Abstract

Normal aging is accompanied by structural changes in the heart architecture. To explore this remodeling, we used a serial optical coherence tomography scanner to image entire mouse hearts at micron scale resolution. Ex vivo hearts of 7 young (4 months) and 5 old (24 months) C57BL/6 mice were acquired with the imaging platform. OCT of the myocardium revealed myofiber orientation changing linearly from the endocardium to the epicardium. In old mice, this rate of change was lower when compared to young mice while the average volume of old mice hearts was significantly larger (p<0.05). Myocardial wall thickening was also accompanied by extracellular spacing in the endocardium, resulting in a lower OCT attenuation coefficient in old mice endocardium (p<0.05). Prior to serial sectioning, cardiac function of the same hearts was imaged in vivo using MRI and revealed a reduced ejection fraction with aging. The use of a serial optical coherence tomography scanner allows new insight into fine age-related changes of the heart associated with changes in heart function.

© 2017 Optical Society of America

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References

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2017 (1)

J. Lefebvre, A. Castonguay, P. Pouliot, M. Descoteaux, and F. Lesage, “Whole mouse brain imaging using optical coherence tomography: reconstruction, normalization, segmentation, and comparison with diffusion MRI,” Neurophotonics 4(4), 041501 (2017).
[PubMed]

2016 (3)

S. P. Amato, F. Pan, J. Schwartz, and T. M. Ragan, “Whole Brain Imaging with Serial Two-Photon Tomography,” Front. Neuroanat. 10, 31 (2016).
[PubMed]

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

C. J. Goergen, H. H. Chen, S. Sakadžić, V. J. Srinivasan, and D. E. Sosnovik, “Microstructural characterization of myocardial infarction with optical coherence tractography and two-photon microscopy,” Physiol. Rep. 4(18), e12894 (2016).
[PubMed]

2014 (3)

H. Wang, J. Zhu, and T. Akkin, “Serial optical coherence scanner for large-scale brain imaging at microscopic resolution,” Neuroimage 84, 1007–1017 (2014).
[PubMed]

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

Y. Wang, K. Zhang, N. B. Wasala, X. Yao, D. Duan, and G. Yao, “Histology validation of mapping depth-resolved cardiac fiber orientation in fresh mouse heart using optical polarization tractography,” Biomed. Opt. Express 5(8), 2843–2855 (2014).
[PubMed]

2013 (3)

2012 (3)

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt. 17(7), 071309 (2012).
[PubMed]

T. Ragan, L. R. Kadiri, K. U. Venkataraju, K. Bahlmann, J. Sutin, J. Taranda, I. Arganda-Carreras, Y. Kim, H. S. Seung, and P. Osten, “Serial two-photon tomography for automated ex vivo mouse brain imaging,” Nat. Methods 9(3), 255–258 (2012).
[PubMed]

C. J. Goergen, H. Radhakrishnan, S. Sakadžić, E. T. Mandeville, E. H. Lo, D. E. Sosnovik, and V. J. Srinivasan, “Optical coherence tractography using intrinsic contrast,” Opt. Lett. 37(18), 3882–3884 (2012).
[PubMed]

2011 (1)

H. Wang, A. J. Black, J. Zhu, T. W. Stigen, M. K. Al-Qaisi, T. I. Netoff, A. Abosch, and T. Akkin, “Reconstructing micrometer-scale fiber pathways in the brain: Multi-contrast optical coherence tomography based tractography,” Neuroimage 58(4), 984–992 (2011).
[PubMed]

2010 (1)

E. Heiberg, J. Sjögren, M. Ugander, M. Carlsson, H. Engblom, and H. Arheden, “Design and validation of Segment--freely available software for cardiovascular image analysis,” BMC Med. Imaging 10, 1 (2010).
[PubMed]

2009 (3)

D. E. Sosnovik, R. Wang, G. Dai, T. G. Reese, and V. J. Wedeen, “Diffusion MR tractography of the heart,” J. Cardiovasc. Magn. Reson. 11, 47 (2009).
[PubMed]

W. Li, M. Lu, S. Banerjee, J. Zhong, A. Ye, J. Molter, and X. Yu, “Ex vivo diffusion tensor MRI reflects microscopic structural remodeling associated with aging and disease progression in normal and cardiomyopathic Syrian hamsters,” NMR Biomed. 22(8), 819–825 (2009).
[PubMed]

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. J. M. Peeters, A. Vilanova, M. C. van Prooijen, H. M. H. F. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed. 22(2), 182–190 (2009).
[PubMed]

2008 (1)

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt. 13(3), 030505 (2008).
[PubMed]

2004 (1)

P. J. Cassidy, J. E. Schneider, S. M. Grieve, C. Lygate, S. Neubauer, and K. Clarke, “Assessment of motion gating strategies for mouse magnetic resonance at high magnetic fields,” J. Magn. Reson. Imaging 19(2), 229–237 (2004).
[PubMed]

2003 (4)

J. E. Schneider, P. J. Cassidy, C. Lygate, D. J. Tyler, F. Wiesmann, S. M. Grieve, K. Hulbert, K. Clarke, and S. Neubauer, “Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system,” J. Magn. Reson. Imaging 18(6), 691–701 (2003).
[PubMed]

A. Brooks, V. Schinde, A. C. Bateman, and P. J. Gallagher, “Interstitial fibrosis in the dilated non-ischaemic myocardium,” Heart 89(10), 1255–1256 (2003).
[PubMed]

E. G. Lakatta and D. Levy, “Arterial and Cardiac Aging: Major Shareholders in Cardiovascular Disease Enterprises: Part I: Aging Arteries: A “Set Up” for Vascular Disease,” Circulation 107(1), 139–146 (2003).
[PubMed]

E. G. Lakatta and D. Levy, “Arterial and Cardiac Aging: Major Shareholders in Cardiovascular Disease Enterprises: Part II: The Aging Heart in Health: Links to Heart Disease,” Circulation 107(2), 346–354 (2003).
[PubMed]

1999 (1)

A. Mosterd, A. W. Hoes, M. C. de Bruyne, J. W. Deckers, D. T. Linker, A. Hofman, and D. E. Grobbee, “Prevalence of heart failure and left ventricular dysfunction in the general population; The Rotterdam Study,” Eur. Heart J. 20(6), 447–455 (1999).
[PubMed]

1998 (2)

A. W. Haider, M. G. Larson, E. J. Benjamin, and D. Levy, “Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death,” J. Am. Coll. Cardiol. 32(5), 1454–1459 (1998).
[PubMed]

D. F. Scollan, A. Holmes, R. Winslow, and J. Forder, “Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging,” Am. J. Physiol. 275(6 Pt 2), H2308–H2318 (1998).
[PubMed]

1995 (2)

T. G. Reese, R. M. Weisskoff, R. N. Smith, B. R. Rosen, R. E. Dinsmore, and V. J. Wedeen, “Imaging myocardial fiber architecture in vivo with magnetic resonance,” Magn. Reson. Med. 34(6), 786–791 (1995).
[PubMed]

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol. 269(2 Pt 2), H571–H582 (1995).
[PubMed]

1994 (1)

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation 90(6), 3076–3090 (1994).
[PubMed]

1992 (2)

S. P. Schulman, E. G. Lakatta, J. L. Fleg, L. Lakatta, L. C. Becker, and G. Gerstenblith, “Age-related decline in left ventricular filling at rest and exercise,” Am. J. Physiol. 263(6 Pt 2), H1932–H1938 (1992).
[PubMed]

C. J. Swinne, E. P. Shapiro, S. D. Lima, and J. L. Fleg, “Age-associated changes in left ventricular diastolic performance during isometric exercise in normal subjects,” Am. J. Cardiol. 69(8), 823–826 (1992).
[PubMed]

1990 (1)

D. Levy, R. J. Garrison, D. D. Savage, W. B. Kannel, and W. P. Castelli, “Prognostic Implications of Echocardiographically Determined Left Ventricular Mass in the Framingham Heart Study,” N. Engl. J. Med. 322(22), 1561–1566 (1990).
[PubMed]

1979 (1)

N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst. Man Cybern. 9, 62–66 (1979).

1977 (1)

G. Gerstenblith, J. Frederiksen, F. C. Yin, N. J. Fortuin, E. G. Lakatta, and M. L. Weisfeldt, “Echocardiographic assessment of a normal adult aging population,” Circulation 56(2), 273–278 (1977).
[PubMed]

1973 (1)

D. D. Streeter and W. T. Hanna, “Engineering mechanics for successive states in canine left ventricular myocardium. II. Fiber angle and sarcomere length,” Circ. Res. 33(6), 656–664 (1973).
[PubMed]

1969 (1)

D. D. Streeter, H. M. Spotnitz, D. P. Patel, J. Ross, and E. H. Sonnenblick, “Fiber Orientation in the Canine Left Ventricle during Diastole and Systole,” Circ. Res. 24(3), 339–347 (1969).
[PubMed]

1966 (1)

D. D. Streeter and D. L. Bassett, “An engineering analysis of myocardial fiber orientation in pig’s left ventricle in systole,” Anat. Rec. 155, 503–511 (1966).

Abosch, A.

H. Wang, A. J. Black, J. Zhu, T. W. Stigen, M. K. Al-Qaisi, T. I. Netoff, A. Abosch, and T. Akkin, “Reconstructing micrometer-scale fiber pathways in the brain: Multi-contrast optical coherence tomography based tractography,” Neuroimage 58(4), 984–992 (2011).
[PubMed]

Abran, M.

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

Abulrob, A.

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

Akkin, T.

H. Wang, J. Zhu, and T. Akkin, “Serial optical coherence scanner for large-scale brain imaging at microscopic resolution,” Neuroimage 84, 1007–1017 (2014).
[PubMed]

H. Wang, A. J. Black, J. Zhu, T. W. Stigen, M. K. Al-Qaisi, T. I. Netoff, A. Abosch, and T. Akkin, “Reconstructing micrometer-scale fiber pathways in the brain: Multi-contrast optical coherence tomography based tractography,” Neuroimage 58(4), 984–992 (2011).
[PubMed]

Al-Qaisi, M. K.

H. Wang, A. J. Black, J. Zhu, T. W. Stigen, M. K. Al-Qaisi, T. I. Netoff, A. Abosch, and T. Akkin, “Reconstructing micrometer-scale fiber pathways in the brain: Multi-contrast optical coherence tomography based tractography,” Neuroimage 58(4), 984–992 (2011).
[PubMed]

Amato, S. P.

S. P. Amato, F. Pan, J. Schwartz, and T. M. Ragan, “Whole Brain Imaging with Serial Two-Photon Tomography,” Front. Neuroanat. 10, 31 (2016).
[PubMed]

Ambrosi, C. M.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt. 17(7), 071309 (2012).
[PubMed]

Arganda-Carreras, I.

T. Ragan, L. R. Kadiri, K. U. Venkataraju, K. Bahlmann, J. Sutin, J. Taranda, I. Arganda-Carreras, Y. Kim, H. S. Seung, and P. Osten, “Serial two-photon tomography for automated ex vivo mouse brain imaging,” Nat. Methods 9(3), 255–258 (2012).
[PubMed]

Arheden, H.

E. Heiberg, J. Sjögren, M. Ugander, M. Carlsson, H. Engblom, and H. Arheden, “Design and validation of Segment--freely available software for cardiovascular image analysis,” BMC Med. Imaging 10, 1 (2010).
[PubMed]

Bahlmann, K.

T. Ragan, L. R. Kadiri, K. U. Venkataraju, K. Bahlmann, J. Sutin, J. Taranda, I. Arganda-Carreras, Y. Kim, H. S. Seung, and P. Osten, “Serial two-photon tomography for automated ex vivo mouse brain imaging,” Nat. Methods 9(3), 255–258 (2012).
[PubMed]

Banerjee, S.

W. Li, M. Lu, S. Banerjee, J. Zhong, A. Ye, J. Molter, and X. Yu, “Ex vivo diffusion tensor MRI reflects microscopic structural remodeling associated with aging and disease progression in normal and cardiomyopathic Syrian hamsters,” NMR Biomed. 22(8), 819–825 (2009).
[PubMed]

Baruffi, S.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation 90(6), 3076–3090 (1994).
[PubMed]

Bassett, D. L.

D. D. Streeter and D. L. Bassett, “An engineering analysis of myocardial fiber orientation in pig’s left ventricle in systole,” Anat. Rec. 155, 503–511 (1966).

Bateman, A. C.

A. Brooks, V. Schinde, A. C. Bateman, and P. J. Gallagher, “Interstitial fibrosis in the dilated non-ischaemic myocardium,” Heart 89(10), 1255–1256 (2003).
[PubMed]

Becker, L. C.

S. P. Schulman, E. G. Lakatta, J. L. Fleg, L. Lakatta, L. C. Becker, and G. Gerstenblith, “Age-related decline in left ventricular filling at rest and exercise,” Am. J. Physiol. 263(6 Pt 2), H1932–H1938 (1992).
[PubMed]

Benjamin, E. J.

A. W. Haider, M. G. Larson, E. J. Benjamin, and D. Levy, “Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death,” J. Am. Coll. Cardiol. 32(5), 1454–1459 (1998).
[PubMed]

Bertrand, M.-J.

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
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Black, A. J.

H. Wang, A. J. Black, J. Zhu, T. W. Stigen, M. K. Al-Qaisi, T. I. Netoff, A. Abosch, and T. Akkin, “Reconstructing micrometer-scale fiber pathways in the brain: Multi-contrast optical coherence tomography based tractography,” Neuroimage 58(4), 984–992 (2011).
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Blankesteijn, W. M.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. J. M. Peeters, A. Vilanova, M. C. van Prooijen, H. M. H. F. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed. 22(2), 182–190 (2009).
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Bouts, A.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. J. M. Peeters, A. Vilanova, M. C. van Prooijen, H. M. H. F. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed. 22(2), 182–190 (2009).
[PubMed]

Brooks, A.

A. Brooks, V. Schinde, A. C. Bateman, and P. J. Gallagher, “Interstitial fibrosis in the dilated non-ischaemic myocardium,” Heart 89(10), 1255–1256 (2003).
[PubMed]

Busseuil, D.

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

Carlsson, M.

E. Heiberg, J. Sjögren, M. Ugander, M. Carlsson, H. Engblom, and H. Arheden, “Design and validation of Segment--freely available software for cardiovascular image analysis,” BMC Med. Imaging 10, 1 (2010).
[PubMed]

Cassidy, P. J.

P. J. Cassidy, J. E. Schneider, S. M. Grieve, C. Lygate, S. Neubauer, and K. Clarke, “Assessment of motion gating strategies for mouse magnetic resonance at high magnetic fields,” J. Magn. Reson. Imaging 19(2), 229–237 (2004).
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J. E. Schneider, P. J. Cassidy, C. Lygate, D. J. Tyler, F. Wiesmann, S. M. Grieve, K. Hulbert, K. Clarke, and S. Neubauer, “Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system,” J. Magn. Reson. Imaging 18(6), 691–701 (2003).
[PubMed]

Castelli, W. P.

D. Levy, R. J. Garrison, D. D. Savage, W. B. Kannel, and W. P. Castelli, “Prognostic Implications of Echocardiographically Determined Left Ventricular Mass in the Framingham Heart Study,” N. Engl. J. Med. 322(22), 1561–1566 (1990).
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Castonguay, A.

J. Lefebvre, A. Castonguay, P. Pouliot, M. Descoteaux, and F. Lesage, “Whole mouse brain imaging using optical coherence tomography: reconstruction, normalization, segmentation, and comparison with diffusion MRI,” Neurophotonics 4(4), 041501 (2017).
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P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

Chai, L. Z.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol. 269(2 Pt 2), H571–H582 (1995).
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Chen, H. H.

C. J. Goergen, H. H. Chen, S. Sakadžić, V. J. Srinivasan, and D. E. Sosnovik, “Microstructural characterization of myocardial infarction with optical coherence tractography and two-photon microscopy,” Physiol. Rep. 4(18), e12894 (2016).
[PubMed]

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

Clarke, K.

P. J. Cassidy, J. E. Schneider, S. M. Grieve, C. Lygate, S. Neubauer, and K. Clarke, “Assessment of motion gating strategies for mouse magnetic resonance at high magnetic fields,” J. Magn. Reson. Imaging 19(2), 229–237 (2004).
[PubMed]

J. E. Schneider, P. J. Cassidy, C. Lygate, D. J. Tyler, F. Wiesmann, S. M. Grieve, K. Hulbert, K. Clarke, and S. Neubauer, “Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system,” J. Magn. Reson. Imaging 18(6), 691–701 (2003).
[PubMed]

Dai, G.

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
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D. E. Sosnovik, R. Wang, G. Dai, T. G. Reese, and V. J. Wedeen, “Diffusion MR tractography of the heart,” J. Cardiovasc. Magn. Reson. 11, 47 (2009).
[PubMed]

de Boer, J. F.

de Bruyne, M. C.

A. Mosterd, A. W. Hoes, M. C. de Bruyne, J. W. Deckers, D. T. Linker, A. Hofman, and D. E. Grobbee, “Prevalence of heart failure and left ventricular dysfunction in the general population; The Rotterdam Study,” Eur. Heart J. 20(6), 447–455 (1999).
[PubMed]

Deckers, J. W.

A. Mosterd, A. W. Hoes, M. C. de Bruyne, J. W. Deckers, D. T. Linker, A. Hofman, and D. E. Grobbee, “Prevalence of heart failure and left ventricular dysfunction in the general population; The Rotterdam Study,” Eur. Heart J. 20(6), 447–455 (1999).
[PubMed]

Descoteaux, M.

J. Lefebvre, A. Castonguay, P. Pouliot, M. Descoteaux, and F. Lesage, “Whole mouse brain imaging using optical coherence tomography: reconstruction, normalization, segmentation, and comparison with diffusion MRI,” Neurophotonics 4(4), 041501 (2017).
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Dinsmore, R. E.

T. G. Reese, R. M. Weisskoff, R. N. Smith, B. R. Rosen, R. E. Dinsmore, and V. J. Wedeen, “Imaging myocardial fiber architecture in vivo with magnetic resonance,” Magn. Reson. Med. 34(6), 786–791 (1995).
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Duan, D.

Edgar, S. G.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol. 269(2 Pt 2), H571–H582 (1995).
[PubMed]

Efimov, I. R.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt. 17(7), 071309 (2012).
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C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt. 13(3), 030505 (2008).
[PubMed]

Engblom, H.

E. Heiberg, J. Sjögren, M. Ugander, M. Carlsson, H. Engblom, and H. Arheden, “Design and validation of Segment--freely available software for cardiovascular image analysis,” BMC Med. Imaging 10, 1 (2010).
[PubMed]

Ershler, P. R.

B. Taccardi, E. Macchi, R. L. Lux, P. R. Ershler, S. Spaggiari, S. Baruffi, and Y. Vyhmeister, “Effect of myocardial fiber direction on epicardial potentials,” Circulation 90(6), 3076–3090 (1994).
[PubMed]

Fan, C.

Fedorov, V. V.

C. M. Ambrosi, V. V. Fedorov, R. B. Schuessler, A. M. Rollins, and I. R. Efimov, “Quantification of fiber orientation in the canine atrial pacemaker complex using optical coherence tomography,” J. Biomed. Opt. 17(7), 071309 (2012).
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Fleg, J. L.

C. J. Swinne, E. P. Shapiro, S. D. Lima, and J. L. Fleg, “Age-associated changes in left ventricular diastolic performance during isometric exercise in normal subjects,” Am. J. Cardiol. 69(8), 823–826 (1992).
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S. P. Schulman, E. G. Lakatta, J. L. Fleg, L. Lakatta, L. C. Becker, and G. Gerstenblith, “Age-related decline in left ventricular filling at rest and exercise,” Am. J. Physiol. 263(6 Pt 2), H1932–H1938 (1992).
[PubMed]

Fleming, C. P.

C. P. Fleming, C. M. Ripplinger, B. Webb, I. R. Efimov, and A. M. Rollins, “Quantification of cardiac fiber orientation using optical coherence tomography,” J. Biomed. Opt. 13(3), 030505 (2008).
[PubMed]

Forder, J.

D. F. Scollan, A. Holmes, R. Winslow, and J. Forder, “Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging,” Am. J. Physiol. 275(6 Pt 2), H2308–H2318 (1998).
[PubMed]

Fortuin, N. J.

G. Gerstenblith, J. Frederiksen, F. C. Yin, N. J. Fortuin, E. G. Lakatta, and M. L. Weisfeldt, “Echocardiographic assessment of a normal adult aging population,” Circulation 56(2), 273–278 (1977).
[PubMed]

Frederiksen, J.

G. Gerstenblith, J. Frederiksen, F. C. Yin, N. J. Fortuin, E. G. Lakatta, and M. L. Weisfeldt, “Echocardiographic assessment of a normal adult aging population,” Circulation 56(2), 273–278 (1977).
[PubMed]

Gallagher, P. J.

A. Brooks, V. Schinde, A. C. Bateman, and P. J. Gallagher, “Interstitial fibrosis in the dilated non-ischaemic myocardium,” Heart 89(10), 1255–1256 (2003).
[PubMed]

Garrison, R. J.

D. Levy, R. J. Garrison, D. D. Savage, W. B. Kannel, and W. P. Castelli, “Prognostic Implications of Echocardiographically Determined Left Ventricular Mass in the Framingham Heart Study,” N. Engl. J. Med. 322(22), 1561–1566 (1990).
[PubMed]

Gavin, J. B.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol. 269(2 Pt 2), H571–H582 (1995).
[PubMed]

Geoffroy, P.

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

Gerstenblith, G.

S. P. Schulman, E. G. Lakatta, J. L. Fleg, L. Lakatta, L. C. Becker, and G. Gerstenblith, “Age-related decline in left ventricular filling at rest and exercise,” Am. J. Physiol. 263(6 Pt 2), H1932–H1938 (1992).
[PubMed]

G. Gerstenblith, J. Frederiksen, F. C. Yin, N. J. Fortuin, E. G. Lakatta, and M. L. Weisfeldt, “Echocardiographic assessment of a normal adult aging population,” Circulation 56(2), 273–278 (1977).
[PubMed]

Goergen, C. J.

C. J. Goergen, H. H. Chen, S. Sakadžić, V. J. Srinivasan, and D. E. Sosnovik, “Microstructural characterization of myocardial infarction with optical coherence tractography and two-photon microscopy,” Physiol. Rep. 4(18), e12894 (2016).
[PubMed]

C. J. Goergen, H. Radhakrishnan, S. Sakadžić, E. T. Mandeville, E. H. Lo, D. E. Sosnovik, and V. J. Srinivasan, “Optical coherence tractography using intrinsic contrast,” Opt. Lett. 37(18), 3882–3884 (2012).
[PubMed]

Grieve, S. M.

P. J. Cassidy, J. E. Schneider, S. M. Grieve, C. Lygate, S. Neubauer, and K. Clarke, “Assessment of motion gating strategies for mouse magnetic resonance at high magnetic fields,” J. Magn. Reson. Imaging 19(2), 229–237 (2004).
[PubMed]

J. E. Schneider, P. J. Cassidy, C. Lygate, D. J. Tyler, F. Wiesmann, S. M. Grieve, K. Hulbert, K. Clarke, and S. Neubauer, “Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system,” J. Magn. Reson. Imaging 18(6), 691–701 (2003).
[PubMed]

Grobbee, D. E.

A. Mosterd, A. W. Hoes, M. C. de Bruyne, J. W. Deckers, D. T. Linker, A. Hofman, and D. E. Grobbee, “Prevalence of heart failure and left ventricular dysfunction in the general population; The Rotterdam Study,” Eur. Heart J. 20(6), 447–455 (1999).
[PubMed]

Guan, J.

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

Haider, A. W.

A. W. Haider, M. G. Larson, E. J. Benjamin, and D. Levy, “Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death,” J. Am. Coll. Cardiol. 32(5), 1454–1459 (1998).
[PubMed]

Hanna, W. T.

D. D. Streeter and W. T. Hanna, “Engineering mechanics for successive states in canine left ventricular myocardium. II. Fiber angle and sarcomere length,” Circ. Res. 33(6), 656–664 (1973).
[PubMed]

Heiberg, E.

E. Heiberg, J. Sjögren, M. Ugander, M. Carlsson, H. Engblom, and H. Arheden, “Design and validation of Segment--freely available software for cardiovascular image analysis,” BMC Med. Imaging 10, 1 (2010).
[PubMed]

Heijman, E.

G. J. Strijkers, A. Bouts, W. M. Blankesteijn, T. H. J. M. Peeters, A. Vilanova, M. C. van Prooijen, H. M. H. F. Sanders, E. Heijman, and K. Nicolay, “Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse,” NMR Biomed. 22(2), 182–190 (2009).
[PubMed]

Hoes, A. W.

A. Mosterd, A. W. Hoes, M. C. de Bruyne, J. W. Deckers, D. T. Linker, A. Hofman, and D. E. Grobbee, “Prevalence of heart failure and left ventricular dysfunction in the general population; The Rotterdam Study,” Eur. Heart J. 20(6), 447–455 (1999).
[PubMed]

Hofman, A.

A. Mosterd, A. W. Hoes, M. C. de Bruyne, J. W. Deckers, D. T. Linker, A. Hofman, and D. E. Grobbee, “Prevalence of heart failure and left ventricular dysfunction in the general population; The Rotterdam Study,” Eur. Heart J. 20(6), 447–455 (1999).
[PubMed]

Holmes, A.

D. F. Scollan, A. Holmes, R. Winslow, and J. Forder, “Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging,” Am. J. Physiol. 275(6 Pt 2), H2308–H2318 (1998).
[PubMed]

Huang, S.

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

Hulbert, K.

J. E. Schneider, P. J. Cassidy, C. Lygate, D. J. Tyler, F. Wiesmann, S. M. Grieve, K. Hulbert, K. Clarke, and S. Neubauer, “Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system,” J. Magn. Reson. Imaging 18(6), 691–701 (2003).
[PubMed]

Hunter, P. J.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol. 269(2 Pt 2), H571–H582 (1995).
[PubMed]

Jackowski, M. P.

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

Kadiri, L. R.

T. Ragan, L. R. Kadiri, K. U. Venkataraju, K. Bahlmann, J. Sutin, J. Taranda, I. Arganda-Carreras, Y. Kim, H. S. Seung, and P. Osten, “Serial two-photon tomography for automated ex vivo mouse brain imaging,” Nat. Methods 9(3), 255–258 (2012).
[PubMed]

Kannel, W. B.

D. Levy, R. J. Garrison, D. D. Savage, W. B. Kannel, and W. P. Castelli, “Prognostic Implications of Echocardiographically Determined Left Ventricular Mass in the Framingham Heart Study,” N. Engl. J. Med. 322(22), 1561–1566 (1990).
[PubMed]

Kim, Y.

T. Ragan, L. R. Kadiri, K. U. Venkataraju, K. Bahlmann, J. Sutin, J. Taranda, I. Arganda-Carreras, Y. Kim, H. S. Seung, and P. Osten, “Serial two-photon tomography for automated ex vivo mouse brain imaging,” Nat. Methods 9(3), 255–258 (2012).
[PubMed]

Kostis, W. J.

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

Kozerke, S.

D. E. Sosnovik, C. Mekkaoui, S. Huang, H. H. Chen, G. Dai, C. T. Stoeck, S. Ngoy, J. Guan, R. Wang, W. J. Kostis, M. P. Jackowski, V. J. Wedeen, S. Kozerke, and R. Liao, “Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo,” Circulation 129(17), 1731–1741 (2014).
[PubMed]

L’Allier, P.

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

Lakatta, E. G.

E. G. Lakatta and D. Levy, “Arterial and Cardiac Aging: Major Shareholders in Cardiovascular Disease Enterprises: Part I: Aging Arteries: A “Set Up” for Vascular Disease,” Circulation 107(1), 139–146 (2003).
[PubMed]

E. G. Lakatta and D. Levy, “Arterial and Cardiac Aging: Major Shareholders in Cardiovascular Disease Enterprises: Part II: The Aging Heart in Health: Links to Heart Disease,” Circulation 107(2), 346–354 (2003).
[PubMed]

S. P. Schulman, E. G. Lakatta, J. L. Fleg, L. Lakatta, L. C. Becker, and G. Gerstenblith, “Age-related decline in left ventricular filling at rest and exercise,” Am. J. Physiol. 263(6 Pt 2), H1932–H1938 (1992).
[PubMed]

G. Gerstenblith, J. Frederiksen, F. C. Yin, N. J. Fortuin, E. G. Lakatta, and M. L. Weisfeldt, “Echocardiographic assessment of a normal adult aging population,” Circulation 56(2), 273–278 (1977).
[PubMed]

Lakatta, L.

S. P. Schulman, E. G. Lakatta, J. L. Fleg, L. Lakatta, L. C. Becker, and G. Gerstenblith, “Age-related decline in left ventricular filling at rest and exercise,” Am. J. Physiol. 263(6 Pt 2), H1932–H1938 (1992).
[PubMed]

Larson, M. G.

A. W. Haider, M. G. Larson, E. J. Benjamin, and D. Levy, “Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death,” J. Am. Coll. Cardiol. 32(5), 1454–1459 (1998).
[PubMed]

Lefebvre, J.

J. Lefebvre, A. Castonguay, P. Pouliot, M. Descoteaux, and F. Lesage, “Whole mouse brain imaging using optical coherence tomography: reconstruction, normalization, segmentation, and comparison with diffusion MRI,” Neurophotonics 4(4), 041501 (2017).
[PubMed]

P.-L. Tardif, M.-J. Bertrand, M. Abran, A. Castonguay, J. Lefebvre, B. E. Stähli, N. Merlet, T. Mihalache-Avram, P. Geoffroy, M. Mecteau, D. Busseuil, F. Ni, A. Abulrob, É. Rhéaume, P. L’Allier, J.-C. Tardif, and F. Lesage, “Validating Intravascular Imaging with Serial Optical Coherence Tomography and Confocal Fluorescence Microscopy,” Int. J. Mol. Sci. 17(12), 2110 (2016).
[PubMed]

LeGrice, I. J.

I. J. LeGrice, B. H. Smaill, L. Z. Chai, S. G. Edgar, J. B. Gavin, and P. J. Hunter, “Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog,” Am. J. Physiol. 269(2 Pt 2), H571–H582 (1995).
[PubMed]

Lemij, H. G.

Lesage, F.

J. Lefebvre, A. Castonguay, P. Pouliot, M. Descoteaux, and F. Lesage, “Whole mouse brain imaging using optical coherence tomography: reconstruction, normalization, segmentation, and comparison with diffusion MRI,” Neurophotonics 4(4), 041501 (2017).
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Molter, J.

W. Li, M. Lu, S. Banerjee, J. Zhong, A. Ye, J. Molter, and X. Yu, “Ex vivo diffusion tensor MRI reflects microscopic structural remodeling associated with aging and disease progression in normal and cardiomyopathic Syrian hamsters,” NMR Biomed. 22(8), 819–825 (2009).
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C. J. Goergen, H. H. Chen, S. Sakadžić, V. J. Srinivasan, and D. E. Sosnovik, “Microstructural characterization of myocardial infarction with optical coherence tractography and two-photon microscopy,” Physiol. Rep. 4(18), e12894 (2016).
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T. Ragan, L. R. Kadiri, K. U. Venkataraju, K. Bahlmann, J. Sutin, J. Taranda, I. Arganda-Carreras, Y. Kim, H. S. Seung, and P. Osten, “Serial two-photon tomography for automated ex vivo mouse brain imaging,” Nat. Methods 9(3), 255–258 (2012).
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Figures (5)

Fig. 1
Fig. 1 Heart reconstruction from serial OCT imaging. (a) Schematic of the heart positioning for serial sectioning. Red borders delimit the volume acquired by the system. Red area shows volumetric data imaged by one serially scanned section with green lines delimiting adjacent tiles imaged by the microscope. (b) Long axis view of the heart showing left and right ventricles. Red lines show position of short axis views in (c). (c) short axis views spaced by one millimeter. Scale bar: 1mm.
Fig. 2
Fig. 2 Myofiber architecture. (a) 3D representation of a young mouse heart. (b) short axis AIP over 200µm around red plane depicted in (a). Scale bar: 1mm. (c) Detailed view of region presented in (b) with ODFs showing preferred orientation in region of interest of (200 x 200) µm. (d) 3D in plane orientation of heart shown in (a). (e). In plane orientation of short axis view in (b). Arrow shows local fiber oriented at an angle described in Cartesian coordinates (θ) and in polar coordinates (φ) relative to the center O of the slice. (f) Fiber orientation converted to polar coordinates, relative to the center of the slice. r: distance to the center. (g) Average fiber orientation along depth from endocardial surface for the slice presented in (f). Fitted line to the measured data shows an orientation change of 0.07°/µm. (h) Left ventricle wall thickness as a function of the radial position of slice in (f).
Fig. 3
Fig. 3 Age dependent changes in heart architecture. (a) Average myofiber orientation changes as a function of distance from apex for young and aged mice. A paired t-test showed a significant (p<0.01) orientation difference between young and old mice. (b) Average left ventricle wall thickness as a function of distance from the apex for young and old mice. (c) Tissue masking of a short axis view. (d) Heart volume up to 4mm from the apex measured from masked AIPs. A significant heart volume increase was observed in old mice (p<0.05). Error bar in (a) and (b) show standard error.
Fig. 4
Fig. 4 Light attenuation. (a) Short axis views taken at 1mm from apex form three young mice (left) and three old mice (right). Red boxes of (500x500) µm were used to evaluate tissue attenuation. Scale bar: 1mm. (b) Tissue attenuation from regions of interest in (b). Grey lines: 4 months mice. Black lines: 24 months mice. (c) When looking at all mice, light attenuation in endocardium showed a significant decrease (p<0.05) in old mice.
Fig. 5
Fig. 5 In vivo MRI heart imaging. (a) Example of end-diastole (left) and end-systole (right) timeframes in a young heart. Each image has a field of view of (10x10) mm and 0.8 mm thick. Green lines delimit epicardial surface and red lines show endocardial surface segmented with Segment software. (b) Fraction of left ventricle contraction as a distance from the apex. (c) Fiber orientation change plotted against the LV-slice contraction. Dashed line: linear fit to the 4 months group (R2 = 0.885). Full line: linear fit to the 24 months group (R2 = 0.852)

Tables (1)

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Table 1 Cardiac functional parameters of two aged groups

Equations (1)

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ODF( θ )=  | F w ( f x , f y ) | 2 H( f x , f y )df

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