubMedCentral Ugander M, Bagi PS, Oki AJ, Chen B, Hsu L-Y, Aletras AH, Shah S, Greiser A, Kellman P, Arai AE. Myocardial Edema as Detected by Pre-Contrast T1 and T2 CMR Delineates Area at Risk Associated With Acute Myocardial Infarction. JACC Cardiovasc Imaging. 2012;5:596–603.CrossRefPubMedPubMedCentral
21.
go back to reference Arheden H, Saeed M, Higgins CB, Gao DW, Bremerich J, Wyttenbach R, Dae MW, Wendland MF. Measurement of the distribution volume of gadopentetate dimeglumine at echo-planar MR imaging to quantify myocardial infarction: comparison with 99mTc-DTPA autoradiography in rats. Radiology. 1999;211:698–708.CrossRefPubMed Arheden H, Saeed M, Higgins CB, Gao DW, Bremerich J, Wyttenbach R, Dae MW, Wendland MF. Measurement of the distribution volume of gadopentetate dimeglumine at echo-planar MR imaging to quantify myocardial infarction: comparison with 99mTc-DTPA autoradiography in rats. Radiology. 1999;211:698–708.CrossRefPubMed
22.
go back to reference Arheden H, Saeed M, Higgins CB, Gao DW, Ursell PC, Bremerich J, Wyttenbach R, Dae MW, Wendland MF. Reperfused rat myocardium subjected to various durations of ischemia: estimation of the distribution volume of contrast material with echo-planar MR imaging. Radiology. 2000;215:520–8.CrossRefPubMed Arheden H, Saeed M, Higgins CB, Gao DW, Ursell PC, Bremerich J, Wyttenbach R, Dae MW, Wendland MF. Reperfused rat myocardium subjected to various durations of ischemia: estimation of the distribution volume of contrast material with echo-planar MR imaging. Radiology. 2000;215:520–8.CrossRefPubMed
23.
go back to reference Jablonowski R, Engblom H, Kanski M, Nordlund D, Koul S, van der Pals J, Englund E, Heiberg E, Erlinge D, Carlsson M, Arheden H. Contrast-Enhanced CMR Overestimates Early Myocardial Infarct Size: Mechanistic Insights Using ECV Measurements on Day 1 and Day 7. JACC Cardiovasc Imaging. 2015;8:1379–89.CrossRefPubMed Jablonowski R, Engblom H, Kanski M, Nordlund D, Koul S, van der Pals J, Englund E, Heiberg E, Erlinge D, Carlsson M, Arheden H. Contrast-Enhanced CMR Overestimates Early Myocardial Infarct Size: Mechanistic Insights Using ECV Measurements on Day 1 and Day 7. JACC Cardiovasc Imaging. 2015;8:1379–89.CrossRefPubMed
24.
go back to reference Wendland MF, Saeed M, Lauerma K, Derugin N, Mintorovitch J, Cavagna FM, Higgins CB. Alterations inT1 of normal and reperfused infarcted myocardium after Gd-BOPTA versus GD-DTPA on inversion recovery EPI. Magn Reson Med. 1997;37:448–56.CrossRefPubMed Wendland MF, Saeed M, Lauerma K, Derugin N, Mintorovitch J, Cavagna FM, Higgins CB. Alterations inT1 of normal and reperfused infarcted myocardium after Gd-BOPTA versus GD-DTPA on inversion recovery EPI. Magn Reson Med. 1997;37:448–56.CrossRefPubMed
25.
go back to reference Ugander M, Oki AJ, Hsu LY, Kellman P, Greiser A, Aletras AH, Sibley CT, Chen MY, Patricia Bandettini W, Arai AE. Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. Eur Heart J. 2012;33:1268–78.CrossRefPubMedPubMedCentral Ugander M, Oki AJ, Hsu LY, Kellman P, Greiser A, Aletras AH, Sibley CT, Chen MY, Patricia Bandettini W, Arai AE. Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. Eur Heart J. 2012;33:1268–78.CrossRefPubMedPubMedCentral
26.
go back to reference Khoshnood A, Carlsson M, Akbarzadeh M, Bhiladvala P, Roijer A, Bodetoft S, Höglund P, Zughaft D, Todorova L, Erlinge DEU. The Effects of Oxygen Therapy on Myocardial Salvage in ST Elevation Myocardial Infarction Treated with Acute Percutaneous Coronary Intervention: The Supplemental Oxygen in Catheterized Coronary Emergency Reperfusion (SOCCER) Study. Cardiology. 2015;132:16–21.CrossRefPubMed Khoshnood A, Carlsson M, Akbarzadeh M, Bhiladvala P, Roijer A, Bodetoft S, Höglund P, Zughaft D, Todorova L, Erlinge DEU. The Effects of Oxygen Therapy on Myocardial Salvage in ST Elevation Myocardial Infarction Treated with Acute Percutaneous Coronary Intervention: The Supplemental Oxygen in Catheterized Coronary Emergency Reperfusion (SOCCER) Study. Cardiology. 2015;132:16–21.CrossRefPubMed
27.
go back to reference De Coster PM, Wijns W, Cauwe F, Robert A, Beckers C, Melin JA. Area-at-risk determination by technetium-99 m-hexakis-2-methoxyisobutyl isonitrile in experimental reperfused myocardial infarction. Circulation. 1990;82:2152–62.CrossRefPubMed De Coster PM, Wijns W, Cauwe F, Robert A, Beckers C, Melin JA. Area-at-risk determination by technetium-99 m-hexakis-2-methoxyisobutyl isonitrile in experimental reperfused myocardial infarction. Circulation. 1990;82:2152–62.CrossRefPubMed
28.
go back to reference Garcia-Dorado D, Théroux P, Duran JM, Solares J, Alonso J, Sanz E, Munoz R, Elizaga J, Botas J, Fernandez-Avilés F. Selective inhibition of the contractile apparatus. A new approach to modification of infarct size, infarct composition, and infarct geometry during coronary artery occlusion and reperfusion. Circulation. 1992;85:1160–74.CrossRefPubMed Garcia-Dorado D, Théroux P, Duran JM, Solares J, Alonso J, Sanz E, Munoz R, Elizaga J, Botas J, Fernandez-Avilés F. Selective inhibition of the contractile apparatus. A new approach to modification of infarct size, infarct composition, and infarct geometry during coronary artery occlusion and reperfusion. Circulation. 1992;85:1160–74.CrossRefPubMed
29.
go back to reference Engblom H, Heiberg E, Erlinge D, Jensen SE, Nordrehaug JE, Dubois-Randé J-L, Halvorsen S, Hoffmann P, Koul S, Carlsson M, Atar D, Arheden H. Sample Size in Clinical Cardioprotection Trials Using Myocardial Salvage Index, Infarct Size, or Biochemical Markers as Endpoint. J Am Heart Assoc. 2016;5:e002708.CrossRefPubMedPubMedCentral Engblom H, Heiberg E, Erlinge D, Jensen SE, Nordrehaug JE, Dubois-Randé J-L, Halvorsen S, Hoffmann P, Koul S, Carlsson M, Atar D, Arheden H. Sample Size in Clinical Cardioprotection Trials Using Myocardial Salvage Index, Infarct Size, or Biochemical Markers as Endpoint. J Am Heart Assoc. 2016;5:e002708.CrossRefPubMedPubMedCentral
30.
go back to reference Bulluck H, White SK, Rosmini S, Bhuva A, Treibel TA, Fontana M, Abdel-Gadir A, Herrey A, Manisty C, Wan SMY, Groves A, Menezes L, Moon JC, Hausenloy DJ. T1 mapping and T2 mapping at 3 T for quantifying the area-at-risk in reperfused STEMI patients. J Cardiovasc Magn Reson. 2015;17:73.CrossRefPubMedPubMedCentral Bulluck H, White SK, Rosmini S, Bhuva A, Treibel TA, Fontana M, Abdel-Gadir A, Herrey A, Manisty C, Wan SMY, Groves A, Menezes L, Moon JC, Hausenloy DJ. T1 mapping and T2 mapping at 3 T for quantifying the area-at-risk in reperfused STEMI patients. J Cardiovasc Magn Reson. 2015;17:73.CrossRefPubMedPubMedCentral
Metadata
Title
Experimental validation of contrast-enhanced SSFP cine CMR for quantification of myocardium at risk in acute myocardial infarction
Authors
David Nordlund
Mikael Kanski
Robert Jablonowski
Sasha Koul
David Erlinge
Marcus Carlsson
Henrik Engblom
Anthony H. Aletras
Håkan Arheden
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-017-0325-y

Other articles of this Issue 1/2017

Journal of Cardiovascular Magnetic Resonance 1/2017 Go to the issue