Abstract

Skeletal muscle fibers are a known source of form birefringence in biological tissue. The birefringence present in skeletal muscle is associated with the ultrastructure of individual sarcomeres, specifically the arrangement of A-bands corresponding to the thick myosin filaments. Certain structural proteins that prevent damage and maintain the structural and functional health of the muscle fiber preserve the organization of the A-bands in skeletal muscle. Therefore, the level of birefringence detected can estimate the health of the muscle as well as the damage incurred during exercise. Murine skeletal muscle from both genetically-altered (mdx) and normal (wild-type) specimens were imaged in vivo with a fiber-based PS-OCT imaging system to quantitatively determine the level of birefringence present in the tissue before and after exercise. The mdx muscle lacks dystrophin, a structural protein that is mutated in Duchenne muscular dystrophy in humans. Muscle from these mdx mice exhibited a marked decrease in birefringence after exercise, whereas the wild-type muscle was highly birefringent before and after exercise. The quantitative results from this tissue optics study suggest for the first time that there is a distinct relationship between the degree of birefringence detected using PS-OCT and the sarcomeric ultrastructure present within skeletal muscle.

© 2006 Optical Society of America

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2005 (5)

2004 (4)

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

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[PubMed]

S. Guo, J. Zhang, L. Wang, J. S. Nelson, and Z. Chen, "Depth-resolved birefringence and differential optical axis orientation measurements with fiber-based polarization-sensitive optical coherence tomography," Opt. Lett. 29, 2025 (2004).
[CrossRef] [PubMed]

B. H. Park, M. C. Pierce, B. Cense, and J. F. de Boer, "Jones matrix analysis for a polarization-sensitive optical coherence tomography system using fiber-optic components," Opt. Lett. 29, 2512 (2004).
[CrossRef] [PubMed]

2002 (2)

T. E. Milner and J. F. de Boer, "Review of polarization sensitive optical coherence tomography and Stokes vector determination," J. Biomed. Opt. 7, 359 (2002).
[CrossRef]

J. F. Watchko, T. L. O’Day, and E. P. Hoffman, "Functional characteristics of dystrophic skeletal muscle: insights from animal models," J. Appl. Physiol. 93, 407 (2002).
[PubMed]

2001 (2)

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

C. Hitzenberger, E. Goetzinger, M. Sticker, M. Pircher, and A. F. Fercher, "Measurement and imaging of birefringence and optic axis orientation by phase resolved polarization sensitive optical coherence tomography," Opt. Express 9, 780-790 (2001).
[CrossRef]

1999 (2)

1997 (1)

1992 (1)

1987 (1)

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Brezinski, M. E.

N. A. Patel, J. Zoeller, D. L. Stamper, J. G. Fujimoto, and M. E. Brezinski, "Monitoring osteoarthritis in the rat model using optical coherence tomography," IEEE Trans. Med. Imaging 24, 155 (2005).
[CrossRef] [PubMed]

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Cense, B.

B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, "Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 45, 2606 (2004).
[PubMed]

B. H. Park, M. C. Pierce, B. Cense, and J. F. de Boer, "Jones matrix analysis for a polarization-sensitive optical coherence tomography system using fiber-optic components," Opt. Lett. 29, 2512 (2004).
[CrossRef] [PubMed]

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

Chen, T. C.

B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, "Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 45, 2606 (2004).
[PubMed]

Chen, Y.

Chen, Z.

de Boer, J.

de Boer, J. F.

B. H. Park, M. C. Pierce, B. Cense, and J. F. de Boer, "Jones matrix analysis for a polarization-sensitive optical coherence tomography system using fiber-optic components," Opt. Lett. 29, 2512 (2004).
[CrossRef] [PubMed]

B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, "Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 45, 2606 (2004).
[PubMed]

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

T. E. Milner and J. F. de Boer, "Review of polarization sensitive optical coherence tomography and Stokes vector determination," J. Biomed. Opt. 7, 359 (2002).
[CrossRef]

J. F. de Boer, T. E. Milner, and J. S. Nelson, "Determination of the depth-resolved Stokes parameters of light backscattered from turbid media by use of polarization-sensitive optical coherence tomography," Opt. Lett. 24, 300-302 (1999).
[CrossRef] [PubMed]

De la Porte, S.

S. De la Porte, S. Morin, and J. Koenig, "Characteristics of skeletal muscle in mdx mutant mice," Int. Rev. Cytol 191, 99 (1999).
[CrossRef] [PubMed]

Drexler, W.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Evans, W. J.

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Fercher, A. F.

Fielding, R. A.

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Ford, L. E.

A. V. Smolensky, J. Ragozzino, S. H. Gilbert, C. Y. Seow, and L. E. Ford, "Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle," J. Physiol. 563, 517 (2005).
[CrossRef]

Frontera, W. R.

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Fujimoto, J. G.

N. A. Patel, J. Zoeller, D. L. Stamper, J. G. Fujimoto, and M. E. Brezinski, "Monitoring osteoarthritis in the rat model using optical coherence tomography," IEEE Trans. Med. Imaging 24, 155 (2005).
[CrossRef] [PubMed]

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

M. R. Hee, D. Huang, E. A. Swanson, J. G. Fujimoto, "Polarization-sensitive low-coherence reflectometer for birefringence characterization and ranging", J. Opt. Soc. Am. B 9, 903-908 (1992).
[CrossRef] [PubMed]

Gilbert, S. H.

A. V. Smolensky, J. Ragozzino, S. H. Gilbert, C. Y. Seow, and L. E. Ford, "Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle," J. Physiol. 563, 517 (2005).
[CrossRef]

Goetzinger, E.

Guo, S.

Hee, M. R.

Hitzenberger, C.

Hoffman, E. P.

J. F. Watchko, T. L. O’Day, and E. P. Hoffman, "Functional characteristics of dystrophic skeletal muscle: insights from animal models," J. Appl. Physiol. 93, 407 (2002).
[PubMed]

Huang, D.

Jesser, C.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Jiao, S.

Kemp, N.

Koenig, J.

S. De la Porte, S. Morin, and J. Koenig, "Characteristics of skeletal muscle in mdx mutant mice," Int. Rev. Cytol 191, 99 (1999).
[CrossRef] [PubMed]

Li, X.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Lodge, M. B.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Martin, S.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Meredith, C. N.

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Milner, T.

Milner, T. E.

Morin, S.

S. De la Porte, S. Morin, and J. Koenig, "Characteristics of skeletal muscle in mdx mutant mice," Int. Rev. Cytol 191, 99 (1999).
[CrossRef] [PubMed]

Nelson, J.

Nelson, J. S.

O’Day, T. L.

J. F. Watchko, T. L. O’Day, and E. P. Hoffman, "Functional characteristics of dystrophic skeletal muscle: insights from animal models," J. Appl. Physiol. 93, 407 (2002).
[PubMed]

O'Reilly, K. P.

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Otis, L.

Park, B. H.

B. H. Park, M. C. Pierce, B. Cense, and J. F. de Boer, "Jones matrix analysis for a polarization-sensitive optical coherence tomography system using fiber-optic components," Opt. Lett. 29, 2512 (2004).
[CrossRef] [PubMed]

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, "Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 45, 2606 (2004).
[PubMed]

Park, J.

Patel, N. A.

N. A. Patel, J. Zoeller, D. L. Stamper, J. G. Fujimoto, and M. E. Brezinski, "Monitoring osteoarthritis in the rat model using optical coherence tomography," IEEE Trans. Med. Imaging 24, 155 (2005).
[CrossRef] [PubMed]

Piao, D.

Pierce, M. C.

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, "Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 45, 2606 (2004).
[PubMed]

B. H. Park, M. C. Pierce, B. Cense, and J. F. de Boer, "Jones matrix analysis for a polarization-sensitive optical coherence tomography system using fiber-optic components," Opt. Lett. 29, 2512 (2004).
[CrossRef] [PubMed]

Pircher, M.

Pitris, C.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Ragozzino, J.

A. V. Smolensky, J. Ragozzino, S. H. Gilbert, C. Y. Seow, and L. E. Ford, "Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle," J. Physiol. 563, 517 (2005).
[CrossRef]

Rylander, H.

Saunders, K.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Seow, C. Y.

A. V. Smolensky, J. Ragozzino, S. H. Gilbert, C. Y. Seow, and L. E. Ford, "Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle," J. Physiol. 563, 517 (2005).
[CrossRef]

Smolensky, A. V.

A. V. Smolensky, J. Ragozzino, S. H. Gilbert, C. Y. Seow, and L. E. Ford, "Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle," J. Physiol. 563, 517 (2005).
[CrossRef]

Stamper, D.

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Stamper, D. L.

N. A. Patel, J. Zoeller, D. L. Stamper, J. G. Fujimoto, and M. E. Brezinski, "Monitoring osteoarthritis in the rat model using optical coherence tomography," IEEE Trans. Med. Imaging 24, 155 (2005).
[CrossRef] [PubMed]

Sticker, M.

Stoica, G.

Strasswimmer, J.

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

Swanson, E. A.

Todorovic, M.

van Gemert, M.

Wang, L.

Wang, L. V.

Warhol, M. J.

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

Watchko, J. F.

J. F. Watchko, T. L. O’Day, and E. P. Hoffman, "Functional characteristics of dystrophic skeletal muscle: insights from animal models," J. Appl. Physiol. 93, 407 (2002).
[PubMed]

Zaatari, H.

Zhang, J.

Zhu, Q.

Zoeller, J.

N. A. Patel, J. Zoeller, D. L. Stamper, J. G. Fujimoto, and M. E. Brezinski, "Monitoring osteoarthritis in the rat model using optical coherence tomography," IEEE Trans. Med. Imaging 24, 155 (2005).
[CrossRef] [PubMed]

Appl. Opt. (2)

IEEE Trans. Med. Imaging (1)

N. A. Patel, J. Zoeller, D. L. Stamper, J. G. Fujimoto, and M. E. Brezinski, "Monitoring osteoarthritis in the rat model using optical coherence tomography," IEEE Trans. Med. Imaging 24, 155 (2005).
[CrossRef] [PubMed]

Int. Rev. Cytol (1)

S. De la Porte, S. Morin, and J. Koenig, "Characteristics of skeletal muscle in mdx mutant mice," Int. Rev. Cytol 191, 99 (1999).
[CrossRef] [PubMed]

Invest. Ophthalmol. Vis. Sci. (1)

B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, "Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography," Invest. Ophthalmol. Vis. Sci. 45, 2606 (2004).
[PubMed]

J. Appl. Physiol. (2)

K. P. O'Reilly, M. J. Warhol, R. A. Fielding, W. R. Frontera, C. N. Meredith, and W. J. Evans, "Eccentric exercise-induced muscle damage impairs muscle glycogen repletion," J. Appl. Physiol. 63, 252 (1987).
[PubMed]

J. F. Watchko, T. L. O’Day, and E. P. Hoffman, "Functional characteristics of dystrophic skeletal muscle: insights from animal models," J. Appl. Physiol. 93, 407 (2002).
[PubMed]

J. Biomed. Opt. (2)

M. C. Pierce, J. Strasswimmer, B. H. Park, B. Cense, and J. F. de Boer, "Birefringence measurements in human skin using polarization-sensitive optical coherence tomography," J. Biomed. Opt. 9, 287 (2004).
[CrossRef] [PubMed]

T. E. Milner and J. F. de Boer, "Review of polarization sensitive optical coherence tomography and Stokes vector determination," J. Biomed. Opt. 7, 359 (2002).
[CrossRef]

J. Opt. Soc. Am. B (1)

J. Physiol. (1)

A. V. Smolensky, J. Ragozzino, S. H. Gilbert, C. Y. Seow, and L. E. Ford, "Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle," J. Physiol. 563, 517 (2005).
[CrossRef]

J. Rheumatol. (1)

W. Drexler, D. Stamper, C. Jesser, X. Li, C. Pitris, K. Saunders, S. Martin, M. B. Lodge, J. G. Fujimoto, and M. E. Brezinski, "Correlation of collagen organization with polarization sensitive imaging of in vitro cartilage: implications for osteoarthritis," J. Rheumatol. 28, 1311 (2001).
[CrossRef] [PubMed]

Opt. Express (2)

Opt. Lett. (4)

Other (1)

J. Sherman, A. Vander, and D. Luciano, Human Physiology: The Mechanisms of Body Function, 8th ed. (McGraw-Hill Companies Inc., New York, NY 2001).

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Figures (8)

Fig. 1.
Fig. 1.

Schematic of the PS-OCT system. Abbreviations: SLD, super luminescent diode; Pol., linear polarizer; Pol. Mod., polarization modulator; 90/10, 50/50, fiber couplers; RSOD, rapid scanning optical delay; OC, optical circulator; P#, polarization paddles; PBS, polarization beam splitter; P.D., photodetector.

Fig. 2.
Fig. 2.

Synchronized signals used to control the RSOD delay galvanometer (blue), the polarization modulator (red), the analog two-channel multiplexer (orange), and the x-galvanometer (green). Fringe data was collected during the rising slope of the pseudo-sawtooth delay waveform (blue).

Fig. 3.
Fig. 3.

Non-exercised wild-type murine skeletal muscle. A) Structural OCT image. B) False-color birefringence image. The black box outlines the region over which the mean zero-crossing distance was calculated and the black points represent the zero-crossing points identified by the algorithm. Histological images are shown using (C) Evans blue fluorescence at 20x, (D) H&E at 20x, and (E) TEM at 5000x magnifications. Scale bar represents 500 μm.

Fig. 4.
Fig. 4.

Non-exercised mdx murine skeletal muscle. A) Structural OCT image. B) False-color birefringence image. The black box outlines the region over which the mean zero-crossing distance was calculated and the black points represent the zero-crossing points identified by the algorithm. Histological images are shown using (C) Evans blue fluorescence at 10x, (D) H&E at 10x, and (E) TEM at 5000x magnifications. Scale bar represents 500 μm.

Fig. 5.
Fig. 5.

Exercised wild-type murine skeletal muscle. A) Structural OCT image. B) False-color birefringence image. The black box outlines the region over which the mean zero-crossing distance was calculated and the black points represent the zero-crossing points identified by the algorithm. Histological images are shown using (C) Evans blue fluorescence at 20x, (D) H&E at 20x, and (E) TEM at 5000x magnifications. Scale bar represents 500 μm.

Fig. 6.
Fig. 6.

Exercised mdx murine skeletal muscle. A) Structural OCT image. B) False-color birefringence image. The black box outlines the region over which the mean zero-crossing distance was calculated and the black points represent the zero-crossing points identified by the algorithm. Histological images are shown using (C) Evans blue fluorescence at 10x, (D) H&E at 10x, and (E) TEM at 5000x magnifications. Scale bar represents 500 μm.

Fig. 7.
Fig. 7.

Quantitative comparison of birefringence values from skeletal muscle types. Error bars represent the standard deviation of the birefringence.

Fig. 8.
Fig. 8.

Plot showing calculated birefringence values vs. measured Evans blue positive fiber count for the four muscle types. Error bars represent standard deviation of the birefringence.

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