Journal of the American Society of Echocardiography
Volume 23, Issue 3 , Pages 315-323 , March 2010

Ventricular Rotation Is Independent of Cardiac Looping: A Study in Mice With Situs Inversus Totalis Using Speckle-Tracking Echocardiography

  • Lowell H. Frank, MD

      Affiliations

    • Laboratory of Developmental Biology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
    • Children's National Heart Institute, Children's National Medical Center, Washington, DC
    • Corresponding Author InformationReprint requests: Lowell H. Frank, MD, Children's National Medical Center, Division of Cardiology, 111 Michigan Avenue, NW, Washington, DC 20010.
  • ,
  • Qing Yu, MD

      Affiliations

    • Laboratory of Developmental Biology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
  • ,
  • Richard Francis, PhD

      Affiliations

    • Laboratory of Developmental Biology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
  • ,
  • Xin Tian, PhD

      Affiliations

    • Office of Biostatistics Research, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
  • ,
  • Rajeev Samtani

      Affiliations

    • Laboratory of Developmental Biology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
  • ,
  • David J. Sahn, MD

      Affiliations

    • Department of Pediatric Cardiology, Oregon Health and Science University, Portland, Oregon
  • ,
  • Linda Leatherbury, MD

      Affiliations

    • Laboratory of Developmental Biology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
    • Children's National Heart Institute, Children's National Medical Center, Washington, DC
  • ,
  • Cecilia W. Lo, PhD

      Affiliations

    • Laboratory of Developmental Biology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland
    • Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania

References 

  1. Torrent-Guasp F, Buckberg GD, Clemente C, Cox JL, Coghlan HC, Gharib M. The structure and function of the helical heart and its buttress wrapping. I. The normal macroscopic structure of the heart. Semin Thorac Cardiovasc Surg. 2001;13:301–319
  2. Bovendeerd PH, Huyghe JM, Arts T, van Campen DH, Reneman RS. Influence of endocardial-epicardial crossover of muscle fibers on left ventricular wall mechanics. J Biomech. 1994;27:941–951
  3. Taber LA, Yang M, Podszus WW. Mechanics of ventricular torsion. J Biomech. 1996;29:745–752
  4. Delhaas T, Decaluwe W, Rubbens M, Kerckhoffs R, Arts T. Cardiac fiber orientation and the left-right asymmetry determining mechanism. Ann N Y Acad Sci. 2004;1015:190–201
  5. Corno AF, Kocica MJ. Potential implications of the helical heart in congenital heart defects. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu. 2007;61–67
  6. Tan SY, Rosenthal J, Zhao XQ, Francis RJ, Chatterjee B, Sabol SL, et al. Heterotaxy and complex structural heart defects in a mutant mouse model of primary ciliary dyskinesia. J Clin Invest. 2007;117:3742–3752
  7. Hornef N, Olbrich H, Horvath J, Zariwala MA, Fliegauf M, Loges NT, et al. DNAH5 mutations are a common cause of primary ciliary dyskinesia with outer dynein arm defects. Am J Respir Crit Care Med. 2006;174:120–126
  8. Olbrich H, Haffner K, Kispert A, Volkel A, Volz A, Sasmaz G, et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet. 2002;30:143–144
  9. Bose AK, Mathewson JW, Anderson BE, Andrews AM, Martin Gerdes A, Benjamin Perryman M, et al. Initial experience with high frequency ultrasound for the newborn C57BL mouse. Echocardiography. 2007;24:412–419
  10. Zhou YQ, Foster FS, Qu DW, Zhang M, Harasiewicz KA, Adamson SL. Applications for multifrequency ultrasound biomicroscopy in mice from implantation to adulthood. Physiol Genomics. 2002;10:113–126
  11. Burns AT, McDonald IG, Thomas JD, Macisaac A, Prior D. Doin' the twist: new tools for an old concept of myocardial function. Heart. 2008;94:978–983
  12. Lorenz CH, Pastorek JS, Bundy JM. Delineation of normal human left ventricular twist throughout systole by tagged cine magnetic resonance imaging. J Cardiovasc Magn Reson. 2000;2:97–108
  13. Streeter DD, Spotnitz HM, Patel DP, Ross J, Sonnenblick EH. Fiber orientation in the canine left ventricle during diastole and systole. Circ Res. 1969;24:339–347
  14. Gorman JH, Gupta KB, Streicher JT, Gorman RC, Jackson BM, Ratcliffe MB, et al. Dynamic three-dimensional imaging of the mitral valve and left ventricle by rapid sonomicrometry array localization. J Thorac Cardiovasc Surg. 1996;112:712–726
  15. Buchalter MB, Weiss JL, Rogers WJ, Zerhouni EA, Weisfeldt ML, Beyar R, et al. Noninvasive quantification of left ventricular rotational deformation in normal humans using magnetic resonance imaging myocardial tagging. Circulation. 1990;81:1236–1244
  16. Henson RE, Song SK, Pastorek JS, Ackerman JJ, Lorenz CH. Left ventricular torsion is equal in mice and humans. Am J Physiol Heart Circ Physiol. 2000;278:H1117–H1123
  17. Liu W, Ashford MW, Chen J, Watkins MP, Williams TA, Wickline SA, et al. MR tagging demonstrates quantitative differences in regional ventricular wall motion in mice, rats, and men. Am J Physiol Heart Circ Physiol. 2006;291:H2515–H2521
  18. Arts T, Meerbaum S, Reneman RS, Corday E. Torsion of the left ventricle during the ejection phase in the intact dog. Cardiovasc Res. 1984;18:183–193
  19. Gibbons Kroeker CA, Ter Keurs HE, Knudtson ML, Tyberg JV, Beyar R. An optical device to measure the dynamics of apex rotation of the left ventricle. Am J Physiol. 1993;265:H1444–H1449
  20. Kroeker CA, Tyberg JV, Beyar R. Effects of ischemia on left ventricular apex rotation. An experimental study in anesthetized dogs. Circulation. 1995;92:3539–3548
  21. Amundsen BH, Helle-Valle T, Edvardsen T, Torp H, Crosby J, Lyseggen E, et al. Noninvasive myocardial strain measurement by speckle tracking echocardiography: validation against sonomicrometry and tagged magnetic resonance imaging. J Am Coll Cardiol. 2006;47:789–793
  22. Ashraf M, Li XK, Young MT, Jensen AJ, Pemberton J, Hui L, et al. Delineation of cardiac twist by a sonographically based 2-dimensional strain analysis method: an in vitro validation study. J Ultrasound Med. 2006;25:1193–1198
  23. Helle-Valle T, Crosby J, Edvardsen T, Lyseggen E, Amundsen BH, Smith HJ, et al. New noninvasive method for assessment of left ventricular rotation: speckle tracking echocardiography. Circulation. 2005;112:3149–3156
  24. Kim HK, Sohn DW, Lee SE, Choi SY, Park JS, Kim YJ, et al. Assessment of left ventricular rotation and torsion with two-dimensional speckle tracking echocardiography. J Am Soc Echocardiogr. 2007;20:45–53
  25. Notomi Y, Lysyansky P, Setser RM, Shiota T, Popovic ZB, Martin-Miklovic MG, et al. Measurement of ventricular torsion by two-dimensional ultrasound speckle tracking imaging. J Am Coll Cardiol. 2005;45:2034–2041
  26. Pirat B, Khoury DS, Hartley CJ, Tiller L, Rao L, Schulz DG, et al. A novel feature-tracking echocardiographic method for the quantitation of regional myocardial function: validation in an animal model of ischemia-reperfusion. J Am Coll Cardiol. 2008;51:651–659
  27. Asami I, Koizumi K. The vortex cordis is never reversely directed, even in situs inversus and L-loop anomaly [article in Japanese]. Kaibogaku Zasshi. 1989;64:36–45
  28. Taussig H. The anatomy of the heart in two cases of situs transversus. Bull Johns Hopkins Hosp. 1926;39:199–202
  29. Delhaas T, Kroon W, Bovendeerd P, Arts T. Left ventricular apical torsion and architecture are not inverted in situs inversus totalis. Prog Biophys Mol Biol. 2008;97:513–519
  30. Delhaas T, Kroon W, Decaluwe W, Rubbens M, Bovendeerd P, Arts T. Structure and torsion of the normal and situs inversus totalis cardiac left ventricle. I. Experimental data in humans. Am J Physiol Heart Circ Physiol. 2008;295:H197–H201
  31. Zhang L, Xie M, Fu M. Assessment of age-related changes in left ventricular twist by two-dimensional ultrasound speckle tracking imaging. J Huazhong Univ Sci Technolog Med Sci. 2007;27:691–695
  32. Rosenthal J, Mangal V, Walker D, Bennett M, Mohun TJ, Lo CW. Rapid high resolution three dimensional reconstruction of embryos with episcopic fluorescence image capture. Birth Defects Res C Embryo Today. 2004;72:213–223
  33. Hui L, Pemberton J, Hickey E, Li XK, Lysyansky P, Ashraf M, et al. The contribution of left ventricular muscle bands to left ventricular rotation: assessment by a 2-dimensional speckle tracking method. J Am Soc Echocardiogr. 2007;20:486–491
  34. Ingels NB, Hansen DE, Daughters GT, Stinson EB, Alderman EL, Miller DC. Relation between longitudinal, circumferential, and oblique shortening and torsional deformation in the left ventricle of the transplanted human heart. Circ Res. 1989;64:915–927
  35. Takeuchi M, Nishikage T, Nakai H, Kokumai M, Otani S, Lang RM. The assessment of left ventricular twist in anterior wall myocardial infarction using two-dimensional speckle tracking imaging. J Am Soc Echocardiogr. 2007;20:36–44
  36. Opdahl A, Helle-Valle T, Remme EW, Vartdal T, Pettersen E, Lunde K, et al. Apical rotation by speckle tracking echocardiography: a simplified bedside index of left ventricular twist. J Am Soc Echocardiogr. 2008;21:1121–1128
  37. Kroon W, Delhaas T, Bovendeerd P, Arts T. Structure and torsion in the normal and situs inversus totalis cardiac left ventricle. II. Modeling cardiac adaptation to mechanical load. Am J Physiol Heart Circ Physiol. 2008;295:H202–H210
  38. Rademakers FE, Buchalter MB, Rogers WJ, Zerhouni EA, Weisfeldt ML, Weiss JL, et al. Dissociation between left ventricular untwisting and filling. Accentuation by catecholamines. Circulation. 1992;85:1572–1581
  39. Michelfelder EC, Khoury P, Witt SA, Glascock BJ, Kimball TR. Noncircumferential myofiber function: impact on early diastolic filling in children. J Am Soc Echocardiogr. 2001;14:1065–1069
  40. Cherin E, Williams R, Needles A, Liu G, White C, Brown AS, et al. Ultrahigh frame rate retrospective ultrasound microimaging and blood flow visualization in mice in vivo. Ultrasound Med Biol. 2006;32:683–691
  41. Teske AJ, De Boeck BW, Melman PG, Sieswerda GT, Doevendans PA, Cramer MJ. Echocardiographic quantification of myocardial function using tissue deformation imaging, a guide to image acquisition and analysis using tissue Doppler and speckle tracking. Cardiovasc Ultrasound. 2007;5:27

 This work was supported by grant ZO1-HL005701 from the Division of Intramural Research, National Heart, Lung, and Blood Institute (Bethesda, MD).

PII: S0894-7317(09)01107-9

doi: 10.1016/j.echo.2009.11.024

Journal of the American Society of Echocardiography
Volume 23, Issue 3 , Pages 315-323 , March 2010