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Published in: Journal of Cardiovascular Magnetic Resonance 1/2014

Open Access 01-12-2014 | Research

Non-invasive assessment of cardiac function and pulmonary vascular resistance in an canine model of acute thromboembolic pulmonary hypertension using 4D flow cardiovascular magnetic resonance

Authors: Alejandro Roldán-Alzate, Alex Frydrychowicz, Kevin M Johnson, Heidi Kellihan, Naomi C Chesler, Oliver Wieben, Christopher J François

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2014

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Abstract

Background

The purpose of this study was to quantify right (RV) and left (LV) ventricular function, pulmonary artery flow (QP), tricuspid valve regurgitation velocity (TRV), and aorta flow (QS) from a single 4D flow cardiovascular magnetic resonance (CMR) (time-resolved three-directionally motion encoded CMR) sequence in a canine model of acute thromboembolic pulmonary hypertension (PH).

Methods

Acute PH was induced in six female beagles by microbead injection into the right atrium. Pulmonary arterial (PAP) and pulmonary capillary wedge (PCWP) pressures and cardiac output (CO) were measured by right heart catheterization (RHC) at baseline and following induction of acute PH. Pulmonary vascular resistance (PVRRHC) was calculated from RHC values of PAP, PCWP and CO (PVRRHC = (PAP-PCWP)/CO). Cardiac magnetic resonance (CMR) was performed on a 3 T scanner at baseline and following induction of acute PH. RV and LV end-diastolic (EDV) and end-systolic (ESV) volumes were determined from both CINE balanced steady-state free precession (bSSFP) and 4D flow CMR magnitude images. QP, TRV, and QS were determined from manually placed cutplanes in the 4D flow CMR flow-sensitive images in the main (MPA), right (RPA), and left (LPA) pulmonary arteries, the tricuspid valve (TRV), and aorta respectively. MPA, RPA, and LPA flow was also measured using two-dimensional flow-sensitive (2D flow) CMR.

Results

Biases between 4D flow CMR and bSSFP were 0.8 mL and 1.6 mL for RV EDV and RV ESV, respectively, and 0.8 mL and 4 mL for LV EDV and LV ESV, respectively. Flow in the MPA, RPA, and LPA did not change after induction of acute PAH (p = 0.42-0.81). MPA, RPA, and LPA flow determined with 4D flow CMR was significantly lower than with 2D flow (p < 0.05). The correlation between QP/TRV and PVRRHC was 0.95. The average QP/QS was 0.96 ± 0.11.

Conclusions

Using both magnitude and flow-sensitive data from a single 4D flow CMR acquisition permits simultaneous quantification of cardiac function and cardiopulmonary hemodynamic parameters important in the assessment of PH.
Appendix
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Literature
1.
go back to reference D’Alonzo GE, Barst RJ, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, Fishman AP, Goldring RM, Groves BM, Kernis JT, Levy PS, Pietra GG, Reid LM, Reeves JT, Rich S, Vreim CE, Williams GW, Wu M: Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann Intern Med. 1991, 115: 343-9. 10.7326/0003-4819-115-5-343.CrossRefPubMed D’Alonzo GE, Barst RJ, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, Fishman AP, Goldring RM, Groves BM, Kernis JT, Levy PS, Pietra GG, Reid LM, Reeves JT, Rich S, Vreim CE, Williams GW, Wu M: Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann Intern Med. 1991, 115: 343-9. 10.7326/0003-4819-115-5-343.CrossRefPubMed
2.
go back to reference Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, Solomon SD, Louie EK, Schiller NB: Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American society of echocardiography endorsed by the European association of echocardiography, a registered branch of the European society of cardiology, and the Canadian society of echocardiography. J Am Soc Echocardiogr. 2010, 23: 685-713. 10.1016/j.echo.2010.05.010. quiz 786–688CrossRefPubMed Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, Solomon SD, Louie EK, Schiller NB: Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American society of echocardiography endorsed by the European association of echocardiography, a registered branch of the European society of cardiology, and the Canadian society of echocardiography. J Am Soc Echocardiogr. 2010, 23: 685-713. 10.1016/j.echo.2010.05.010. quiz 786–688CrossRefPubMed
4.
go back to reference Simonneau G, Robbins IM, Beghetti M, Channick RN, Delcroix M, Denton CP, Elliott CG, Gaine SP, Gladwin MT, Jing ZC, Krowka MJ, Langleben D, Nakanishi N, Souza R: Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol. 2009, 54: S43-54. 10.1016/j.jacc.2009.04.012.CrossRefPubMed Simonneau G, Robbins IM, Beghetti M, Channick RN, Delcroix M, Denton CP, Elliott CG, Gaine SP, Gladwin MT, Jing ZC, Krowka MJ, Langleben D, Nakanishi N, Souza R: Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol. 2009, 54: S43-54. 10.1016/j.jacc.2009.04.012.CrossRefPubMed
5.
go back to reference Abbas AE, Fortuin FD, Schiller NB, Appleton CP, Moreno CA, Lester SJ: A simple method for noninvasive estimation of pulmonary vascular resistance. J Am Coll Cardiol. 2003, 41: 1021-7. 10.1016/S0735-1097(02)02973-X.CrossRefPubMed Abbas AE, Fortuin FD, Schiller NB, Appleton CP, Moreno CA, Lester SJ: A simple method for noninvasive estimation of pulmonary vascular resistance. J Am Coll Cardiol. 2003, 41: 1021-7. 10.1016/S0735-1097(02)02973-X.CrossRefPubMed
6.
go back to reference Clay S, Alfakih K, Messroghli DR, Jones T, Ridgway JP, Sivananthan MU: The reproducibility of left ventricular volume and mass measurements: a comparison between dual-inversion-recovery black-blood sequence and SSFP. Eur Radiol. 2006, 16: 32-7. 10.1007/s00330-005-2853-3.CrossRefPubMed Clay S, Alfakih K, Messroghli DR, Jones T, Ridgway JP, Sivananthan MU: The reproducibility of left ventricular volume and mass measurements: a comparison between dual-inversion-recovery black-blood sequence and SSFP. Eur Radiol. 2006, 16: 32-7. 10.1007/s00330-005-2853-3.CrossRefPubMed
7.
go back to reference Hudsmith LE, Petersen SE, Francis JM, Robson MD, Neubauer S: Normal human left and right ventricular and left atrial dimensions using steady state free precession magnetic resonance imaging. J Cardiovasc Magn Reson. 2005, 7: 775-82. 10.1080/10976640500295516.CrossRefPubMed Hudsmith LE, Petersen SE, Francis JM, Robson MD, Neubauer S: Normal human left and right ventricular and left atrial dimensions using steady state free precession magnetic resonance imaging. J Cardiovasc Magn Reson. 2005, 7: 775-82. 10.1080/10976640500295516.CrossRefPubMed
8.
go back to reference Maceira AM, Prasad SK, Khan M, Pennell DJ: Normalized left ventricular systolic and diastolic function by steady state free precession cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2006, 8: 417-26. 10.1080/10976640600572889.CrossRefPubMed Maceira AM, Prasad SK, Khan M, Pennell DJ: Normalized left ventricular systolic and diastolic function by steady state free precession cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2006, 8: 417-26. 10.1080/10976640600572889.CrossRefPubMed
9.
go back to reference Grothues F, Moon JC, Bellenger NG, Smith GS, Klein HU, Pennell DJ: Interstudy reproducibility of right ventricular volumes, function, and mass with cardiovascular magnetic resonance. Am Heart J. 2004, 147: 218-23. 10.1016/j.ahj.2003.10.005.CrossRefPubMed Grothues F, Moon JC, Bellenger NG, Smith GS, Klein HU, Pennell DJ: Interstudy reproducibility of right ventricular volumes, function, and mass with cardiovascular magnetic resonance. Am Heart J. 2004, 147: 218-23. 10.1016/j.ahj.2003.10.005.CrossRefPubMed
10.
go back to reference Catalano O, Antonaci S, Opasich C, Moro G, Mussida M, Perotti M, Calsamiglia G, Frascaroli M, Baldi M, Cobelli F: Intra-observer and interobserver reproducibility of right ventricle volumes, function and mass by cardiac magnetic resonance. J Cardiovasc Med (Hagerstown). 2007, 8: 807-14. 10.2459/JCM.0b013e32801105ef.CrossRef Catalano O, Antonaci S, Opasich C, Moro G, Mussida M, Perotti M, Calsamiglia G, Frascaroli M, Baldi M, Cobelli F: Intra-observer and interobserver reproducibility of right ventricle volumes, function and mass by cardiac magnetic resonance. J Cardiovasc Med (Hagerstown). 2007, 8: 807-14. 10.2459/JCM.0b013e32801105ef.CrossRef
11.
go back to reference Maceira AM, Prasad SK, Khan M, Pennell DJ: Reference right ventricular systolic and diastolic function normalized to age, gender and body surface area from steady-state free precession cardiovascular magnetic resonance. Eur Heart J. 2006, 27: 2879-88. 10.1093/eurheartj/ehl336.CrossRefPubMed Maceira AM, Prasad SK, Khan M, Pennell DJ: Reference right ventricular systolic and diastolic function normalized to age, gender and body surface area from steady-state free precession cardiovascular magnetic resonance. Eur Heart J. 2006, 27: 2879-88. 10.1093/eurheartj/ehl336.CrossRefPubMed
12.
go back to reference Gu T, Korosec FR, Block WF, Fain SB, Turk Q, Lum D, Zhou Y, Grist TM, Haughton V, Mistretta CA: PC VIPR: a high-speed 3D phase-contrast method for flow quantification and high-resolution angiography. AJNR Am J Neuroradiol. 2005, 26: 743-9.PubMed Gu T, Korosec FR, Block WF, Fain SB, Turk Q, Lum D, Zhou Y, Grist TM, Haughton V, Mistretta CA: PC VIPR: a high-speed 3D phase-contrast method for flow quantification and high-resolution angiography. AJNR Am J Neuroradiol. 2005, 26: 743-9.PubMed
13.
go back to reference Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O: 4D flow MRI. J Magn Reson Imaging. 2012, 36: 1015-36. 10.1002/jmri.23632.CrossRefPubMed Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O: 4D flow MRI. J Magn Reson Imaging. 2012, 36: 1015-36. 10.1002/jmri.23632.CrossRefPubMed
14.
15.
go back to reference Frydrychowicz A, Wieben O, Niespodzany E, Reeder SB, Johnson KM, Francois CJ: Quantification of thoracic blood flow using volumetric magnetic resonance imaging with radial velocity encoding: in vivo validation. Invest Radiol. 2013, 48: 819-25. 10.1097/RLI.0b013e31829a4f2f.CrossRefPubMed Frydrychowicz A, Wieben O, Niespodzany E, Reeder SB, Johnson KM, Francois CJ: Quantification of thoracic blood flow using volumetric magnetic resonance imaging with radial velocity encoding: in vivo validation. Invest Radiol. 2013, 48: 819-25. 10.1097/RLI.0b013e31829a4f2f.CrossRefPubMed
16.
go back to reference Liu J, Wieben O, Jung Y, Samsonov AA, Reeder SB, Block WF: Single breathhold cardiac CINE imaging with multi-echo three-dimensional hybrid radial SSFP acquisition. J Magn Reson Imaging. 2010, 32: 434-40. 10.1002/jmri.22269.CrossRefPubMed Liu J, Wieben O, Jung Y, Samsonov AA, Reeder SB, Block WF: Single breathhold cardiac CINE imaging with multi-echo three-dimensional hybrid radial SSFP acquisition. J Magn Reson Imaging. 2010, 32: 434-40. 10.1002/jmri.22269.CrossRefPubMed
17.
go back to reference Garcia-Alvarez A, Fernandez-Friera L, Mirelis JG, Sawit S, Nair A, Kallman J, Fuster V, Sanz J: Non-invasive estimation of pulmonary vascular resistance with cardiac magnetic resonance. Eur Heart J. 2011, 32: 2438-45. 10.1093/eurheartj/ehr173.CrossRefPubMed Garcia-Alvarez A, Fernandez-Friera L, Mirelis JG, Sawit S, Nair A, Kallman J, Fuster V, Sanz J: Non-invasive estimation of pulmonary vascular resistance with cardiac magnetic resonance. Eur Heart J. 2011, 32: 2438-45. 10.1093/eurheartj/ehr173.CrossRefPubMed
18.
go back to reference Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M: Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med. 2008, 60: 1218-31. 10.1002/mrm.21778.CrossRefPubMed Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M: Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med. 2008, 60: 1218-31. 10.1002/mrm.21778.CrossRefPubMed
19.
go back to reference Oudiz RJ: Pulmonary hypertension associated with left-sided heart disease. Clin Chest Med. 2007, 28: 233-41. 10.1016/j.ccm.2006.12.001.CrossRefPubMed Oudiz RJ: Pulmonary hypertension associated with left-sided heart disease. Clin Chest Med. 2007, 28: 233-41. 10.1016/j.ccm.2006.12.001.CrossRefPubMed
20.
go back to reference Greil GF, Boettger T, Germann S, Klumpp B, Baltes C, Kozerke S, Bialkowski A, Urschitz MS, Miller S, Wolf I, Meinzer HP, Sieverding L: Quantitative assessment of ventricular function using three-dimensional SSFP magnetic resonance angiography. J Magn Reson Imaging. 2007, 26: 288-95. 10.1002/jmri.20967.CrossRefPubMed Greil GF, Boettger T, Germann S, Klumpp B, Baltes C, Kozerke S, Bialkowski A, Urschitz MS, Miller S, Wolf I, Meinzer HP, Sieverding L: Quantitative assessment of ventricular function using three-dimensional SSFP magnetic resonance angiography. J Magn Reson Imaging. 2007, 26: 288-95. 10.1002/jmri.20967.CrossRefPubMed
21.
go back to reference Peters DC, Korosec FR, Grist TM, Block WF, Holden JE, Vigen KK, Mistretta CA: Undersampled projection reconstruction applied to MR angiography. Magn Reson Med. 2000, 43: 91-101. 10.1002/(SICI)1522-2594(200001)43:1<91::AID-MRM11>3.0.CO;2-4.CrossRefPubMed Peters DC, Korosec FR, Grist TM, Block WF, Holden JE, Vigen KK, Mistretta CA: Undersampled projection reconstruction applied to MR angiography. Magn Reson Med. 2000, 43: 91-101. 10.1002/(SICI)1522-2594(200001)43:1<91::AID-MRM11>3.0.CO;2-4.CrossRefPubMed
22.
go back to reference Garcia-Alvarez A, Fernandez-Friera L, Garcia-Ruiz JM, Nuno-Ayala M, Pereda D, Fernandez-Jimenez R, Guzman G, Sanchez-Quintana D, Alberich-Bayarri A, Pastor-Escuredo D, Sanz-Rosa D, Garcia-Preito J, Gonzalez-Mirelis JG, Pizarro G, Jimenez-Borreguero LJ, Fuster V, Sanz J, Ibanez B: Noninvasive monitoring of serial changes in pulmonary vascular resistance and acute vasodilator testing using cardiac magnetic resonance. J Am Coll Cardiol. 2013, 62: 1621-31. 10.1016/j.jacc.2013.07.037.CrossRefPubMed Garcia-Alvarez A, Fernandez-Friera L, Garcia-Ruiz JM, Nuno-Ayala M, Pereda D, Fernandez-Jimenez R, Guzman G, Sanchez-Quintana D, Alberich-Bayarri A, Pastor-Escuredo D, Sanz-Rosa D, Garcia-Preito J, Gonzalez-Mirelis JG, Pizarro G, Jimenez-Borreguero LJ, Fuster V, Sanz J, Ibanez B: Noninvasive monitoring of serial changes in pulmonary vascular resistance and acute vasodilator testing using cardiac magnetic resonance. J Am Coll Cardiol. 2013, 62: 1621-31. 10.1016/j.jacc.2013.07.037.CrossRefPubMed
23.
go back to reference Swift AJ, Rajaram S, Hurdman J, Hill C, Davies C, Sproson TW, Morton AC, Capener D, Elliot C, Condliffe R, Wild JM, Kiely DG: Noninvasive estimation of PA pressure, flow, and resistance with CMR imaging: derivation and prospective validation study from the ASPIRE registry. JACC Cardiovasc Imaging. 2013, 6: 1036-47. 10.1016/j.jcmg.2013.01.013.CrossRefPubMed Swift AJ, Rajaram S, Hurdman J, Hill C, Davies C, Sproson TW, Morton AC, Capener D, Elliot C, Condliffe R, Wild JM, Kiely DG: Noninvasive estimation of PA pressure, flow, and resistance with CMR imaging: derivation and prospective validation study from the ASPIRE registry. JACC Cardiovasc Imaging. 2013, 6: 1036-47. 10.1016/j.jcmg.2013.01.013.CrossRefPubMed
24.
go back to reference Reiter G, Reiter U, Kovacs G, Kainz B, Schmidt K, Maier R, Olschewski H, Rienmueller R: Magnetic resonance-derived 3-dimensional blood flow patterns in the main pulmonary artery as a marker of pulmonary hypertension and a measure of elevated mean pulmonary arterial pressure. Circ Cardiovasc Imaging. 2008, 1: 23-30. 10.1161/CIRCIMAGING.108.780247.CrossRefPubMed Reiter G, Reiter U, Kovacs G, Kainz B, Schmidt K, Maier R, Olschewski H, Rienmueller R: Magnetic resonance-derived 3-dimensional blood flow patterns in the main pulmonary artery as a marker of pulmonary hypertension and a measure of elevated mean pulmonary arterial pressure. Circ Cardiovasc Imaging. 2008, 1: 23-30. 10.1161/CIRCIMAGING.108.780247.CrossRefPubMed
25.
go back to reference Fratz S, Schuhbaeck A, Buchner C, Busch R, Meierhofer C, Martinoff S, Hess J, Stern H: Comparison of accuracy of axial slices versus short-axis slices for measuring ventricular volumes by cardiac magnetic resonance in patients with corrected tetralogy of fallot. Am J Cardiol. 2009, 103: 1764-9. 10.1016/j.amjcard.2009.02.030.CrossRefPubMed Fratz S, Schuhbaeck A, Buchner C, Busch R, Meierhofer C, Martinoff S, Hess J, Stern H: Comparison of accuracy of axial slices versus short-axis slices for measuring ventricular volumes by cardiac magnetic resonance in patients with corrected tetralogy of fallot. Am J Cardiol. 2009, 103: 1764-9. 10.1016/j.amjcard.2009.02.030.CrossRefPubMed
26.
go back to reference Hui-li G: The management of acute pulmonary arterial hypertension. Cardiovasc Ther. 2011, 29: 153-75. 10.1111/j.1755-5922.2009.00095.x.CrossRefPubMed Hui-li G: The management of acute pulmonary arterial hypertension. Cardiovasc Ther. 2011, 29: 153-75. 10.1111/j.1755-5922.2009.00095.x.CrossRefPubMed
27.
go back to reference Bieging ET, Frydrychowicz A, Wentland A, Landgraf BR, Johnson KM, Wieben O, Francois CJ: In vivo three-dimensional MR wall shear stress estimation in ascending aortic dilatation. J Magn Reson Imaging. 2011, 33: 589-97. 10.1002/jmri.22485.CrossRefPubMed Bieging ET, Frydrychowicz A, Wentland A, Landgraf BR, Johnson KM, Wieben O, Francois CJ: In vivo three-dimensional MR wall shear stress estimation in ascending aortic dilatation. J Magn Reson Imaging. 2011, 33: 589-97. 10.1002/jmri.22485.CrossRefPubMed
28.
go back to reference Frydrychowicz A, Berger A, Russe MF, Stalder AF, Harloff A, Dittrich S, Hennig J, Langer M, Markl M: Time-resolved magnetic resonance angiography and flow-sensitive 4-dimensional magnetic resonance imaging at 3 Tesla for blood flow and wall shear stress analysis. J Thorac Cardiovasc Surg. 2008, 136: 400-7. 10.1016/j.jtcvs.2008.02.062.CrossRefPubMed Frydrychowicz A, Berger A, Russe MF, Stalder AF, Harloff A, Dittrich S, Hennig J, Langer M, Markl M: Time-resolved magnetic resonance angiography and flow-sensitive 4-dimensional magnetic resonance imaging at 3 Tesla for blood flow and wall shear stress analysis. J Thorac Cardiovasc Surg. 2008, 136: 400-7. 10.1016/j.jtcvs.2008.02.062.CrossRefPubMed
29.
go back to reference Markl M, Wallis W, Brendecke S, Simon J, Frydrychowicz A, Harloff A: Estimation of global aortic pulse wave velocity by flow-sensitive 4D MRI. Magn Reson Med. 2010, 63: 1575-82. 10.1002/mrm.22353.CrossRefPubMed Markl M, Wallis W, Brendecke S, Simon J, Frydrychowicz A, Harloff A: Estimation of global aortic pulse wave velocity by flow-sensitive 4D MRI. Magn Reson Med. 2010, 63: 1575-82. 10.1002/mrm.22353.CrossRefPubMed
30.
go back to reference Wentland AL, Wieben O, Francois CJ, Boncyk C, Munoz Del Rio A, Johnson KM, Grist TM, Frydrychowicz A: Aortic pulse wave velocity measurements with undersampled 4D flow-sensitive MRI: comparison with 2D and algorithm determination. J Magn Reson Imaging. 2013, 37: 853-9. 10.1002/jmri.23877.PubMedCentralCrossRefPubMed Wentland AL, Wieben O, Francois CJ, Boncyk C, Munoz Del Rio A, Johnson KM, Grist TM, Frydrychowicz A: Aortic pulse wave velocity measurements with undersampled 4D flow-sensitive MRI: comparison with 2D and algorithm determination. J Magn Reson Imaging. 2013, 37: 853-9. 10.1002/jmri.23877.PubMedCentralCrossRefPubMed
Metadata
Title
Non-invasive assessment of cardiac function and pulmonary vascular resistance in an canine model of acute thromboembolic pulmonary hypertension using 4D flow cardiovascular magnetic resonance
Authors
Alejandro Roldán-Alzate
Alex Frydrychowicz
Kevin M Johnson
Heidi Kellihan
Naomi C Chesler
Oliver Wieben
Christopher J François
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2014
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/1532-429X-16-23

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