Abstract

We present three-dimensional Fourier transform-second-harmonic generation (3D FT-SHG) imaging, a generalization of the previously reported two-dimensional FT-SHG, to quantify collagen fiber organization from 3D image stacks of biological tissues. The current implementation calculates 3D preferred orientation of a region of interest, and classifies regions of interest based on orientation anisotropy and average voxel intensity. Presented are some example applications of the technique which reveal the layered structure of collagen fibers in porcine sclera, and estimates the cut angle of porcine tendon tissues. This technique shows promising potential for studying biological tissues that contain fibrillar structures in 3D.

©2012 Optical Society of America

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2012 (5)

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
[Crossref] [PubMed]

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

T. Abraham, D. Kayra, B. McManus, and A. Scott, “Quantitative assessment of forward and backward second harmonic three dimensional images of collagen type I matrix remodeling in a stimulated cellular environment,” J. Struct. Biol. (2012), http://dx.doi.org/10.1016/j.jsb.2012.05.004.
[Crossref] [PubMed]

R. Ambekar, T.-Y. Lau, M. Walsh, R. Bhargava, and K. C. Toussaint, “Quantifying collagen structure in breast biopsies using second-harmonic generation imaging,” Biomed. Opt. Express 3(9), 2021–2035 (2012).
[Crossref]

2011 (4)

C. Thrasivoulou, G. Virich, T. Krenacs, I. Korom, and D. L. Becker, “Optical delineation of human malignant melanoma using second harmonic imaging of collagen,” Biomed. Opt. Express 2(5), 1282–1295 (2011).
[Crossref] [PubMed]

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci. 52(12), 8818–8827 (2011).
[Crossref] [PubMed]

R. Ambekar, K. C. Toussaint, and A. Wagoner Johnson, “The effect of keratoconus on the structural, mechanical, and optical properties of the cornea,” J. Mech. Behav. Biomed. Mater. 4(3), 223–236 (2011).
[Crossref] [PubMed]

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 52(2), 911–915 (2011).
[Crossref] [PubMed]

2010 (10)

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by second harmonic generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer 46(7), 1181–1188 (2010).
[Crossref] [PubMed]

J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
[Crossref] [PubMed]

T. Abraham and J. Hogg, “Extracellular matrix remodeling of lung alveolar walls in three dimensional space identified using second harmonic generation and multiphoton excitation fluorescence,” J. Struct. Biol. 171(2), 189–196 (2010).
[Crossref] [PubMed]

N. Toussaint, M. Sermesant, C. T. Stoeck, S. Kozerke, and P. G. Batchelor, “In vivo human 3D cardiac fibre architecture: reconstruction using curvilinear interpolation of diffusion tensor images,” Med. Image Comput. Comput. Assist Interv. 13(Pt 1), 418–425 (2010).
[PubMed]

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol. 86(2), 302–310 (2010).
[Crossref] [PubMed]

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

I. Amat-Roldan, S. Psilodimitrakopoulos, P. Loza-Alvarez, and D. Artigas, “Fast image analysis in polarization SHG microscopy,” Opt. Express 18(16), 17209–17219 (2010).
[Crossref] [PubMed]

M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express 18(24), 24983–24993 (2010).
[Crossref] [PubMed]

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
[Crossref] [PubMed]

2009 (4)

N. Morishige, N. Yamada, S. Teranishi, T.-i. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[Crossref] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett. 94, 3 (2009).

R. A. Rao, M. R. Mehta, and K. C. Toussaint., “Fourier transform-second-harmonic generation imaging of biological tissues,” Opt. Express 17(17), 14534–14542 (2009).
[Crossref] [PubMed]

R. A. Rao, M. R. Mehta, S. Leithem, and K. C. Toussaint., “Quantitative analysis of forward and backward second-harmonic images of collagen fibers using Fourier transform second-harmonic-generation microscopy,” Opt. Lett. 34(24), 3779–3781 (2009).
[Crossref] [PubMed]

2008 (2)

K. Brockbank, W. MacLellan, J. Xie, S. Hamm-Alvarez, Z. Chen, and K. Schenke-Layland, “Quantitative second harmonic generation imaging of cartilage damage,” Cell Tissue Banking 9, 299–307 (2008).

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt. 13(5), 054050 (2008).
[Crossref] [PubMed]

2007 (2)

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
[Crossref] [PubMed]

F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express 15(19), 12286–12295 (2007).
[Crossref] [PubMed]

2006 (3)

O. Friman, G. Farnebäck, and C. F. Westin, “A Bayesian approach for stochastic white matter tractography,” IEEE Trans. Med. Imaging 25(8), 965–978 (2006).
[Crossref] [PubMed]

M. J. Silva, M. D. Brodt, B. Wopenka, S. Thomopoulos, D. Williams, M. H. M. Wassen, M. Ko, N. Kusano, and R. A. Bank, “Decreased collagen organization and content are associated with reduced strength of demineralized and intact bone in the SAMP6 mouse,” J. Bone Miner. Res. 21(1), 78–88 (2006).
[Crossref] [PubMed]

S. Viguet-Carrin, P. Garnero, and P. D. Delmas, “The role of collagen in bone strength,” Osteoporosis Int. 17(3), 319–336 (2006).
[Crossref] [PubMed]

2005 (3)

C. Boote, S. Dennis, Y. Huang, A. J. Quantock, and K. M. Meek, “Lamellar orientation in human cornea in relation to mechanical properties,” J. Struct. Biol. 149(1), 1–6 (2005).
[Crossref] [PubMed]

B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Sys. Signal Process. 19(5), 1152–1161 (2005).
[Crossref]

P. Helm, M. F. Beg, M. I. Miller, and R. L. Winslow, “Measuring and mapping cardiac fiber and laminar architecture using diffusion tensor MR imaging,” Ann. N. Y. Acad. Sci. 1047(1), 296–307 (2005).
[Crossref] [PubMed]

2004 (1)

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

2003 (5)

L. Loew, A. Millard, P. J. Campagnola, W. Mohler, and A. Lewis, “Second harmonic imaging microscopy,” Microsc. Microanal. 9, 170–171 (2003).

J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
[Crossref] [PubMed]

M. F. Young, “Bone matrix proteins: their function, regulation, and relationship to osteoporosis,” Osteoporosis Int. 14, 35–42 (2003).

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[Crossref] [PubMed]

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref] [PubMed]

2002 (4)

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

P. Stoller, B.-M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7(2), 205–214 (2002).
[Crossref] [PubMed]

S. Mori and P. C. van Zijl, “Fiber tracking: principles and strategies - a technical review,” NMR Biomed. 15(7-8), 468–480 (2002).
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B. Pourdeyhimi and H. S. Kim, “Measuring fiber orientation in nonwovens: the hough transform,” Text. Res. J. 72(9), 803–809 (2002).
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2001 (2)

A. A. A. Jaddi, H. S. Kim, and B. Pourdeyhimi, “Measurement of fiber orientation in nonwovens optical Fourier transform,” Inter. Nonwovens J. 10, 10–16 (2001).

D. F. Holmes, C. J. Gilpin, C. Baldock, U. Ziese, A. J. Koster, and K. E. Kadler, “Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organization,” Proc. Natl. Acad. Sci. U.S.A. 98(13), 7307–7312 (2001).
[Crossref] [PubMed]

2000 (3)

S. M. Weis, J. L. Emery, K. D. Becker, D. J. McBride, J. H. Omens, and A. D. McCulloch, “Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (oim),” Circ. Res. 87(8), 663–669 (2000).
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W. Yi and S. Marshall, “Principal component analysis in application to object orientation,” Geo-Spat. Inf. Sci. 3, 76–78 (2000).

A. K. Jain, S. Prabhakar, L. Hong, and S. Pankanti, “Filterbank-based fingerprint matching,” IEEE Trans. Image Process. 9(5), 846–859 (2000).
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1999 (1)

C. C. Van Donkelaar, L. J. G. Kretzers, P. H. M. Bovendeerd, L. M. A. Lataster, K. Nicolay, J. D. Janssen, and M. R. Drost, “Diffusion tensor imaging in biomechanical studies of skeletal muscle function,” J. Anat. 194(1), 79–88 (1999).
[Crossref] [PubMed]

1992 (1)

R. H. Bamberger and M. J. T. Smith, “A filter bank for the directional decomposition of images: theory and design,” IEEE Trans. Signal Process. 40(4), 882–893 (1992).
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1991 (1)

Y. Komai and T. Ushiki, “The three-dimensional organization of collagen fibrils in the human cornea and sclera,” Invest. Ophthalmol. Visual Sci. 32(8), 2244–2258 (1991).
[PubMed]

1986 (1)

J. Canny, “A computational approach to edge detection,” IEEE Trans. Pattern Anal. Mach. Intell. PAMI-8 (6), 679–698 (1986).
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Abdulghani, S.

J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
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Abraham, T.

T. Abraham, D. Kayra, B. McManus, and A. Scott, “Quantitative assessment of forward and backward second harmonic three dimensional images of collagen type I matrix remodeling in a stimulated cellular environment,” J. Struct. Biol. (2012), http://dx.doi.org/10.1016/j.jsb.2012.05.004.
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T. Abraham and J. Hogg, “Extracellular matrix remodeling of lung alveolar walls in three dimensional space identified using second harmonic generation and multiphoton excitation fluorescence,” J. Struct. Biol. 171(2), 189–196 (2010).
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Amaral, P. M.

J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
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Amat-Roldan, I.

Ambekar, R.

R. Ambekar, T.-Y. Lau, M. Walsh, R. Bhargava, and K. C. Toussaint, “Quantifying collagen structure in breast biopsies using second-harmonic generation imaging,” Biomed. Opt. Express 3(9), 2021–2035 (2012).
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R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
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R. Ambekar, K. C. Toussaint, and A. Wagoner Johnson, “The effect of keratoconus on the structural, mechanical, and optical properties of the cornea,” J. Mech. Behav. Biomed. Mater. 4(3), 223–236 (2011).
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M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express 18(24), 24983–24993 (2010).
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Artigas, D.

Baldock, C.

D. F. Holmes, C. J. Gilpin, C. Baldock, U. Ziese, A. J. Koster, and K. E. Kadler, “Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organization,” Proc. Natl. Acad. Sci. U.S.A. 98(13), 7307–7312 (2001).
[Crossref] [PubMed]

Bamberger, R. H.

R. H. Bamberger and M. J. T. Smith, “A filter bank for the directional decomposition of images: theory and design,” IEEE Trans. Signal Process. 40(4), 882–893 (1992).
[Crossref]

Bank, R. A.

M. J. Silva, M. D. Brodt, B. Wopenka, S. Thomopoulos, D. Williams, M. H. M. Wassen, M. Ko, N. Kusano, and R. A. Bank, “Decreased collagen organization and content are associated with reduced strength of demineralized and intact bone in the SAMP6 mouse,” J. Bone Miner. Res. 21(1), 78–88 (2006).
[Crossref] [PubMed]

Barkan, D.

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer 46(7), 1181–1188 (2010).
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Batchelor, P. G.

N. Toussaint, M. Sermesant, C. T. Stoeck, S. Kozerke, and P. G. Batchelor, “In vivo human 3D cardiac fibre architecture: reconstruction using curvilinear interpolation of diffusion tensor images,” Med. Image Comput. Comput. Assist Interv. 13(Pt 1), 418–425 (2010).
[PubMed]

Beaurepaire, E.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
[Crossref] [PubMed]

Becker, D. L.

Becker, K. D.

S. M. Weis, J. L. Emery, K. D. Becker, D. J. McBride, J. H. Omens, and A. D. McCulloch, “Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (oim),” Circ. Res. 87(8), 663–669 (2000).
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Beg, M. F.

P. Helm, M. F. Beg, M. I. Miller, and R. L. Winslow, “Measuring and mapping cardiac fiber and laminar architecture using diffusion tensor MR imaging,” Ann. N. Y. Acad. Sci. 1047(1), 296–307 (2005).
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Bhargava, R.

Boote, C.

C. Boote, S. Dennis, Y. Huang, A. J. Quantock, and K. M. Meek, “Lamellar orientation in human cornea in relation to mechanical properties,” J. Struct. Biol. 149(1), 1–6 (2005).
[Crossref] [PubMed]

Bovendeerd, P. H. M.

C. C. Van Donkelaar, L. J. G. Kretzers, P. H. M. Bovendeerd, L. M. A. Lataster, K. Nicolay, J. D. Janssen, and M. R. Drost, “Diffusion tensor imaging in biomechanical studies of skeletal muscle function,” J. Anat. 194(1), 79–88 (1999).
[Crossref] [PubMed]

Brewer, M. A.

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by second harmonic generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

Brockbank, K.

K. Brockbank, W. MacLellan, J. Xie, S. Hamm-Alvarez, Z. Chen, and K. Schenke-Layland, “Quantitative second harmonic generation imaging of cartilage damage,” Cell Tissue Banking 9, 299–307 (2008).

Brodt, M. D.

M. J. Silva, M. D. Brodt, B. Wopenka, S. Thomopoulos, D. Williams, M. H. M. Wassen, M. Ko, N. Kusano, and R. A. Bank, “Decreased collagen organization and content are associated with reduced strength of demineralized and intact bone in the SAMP6 mouse,” J. Bone Miner. Res. 21(1), 78–88 (2006).
[Crossref] [PubMed]

Brown, C. P.

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Brown, D. J.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci. 52(12), 8818–8827 (2011).
[Crossref] [PubMed]

Brun, A.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

Burton, D. R.

B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Sys. Signal Process. 19(5), 1152–1161 (2005).
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Buttgereit, A.

C. S. Garbe, A. Buttgereit, S. Schurmann, and O. Friedrich, “Automated multiscale morphometry of muscle disease from second harmonic generation microscopy using tensor-based image processing,” IEEE Trans. Biomed. Eng. 59, 39–44 (2012).

Caetano-Lopes, J.

J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
[Crossref] [PubMed]

Campagnola, P. J.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by second harmonic generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[Crossref] [PubMed]

L. Loew, A. Millard, P. J. Campagnola, W. Mohler, and A. Lewis, “Second harmonic imaging microscopy,” Microsc. Microanal. 9, 170–171 (2003).

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

Canhão, H.

J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
[Crossref] [PubMed]

Canny, J.

J. Canny, “A computational approach to edge detection,” IEEE Trans. Pattern Anal. Mach. Intell. PAMI-8 (6), 679–698 (1986).
[Crossref] [PubMed]

Cascão, R.

J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
[Crossref] [PubMed]

Chai, D.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci. 52(12), 8818–8827 (2011).
[Crossref] [PubMed]

Chambers, A. F.

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer 46(7), 1181–1188 (2010).
[Crossref] [PubMed]

Chang, S. J.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
[Crossref] [PubMed]

Chen, H. C.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

Chen, M.

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
[Crossref] [PubMed]

Chen, T. H.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
[Crossref] [PubMed]

Chen, W. L.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
[Crossref] [PubMed]

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett. 94, 3 (2009).

Chen, X.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

Chen, Y. F.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

Chen, Z.

K. Brockbank, W. MacLellan, J. Xie, S. Hamm-Alvarez, Z. Chen, and K. Schenke-Layland, “Quantitative second harmonic generation imaging of cartilage damage,” Cell Tissue Banking 9, 299–307 (2008).

Chiang, C. S.

J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
[Crossref] [PubMed]

Chikama, T.

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 52(2), 911–915 (2011).
[Crossref] [PubMed]

Chikama, T.-i.

N. Morishige, N. Yamada, S. Teranishi, T.-i. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[Crossref] [PubMed]

Chiou, L. L.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

Chittenden, M.

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
[Crossref] [PubMed]

Chou, C. K.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
[Crossref] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett. 94, 3 (2009).

Cox, G.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref] [PubMed]

Crestani, B.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
[Crossref] [PubMed]

Da Silva, L. B.

P. Stoller, B.-M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7(2), 205–214 (2002).
[Crossref] [PubMed]

de Isla, N.

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol. 86(2), 302–310 (2010).
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de Lange Davies, C.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt. 13(5), 054050 (2008).
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Débarre, D.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
[Crossref] [PubMed]

Delmas, P. D.

S. Viguet-Carrin, P. Garnero, and P. D. Delmas, “The role of collagen in bone strength,” Osteoporosis Int. 17(3), 319–336 (2006).
[Crossref] [PubMed]

Dennis, S.

C. Boote, S. Dennis, Y. Huang, A. J. Quantock, and K. M. Meek, “Lamellar orientation in human cornea in relation to mechanical properties,” J. Struct. Biol. 149(1), 1–6 (2005).
[Crossref] [PubMed]

Dong, C. Y.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
[Crossref] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett. 94, 3 (2009).

Drost, M. R.

C. C. Van Donkelaar, L. J. G. Kretzers, P. H. M. Bovendeerd, L. M. A. Lataster, K. Nicolay, J. D. Janssen, and M. R. Drost, “Diffusion tensor imaging in biomechanical studies of skeletal muscle function,” J. Anat. 194(1), 79–88 (1999).
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G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
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D. F. Holmes, C. J. Gilpin, C. Baldock, U. Ziese, A. J. Koster, and K. E. Kadler, “Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organization,” Proc. Natl. Acad. Sci. U.S.A. 98(13), 7307–7312 (2001).
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B. Pourdeyhimi and H. S. Kim, “Measuring fiber orientation in nonwovens: the hough transform,” Text. Res. J. 72(9), 803–809 (2002).
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T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
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Korom, I.

Koster, A. J.

D. F. Holmes, C. J. Gilpin, C. Baldock, U. Ziese, A. J. Koster, and K. E. Kadler, “Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organization,” Proc. Natl. Acad. Sci. U.S.A. 98(13), 7307–7312 (2001).
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Kriling, S.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci. 52(12), 8818–8827 (2011).
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Kubicki, M.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
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M. J. Silva, M. D. Brodt, B. Wopenka, S. Thomopoulos, D. Williams, M. H. M. Wassen, M. Ko, N. Kusano, and R. A. Bank, “Decreased collagen organization and content are associated with reduced strength of demineralized and intact bone in the SAMP6 mouse,” J. Bone Miner. Res. 21(1), 78–88 (2006).
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O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by second harmonic generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
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B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Sys. Signal Process. 19(5), 1152–1161 (2005).
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C. C. Van Donkelaar, L. J. G. Kretzers, P. H. M. Bovendeerd, L. M. A. Lataster, K. Nicolay, J. D. Janssen, and M. R. Drost, “Diffusion tensor imaging in biomechanical studies of skeletal muscle function,” J. Anat. 194(1), 79–88 (1999).
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Lau, T.-Y.

Lee, H. S.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
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T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
[Crossref] [PubMed]

Légaré, F.

C. P. Brown, M. A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater. 5(1), 62–70 (2012).
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Lewis, A.

L. Loew, A. Millard, P. J. Campagnola, W. Mohler, and A. Lewis, “Second harmonic imaging microscopy,” Microsc. Microanal. 9, 170–171 (2003).

Li, T. H.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials 31(36), 9415–9421 (2010).
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Lin, S. J.

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett. 94, 3 (2009).

Lin, W. C.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. C. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002–036006 (2010).
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Lindgren, M.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt. 13(5), 054050 (2008).
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Lindmo, T.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt. 13(5), 054050 (2008).
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P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
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Loza-Alvarez, P.

Luedtke, D.

MacLellan, W.

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Supplementary Material (4)

» Media 1: AVI (228 KB)     
» Media 2: AVI (227 KB)     
» Media 3: AVI (273 KB)     
» Media 4: AVI (290 KB)     

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Figures (6)

Fig. 1
Fig. 1 The porcine tendon tissue was cut along the yellow dashed line at an arbitrary angle φ with respect to the longitudinal direction (red line).

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Fig. 2
Fig. 2 Cylindrical test objects (green) oriented in 3D space and their calculated preferred orientation (red line) oriented at (a) θ = 5.00°, φ = 50.00°, and (b) θ = 9.50°, φ = 1.50°. (c) A test object with spirally curved surfaces (gray) and their calculated preferred orientations within each voxel (red arrows).

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Fig. 3
Fig. 3 Illustrative example of analyzing a region of interest of (a) an image stack (142 μm x 142 μm x 2.24 μm). (b)The center portion (54 μm x 54 μm x 2.24 μm) is analyzed based on (c) fiber orientation, and (d) region labels. Based on the calculation, three histograms are generated to show the distributions of (e) the orientations with respect to z-axis (φ), (f) the lateral orientations along the xy-plane (θ), and (g) the numbers of different regions.

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Fig. 4
Fig. 4 (a) An image from a 102.4 μm x 102.4 μm x 16.2 μm image stack of porcine sclera tissue. (b) 3D model of the image stack. (c) 3D quiver plot shows fiber orientations of anisotropic ROI's (Media 1). Histograms showing (d) orientations of collagen fibers with respect to the z-axis, (e) orientations of collagen fibers on the xy-plane. (f) 3D plot of labeled regions shows location of anisotropic, isotropic, and dark regions (Media 2), and a histogram of the (g) numbers of labeled regions in the analyzed image.

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Fig. 5
Fig. 5 (a) An image from a 142 μm x 142 μm x 21.5 μm image stack of porcine tendon tissue. (b) 3D model of the image stack. (c) 3D quiver plot shows fiber orientations of anisotropic ROI's (Media 3). Histograms showing (d) orientations of collagen fibers with respect to the z-axis, (e) orientations of collagen fibers on the xy-plane. (f) 3D plot of labeled regions shows location of anisotropic, isotropic, and dark regions (Media 4), and a histogram of the (g) numbers of labeled regions in the analyzed image.

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Fig. 6
Fig. 6 (a), (b) Overlaid plots of the quiver plot of calculated orientation and the analyzed image of a porcine tendon tissue sample. Histograms showing (c), (d) orientations of collagen fibers on the xy-plane, (e) orientations of collagen fibers with respect to the z-axis, and (f, g) numbers of labeled regions in the analyzed image.

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