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Magnetic resonance imaging of regional cardiac function in the mouse

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Abstract

In this paper we introduce an improved harmonic phase (HARP) analysis for complementary spatial modulation of magnetization (CSPAMM) tagging of the mouse left ventricular wall, which enables the determination of regional displacement fields with the same resolution as the corresponding CINE anatomical images. CINE MRI was used to measure global function, such as the ejection fraction. The method was tested on two healthy mouse hearts and two mouse hearts with a myocardial infarction, which was induced by a ligation of the left anterior descending coronary artery. We show that the regional displacement fields can be determined. The mean circumferential strain for the left ventricular wall of one of the healthy mice was −0.09 ± 0.04 (mean ± standard deviation), while for one of the infarcted mouse hearts strains of −0.02 ± 0.02 and −0.10 ± 0.03 were found in the infarcted and remote regions, respectively.

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References

  1. Ross R (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362:801–809

    Article  CAS  PubMed  Google Scholar 

  2. Glass CK, Witztum JL (2001) Atherosclerosis: the road ahead. Cell 104:503–516

    CAS  PubMed  Google Scholar 

  3. de Roos A, Kunz P, Lamb H, Kroft L, Langerak S, Doornbos J, van der WE (1999) Magnetic resonance imaging of ischemic heart disease: why cardiac magnetic resonance imaging will play a significant role in the management of patients with coronary artery disease. J Comput Assist Tomogr 23 (Suppl 1):S135-S141

    Google Scholar 

  4. Semelka RC, Tomei E, Wagner S, Mayo J, Caputo G, O‘Sullivan M, Parmley WW, Chatterjee K, Wolfe C, Higgins CB (1990) Interstudy reproducibility of dimensional and functional measurements between cine magnetic resonance studies in the morphologically abnormal left ventricle. Am Heart J 119:1367–1373

    CAS  PubMed  Google Scholar 

  5. Semelka RC, Tomei E, Wagner S, Mayo J, Kondo C, Suzuki J, Caputo GR, Higgins CB (1990) Normal left ventricular dimensions and function: interstudy reproducibility of measurements with cine MR imaging. Radiology 174:763–768

    CAS  PubMed  Google Scholar 

  6. Florentine MS, Grosskreutz CL, Chang W, Hartnett JA, Dunn VD, Ehrhardt JC, Fleagle SR, Collins SM, Marcus ML, Skorton DJ (1986) Measurement of left ventricular mass in vivo using gated nuclear magnetic resonance imaging. J Am Coll Cardiol 8:107–112

    Article  CAS  PubMed  Google Scholar 

  7. van der Geest RJ, Reiber JH (1999) Quantification in cardiac MRI . J Magn Reson Imaging 10:602–608

    Google Scholar 

  8. Reeder SB, Holmes AA, McVeigh ER, Forder JR (1999) Simultaneous noninvasive determination of regional myocardial perfusion and oxygen content in rabbits: toward direct measurement of myocardial oxygen consumption at MR imaging. Radiology 212:739–747

    CAS  PubMed  Google Scholar 

  9. Kroft LJ, de Roos A (1999) Blood pool contrast agents for cardiovascular MR imaging. J Magn Reson Imaging 10:395–403

    CAS  PubMed  Google Scholar 

  10. Streif JU, Herold V, Szimtenings M, Lanz TE, Nahrendorf M, Wiesmann F, Rommel E, Haase A (2003) In vivo time-resolved quantitative motion mapping of the murine myocardium with phase contrast MRI . Magn Reson Med 49:315–321

    PubMed  Google Scholar 

  11. Castillo E, Lima JA, Bluemke DA (2003) Regional myocardial function: advances in MR imaging and analysis. Radiographics 23 Spec No:S127-S140

    Google Scholar 

  12. Epstein FH, Yang Z, Gilson WD, Berr SS, Kramer CM, French BA (2002) MR tagging early after myocardial infarction in mice demonstrates contractile dysfunction in adjacent and remote regions. Magn Reson Med 48:399–403

    Article  PubMed  Google Scholar 

  13. Henson RE, Song SK, Pastorek JS, Ackerman JJ, Lorenz CH (2000) Left ventricular torsion is equal in mice and humans. Am J Physiol Heart Circ Physiol 278:H1117-H1123

    CAS  PubMed  Google Scholar 

  14. Zhou R, Pickup S, Glickson JD, Scott CH, Ferrari VA (2003) Assessment of global and regional myocardial function in the mouse using cine and tagged MRI . Magn Reson Med 49:760–764

    Article  PubMed  Google Scholar 

  15. Schaefer S, Balaban RS (1993) Cardiovascular magnetic resonance spectroscopy. Kluwer, Boston, p. 230

  16. Chacko VP, Aresta F, Chacko SM, Weiss RG (2000) MRI/MRS assessment of in vivo murine cardiac metabolism, morphology, and function at physiological heart rates. Am J Physiol Heart Circ Physiol 279:H2218-H2224

    CAS  PubMed  Google Scholar 

  17. Omerovic E, Basetti M, Bollano E, Bohlooly M, Tornell J, Isgaard J, Hjalmarson A, Soussi B, Waagstein F (2000) In vivo metabolic imaging of cardiac bioenergetics in transgenic mice. Biochem Biophys Res Commun 271:222–228

    CAS  PubMed  Google Scholar 

  18. Hu TC, Pautler RG, MacGowan GA, Koretsky AP (2001) Manganese-enhanced MRI of mouse heart during changes in inotropy. Magn Reson Med 46:884–890

    CAS  PubMed  Google Scholar 

  19. Wiesmann F, Szimtenings M, Frydrychowicz A, Illinger R, Hunecke A, Rommel E, Neubauer S, Haase A (2003) High-resolution MRI with cardiac and respiratory gating allows for accurate in vivo atherosclerotic plaque visualization in the murine aortic arch. Magn Reson Med 50:69–74

    Article  PubMed  Google Scholar 

  20. Choudhury RP, Fayad ZA, Aguinaldo JG, Itskovich VV, Rong JX, Fallon JT, Fisher EA (2003) Serial, noninvasive, in vivo magnetic resonance microscopy detects the development of atherosclerosis in apolipoprotein E-deficient mice and its progression by arterial wall remodeling. J Magn Reson Imaging 17:184–189

    Article  PubMed  Google Scholar 

  21. Choudhury RP, Aguinaldo JG, Rong JX, Kulak JL, Kulak AR, Reis ED, Fallon JT, Fuster V, Fisher EA, Fayad ZA (2002) Atherosclerotic lesions in genetically modified mice quantified in vivo by non-invasive high-resolution magnetic resonance microscopy. Atherosclerosis 162:315–321

    Article  CAS  PubMed  Google Scholar 

  22. Fayad ZA, Fallon JT, Shinnar M, Wehrli S, Dansky HM, Poon M, Badimon JJ, Charlton SA, Fisher EA, Breslow JL, Fuster V (1998) Noninvasive in vivo high-resolution magnetic resonance imaging of atherosclerotic lesions in genetically engineered mice. Circulation 98:1541–1547

    CAS  PubMed  Google Scholar 

  23. Itskovich VV, Choudhury RP, Aguinaldo JG, Fallon JT, Omerhodzic S, Fisher EA, Fayad ZA (2003) Characterization of aortic root atherosclerosis in ApoE knockout mice: high-resolution in vivo and ex vivo MRM with histological correlation. Magn Reson Med 49:381–385

    Article  CAS  PubMed  Google Scholar 

  24. Franco F, Dubois SK, Peshock RM, Shohet RV (1998) Magnetic resonance imaging accurately estimates LV mass in a transgenic mouse model of cardiac hypertrophy. Am J Physiol 274:H679-H683

    CAS  PubMed  Google Scholar 

  25. Nahrendorf M, Wiesmann F, Hiller KH, Han H, Hu K, Waller C, Ruff J, Haase A, Ertl G, Bauer WR (2000) In vivo assessment of cardiac remodeling after myocardial infarction in rats by cine-magnetic resonance imaging. J Cardiovasc Magn Reson 2:171–180

    CAS  PubMed  Google Scholar 

  26. Nahrendorf M, Wiesmann F, Hiller KH, Hu K, Waller C, Ruff J, Lanz TE, Neubauer S, Haase A, Ertl G, Bauer WR (2001) Serial cine-magnetic resonance imaging of left ventricular remodeling after myocardial infarction in rats. J Magn Reson Imaging 14:547–555

    Article  CAS  PubMed  Google Scholar 

  27. Nahrendorf M, Hiller KH, Hu K, Ertl G, Haase A, Bauer WR (2003) Cardiac magnetic resonance imaging in small animal models of human heart failure. Med Image Anal 7:369–375

    Article  CAS  PubMed  Google Scholar 

  28. Nahrendorf M, Hu K, Fraccarollo D, Hiller KH, Haase A, Bauer WR, Ertl G (2003) Time course of right ventricular remodeling in rats with experimental myocardial infarction. Am J Physiol Heart Circ Physiol 284:H241-H248

    CAS  PubMed  Google Scholar 

  29. Waller C, Hiller KH, Kahler E, Hu K, Nahrendorf M, Voll S, Haase A, Ertl G, Bauer WR (2001) Serial magnetic resonance imaging of microvascular remodeling in the infarcted rat heart. Circulation 103:1564–1569

    CAS  PubMed  Google Scholar 

  30. Ross AJ, Yang Z, Berr SS, Gilson WD, Petersen WC, Oshinski JN, French BA (2002) Serial MRI evaluation of cardiac structure and function in mice after reperfused myocardial infarction. Magn Reson Med 47:1158–1168

    Article  PubMed  Google Scholar 

  31. Markl MM, Chan FP, Alley MT, Wedding KL, Draney MT, Elkins CJ, Parker DW, Wicker R, Taylor CA, Herfkens RJ, Pelc NJ (2003) Time resolved three-dimensional phase-contrast MRI . J Magn Reson Imaging 17:499–506

    Article  PubMed  Google Scholar 

  32. Wedding KL, Draney MT, Herfkens RJ, Zarins CK, Taylor CA, Pelc NJ (2002) Measurement of vessel wall strain using cine phase contrast MRI . J Magn Reson Imaging 15:418–428

    PubMed  Google Scholar 

  33. Arai AE, Gaither CC, Epstein FH, Balaban RS, Wolff SD, et al. (1999) Myocardial velocity gradient imaging by phase contrast MRI with application to regional function in myocardial ischemia. Magn Reson Med 42:98–109

    CAS  PubMed  Google Scholar 

  34. Gilson WD, Yang Z, French BA, Epstein FH (2004) Complementary displacement-encoded MRI for constrast enhanced infarct detection and quatification of myocardial function in mice. Magn Reson Med 51:744–752

    PubMed  Google Scholar 

  35. Ryf S, Spiegel MA, Gerber M, Boesiger P (2002) Myocardial tagging with 3D-SPAMM . J Magn Reson 16:320–325

    Google Scholar 

  36. Kuijer JPA, Jansen E, Marcus JT, van Rossum AC, Heethaar RM (2001) Improved harmonic phase myocardial strain maps. Magn Reson Med 46:993–999

    CAS  PubMed  Google Scholar 

  37. Lutgens E, Daemen MJ, de Muinck ED, Debets J, Leenders P, Smits JF (1999) Chronic myocardial infarction in the mouse: cardiac structural and functional changes. Cardiovasc Res 41:586–593

    CAS  PubMed  Google Scholar 

  38. Fischer SE, McKinnon GC, Maier SE, Boesiger P (1993) Improved myocardial tagging contrast. Magn Reson Med 30:191–200

    CAS  PubMed  Google Scholar 

  39. Franco F, Dubois SK, Peshock RM, Shohet RV (1998) Magnetic resonance imaging accurately estimates LV mass in a transgenic mouse model of cardiac hypertrophy. Am J Physiol 274:H679-H683

    CAS  PubMed  Google Scholar 

  40. Franco F, Dubois SK, Peshock RM, Shohet RV (1998) Magnetic resonance imaging accurately estimates LV mass in a transgenic mouse model of cardiac hypertrophy. Am J Physiol 274:H679-H683

    CAS  PubMed  Google Scholar 

  41. Guyton AC, Hall JE (1996) Heart muscle; the heart as a pump. Textbook of medical physiology. Saunders, Philadelphia, pp. 107–119

  42. Franco F, Dubois SK, Peshock RM, Shohet RV (1998) Magnetic resonance imaging accurately estimates LV mass in a transgenic mouse model of cardiac hypertrophy. Am J Physiol 274:H679-H683

    CAS  PubMed  Google Scholar 

  43. Osman NF, Kerwin WS, McVeigh ER, Prince JL (1999) Cardiac motion tracking using CINE harmonic phase (HARP) magnetic resonance imaging. Magn Reson Med 42:1048–1060

    CAS  PubMed  Google Scholar 

  44. Janssen BJA, Smits JFM (2002) Autonomic control of blood pressure in mice: basic physiology and effects of genetic modification. Am J Physiol Regul Integr Comp Physiol 282:R1545-R1564

    CAS  PubMed  Google Scholar 

  45. Cassidy PJ, Schneider JE, Grieve SM, Lygate C, Neubauer S, Clarke K (2004) Assessment of motion gating strategies for mouse magnetic resonance at high magnetic field. J Magn Reson Imaging 19:229–237

    Article  PubMed  Google Scholar 

  46. Haacke FM, Brown RW, Thompson MR, Venkatesan R (1999) Magnetic resonance imaging: physical principles and sequence design. Wiley, New York

    Google Scholar 

  47. Wiesmann F, Ruff J, Hiller KH, Rommel E, Haase A, Neubauer S (2000) Development changes of cardiac function and mass assessed with MRI in neonatal, juvenile and adult mice. Am J Physiol Heart Circ Physiol 278:H652-H657

    CAS  PubMed  Google Scholar 

  48. Chacko VP, Aresta F, Chacko SM, Weiss RG (2000) MRI/MRS assessment of in vivo murine cardiac metabolism, morphology and function at physiological heart rates. Am J Physiol Heart Circ Physiol 279: H2218-H2224

    CAS  PubMed  Google Scholar 

  49. Wiesmann F, Frydrychowicz A, Rautenberg J, Illinger R, Rommel E, Haase A, Neubauer S (2002) Analysis of right ventricular function in healthy mice and a murine model of heart failure by in vivo MRI . Am J Physiol Heart Circ Physiol 283:H1065-H1071

    CAS  PubMed  Google Scholar 

  50. Atalar E, McVeigh ER (1994) Optimization of tag thickness for measuring position with magnetic resonance imaging. IEEE Trans Med Im 13:152–160

    CAS  Google Scholar 

  51. Nieminen M, Heikkila J (1976) Echoventriculography in acute myocardial infarction. III . Clinical correlations and implication of the noninfarcted myocardium. Am J Cardiol 38:1–8

    CAS  PubMed  Google Scholar 

  52. Rigaud M, Rocha P, Boschat J, Farcot JC, Bardet J, Bourdarias JP (1979) Regional left ventricular function assessed by contrast angiography in acute myocardial infarction. Circulation 60:130–139

    CAS  PubMed  Google Scholar 

  53. Lew WY, Chen ZY, Guth B, Covell JW (1985) Mechanisms of augmented segment shortening in nonischemic areas during acute ischemia of the canine left ventricle. Circ Res 56:351–358

    CAS  PubMed  Google Scholar 

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Acknowledgments.

The authors thank Theo Arts, Peter Bovendeerd and Sander Ubbink for the Matlab code for calculating the circumferential strain and fruitful discussions. Larry de Graaf is acknowledged for technical assistance.

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Authors and Affiliations

  1. Biomedical NMR, Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, The Netherlands

    E. Heijman, G. J. Strijkers, J. Habets & K. Nicolay

  2. Department of Pharmacology and Toxicology, Cardiovascular Research Institute Maastricht, Maastricht University, Maastricht, The Netherlands

    B. Janssen

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  1. E. Heijman
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  2. G. J. Strijkers
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  4. B. Janssen
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Correspondence to E. Heijman.

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Heijman, E., Strijkers, G., Habets, J. et al. Magnetic resonance imaging of regional cardiac function in the mouse. MAGMA 17, 170–178 (2004). https://doi.org/10.1007/s10334-004-0082-4

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