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

Lowell H. Frank, Qing Yu, Richard Francis, Xin Tian, Rajeev Samtani, David Sahn, Linda Leatherbury, Cecilia W. Lo

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Background: The authors conducted an ultrasound interrogation of a mutant mouse model with a Dnah5 mutation to determine whether cardiac mechanics may be affected by reversal of cardiac situs. This mutant is a bona fide model of primary ciliary dyskinesia, with surviving homozygous mice showing either situs solitus (SS) or situs inversus totalis (SI). Methods: High-frequency ultrasound interrogations of 27 neonatal and infant Dnah5 mutant mice, 16 with SS and 11 with SI, were conducted using an ultra-high-frequency biomicroscope. Electrocardiographic and respiratory gating were used to reconstruct high-resolution two-dimensional cines at 1,000 Hz, with speckle-tracking echocardiography used to further analyze midchamber and apical rotation. Results: All SS mice exhibited the expected counterclockwise apical rotation as viewed caudocranially, and surprisingly, the same counterclockwise motion was also observed in SI mice. Speckle-tracking analysis confirmed counterclockwise systolic rotation in both SS and SI mice, and this increased in magnitude from the subepicardium to the endocardium and from the papillary muscles to the apex. The magnitude of apical endocardial rotation was not different for SS and SI mice (5.64 ± 0.75° and 5.76 ± 1.90°, respectively, P = .93). The anatomic segments responsible for the largest components of apical endocardial systolic rotation differed between the SS and SI hearts (P = .004). In both, the two largest contributors to rotation were offset 180° from each other, but the anatomic regions differed between them. In SS hearts, maximal regional rotation occurred at the anterior mid-septum and posterolateral free wall, while in SI hearts, it was derived from the posterior septum and the anterolateral free wall. Analysis by episcopic fluorescence image capture histology of representative SI and SS mice showed normal intracardiac and segmental anatomy ({S,D,S} or {I,L,I}) without intracardiac defects. Conclusions: These results show that mirror-image cardiac looping did not result in mirror-image rotation of the morphologic left ventricle. These findings suggest that further studies are warranted to evaluate whether fiber orientation and cardiac mechanics may be abnormal in individuals with reversal of cardiac situs. The results of this study indicate that cardiac looping and myofiber orientation may be independently regulated.

Original languageEnglish (US)
Pages (from-to)315-323
Number of pages9
JournalJournal of the American Society of Echocardiography
Volume23
Issue number3
DOIs
StatePublished - Mar 2010

Fingerprint

Situs Inversus
Echocardiography
Mechanics
Kartagener Syndrome
Endocardium
Papillary Muscles
Heart Ventricles
Anatomy
Histology
Fluorescence
Mutation

Keywords

  • High-frequency ultrasound
  • Rotation
  • Situs inversus
  • Speckle tracking
  • Ventricular twist

ASJC Scopus subject areas

  • Radiology Nuclear Medicine and imaging
  • Cardiology and Cardiovascular Medicine

Cite this

Ventricular Rotation Is Independent of Cardiac Looping : A Study in Mice With Situs Inversus Totalis Using Speckle-Tracking Echocardiography. / Frank, Lowell H.; Yu, Qing; Francis, Richard; Tian, Xin; Samtani, Rajeev; Sahn, David; Leatherbury, Linda; Lo, Cecilia W.

In: Journal of the American Society of Echocardiography, Vol. 23, No. 3, 03.2010, p. 315-323.

Research output: Contribution to journalArticle

Frank, Lowell H. ; Yu, Qing ; Francis, Richard ; Tian, Xin ; Samtani, Rajeev ; Sahn, David ; Leatherbury, Linda ; Lo, Cecilia W. / Ventricular Rotation Is Independent of Cardiac Looping : A Study in Mice With Situs Inversus Totalis Using Speckle-Tracking Echocardiography. In: Journal of the American Society of Echocardiography. 2010 ; Vol. 23, No. 3. pp. 315-323.
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AU - Francis, Richard

AU - Tian, Xin

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AU - Lo, Cecilia W.

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N2 - Background: The authors conducted an ultrasound interrogation of a mutant mouse model with a Dnah5 mutation to determine whether cardiac mechanics may be affected by reversal of cardiac situs. This mutant is a bona fide model of primary ciliary dyskinesia, with surviving homozygous mice showing either situs solitus (SS) or situs inversus totalis (SI). Methods: High-frequency ultrasound interrogations of 27 neonatal and infant Dnah5 mutant mice, 16 with SS and 11 with SI, were conducted using an ultra-high-frequency biomicroscope. Electrocardiographic and respiratory gating were used to reconstruct high-resolution two-dimensional cines at 1,000 Hz, with speckle-tracking echocardiography used to further analyze midchamber and apical rotation. Results: All SS mice exhibited the expected counterclockwise apical rotation as viewed caudocranially, and surprisingly, the same counterclockwise motion was also observed in SI mice. Speckle-tracking analysis confirmed counterclockwise systolic rotation in both SS and SI mice, and this increased in magnitude from the subepicardium to the endocardium and from the papillary muscles to the apex. The magnitude of apical endocardial rotation was not different for SS and SI mice (5.64 ± 0.75° and 5.76 ± 1.90°, respectively, P = .93). The anatomic segments responsible for the largest components of apical endocardial systolic rotation differed between the SS and SI hearts (P = .004). In both, the two largest contributors to rotation were offset 180° from each other, but the anatomic regions differed between them. In SS hearts, maximal regional rotation occurred at the anterior mid-septum and posterolateral free wall, while in SI hearts, it was derived from the posterior septum and the anterolateral free wall. Analysis by episcopic fluorescence image capture histology of representative SI and SS mice showed normal intracardiac and segmental anatomy ({S,D,S} or {I,L,I}) without intracardiac defects. Conclusions: These results show that mirror-image cardiac looping did not result in mirror-image rotation of the morphologic left ventricle. These findings suggest that further studies are warranted to evaluate whether fiber orientation and cardiac mechanics may be abnormal in individuals with reversal of cardiac situs. The results of this study indicate that cardiac looping and myofiber orientation may be independently regulated.

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