Abstract

Second Harmonic Generation (SHG) microscopy offers the opportunity to image collagen of type I without staining. We recently showed that a simple scoring method, based on SHG images of histological human liver biopsies, correlates well with the Metavir assessment of fibrosis level (Gailhouste et al., J. Hepatol., 2010). In this article, we present a detailed study of this new scoring method with two different objective lenses. By using measurements of the objectives point spread functions and of the photomultiplier gain, and a simple model of the SHG intensity, we show that our scoring method, applied to human liver biopsies, is robust to the objective’s numerical aperture (NA) for low NA, the choice of the reference sample and laser power, and the spatial sampling rate. The simplicity and robustness of our collagen scoring method may open new opportunities in the quantification of collagen content in different organs, which is of main importance in providing diagnostic information and evaluation of therapeutic efficiency.

© 2010 OSA

Full Article  |  PDF Article
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References

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2010 (3)

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
[Crossref]

P. Bedossa, “Harmony in liver fibrosis,” J. of Hepatology 52, 313–314 (2010).
[Crossref]

H. Bao, A. Boussioutas, R. Jeremy, S. Russell, and M. Gu, “Second harmonic generation imaging via nonlinear endomicroscopy,” Opt. Express 18, 1255–1260 (2010).
[Crossref] [PubMed]

2009 (5)

C. Odin, C. Heichette, D. Chretien, and Y. Le Grand, “Second harmonic microscopy of axonemes,” Opt. Express 17, 9235–9240 (2009).
[Crossref] [PubMed]

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenousSHG sources in mammalian tissue, based ontheir polarization response,” Opt. Express 17, 10168–10176 (2009).
[Crossref] [PubMed]

S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. Planas, and P. Loza-Alvarez, “Estimation of the effective orientation of the SHG source in primary cortical neurons,” Opt. Express 17, 14418–14425 (2009).
[Crossref] [PubMed]

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
[Crossref] [PubMed]

S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
[Crossref] [PubMed]

2008 (2)

C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microscopy 229, 32–38 (2008).
[Crossref]

C. Odin, T. Guilbert, A. Alkilani, O. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express 16, 16151–16165 (2008).
[Crossref] [PubMed]

2007 (3)

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
[Crossref]

M. Strupler, A. Pena, M. Hernest, P. Tharaux, J. Martin, E. Beaurepaire, and M. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express 15, 4054–4065 (2007).
[Crossref] [PubMed]

H. A. Saleh and A. H. Abu-Rashed, “Liver Biopsy Remains the Gold Standard for Evaluation of Chronic Hepatitis and Fibrosis,” J. Gastrointestin. Liver Dis. 16, 425–426 (2007).

2006 (1)

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys J. 90, 693–703 (2006).
[Crossref]

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]

R. Bataller and D. A. Brenner, “Liver fibrosis,” J. Clin. Invest. 115, 209–218 (2005).
[PubMed]

M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
[Crossref]

2004 (3)

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
[Crossref]

N. H. Afdhal and D. Nunes, “Evaluation of liver fibrosis: a concise review,” Am. J. Gastroenterol. 99, 1160–1174 (2004).
[Crossref] [PubMed]

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[Crossref] [PubMed]

2003 (6)

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

W.R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic : multiphoton microscopy in the biosciences,” Nat.Biotechn 21,1369–1377 (2003).
[Crossref]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
[Crossref] [PubMed]

G. L. Davis, J. E. Albright, S. F. Cook, and D. M. Rosenberg, “Projecting future complications of chronic hepatitis C in the United States,” Liver Transpl. 9, 331–338 (2003).
[Crossref] [PubMed]

P. Bedossa, D. Dargre, and V. Paradis, “Sampling variability of liver fibrosis in chronic hepatitis C,” J. Hepatol. 38, 1356–1358 (2003).

S. L. Friedman, “Liver fibrosis - from bench to bedside,” J. Hepatol. 38, 38–53 (2003).
[Crossref]

2002 (1)

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 20, 11014–11019 (2002).
[Crossref]

2001 (1)

J. Mertz and L. Moreaux, “Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers,” Optics Com. 196, 325–330 (2001).
[Crossref]

2000 (3)

L. I-K Lin, “A note on the concordance correlation coefficient,” Biometrics 56, 324–325 (2000).

K. König (2000), “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104.
[Crossref] [PubMed]

M. Masseroli, T. Caballero, F. OValle, R. M. Del Moral, A. Perez-Milena, and R. G. Del Moral, “Automatic quantification of liver fibrosis design and validation of a new image analysis method: comparison with semi-quantitative indexes of fibrosis,” J. Hepatol. 32, 453–464 (2000).
[Crossref] [PubMed]

1999 (1)

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
[Crossref] [PubMed]

1997 (2)

F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
[Crossref] [PubMed]

N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
[Crossref]

1995 (2)

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
[Crossref] [PubMed]

The French METAVIR Cooperative Study Group, “Intraobserver, interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C,” J. Hepatol. 20, 15–20 (1995).

1991 (1)

P. J. Scheuer, “Classification of of chronic viral hepatitis : a need for reassessment,” J. Hepatol. 13, 372–374 (1991).
[Crossref] [PubMed]

1989 (1)

L. I-K Lin, “A concordance correlation coefficient to evaluate reproducibility,” Biometrics 45, 255–268 (1989).
[Crossref]

1979 (1)

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70, 1637–1643(1979).
[Crossref]

Abu-Rashed, A. H.

H. A. Saleh and A. H. Abu-Rashed, “Liver Biopsy Remains the Gold Standard for Evaluation of Chronic Hepatitis and Fibrosis,” J. Gastrointestin. Liver Dis. 16, 425–426 (2007).

Afdhal, N. H.

N. H. Afdhal and D. Nunes, “Evaluation of liver fibrosis: a concise review,” Am. J. Gastroenterol. 99, 1160–1174 (2004).
[Crossref] [PubMed]

N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
[Crossref]

Albright, J. E.

G. L. Davis, J. E. Albright, S. F. Cook, and D. M. Rosenberg, “Projecting future complications of chronic hepatitis C in the United States,” Liver Transpl. 9, 331–338 (2003).
[Crossref] [PubMed]

Alkilani, A.

Amat-Roldan, I.

Artigas, D.

Aub, C.

F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
[Crossref] [PubMed]

Aube, C.

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
[Crossref] [PubMed]

Baffet, G.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
[Crossref]

C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microscopy 229, 32–38 (2008).
[Crossref]

Banson, F. L.

M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
[Crossref]

Bao, H.

Baptista, A.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
[Crossref] [PubMed]

Bataller, R.

R. Bataller and D. A. Brenner, “Liver fibrosis,” J. Clin. Invest. 115, 209–218 (2005).
[PubMed]

Beaurepaire, E.

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
[Crossref]

M. Strupler, A. Pena, M. Hernest, P. Tharaux, J. Martin, E. Beaurepaire, and M. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express 15, 4054–4065 (2007).
[Crossref] [PubMed]

Bedossa, P.

P. Bedossa, “Harmony in liver fibrosis,” J. of Hepatology 52, 313–314 (2010).
[Crossref]

P. Bedossa, D. Dargre, and V. Paradis, “Sampling variability of liver fibrosis in chronic hepatitis C,” J. Hepatol. 38, 1356–1358 (2003).

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
[Crossref] [PubMed]

F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
[Crossref] [PubMed]

Bessard, A.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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Bianchi, L.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
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M. Masseroli, T. Caballero, F. OValle, R. M. Del Moral, A. Perez-Milena, and R. G. Del Moral, “Automatic quantification of liver fibrosis design and validation of a new image analysis method: comparison with semi-quantitative indexes of fibrosis,” J. Hepatol. 32, 453–464 (2000).
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Callea, F.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
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Cals, P.

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
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F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
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S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys J. 90, 693–703 (2006).
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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. Biotechn. 21, 1356–1360 (2003).
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C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
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Casola, G.

S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
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Chan, H. L.-Y.

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
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Chang, S.

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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Chen, S. Y.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
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Chen, Y. C.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
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Cheng, C. L.

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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Chern, G. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
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Chia, S. M.

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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Chim, A. M.-L.

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
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Chretien, D.

Christie, R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
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Chu, S. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
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Chung, C. Y.

M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
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Cohen, S. B.

N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
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G. L. Davis, J. E. Albright, S. F. Cook, and D. M. Rosenberg, “Projecting future complications of chronic hepatitis C in the United States,” Liver Transpl. 9, 331–338 (2003).
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Crestani, B.

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
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Dargre, D.

P. Bedossa, D. Dargre, and V. Paradis, “Sampling variability of liver fibrosis in chronic hepatitis C,” J. Hepatol. 38, 1356–1358 (2003).

Davis, G. L.

G. L. Davis, J. E. Albright, S. F. Cook, and D. M. Rosenberg, “Projecting future complications of chronic hepatitis C in the United States,” Liver Transpl. 9, 331–338 (2003).
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Dbarre, D.

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
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De Groote, J.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
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Del Moral, R. G.

M. Masseroli, T. Caballero, F. OValle, R. M. Del Moral, A. Perez-Milena, and R. G. Del Moral, “Automatic quantification of liver fibrosis design and validation of a new image analysis method: comparison with semi-quantitative indexes of fibrosis,” J. Hepatol. 32, 453–464 (2000).
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Del Moral, R. M.

M. Masseroli, T. Caballero, F. OValle, R. M. Del Moral, A. Perez-Milena, and R. G. Del Moral, “Automatic quantification of liver fibrosis design and validation of a new image analysis method: comparison with semi-quantitative indexes of fibrosis,” J. Hepatol. 32, 453–464 (2000).
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Denk, H.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
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Desmet, V.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
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Dsille, Y.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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Ezan, F.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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Fabre, A.

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
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Faria, S. C.

S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
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Fleszler, F.

M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
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Freund, I.

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70, 1637–1643(1979).
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M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
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Friedenberg, M. A.

M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
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S. L. Friedman, “Liver fibrosis - from bench to bedside,” J. Hepatol. 38, 38–53 (2003).
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L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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Gailhouste, L.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
[Crossref]

C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microscopy 229, 32–38 (2008).
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Gallois, Y.

F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
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Ganesan, K.

S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
[Crossref] [PubMed]

Go, M. Y.-Y.

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
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Gu, M.

Gudat, F.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
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Guilbert, T.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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C. Odin, T. Guilbert, A. Alkilani, O. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express 16, 16151–16165 (2008).
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Guyader, D.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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Heichette, C.

Hernest, M.

Hui, A. Y.

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
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Hyman, B. T.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
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I-K Lin, L.

L. I-K Lin, “A note on the concordance correlation coefficient,” Biometrics 56, 324–325 (2000).

L. I-K Lin, “A concordance correlation coefficient to evaluate reproducibility,” Biometrics 45, 255–268 (1989).
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Ishak, K.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
[Crossref] [PubMed]

Jeremy, R.

Kang, C. H.

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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Keaveny, A. P.

N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
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K. König (2000), “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104.
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Kono, Y.

S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
[Crossref] [PubMed]

Koralin, N.

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
[Crossref] [PubMed]

Korb, G.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
[Crossref] [PubMed]

Le Grand, Y.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
[Crossref]

C. Odin, C. Heichette, D. Chretien, and Y. Le Grand, “Second harmonic microscopy of axonemes,” Opt. Express 17, 9235–9240 (2009).
[Crossref] [PubMed]

C. Odin, T. Guilbert, A. Alkilani, O. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express 16, 16151–16165 (2008).
[Crossref] [PubMed]

C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microscopy 229, 32–38 (2008).
[Crossref]

Leung, N. W.-Y.

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
[Crossref]

Li Wei, C.

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
[Crossref] [PubMed]

Liew, C.-T.

A. Y. Hui, C.-T. Liew, M. Y.-Y. Go, A. M.-L. Chim, H. L.-Y. Chan, N. W.-Y. Leung, and J. J.-Y. Sung, “Quantitative assessment of fibrosis in liver biopsies from patients with chronic hepatitis B,” Liver Intl. 24, 611–618 (2004).
[Crossref]

Lin, B. L.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[Crossref] [PubMed]

Loew, L. M.

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

Loisel, D.

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
[Crossref] [PubMed]

Loza-Alvarez, P.

MacSween, R. N.

K. Ishak, A. Baptista, L. Bianchi, F. Callea, J. De Groote, F. Gudat, H. Denk, V. Desmet, G. Korb, and R. N. MacSween, “Histological grading and staging of chronic hepatitis,” J. Hepatol. 22, 696–699 (1995).
[Crossref] [PubMed]

Maga, M. Y.

C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
[Crossref] [PubMed]

F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
[Crossref] [PubMed]

Maldonado, N.

N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
[Crossref]

Marchal-Somme, J.

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
[Crossref]

Martin, J.

Martin, J.-L.

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S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys J. 90, 693–703 (2006).
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N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
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N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
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F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
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M. Masseroli, T. Caballero, F. OValle, R. M. Del Moral, A. Perez-Milena, and R. G. Del Moral, “Automatic quantification of liver fibrosis design and validation of a new image analysis method: comparison with semi-quantitative indexes of fibrosis,” J. Hepatol. 32, 453–464 (2000).
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Peterson, M.

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Plotnikov, S. V.

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C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microscopy 229, 32–38 (2008).
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C. Aube, F. Oberti, N. Koralin, M.-A. Namour, D. Loisel, M. C. Rousselet, P. Bedossa, H. Rifflet, M. Y. Maga, C. Penneau, C. Caron, and P. Cals, “Ultrasonographic diagnosis of hepatic fibrosis or cirrhosis,” J. Hepatol. 30, 472–478 (1999).
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F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
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S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
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Schanne-Klein, M.-C.

A.-M. Pena, A. Fabre, D. Dbarre, 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, 162–170 (2007).
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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N. H. Afdhal, A. P. Keaveny, S. B. Cohen, D. P. Nunes, N. Maldonado, M. O’Brien, and P. J. Stone, “Urinary assays for desmosine and hydroxylysylpyridinoline in the detection of cirrhosis,” J. Hepatol. 27, 993–1002 (1997).
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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Theret, N.

L. Gailhouste, Y. Le Grand, C. Odin, D. Guyader, B. Turlin, F. Ezan, Y. Dsille, T. Guilbert, A. Bessard, C. Frmin, N. Theret, and G. Baffet, “Fibrillar Collagen Scoring by Second Harmonic Microscopy as a New Tool in the Assessment of Liver Fibrosis,” J. of Hepatology 52, 398–406 (2010).
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M. A. Friedenberg, L. Miller, C. Y. Chung, F. Fleszler, F. L. Banson, R. Thomas, K. P. Swartz, and F. K. Friedenberg, “Simplified method of hepatic fibrosis quantification: design of a new morphometric analysis application,” Liver Intl. 25, 1156–1161 (2005).
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A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 20, 11014–11019 (2002).
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Tsai, T. H.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C.K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
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F. Oberti, E. Valsesia, C. Pilette, M. C. Rousselet, P. Bedossa, C. Aub, Y. Gallois, H. Rifflet, M. Y. Maga, D. Penneau-Fontbonne, and P. Cals, “Noninvasive diagnosis of hepatic fibrosis or cirrhosis,” Gastroenterology 113, 1609–1616 (1997).
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S. C. Faria, K. Ganesan, I. Mwangi, M. Shiehmorteza, B. Viamonte, S. Mazhar, M. Peterson, Y. Kono, C. Santillan, G. Casola, and C. B. Sirlin, “MR Imaging of Liver Fibrosis: Current State of the Art,” Radiographics 29, 1615–1635 (2009).
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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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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
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W.R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic : multiphoton microscopy in the biosciences,” Nat.Biotechn 21,1369–1377 (2003).
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Wee, A.

D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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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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W.R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic : multiphoton microscopy in the biosciences,” Nat.Biotechn 21,1369–1377 (2003).
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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 20, 11014–11019 (2002).
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D. C. S. Tai, N. Tan, S. Xu, C. H. Kang, S. M. Chia, C. L. Cheng, A. Wee, C. Li Wei, A. M. Raja, G. Xiao, S. Chang, J. C. Rajapakse, P. T. C. So, H-H. Tang, C. Shing Chen, and H. Yu, “Fibro-C-Index: comprehensive, morphology-based quantification of liver fibrosis using second harmonic generation and two-photon microscopy,” J. Biomed. Opt. 14(4), 044013-1-10 (2009),
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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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Opt. Express (6)

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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. USA. 100, 7075–7080 (2003).
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X. Han, R. M. Burke, M. L. Zettel, P. Tang, and E. B. Brown, “Second harmonic properties of tumor collagen: determining the structural relationship between reactive stroma and healthy stroma,” Opt. Express16, 1846–1859 (2008). http://www.opticsinfobase.org/abstract.cfm?URI=oe-16-3-1846
[Crossref] [PubMed]

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Figures (7)

Fig. 1
Fig. 1

(Color inline) SHG images acquired with a 4x-objective of a F1 biopsies. (a) PMT gain g1 was set to obtain an image with almost no saturated pixels (3.5×3.5mm2) ; (b) Same image as in a), but multiplied by 4.7 and shown with a scale limited to the 12-bits range [0 4095];(c) Experimental image with a PMT gain set to 4.7×g1 ;(d) Comparison of image intensity histograms for three PMT gains g1, 2.15 × g1, and 4.7 × g1.

Fig. 2
Fig. 2

(Color inline) (a) Schematic representation of the PSF2 of the objectives (1/e contour lines) as compared to the sample thickness ; (b) Experimental z-profiles of the PSF2 of the 4x(•) and 10x (♦) objectives. Intensity z-profile (▪) of a 50μm thick sample reconstructed from slices acquired with the 10x objective. Continuous lines are fits as explained in the text. (c) Typical images of a z-stack recorded with the 10x objective (scale bar=400μm).

Fig. 3
Fig. 3

a) Example of non fibrotic ECM on a F4 sample, delineated by white boxes ; b) Boxplot of mean intensities of different non-fibrotic ECM ROIs selected from different Metavir-graded samples. The PMT gain is the same for all samples, and was set to obtain r =4%(<ISHG>= 164, horizontal line) on a F0 sample with the 4x objective.

Fig. 4
Fig. 4

Images of non-fibrotic ECM ROIs for different PMT gains corresponding to r =2,3,4,5% : (a) for the 4x objective lens ; (b) 10x objective lens. c) Corresponding PMT gains ; (d) Correlation between the PMT gains of the 10x and 4x objective lens.

Fig. 5
Fig. 5

SHG images of histological serial sections of a surgical biopsie of a F4 patient, with thicknesses : (a)5μm,(b) 15μm,(c) 50μm. d) Correlation between the PMT gain and the inverse of the geometrical factor f (Eq. (3)).

Fig. 6
Fig. 6

Example of 4x (first line) and 10x (second line) images when r=4%, for the same field of view 3525×3525μm2 (4x : 512×512 pixels; 10x : 1300×1300 pixels).(a,b,c,d) F1 Metavir grade. (e,f,g,h) F4 Metavir grade. (a,b,e,f) 4x-obj. (c,d,g,h) 10x-obj

Fig. 7
Fig. 7

Comparison of the scores obtained at r =2,3,5% with the score at r =4% for :(a) the 4x lens ; (b) the 10x lens. (c) Comparison of 4x and 10x scores.

Tables (3)

Tables Icon

Table 1 (1) : Estimation of the lateral and axial 1/e radii of the diffraction-limited PSF2 of the two objective lenses used in the experiments, assuming a Gaussian shape, from ref. [20]. (2) Measured value. Excitation wavelength=810nm; FOV=Field of View of our microscope.

Tables Icon

Table 2 Data of the experimental set up.(1) : Average laser power at the focal plane measured with a calibrated power-meter OPHIR PD300; (2) PMT supplied voltage used for experiments performed with 4% SHG mean intensity from the basal collagen of the ECM.

Tables Icon

Table 3 Slope from a least-square linear fit Y = a × X and Pearson’s linear correlation coefficient R between different scores, and the sample concordance correlation coefficient ρL proposed by Lin (1989) [38].

Equations (6)

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S ¯ ( t ) = 1 N 2 i , j = 1 N H ( I i j t )
I SHG g PMT T 2 I o 2 d 3 r P ( r ) C ¯
f Ω N A 2 e / 2 e / 2 exp ( z 2 / w z 2 ) d z N A 2 w z erf ( e 2 w z ) N A 4 erf ( e 2 w z )
I S H G g P M T T 2 f C ¯
I S H G = r I S a t C ¯ C r e f
g P M T 10 x = ( T 4 x T 10 x ) 2 f 4 x g P M T 4 x

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