Advertisement

Preliminary Feasibility of Stress Myocardial Elastography for the Detection of Coronary Artery Disease

  • Jad El Harake
    Affiliations
    Department of Biomedical Engineering, Columbia University, New York, New York, USA
    Search for articles by this author
  • Vincent Sayseng
    Affiliations
    Department of Biomedical Engineering, Columbia University, New York, New York, USA
    Search for articles by this author
  • Julien Grondin
    Affiliations
    Department of Radiology, Columbia University Irving Medical Center and New York–Presbyterian Hospital, New York, New York, USA
    Search for articles by this author
  • Rachel Weber
    Affiliations
    Department of Biomedical Engineering, Columbia University, New York, New York, USA
    Search for articles by this author
  • Andrew J. Einstein
    Affiliations
    Department of Radiology, Columbia University Irving Medical Center and New York–Presbyterian Hospital, New York, New York, USA

    Division of Cardiology, Columbia University Irving Medical Center and New York–Presbyterian Hospital, New York, New York, USA

    Department of Medicine, Columbia University Irving Medical Center and New York-Presbyterian Hospital, New York, New York, USA
    Search for articles by this author
  • Elisa Konofagou
    Correspondence
    Address correspondence to: Elisa Konofagou, Department of Biomedical Engineering, 1210 Amsterdam Avenue, ET 351, MC 8904, New York, NY 10027, USA.
    Affiliations
    Department of Biomedical Engineering, Columbia University, New York, New York, USA

    Department of Radiology, Columbia University Irving Medical Center and New York–Presbyterian Hospital, New York, New York, USA
    Search for articles by this author

      Abstract

      Myocardial elastography (ME) is a cardiac strain imaging technique that has been found capable of detecting a decrease in radial strain caused by ischemia or infarction in patients with coronary artery disease (CAD) as well as in a canine model. Prior studies have focused on rest imaging, but stress testing can reveal functional deficits caused by stenoses that are asymptomatic at rest. Therefore, it has been proposed that stress ME (S-ME) improves the detection of CAD. A novel strain difference (Δε) metric is presented and investigated in a canine model of induced ischemia, as well as in a study in human patients with CAD validated by myocardial perfusion imaging. In the canine model study, flow-limiting stenosis was induced by partial ligation in n = 2 canines, and stenosis was found to consistently reduce Δε in the affected myocardial regions compared with baseline, as well as compared to myocardial regions that are remote to the induced stenosis. In the clinical study, the median Δε was significantly lower (p < 0.05) in infarcted myocardial regions (–6.29%) than in those with normal perfusion (4.62%), with Δε in ischemic regions falling in between (–2.91%). The same trend was observed when considering radial strain during stress and, to a lesser degree, at rest alone. The results indicate that S-ME may be more sensitive to mild cases of CAD that are functionally asymptomatic at rest.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Ultrasound in Medicine and Biology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Al Moudi M
        • Sun Z
        • Lenzo N
        Diagnostic value of SPECT, PET and PET/CT in the diagnosis of coronary artery disease: A systematic review.
        Biomed Imaging Interv J. 2011; 7: e9
        • Amzulescu MS
        • De Craene M
        • Langet H
        • Pasquet A
        • Vancraeynest D
        • Pouleur AC
        • Vanoverschelde JL
        • Gerber BL.
        Myocardial strain imaging: Review of general principles, validation, and sources of discrepancies.
        Eur Heart J Cardiovasc Imaging. 2019; 20: 605-619
        • Biering-Sørensen T
        • Hoffmann S
        • Mogelvang R
        • Zeeberg Iversen A
        • Galatius S
        • Fritz-Hansen T
        • Bech J
        • Jensen JS
        Myocardial strain analysis by 2-dimensional speckle tracking echocardiography improves diagnostics of coronary artery stenosis in stable angina pectoris.
        Circ Cardiovasc Imaging. 2014; 7: 58-65
        • Cerqueira MD
        • Weissman NJ
        • Dilsizian V
        • Jacobs AK
        • Kaul S
        • Laskey WK
        • Pennell DJ
        • Rumberger JA
        • Ryan T
        • Verani MS
        American Heart Association Writing Group on Myocardial Segmentation and Registration for Cardiac Imaging. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the Cardiac Imaging Committee of the Council on.
        Clinical Cardiology of the American Heart Association. Circulation. 2002; 105: 539-542
        • Chen H
        • Shi H
        • Varghese T.
        Improvement of elastographic displacement estimation using a two-step cross-correlation method.
        Ultrasound Med Biol. 2007; 33: 48-56
        • Cusmà-Piccione M
        • Zito C
        • Oreto L
        • D'Angelo M
        • Tripepi S
        • Di Bella G
        • Todaro MC
        • Oreto G
        • Khandheria BK
        • Carerj S
        Longitudinal strain by automated function imaging detects single-vessel coronary artery disease in patients undergoing dipyridamole stress echocardiography.
        J Am Soc Echocardiogr. 2015; 28: 1214-1221
        • Dattilo G
        • Imbalzano E
        • Lamari A
        • Casale M
        • Paunovic N
        • Busacca P
        • Di Bella G.
        Ischemic heart disease and early diagnosis: Study on the predictive value of 2D strain.
        Int J Cardiol. 2016; 215: 150-156
        • Delgado V
        • Ypenburg C
        • van BRJ
        • Tops LF
        • Mollema SA
        • Marsan NA
        • Bleeker GB
        • Schalij MJ
        • Bax JJ.
        Assessment of left ventricular dyssynchrony by speckle tracking strain imaging.
        J Am Coll Cardiol. 2008; 51: 1944-1952
        • Einstein AJ
        • Weiner SD
        • Bernheim A
        • Kulon M
        • Bokhari S
        • Johnson LL
        • Moses JW
        • Balter S.
        Multiple testing, cumulative radiation dose, and clinical indications in patients undergoing myocardial perfusion imaging.
        JAMA. 2010; 304: 2137-2144
        • Ejlersen JA
        • Poulsen SH
        • Mortensen J
        • May O.
        Diagnostic value of layer-specific global longitudinal strain during adenosine stress in patients suspected of coronary artery disease.
        Int J Cardiovasc Imaging. 2017; 33: 473-480
        • Grondin J
        • Waase M
        • Gambhir A
        • Bunting E
        • Sayseng V
        • Konofagou EE.
        Evaluation of coronary artery disease using myocardial elastography with diverging wave imaging: Validation against myocardial perfusion imaging and coronary angiography.
        Ultrasound Med Biol. 2017; 43: 893-902
        • Grondin J
        • Lee C
        • Weber R
        • Konofagou EE.
        Myocardial strain imaging with electrocardiogram-gated and coherent compounding for early diagnosis of coronary artery disease.
        Ultrasound Med Biol. 2022; 48: 626-637
        • Hanekom L
        • Cho GY
        • Leano R
        • Jeffriess L
        • Marwick TH.
        Comparison of two-dimensional speckle and tissue Doppler strain measurement during dobutamine stress echocardiography: an angiographic correlation.
        Eur Heart J. 2007; 28: 1765-1772
        • Heyde B
        • Dei K
        • Byram B.
        Non-linear beamforming with ADMIRE to facilitate deformation imaging in cluttered cardiac ultrasound.
        Proc IEEE Int Ultrason Symp. 2016; : 1-4
        • Javadi MS
        • Lautamäki R
        • Merrill J
        • Voicu C
        • Epley W
        • McBride G
        • Bengel FM.
        Definition of vascular territories on myocardial perfusion images by integration with true coronary anatomy: A hybrid PET/CT analysis.
        J Nucl Med. 2010; 51: 198-203
        • Kallel F
        • Ophir J.
        A least-squares strain estimator for elastography.
        Ultrason Imaging. 1997; 19: 195-208
        • Kannel WB
        • Feinleib M.
        Natural history of angina pectoris in the Framingham study: Prognosis and survival.
        Am J Cardiol. 1972; 29: 154-163
        • Karacavus S
        • Celik A
        • Tutus A
        • Kula M
        • Oguzhan A
        • Ozdogru I
        • Kalay N.
        A comparison between quantitative gated myocardial perfusion scintigraphy and strain echocardiography as indicators of ventricular functions in patients with anterior myocardial infarction.
        World J Nucl Med. 2014; 13: 184-189
        • Knuuti J
        • Wijns W
        • Saraste A
        • Capodanno D
        • Barbato E
        • Funck-Brentano C
        • Prescott E
        • Storey RF
        • Deaton C
        • Cuisset T
        • Agewall S
        • Dickstein K
        • Edvardsen T
        • Escaned J
        • Gersh BJ
        • Svitil P
        • Gilard M
        • Hasdai D
        • Hatala R
        • Mahfoud F
        • Masip J
        • Muneretto C
        • Valgimigli M
        • Achenbach S
        • Bax JJ
        • ESC Scientific Document Group
        2019 ESC guidelines for the diagnosis and management of chronic coronary syndromes: The Task Force for the diagnosis and management of chronic coronary syndromes of the European Society of Cardiology (ESC).
        Eur Heart J. 2020; 41: 407-477
        • Konofagou EE
        • D'Hooge J
        • Ophir J
        Myocardial elastography—A feasibility study in vivo.
        Ultrasound Med Biol. 2002; 28: 475-482
        • Lee W
        • Ingrassia CM
        • Fung-kee-fung SD
        • Costa KD
        • Holmes JW
        • Konofagou EE.
        Theoretical quality assessment of myocardial elastography with in vivo validation.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2007; 54: 2233-2245
        • Lee WN
        • Provost J
        • Fujikura K
        • Wang J
        • Konofagou EE.
        In vivo study of myocardial elastography under graded ischemia conditions.
        Phys Med Biol. 2011; 56: 1155-1172
        • Lopata RGP
        • Nillesen MM
        • Thijssen JM
        • Kapusta L
        • de Korte CL.
        Three-dimensional cardiac strain imaging in healthy children using RF-data.
        Ultrasound Med Biol. 2011; 37: 1399-1408
        • Luo J
        • Fujikura K
        • Homma S
        • Konofagou EE.
        Myocardial elastography at both high temporal and spatial resolution for the detection of infarcts.
        Ultrasound Med Biol. 2007; 33: 1206-1223
        • Ma C
        • Varghese T.
        Comparison of cardiac displacement and strain imaging using ultrasound radiofrequency and envelope signals.
        Ultrasonics. 2013; 53: 782-792
        • McGowan JH
        • Martin W
        • Burgess MI
        • McCurrach G
        • Ray SG
        • McDonagh TA
        • Cleland JG.
        Validation of an echocardiographic wall motion index in heart failure due to ischaemic heart disease.
        Eur J Heart Fail. 2001; 3: 731-737
        • Montgomery DE
        • Puthumana JJ
        • Fox JM
        • Ogunyankin KO.
        Global longitudinal strain aids the detection of non-obstructive coronary artery disease in the resting echocardiogram.
        Eur Heart J Cardiovasc Imaging. 2012; 13: 579-587
        • Mukaddim RA
        • Meshram NH
        • Mitchell CC
        • Varghese T.
        Hierarchical motion estimation with Bayesian regularization in cardiac elastography: Simulation and in-vivo Validation.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2019; 66: 1708-1722
        • Mukaddim RA
        • Meshram NH
        • Varghese T.
        Locally optimized correlation-guided bayesian adaptive regularization for ultrasound strain imaging.
        Phys Med Biol. 2020; 65065008
        • Nagata Y
        • Kado Y
        • Onoue T
        • Otani K
        • Nakazono A
        • Otsuji Y
        • Takeuchi M.
        Impact of image quality on reliability of the measurements of left ventricular systolic function and global longitudinal strain in 2D echocardiography.
        Echo Res Pract. 2018; 5: 27-39
        • Potter E
        • Marwick TH.
        Assessment of left ventricular function by echocardiography.
        JACC Cardiovasc Imaging. 2018; 11: 260-274
        • Rumbinaite E
        • Zaliaduonyte-Peksiene D
        • Lapinskas T
        • Zvirblyte R
        • Karuzas A
        • Jonauskiene I
        • Viezelis M
        • Ceponiene I
        • Gustiene O
        • Slapikas R
        • Vaskelyte JJ.
        Early and late diastolic strain rate vs global longitudinal strain at rest and during dobutamine stress for the assessment of significant coronary artery stenosis in patients with a moderate and high probability of coronary artery disease.
        Echocardiography. 2016; 33: 1512-1522
        • Saraste A
        • Barbato E
        • Capodanno D
        • Edvardsen T
        • Prescott E
        • Achenbach S
        • Bax JJ
        • Wijns W
        • Knuuti J.
        Imaging in ESC clinical guidelines: Chronic coronary syndromes.
        Eur Heart J Cardiovasc Imaging. 2019; 20: 1187-1197
        • Sayseng V
        • Grondin J
        • Konofagou E.
        Optimization of transmit parameters in cardiac strain imaging with full and partial aperture coherent compounding.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2018; 65: 684-696
        • Sayseng V
        • Grondin J
        • Weber RA
        • Konofagou E.
        A comparison between unfocused and focused transmit strategies in cardiac strain imaging.
        Phys Med Biol. 2020; 65: 03NT01
        • Sayseng V
        • Ober RA
        • Grubb CS
        • Weber RA
        • Konofagou E.
        Monitoring canine myocardial infarction formation and recovery via transthoracic cardiac strain imaging.
        Ultrasound Med Biol. 2020; 46: 2785-2800
        • Senior R
        • Monaghan M
        • Becher H
        • Mayet J
        • Nihoyannopoulos P.
        Stress echocardiography for the diagnosis and risk stratification of patients with suspected or known coronary artery disease: A critical appraisal.
        Heart. 2005; 91: 427-436
        • Stankovic I
        • Putnikovic B
        • Cvjetan R
        • Milicevic P
        • Panic M
        • Kalezic-Radmili T
        • Mandaric T
        • Vidakovic R
        • Cvorovic V
        • Neskovic AN.
        Visual assessment vs. strain imaging for the detection of critical stenosis of the left anterior descending coronary artery in patients without a history of myocardial infarction.
        Eur Heart J Cardiovasc Imaging. 2015; 16: 402-409
        • Stendahl JC
        • Parajuli N
        • Lu A
        • Boutagy NE
        • Guerrera N
        • Alkhalil I
        • Lin BA
        • Staib LH
        • O'Donnell M
        • Duncan JS
        • Sinusas AJ
        Regional myocardial strain analysis via 2D speckle tracking echocardiography: Validation with sonomicrometry and correlation with regional blood flow in the presence of graded coronary stenoses and dobutamine stress.
        Cardiovasc Ultrasound. 2020; 18: 2
        • Tavakoli V
        • Kemp J
        • Dawn B
        • Stoddard M
        • Amini AA.
        Comparison of myocardial motion estimation methods based on simulated echocardiographic B-mode and RF data.
        Proc SPIE. 2010; 7626 (In: Medical Imaging 2010: Biomedical Applications in Molecular, Structural, and Functional Imaging): 207-218
        • Vesely MR
        • Dilsizian V.
        Nuclear cardiac stress testing in the era of molecular medicine.
        J Nucl Nuclear Med. 2008; 49: 399-413
        • Virani SS
        • Alonso A
        • Benjamin EJ
        • Bittencourt MS
        • Callaway CW
        • Carson AP
        • Chamberlain AM
        • Chang AR
        • Cheng S
        • Delling FN
        • Djousse L
        • Elkind MSV
        • Ferguson JF
        • Fornage M
        • Khan SS
        • Kissela BM
        • Knutson KL
        • Kwan TW
        • Lackland DT
        • Lewis TT
        • Lichtman JH
        • Longenecker CT
        • Loop MS
        • Lutsey PL
        • Martin SS
        • Matsushita K
        • Moran AE
        • Mussolino ME
        • Perak AM
        • Rosamond WD
        • Roth GA
        • Sampson UKA
        • Satou GM
        • Schroeder EB
        • Shah SH
        • Shay CM
        • Spartano NL
        • Stokes A
        • Tirschwell DL
        • VanWagner LB
        • Tsao CW.
        Heart disease and stroke statistics—2020 Update: A Report From the American Heart Association.
        Circulation. 2020; 141: e139-e596
        • Wang S
        • Lee WN
        • Provost J
        • Luo J
        • Konofagou EE.
        A composite high-frame-rate system for clinical cardiovascular imaging.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2008; 55: 2221-2233
        • Wickline SA
        • Verdonk ED
        • Wong AK
        • Shepard RK
        • Miller JG.
        Structural remodeling of human myocardial tissue after infarction: Quantification with ultrasonic backscatter.
        Circulation. 1992; 85: 259-268
        • Zervantonakis IK
        • Fung-Kee-Fung SD
        • Lee WN
        • Konofagou EE.
        A novel, view-independent method for strain mapping in myocardial elastography: Eliminating angle and centroid dependence.
        Phys Med Biol. 2007; 52: 4063-4080