Abstract

Fourier transform-second-harmonic generation imaging is employed to obtain quantitative metrics of collagen fibers in biological tissues. In particular, the preferred orientation and maximum spatial frequency of collagen fibers for selected regions of interest in porcine trachea, ear, and cornea are determined. These metrics remain consistent when applied to collagen fibers in the ear, which can be expected from observation. Collagen fibers in the trachea are more random with large standard deviations in orientation, and large variations in maximum spatial frequency. In addition, these metrics are used to investigate structural changes through a 3D stack of the cornea. This technique can be used as a quantitative marker to assess the structure of collagen fibers that may change due to damage from disease or physical injury.

©2009 Optical Society of America

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2009 (3)

2008 (4)

H. M. Shieh, C. H. Chung, and C. L. Byrne, “Resolution enhancement in computerized tomographic imaging,” Appl. Opt.  47, 4116–4120 (2008).
[Crossref] [PubMed]

K. Schenke-Layland, “Non-invasive multiphoton imaging of extracellular matrix structures,” J. Biophotonics  1, 451–462 (2008).
[Crossref]

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. S. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt.  13, 11 (2008).
[Crossref]

D. Pandian, C. Ciulla, E. Haacke, J. Jiang, and M. Ayaz, “Complex threshold method for identifying pixels that contain predominantly noise in magnetic resonance images,” J. Magn. Reson. Imag.  28, 727–735, (2008).
[Crossref]

2007 (3)

2006 (1)

S. W. Teng, H. Y. Tan, J. L. Peng, H. H. Lin, K. H. Kim, W. Lo, Y. Sun, W. C. Lin, S. J. Lin, S. H. Jee, P. T. C. So, and C. Y. Dong, “Multiphoton autofluorescence and second-harmonic generation imaging of the ex vivo porcine eye,” Invest. Ophthalmol. Vis. Sci.  47, 1216–1224 (2006).
[Crossref] [PubMed]

2005 (3)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.  88, 1377–1386 (2005).
[Crossref]

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

M. Han, G. Giese, and J. F. Bille, “Second harmonic generation imaging of collagen fibrils in cornea and sclera,” Opt. Express  13, 5791–5797 (2005).
[Crossref] [PubMed]

2003 (2)

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.  141, 53–62 (2003).
[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, 1356–1360 (2003).
[Crossref] [PubMed]

2002 (1)

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J.  82, 3330–3342 (2002).
[Crossref] [PubMed]

2001 (1)

J. R. Mao and J. Bristow, “The Ehlers-Danlos syndrome: on beyond collagens,” J. Clin. Invest.  107, 1063–1069 (2001).
[Crossref] [PubMed]

2000 (1)

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, 663–669 (2000).
[PubMed]

1998 (1)

H. G. Adelmann, “Butterworth equations for homomorphic filtering of images,” Comput. Biol. Med.  28, 169–181 (1998).
[Crossref] [PubMed]

1997 (2)

B. M. Palmer and R. Bizios, “Quantitative characterization of vascular endothelial cell morphology and orientation using Fourier transform analysis,” J. Biomech. Eng.-Trans. ASME  119, 159–165 (1997).
[Crossref]

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

1995 (1)

H. Schomberg and J. Timmer, “The gridding method for image-reconstruction by fourier transformation,” IEEE Trans. Med. Imaging  14, 596–607 (1995).
[Crossref] [PubMed]

1991 (2)

D. R. Keene, L. Y. Sakai, and R. E. Burgeson, “Human bone contains type-III collagen, type-VI collagen, and fibrillin - type-III collagen is present on specific fibers that may mediate attachment of tendons, ligaments, and periosteum to calcified bone cortex,” J. Histochem. Cytochem.  39, 59–69 (1991).
[Crossref] [PubMed]

Y. Komai and T. Ushiki, “The 3-dimensional organization of collagen fibrils in the human cornea and sclera,” Invest. Ophthalmol. Vis. Sci.  32, 2244–2258 (1991).
[PubMed]

1977 (1)

L. Klein and J. Chandrarajan, “Collagen degradation in rat skin but not in intestine during rapid growth - effect on collagen type-1 and type-3 from skin,” Proc. Natl. Acad. Sci. USA  74, 1436–1439 (1977).
[Crossref] [PubMed]

Adams, D. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. S. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt.  13, 11 (2008).
[Crossref]

Adelmann, H. G.

H. G. Adelmann, “Butterworth equations for homomorphic filtering of images,” Comput. Biol. Med.  28, 169–181 (1998).
[Crossref] [PubMed]

Alberts, B.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2008).

Ayaz, M.

D. Pandian, C. Ciulla, E. Haacke, J. Jiang, and M. Ayaz, “Complex threshold method for identifying pixels that contain predominantly noise in magnetic resonance images,” J. Magn. Reson. Imag.  28, 727–735, (2008).
[Crossref]

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, 663–669 (2000).
[PubMed]

Bille, J. F.

Billinghurst, R. C.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Bizios, R.

B. M. Palmer and R. Bizios, “Quantitative characterization of vascular endothelial cell morphology and orientation using Fourier transform analysis,” J. Biomech. Eng.-Trans. ASME  119, 159–165 (1997).
[Crossref]

Bourne, R.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Bristow, J.

J. R. Mao and J. Bristow, “The Ehlers-Danlos syndrome: on beyond collagens,” J. Clin. Invest.  107, 1063–1069 (2001).
[Crossref] [PubMed]

Brown, D. J.

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Vis. Sci.  48, 1087–1094 (2007).
[Crossref] [PubMed]

Buhman, K. K.

Burgeson, R. E.

D. R. Keene, L. Y. Sakai, and R. E. Burgeson, “Human bone contains type-III collagen, type-VI collagen, and fibrillin - type-III collagen is present on specific fibers that may mediate attachment of tendons, ligaments, and periosteum to calcified bone cortex,” J. Histochem. Cytochem.  39, 59–69 (1991).
[Crossref] [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. Syst. Signal Proc.  19, 1152–1161 (2005).
[Crossref]

Byrne, C. L.

Campagnola, P. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. S. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt.  13, 11 (2008).
[Crossref]

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

Celliers, P. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J.  82, 3330–3342 (2002).
[Crossref] [PubMed]

Chan, Y. F.

Chandrarajan, J.

L. Klein and J. Chandrarajan, “Collagen degradation in rat skin but not in intestine during rapid growth - effect on collagen type-1 and type-3 from skin,” Proc. Natl. Acad. Sci. USA  74, 1436–1439 (1977).
[Crossref] [PubMed]

Chen, H. T.

Chen, J.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Chen, W. L.

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).

Cheng, J. X.

Chikama, T.

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Vis. Sci.  48, 1087–1094 (2007).
[Crossref] [PubMed]

Chou, C. K.

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).

Chung, C. H.

Cicchi, R.

Ciulla, C.

D. Pandian, C. Ciulla, E. Haacke, J. Jiang, and M. Ayaz, “Complex threshold method for identifying pixels that contain predominantly noise in magnetic resonance images,” J. Magn. Reson. Imag.  28, 727–735, (2008).
[Crossref]

Cox, G.

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

Dahlberg, L.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Dauser, D.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. S. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt.  13, 11 (2008).
[Crossref]

Diekmann, O.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Dong, C. Y.

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).

S. W. Teng, H. Y. Tan, J. L. Peng, H. H. Lin, K. H. Kim, W. Lo, Y. Sun, W. C. Lin, S. J. Lin, S. H. Jee, P. T. C. So, and C. Y. Dong, “Multiphoton autofluorescence and second-harmonic generation imaging of the ex vivo porcine eye,” Invest. Ophthalmol. Vis. Sci.  47, 1216–1224 (2006).
[Crossref] [PubMed]

Dougherty, R. P.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. S. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt.  13, 11 (2008).
[Crossref]

Emery, J. L.

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, 663–669 (2000).
[PubMed]

Fraser, I. K.

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

Fwu, P. T.

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).

Giese, G.

Goodman, J. W.

J. W. Goodman, Introduction to Fourier Optics (McGraw-Hill, 1996).

Gorrell, M. D.

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

Haacke, E.

D. Pandian, C. Ciulla, E. Haacke, J. Jiang, and M. Ayaz, “Complex threshold method for identifying pixels that contain predominantly noise in magnetic resonance images,” J. Magn. Reson. Imag.  28, 727–735, (2008).
[Crossref]

Hambor, J.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Han, M.

Haykin, S.

S. Haykin and B. Van Veen, Signals and Systems (Wiley, 2005).

Huang, H. J.

Ionescu, M.

R. C. Billinghurst, L. Dahlberg, M. Ionescu, A. Reiner, R. Bourne, C. Rorabeck, P. Mitchell, J. Hambor, O. Diekmann, H. Tschesche, J. Chen, H. VanWart, and A. R. Poole, “Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage,” J. Clin. Invest.  99, 1534–1545 (1997).
[Crossref] [PubMed]

Jee, S. H.

S. W. Teng, H. Y. Tan, J. L. Peng, H. H. Lin, K. H. Kim, W. Lo, Y. Sun, W. C. Lin, S. J. Lin, S. H. Jee, P. T. C. So, and C. Y. Dong, “Multiphoton autofluorescence and second-harmonic generation imaging of the ex vivo porcine eye,” Invest. Ophthalmol. Vis. Sci.  47, 1216–1224 (2006).
[Crossref] [PubMed]

Jester, J. V.

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Appl. Opt. (1)

Appl. Phys. Lett. (1)

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).

Biophys. J. (2)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.  88, 1377–1386 (2005).
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P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J.  82, 3330–3342 (2002).
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Circ. Res. (1)

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, 663–669 (2000).
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IEEE Trans. Med. Imaging (1)

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Invest. Ophthalmol. Vis. Sci. (3)

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Vis. Sci.  48, 1087–1094 (2007).
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Supplementary Material (2)

» Media 1: MOV (3035 KB)     
» Media 2: MOV (2930 KB)     

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Figures (6)

Fig. 1.
Fig. 1. Experimental setup of the SHG microscope. Details are provided in text.

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Fig. 2.
Fig. 2. SHG intensity images of porcine tissue specimens from the (a) trachea and (b) ear cartilage, and (c) cornea for an incident wavelength of 780 nm and a second-harmonic wavelength of 390 nm; d) 3D reconstructed view of porcine ear cartilage (Media 1).

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Fig. 3.
Fig. 3. SHG image of porcine (a) ear and (b) trachea cartilage with selected regions of interest (colored and labeled boxes), and (c) estimated preferred orientation for each corresponding region as observed in Fourier space.

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Fig. 4.
Fig. 4. SHG image of porcine a) ear and b) trachea cartilage. The region of interest for estimating Fhigh is a rectangular box of height 2.87 µm. A histogram of the values of Fhigh from all the regions of interest for the c) ear and d) trachea.

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Fig. 5.
Fig. 5. Regions of interest for estimating the highest spatial frequencies in the cornea. The image shown is cropped to 238×163 µm.

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Fig. 6.
Fig. 6. (a) A movie showing the variations of the two quantitative markers, preferred orientation and F high versus depth (Media 2). (b–d) Plot of the estimated preferred orientation, and Fhigh as a function of depth in an SHG image stack of the cornea for regions 1–3 from Fig. 6. Note that our axial resolution is on the order of the wavelength (~700 nm), while we mechanically step through the depth of our sample in 163-nm increments using a precision motor control of the objective focus. Oversampling helps mitigate the effect of Poisson noise by improving the visibility due to more photons per pixel, and improve the precision to which we can locate image features [26]. Thus, our sensitivity to changes in the features is improved.

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