Abstract

Polarimetric second-harmonic generation (P-SHG) microscopy is used to characterize the composition and polarity of collagen fibers in various regions of human cardiac tissue. The boundary between the cardiac conduction system and myocardium is shown to possess a distinct composition of collagen compared to other regions in the heart. Moreover, collagen fibers in this region are macroscopically organized in a unipolar arrangement, which may consequently aid in effective propagation of the electrical signal through the cardiac conduction system.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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  1. F. Martini, R. B. Tallitsch, and J. L. Nath, Human Anatomy (Pearson, 2017).
  2. D. A. D. Parry and A. S. Craig, “Collagen structure and stability,” Biopolymers 16(5), 1015–1031 (1977).
    [Crossref]
  3. G. N. Ramachandran and G. Kartha, “Structure of Collagen,” Nature 176(4482), 593–595 (1955).
    [Crossref]
  4. J. Venius, E. Zurauskas, and R. Rotomskis, “High Resolution Imaging of the Human Cardiac Conduction System Using Reflectance Confocal Microscopy,” Tohoku J. Exp. Med. 229(1), 67–73 (2013).
    [Crossref]
  5. J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
    [Crossref]
  6. I. Freund and M. Deutsch, “Macroscopic polarity of connective tissue is due to discrete polar structures,” Biopolymers 25(4), 601–606 (1986).
    [Crossref]
  7. A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
    [Crossref]
  8. A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
    [Crossref]
  9. A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
    [Crossref]
  10. A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
    [Crossref]
  11. D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
    [Crossref]
  12. E. Fukada and I. Yasuda, “On the piezoelectric effect of bone,” J. Phys. Soc. Jpn. 12(10), 1158–1162 (1957).
    [Crossref]
  13. E. Fukada and I. Yasuda, “Piezoelectric effects in collagen,” Jpn. J. Appl. Phys. 3(2), 117–121 (1964).
    [Crossref]
  14. M. H. Shamos and L. S. Lavine, “Piezoelectricity as a fundamental property of biological tissues,” Nature 213(5073), 267–269 (1967).
    [Crossref]
  15. M. Minary-Jolandan and M. Yu, “Nanoscale characterization of isolated individual type I collagen fibrils: Polarization and piezoelectricity,” Nanotechnology 20(8), 085706 (2009).
    [Crossref]
  16. C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
    [Crossref]
  17. C. A. Dailey, B. J. Burke, and G. J. Simpson, “The general failure of Kleinman symmetry in practical nonlinear optical applications,” Chem. Phys. Lett. 390(1-3), 8–13 (2004).
    [Crossref]
  18. T. F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM J. Optim. 6(2), 418–445 (1996).
    [Crossref]
  19. A. Major, R. Cisek, and V. Barzda, “Femtosecond Yb:KGd(WO4)2 laser oscillator pumped by a high power fiber-coupled diode laser module,” Opt. Express 14(25), 12163–12168 (2006).
    [Crossref]
  20. 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(2), 693–703 (2006).
    [Crossref]
  21. 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]
  22. N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst., Man, Cybern. 9(1), 62–66 (1979).
    [Crossref]

2019 (2)

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

2016 (2)

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
[Crossref]

2014 (1)

2013 (1)

J. Venius, E. Zurauskas, and R. Rotomskis, “High Resolution Imaging of the Human Cardiac Conduction System Using Reflectance Confocal Microscopy,” Tohoku J. Exp. Med. 229(1), 67–73 (2013).
[Crossref]

2012 (2)

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

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]

2011 (1)

J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
[Crossref]

2009 (1)

M. Minary-Jolandan and M. Yu, “Nanoscale characterization of isolated individual type I collagen fibrils: Polarization and piezoelectricity,” Nanotechnology 20(8), 085706 (2009).
[Crossref]

2006 (2)

A. Major, R. Cisek, and V. Barzda, “Femtosecond Yb:KGd(WO4)2 laser oscillator pumped by a high power fiber-coupled diode laser module,” Opt. Express 14(25), 12163–12168 (2006).
[Crossref]

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(2), 693–703 (2006).
[Crossref]

2004 (1)

C. A. Dailey, B. J. Burke, and G. J. Simpson, “The general failure of Kleinman symmetry in practical nonlinear optical applications,” Chem. Phys. Lett. 390(1-3), 8–13 (2004).
[Crossref]

1996 (1)

T. F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM J. Optim. 6(2), 418–445 (1996).
[Crossref]

1986 (1)

I. Freund and M. Deutsch, “Macroscopic polarity of connective tissue is due to discrete polar structures,” Biopolymers 25(4), 601–606 (1986).
[Crossref]

1979 (1)

N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst., Man, Cybern. 9(1), 62–66 (1979).
[Crossref]

1977 (1)

D. A. D. Parry and A. S. Craig, “Collagen structure and stability,” Biopolymers 16(5), 1015–1031 (1977).
[Crossref]

1967 (1)

M. H. Shamos and L. S. Lavine, “Piezoelectricity as a fundamental property of biological tissues,” Nature 213(5073), 267–269 (1967).
[Crossref]

1964 (1)

E. Fukada and I. Yasuda, “Piezoelectric effects in collagen,” Jpn. J. Appl. Phys. 3(2), 117–121 (1964).
[Crossref]

1957 (1)

E. Fukada and I. Yasuda, “On the piezoelectric effect of bone,” J. Phys. Soc. Jpn. 12(10), 1158–1162 (1957).
[Crossref]

1955 (1)

G. N. Ramachandran and G. Kartha, “Structure of Collagen,” Nature 176(4482), 593–595 (1955).
[Crossref]

Akens, M. K.

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Asa, S. L.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Bagdonas, S.

J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
[Crossref]

Barzda, V.

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
[Crossref]

A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
[Crossref]

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

A. Major, R. Cisek, and V. Barzda, “Femtosecond Yb:KGd(WO4)2 laser oscillator pumped by a high power fiber-coupled diode laser module,” Opt. Express 14(25), 12163–12168 (2006).
[Crossref]

Boyd, J. L.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Brown, C. P.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Burke, B. J.

C. A. Dailey, B. J. Burke, and G. J. Simpson, “The general failure of Kleinman symmetry in practical nonlinear optical applications,” Chem. Phys. Lett. 390(1-3), 8–13 (2004).
[Crossref]

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]

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(2), 693–703 (2006).
[Crossref]

Carr, A. J.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

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]

Cisek, R.

Coleman, T. F.

T. F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM J. Optim. 6(2), 418–445 (1996).
[Crossref]

Couture, C.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Craig, A. S.

D. A. D. Parry and A. S. Craig, “Collagen structure and stability,” Biopolymers 16(5), 1015–1031 (1977).
[Crossref]

Dailey, C. A.

C. A. Dailey, B. J. Burke, and G. J. Simpson, “The general failure of Kleinman symmetry in practical nonlinear optical applications,” Chem. Phys. Lett. 390(1-3), 8–13 (2004).
[Crossref]

Deutsch, M.

I. Freund and M. Deutsch, “Macroscopic polarity of connective tissue is due to discrete polar structures,” Biopolymers 25(4), 601–606 (1986).
[Crossref]

Done, S. J.

Freund, I.

I. Freund and M. Deutsch, “Macroscopic polarity of connective tissue is due to discrete polar structures,” Biopolymers 25(4), 601–606 (1986).
[Crossref]

Fukada, E.

E. Fukada and I. Yasuda, “Piezoelectric effects in collagen,” Jpn. J. Appl. Phys. 3(2), 117–121 (1964).
[Crossref]

E. Fukada and I. Yasuda, “On the piezoelectric effect of bone,” J. Phys. Soc. Jpn. 12(10), 1158–1162 (1957).
[Crossref]

Golaraei, A.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
[Crossref]

A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
[Crossref]

Hulley, P. A.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Joseph, A.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Kartha, G.

G. N. Ramachandran and G. Kartha, “Structure of Collagen,” Nature 176(4482), 593–595 (1955).
[Crossref]

Kontenis, L.

Krouglov, S.

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
[Crossref]

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Lavine, L. S.

M. H. Shamos and L. S. Lavine, “Piezoelectricity as a fundamental property of biological tissues,” Nature 213(5073), 267–269 (1967).
[Crossref]

Légaré, F.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Li, Y.

T. F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM J. Optim. 6(2), 418–445 (1996).
[Crossref]

Major, A.

Martini, F.

F. Martini, R. B. Tallitsch, and J. L. Nath, Human Anatomy (Pearson, 2017).

Millard, A. C.

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(2), 693–703 (2006).
[Crossref]

Minary-Jolandan, M.

M. Minary-Jolandan and M. Yu, “Nanoscale characterization of isolated individual type I collagen fibrils: Polarization and piezoelectricity,” Nanotechnology 20(8), 085706 (2009).
[Crossref]

Mirsanaye, K.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

Mohler, W. A.

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(2), 693–703 (2006).
[Crossref]

Nadiarynkh, O.

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]

Nath, J. L.

F. Martini, R. B. Tallitsch, and J. L. Nath, Human Anatomy (Pearson, 2017).

Navab, R.

Niu, C.

Otsu, N.

N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst., Man, Cybern. 9(1), 62–66 (1979).
[Crossref]

Palmer, A. J.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Parry, D. A. D.

D. A. D. Parry and A. S. Craig, “Collagen structure and stability,” Biopolymers 16(5), 1015–1031 (1977).
[Crossref]

Phillips, M.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Plotnikov, S.

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]

Plotnikov, S. V.

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(2), 693–703 (2006).
[Crossref]

Price, A. J.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Ramachandran, G. N.

G. N. Ramachandran and G. Kartha, “Structure of Collagen,” Nature 176(4482), 593–595 (1955).
[Crossref]

Rivard, M.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Ro, Y.

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

Rotomskis, R.

J. Venius, E. Zurauskas, and R. Rotomskis, “High Resolution Imaging of the Human Cardiac Conduction System Using Reflectance Confocal Microscopy,” Tohoku J. Exp. Med. 229(1), 67–73 (2013).
[Crossref]

J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
[Crossref]

Ruediger, A.

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Sakashita, S.

Sandkuijl, D.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Shamos, M. H.

M. H. Shamos and L. S. Lavine, “Piezoelectricity as a fundamental property of biological tissues,” Nature 213(5073), 267–269 (1967).
[Crossref]

Simpson, G. J.

C. A. Dailey, B. J. Burke, and G. J. Simpson, “The general failure of Kleinman symmetry in practical nonlinear optical applications,” Chem. Phys. Lett. 390(1-3), 8–13 (2004).
[Crossref]

Tallitsch, R. B.

F. Martini, R. B. Tallitsch, and J. L. Nath, Human Anatomy (Pearson, 2017).

Tokarz, D.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
[Crossref]

Tsao, M.

Tuer, A. E.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

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J. Venius, E. Zurauskas, and R. Rotomskis, “High Resolution Imaging of the Human Cardiac Conduction System Using Reflectance Confocal Microscopy,” Tohoku J. Exp. Med. 229(1), 67–73 (2013).
[Crossref]

J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
[Crossref]

Whyne, C. M.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Wilson, B. C.

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
[Crossref]

A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
[Crossref]

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
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E. Fukada and I. Yasuda, “Piezoelectric effects in collagen,” Jpn. J. Appl. Phys. 3(2), 117–121 (1964).
[Crossref]

E. Fukada and I. Yasuda, “On the piezoelectric effect of bone,” J. Phys. Soc. Jpn. 12(10), 1158–1162 (1957).
[Crossref]

Yasufuku, K.

Yu, M.

M. Minary-Jolandan and M. Yu, “Nanoscale characterization of isolated individual type I collagen fibrils: Polarization and piezoelectricity,” Nanotechnology 20(8), 085706 (2009).
[Crossref]

Zurauskas, E.

J. Venius, E. Zurauskas, and R. Rotomskis, “High Resolution Imaging of the Human Cardiac Conduction System Using Reflectance Confocal Microscopy,” Tohoku J. Exp. Med. 229(1), 67–73 (2013).
[Crossref]

J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
[Crossref]

Adv. Funct. Mater. (1)

C. P. Brown, J. L. Boyd, A. J. Palmer, M. Phillips, C. Couture, M. Rivard, P. A. Hulley, A. J. Price, A. Ruediger, F. Légaré, and A. J. Carr, “Modulation of Mechanical Interactions by Local Piezoelectric Effects,” Adv. Funct. Mater. 26(42), 7662–7667 (2016).
[Crossref]

Biomed. Opt. Express (2)

Biophys. J. (2)

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(2), 693–703 (2006).
[Crossref]

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical Model of Fibrillar Collagen Organization for Interpreting the Second-Order Susceptibility Tensors in Biological Tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

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I. Freund and M. Deutsch, “Macroscopic polarity of connective tissue is due to discrete polar structures,” Biopolymers 25(4), 601–606 (1986).
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D. A. D. Parry and A. S. Craig, “Collagen structure and stability,” Biopolymers 16(5), 1015–1031 (1977).
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Chem. Phys. Lett. (1)

C. A. Dailey, B. J. Burke, and G. J. Simpson, “The general failure of Kleinman symmetry in practical nonlinear optical applications,” Chem. Phys. Lett. 390(1-3), 8–13 (2004).
[Crossref]

Front. Oncol. (1)

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S. L. Asa, B. C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue Using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
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IEEE Trans. Syst., Man, Cybern. (1)

N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst., Man, Cybern. 9(1), 62–66 (1979).
[Crossref]

J. Biomed. Opt. (1)

J. Venius, S. Bagdonas, E. Zurauskas, and R. Rotomskis, “Visualization of human heart conduction system by means of fluorescence spectroscopy,” J. Biomed. Opt. 16(10), 107001 (2011).
[Crossref]

J. Biophotonics (1)

A. Golaraei, K. Mirsanaye, Y. Ro, S. Krouglov, M. K. Akens, B. C. Wilson, and V. Barzda, “Collagen chirality and 3D orientation studied with polarimetric second-harmonic generation microscopy,” J. Biophotonics 12(1), e201800241 (2019).
[Crossref]

J. Phys. Soc. Jpn. (1)

E. Fukada and I. Yasuda, “On the piezoelectric effect of bone,” J. Phys. Soc. Jpn. 12(10), 1158–1162 (1957).
[Crossref]

Jpn. J. Appl. Phys. (1)

E. Fukada and I. Yasuda, “Piezoelectric effects in collagen,” Jpn. J. Appl. Phys. 3(2), 117–121 (1964).
[Crossref]

Nanotechnology (1)

M. Minary-Jolandan and M. Yu, “Nanoscale characterization of isolated individual type I collagen fibrils: Polarization and piezoelectricity,” Nanotechnology 20(8), 085706 (2009).
[Crossref]

Nat. Protoc. (1)

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]

Nature (2)

M. H. Shamos and L. S. Lavine, “Piezoelectricity as a fundamental property of biological tissues,” Nature 213(5073), 267–269 (1967).
[Crossref]

G. N. Ramachandran and G. Kartha, “Structure of Collagen,” Nature 176(4482), 593–595 (1955).
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Opt. Express (1)

SIAM J. Optim. (1)

T. F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM J. Optim. 6(2), 418–445 (1996).
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Tohoku J. Exp. Med. (1)

J. Venius, E. Zurauskas, and R. Rotomskis, “High Resolution Imaging of the Human Cardiac Conduction System Using Reflectance Confocal Microscopy,” Tohoku J. Exp. Med. 229(1), 67–73 (2013).
[Crossref]

Other (1)

F. Martini, R. B. Tallitsch, and J. L. Nath, Human Anatomy (Pearson, 2017).

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Figures (2)

Fig. 1.
Fig. 1. Representative images from CN, FIB, CD, CMB and MYO regions of the human cardiac tissue. H&E images (a)-(e), total SHG intensity on a logarithmic scale (f)-(j), R- and C-ratios (k)-(p) and (q)-(u), respectively (the occurrence histograms are embedded in their color bars), the in-plane orientation ($\delta$) of the collagen fibers (v)-(z) and their corresponding polar distribution (red and blue lines indicate positive and negative polarities, respectively, the black lines show the fibers in the image plane with $|\textrm {C}| \leq 0.03$). Imaged areas were $110~\mu$m $\times \,110~\mu$m ($128 \times 128$ pixels). Pixels with fewer than 20 photon counts for every polarization state are discarded in analysis. Minimum goodness of fit is $R^{2}=0.8$.
Fig. 2.
Fig. 2. Statistical analysis of R- and C-ratios. The R-ratio distribution from all analyzed images combined, with myosin (black) and collagen (cyan) R-ratios separated by Otsu’s threshold at 1.55 (a). R-ratio mean (b) and C-ratio standard deviation (c) of all scanned regions of the human cardiac tissue. Standard errors are represented by error bars, and asterisks denote statistical significance: $\ast ~ p<0.05,~~ \ast \ast ~ p<0.0001,~~ \ast \ast \ast ~ p<0.001,~~ \ast \ast \ast \ast ~ p<0.02$.

Equations (2)

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I 2 ω | sin ( ϕ δ ) sin ( 2 θ 2 δ ) + 2 C cos ( θ δ ) sin ( θ ϕ ) + cos ( ϕ δ ) sin 2 ( θ δ ) + R cos ( ϕ δ ) cos 2 ( θ δ ) | 2
C = χ x y z ( 2 ) χ z x x ( 2 ) sin ( α ) ,                             R = χ z z z ( 2 ) χ z x x ( 2 ) cos 2 ( α ) + 3 sin 2 ( α )