Abstract

Bone is a unique biological composite material made up of a highly structured collagen mesh matrix and mineral deposits. Although mineral provides stiffness, collagen’s secondary organization provides a critical role in bone elasticity. Here, we performed polarimetric analysis of bone collagen fibers using second harmonic generation (SHG) imaging to evaluate lamella sheets and collagen fiber integrity in intact cranial bone. Our polarimetric data was fitted to a model accounting for diattenuation, polarization cross-talk, and birefringence. We compared our data to the fitted model and found no significant difference between our polarimetric observation and the representation of these scattering properties up to 70 µm deep. We also observed a loss of resolution as we imaged up to 70 µm deep into bone but a conservation of polarimetric response. Polarimetric SHG allows for the discrimination of collagen lamellar sheet structures in intact bone. Our work could allow for label-free identification of disease states and monitor the efficacy of therapies for bone disorders.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
OSA Recommended Articles
Second harmonic generation signal from type I collagen fibers grown in vitro

Cindy Grethel Fuentes-Corona, Jacob Licea-Rodriguez, Rebecca Younger, Raul Rangel-Rojo, Eric O. Potma, and Israel Rocha-Mendoza
Biomed. Opt. Express 10(12) 6449-6461 (2019)

Polarimetric second-harmonic generation microscopy of the hierarchical structure of collagen in stage I-III non-small cell lung carcinoma

Ahmad Golaraei, Leila B. Mostaço-Guidolin, Vaishnavi Raja, Roya Navab, Tao Wang, Shingo Sakashita, Kazuhiro Yasufuku, Ming-Sound Tsao, Brian C. Wilson, and Virginijus Barzda
Biomed. Opt. Express 11(4) 1851-1863 (2020)

Second harmonic generation imaging reveals asymmetry in the rotational helicity of collagen lamellae in chicken corneas

Sheng-Lin Lee, Yang-Fang Chen, and Chen-Yuan Dong
Biomed. Opt. Express 10(10) 5223-5234 (2019)

References

  • View by:
  • |
  • |
  • |

  1. S. R. Stock, “The mineral–collagen interface in bone,” Calcif. Tissue Int. 97(3), 262–280 (2015).
    [Crossref]
  2. R. Christensen, Mechanics of Composite Materials (Krieger, 1991).
  3. M. Saito and K. Marumo, “Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus,” Osteoporosis Int. 21(2), 195–214 (2010).
    [Crossref]
  4. M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
    [Crossref]
  5. A. Forlino and J. C. Marini, “Osteogenesis imperfecta,” Lancet 387(10028), 1657–1671 (2016).
    [Crossref]
  6. G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
    [Crossref]
  7. 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]
  8. J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, “Mechanical properties and the hierarchical structure of bone,” Med. Eng. Phys. 20(2), 92–102 (1998).
    [Crossref]
  9. Z. Zhou, D. Qian, and M. Minary-Jolandan, “Molecular mechanism of polarization and piezoelectric effect in super-twisted collagen,” ACS Biomater. Sci. Eng. 2(6), 929–936 (2016).
    [Crossref]
  10. P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
    [Crossref]
  11. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).
  12. I. Jager and P. Fratzl, “Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles,” Biophys. J. 79(4), 1737–1746 (2000).
    [Crossref]
  13. M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
    [Crossref]
  14. R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint Jr., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: comparison to sem and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
    [Crossref]
  15. R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
    [Crossref]
  16. T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
    [Crossref]
  17. T. Yasui, Y. Tohno, and T. Araki, “Determination of collagen fiber orientation in human tissue by use of polarization measurement of molecular second-harmonic-generation light,” Appl. Opt. 43(14), 2861–2867 (2004).
    [Crossref]
  18. W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
    [Crossref]
  19. P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
    [Crossref]
  20. P. Campagnola, “Second harmonic generation imaging microscopy: Applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
    [Crossref]
  21. E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
    [Crossref]
  22. D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
    [Crossref]
  23. O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
    [Crossref]
  24. K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
    [Crossref]
  25. R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008).
    [Crossref]
  26. J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
    [Crossref]
  27. F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
    [Crossref]
  28. Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
    [Crossref]
  29. R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
    [Crossref]
  30. K. F. Tehrani, P. Kner, and L. J. Mortensen, “Characterization of wavefront errors in mouse cranial bone using second-harmonic generation,” J. Biomed. Opt. 22(3), 036012 (2017).
    [Crossref]
  31. C. Teulon, I. Gusachenko, G. Latour, and M.-C. Schanne-Klein, “Theoretical, numerical and experimental study of geometrical parameters that affect anisotropy measurements in polarization-resolved SHG microscopy,” Opt. Express 23(7), 9313–9328 (2015).
    [Crossref]
  32. I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved second harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
    [Crossref]
  33. C.-H. Lien, K. Tilbury, S.-J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in second harmonic generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
    [Crossref]
  34. K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (ao-storm) using a genetic algorithm,” Opt. Express 23(10), 13677–13692 (2015).
    [Crossref]
  35. S. Weiner, W. Traub, and H. D. Wagner, “Lamellar bone: structure-function relations,” J. Struct. Biol. 126(3), 241–255 (1999).
    [Crossref]
  36. C. P. Adler, Bone Diseases: Macroscopic, Histological, and Radiological Diagnosis of Structural Changes in the Skeleton (Springer Science and Business Media, 2013).
  37. P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(6), 3330–3342 (2002).
    [Crossref]
  38. D. Ait-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express 18(14), 14859–14870 (2010).
    [Crossref]
  39. C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
    [Crossref]
  40. J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
    [Crossref]
  41. D. B. Conkey, A. M. Caravaca-Aguirre, and R. Piestun, “High-speed scattering medium characterization with application to focusing light through turbid media,” Opt. Express 20(2), 1733–1740 (2012).
    [Crossref]
  42. Q. Feng, B. Zhang, Z. Liu, C. Lin, and Y. Ding, “Research on intelligent algorithms for amplitude optimization of wavefront shaping,” Appl. Opt. 56(12), 3240–3244 (2017).
    [Crossref]
  43. J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U. S. A. 109(22), 8434–8439 (2012).
    [Crossref]
  44. P. Garnero, “The role of collagen organization on the properties of bone,” Calcif. Tissue Int. 97(3), 229–240 (2015).
    [Crossref]
  45. J. Caetano-Lopes, A. M. Nery, H. Canhão, J. Duarte, R. Cascão, A. Rodrigues, I. P. Perpétuo, S. Abdulghani, P. M. Amaral, S. Sakaguchi, Y. T. Konttinen, L. Graça, M. F. Vaz, and J. E. Fonseca, “Chronic arthritis leads to disturbances in the bone collagen network,” Arthritis Res. Ther. 12(1), R9 (2010).
    [Crossref]
  46. R. C. Paietta, E. L. Burger, and V. L. Ferguson, “Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine,” J. Struct. Biol. 184(2), 310–320 (2013).
    [Crossref]
  47. S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
    [Crossref]
  48. S. L. Hui, C. W. Slemenda, and C. C. Johnston, “Age and bone mass as predictors of fracture in a prospective study,” J. Clin. Invest. 81(6), 1804–1809 (1988).
    [Crossref]
  49. S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
    [Crossref]
  50. E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
    [Crossref]
  51. D. J. Prockop and K. I. Kivirikko, “Collagens: molecular biology, diseases, and potentials for therapy,” Annu. Rev. Biochem. 64(1), 403–434 (1995).
    [Crossref]
  52. A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
    [Crossref]
  53. E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).
  54. R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
    [Crossref]
  55. A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
    [Crossref]

2019 (1)

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

2018 (1)

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

2017 (4)

Q. Feng, B. Zhang, Z. Liu, C. Lin, and Y. Ding, “Research on intelligent algorithms for amplitude optimization of wavefront shaping,” Appl. Opt. 56(12), 3240–3244 (2017).
[Crossref]

K. F. Tehrani, P. Kner, and L. J. Mortensen, “Characterization of wavefront errors in mouse cranial bone using second-harmonic generation,” J. Biomed. Opt. 22(3), 036012 (2017).
[Crossref]

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
[Crossref]

2016 (3)

A. Forlino and J. C. Marini, “Osteogenesis imperfecta,” Lancet 387(10028), 1657–1671 (2016).
[Crossref]

Z. Zhou, D. Qian, and M. Minary-Jolandan, “Molecular mechanism of polarization and piezoelectric effect in super-twisted collagen,” ACS Biomater. Sci. Eng. 2(6), 929–936 (2016).
[Crossref]

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

2015 (10)

C. Teulon, I. Gusachenko, G. Latour, and M.-C. Schanne-Klein, “Theoretical, numerical and experimental study of geometrical parameters that affect anisotropy measurements in polarization-resolved SHG microscopy,” Opt. Express 23(7), 9313–9328 (2015).
[Crossref]

K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (ao-storm) using a genetic algorithm,” Opt. Express 23(10), 13677–13692 (2015).
[Crossref]

S. R. Stock, “The mineral–collagen interface in bone,” Calcif. Tissue Int. 97(3), 262–280 (2015).
[Crossref]

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

P. Garnero, “The role of collagen organization on the properties of bone,” Calcif. Tissue Int. 97(3), 229–240 (2015).
[Crossref]

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

2014 (2)

M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
[Crossref]

K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
[Crossref]

2013 (2)

C.-H. Lien, K. Tilbury, S.-J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in second harmonic generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[Crossref]

R. C. Paietta, E. L. Burger, and V. L. Ferguson, “Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine,” J. Struct. Biol. 184(2), 310–320 (2013).
[Crossref]

2012 (4)

D. B. Conkey, A. M. Caravaca-Aguirre, and R. Piestun, “High-speed scattering medium characterization with application to focusing light through turbid media,” Opt. Express 20(2), 1733–1740 (2012).
[Crossref]

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U. S. A. 109(22), 8434–8439 (2012).
[Crossref]

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

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 (2)

P. Campagnola, “Second harmonic generation imaging microscopy: Applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
[Crossref]

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref]

2010 (6)

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved second harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref]

D. Ait-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express 18(14), 14859–14870 (2010).
[Crossref]

M. Saito and K. Marumo, “Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus,” Osteoporosis Int. 21(2), 195–214 (2010).
[Crossref]

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

2008 (2)

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008).
[Crossref]

2007 (1)

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

2004 (3)

T. Yasui, Y. Tohno, and T. Araki, “Determination of collagen fiber orientation in human tissue by use of polarization measurement of molecular second-harmonic-generation light,” Appl. Opt. 43(14), 2861–2867 (2004).
[Crossref]

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

2003 (2)

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

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

2002 (2)

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

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(6), 3330–3342 (2002).
[Crossref]

2000 (1)

I. Jager and P. Fratzl, “Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles,” Biophys. J. 79(4), 1737–1746 (2000).
[Crossref]

1999 (1)

S. Weiner, W. Traub, and H. D. Wagner, “Lamellar bone: structure-function relations,” J. Struct. Biol. 126(3), 241–255 (1999).
[Crossref]

1998 (1)

J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, “Mechanical properties and the hierarchical structure of bone,” Med. Eng. Phys. 20(2), 92–102 (1998).
[Crossref]

1995 (1)

D. J. Prockop and K. I. Kivirikko, “Collagens: molecular biology, diseases, and potentials for therapy,” Annu. Rev. Biochem. 64(1), 403–434 (1995).
[Crossref]

1994 (1)

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

1993 (1)

A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
[Crossref]

1988 (1)

S. L. Hui, C. W. Slemenda, and C. C. Johnston, “Age and bone mass as predictors of fracture in a prospective study,” J. Clin. Invest. 81(6), 1804–1809 (1988).
[Crossref]

Abdulghani, S.

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

Acevedo, C.

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

Adler, C. P.

C. P. Adler, Bone Diseases: Macroscopic, Histological, and Radiological Diagnosis of Structural Changes in the Skeleton (Springer Science and Business Media, 2013).

Ahmed, L. A.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Ait-Belkacem, D.

Alberts, B.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

Allain, J. M.

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref]

Alliston, T.

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

Amaral, P. M.

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

Ambekar, R.

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

Aptel, F.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

Araki, T.

Auger, E.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Bailey, A. J.

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
[Crossref]

Bala, Y.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Bancelin, S.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Basta-Pljakic, J.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Beaurepaire, E.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

Bembi, B.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Bjornerem, A.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Boivin, G.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Boskey, A. L.

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

Brasselet, S.

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

D. Ait-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express 18(14), 14859–14870 (2010).
[Crossref]

Brown, C.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Brustlein, S.

Burger, E. L.

R. C. Paietta, E. L. Burger, and V. L. Ferguson, “Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine,” J. Struct. Biol. 184(2), 310–320 (2013).
[Crossref]

Burger, H.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Caetano-Lopes, J.

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

Campagnola, P.

P. Campagnola, “Second harmonic generation imaging microscopy: Applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
[Crossref]

Campagnola, P. J.

K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
[Crossref]

C.-H. Lien, K. Tilbury, S.-J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in second harmonic generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[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]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008).
[Crossref]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

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

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

Canhão, H.

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

Caravaca-Aguirre, A. M.

Cascão, R.

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

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(6), 3330–3342 (2002).
[Crossref]

Chen, S.-J.

K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
[Crossref]

C.-H. Lien, K. Tilbury, S.-J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in second harmonic generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[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]

Chien, Y. H.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Chittenden, M.

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

Christensen, R.

R. Christensen, Mechanics of Composite Materials (Krieger, 1991).

Conkey, D. B.

Couture, C. A.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Cox, G.

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

Cripton, P.

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Cui, M.

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U. S. A. 109(22), 8434–8439 (2012).
[Crossref]

Czapiga, M.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

de Laet, C. E.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Débarre, D.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Deniset-Besseau, A.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

Ding, Y.

Duarte, J.

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

Dvornikov, A.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Ebacher, V.

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Eriksen, E. F.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Evans, R. M.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Evis, Z.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

Farlay, D.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Feng, Q.

Ferguson, V. L.

R. C. Paietta, E. L. Burger, and V. L. Ferguson, “Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine,” J. Struct. Biol. 184(2), 310–320 (2013).
[Crossref]

Flatow, E. L.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Fonseca, J. E.

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

Forlino, A.

A. Forlino and J. C. Marini, “Osteogenesis imperfecta,” Lancet 387(10028), 1657–1671 (2016).
[Crossref]

Fraser, I.

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

Fratzl, P.

I. Jager and P. Fratzl, “Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles,” Biophys. J. 79(4), 1737–1746 (2000).
[Crossref]

Fung, D. T.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Garnero, P.

P. Garnero, “The role of collagen organization on the properties of bone,” Calcif. Tissue Int. 97(3), 229–240 (2015).
[Crossref]

Gasecka, A.

Genthial, R.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Germain, R. N.

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U. S. A. 109(22), 8434–8439 (2012).
[Crossref]

Gorrell, M. D.

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

Goulam Houssen, Y.

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref]

Gourrier, A.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Graça, L.

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

Gratton, E.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Gusachenko, I.

Guy, P.

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Hofman, A.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Holland, E. F.

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

Hong, S.-H.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Hoppe, P. E.

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

Houle, M. A.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Hui, S. L.

S. L. Hui, C. W. Slemenda, and C. C. Johnston, “Age and bone mass as predictors of fracture in a prospective study,” J. Clin. Invest. 81(6), 1804–1809 (1988).
[Crossref]

Huq, R.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Hwu, W. L.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Jager, I.

I. Jager and P. Fratzl, “Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles,” Biophys. J. 79(4), 1737–1746 (2000).
[Crossref]

Jasiuk, I.

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

Jepsen, K. J.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Joakimsen, R. M.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Johnson, A.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

Johnston, C. C.

S. L. Hui, C. W. Slemenda, and C. C. Johnston, “Age and bone mass as predictors of fracture in a prospective study,” J. Clin. Invest. 81(6), 1804–1809 (1988).
[Crossref]

Jones, A.

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

Kable, E.

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

Kalajzic, I.

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

Kato, S.

M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
[Crossref]

Kersh, M. E.

W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
[Crossref]

Kida, Y.

M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
[Crossref]

Kivirikko, K. I.

D. J. Prockop and K. I. Kivirikko, “Collagens: molecular biology, diseases, and potentials for therapy,” Annu. Rev. Biochem. 64(1), 403–434 (1995).
[Crossref]

Kner, P.

K. F. Tehrani, P. Kner, and L. J. Mortensen, “Characterization of wavefront errors in mouse cranial bone using second-harmonic generation,” J. Biomed. Opt. 22(3), 036012 (2017).
[Crossref]

K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (ao-storm) using a genetic algorithm,” Opt. Express 23(10), 13677–13692 (2015).
[Crossref]

Konttinen, Y. T.

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

Kuhn-Spearing, L.

J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, “Mechanical properties and the hierarchical structure of bone,” Med. Eng. Phys. 20(2), 92–102 (1998).
[Crossref]

Lacomb, R.

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008).
[Crossref]

Latour, G.

Laudier, D. M.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Leather, A. T.

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

Lee, W.

W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
[Crossref]

Legare, F.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Legeais, J.-M.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

Levi, M.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Lewis, J.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

Lien, C.-H.

K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
[Crossref]

C.-H. Lien, K. Tilbury, S.-J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in second harmonic generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[Crossref]

Lin, C.

Lin, C. P.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

Liu, Z.

Loew, L. M.

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

Lyritis, G.

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

Malone, C. J.

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

Manconi, F.

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

Mandalia, V.

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

Mansell, J. P.

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

Mansfield, J. C.

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

Marini, J. C.

A. Forlino and J. C. Marini, “Osteogenesis imperfecta,” Lancet 387(10028), 1657–1671 (2016).
[Crossref]

Marumo, K.

M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
[Crossref]

M. Saito and K. Marumo, “Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus,” Osteoporosis Int. 21(2), 195–214 (2010).
[Crossref]

Mattson, J. M.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

McKay, H.

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Mendelsohn, R.

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

Millard, A. C.

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

Minary-Jolandan, M.

Z. Zhou, D. Qian, and M. Minary-Jolandan, “Molecular mechanism of polarization and piezoelectric effect in super-twisted collagen,” ACS Biomater. Sci. Eng. 2(6), 929–936 (2016).
[Crossref]

Mohler, W. A.

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

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

Mortensen, L. J.

K. F. Tehrani, P. Kner, and L. J. Mortensen, “Characterization of wavefront errors in mouse cranial bone using second-harmonic generation,” J. Biomed. Opt. 22(3), 036012 (2017).
[Crossref]

Munhoz, F.

Nadiarnykh, O.

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008).
[Crossref]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[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]

Nery, A. M.

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

Olivier, C.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Olivier, N.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

Osima, M.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Paietta, R. C.

R. C. Paietta, E. L. Burger, and V. L. Ferguson, “Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine,” J. Struct. Biol. 184(2), 310–320 (2013).
[Crossref]

Park, J. H.

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

Paschalis, E. P.

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

Perpétuo, I. P.

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

Peyrin, F.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Piestun, R.

Pioletti, D. P.

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

Pittis, M. G.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Plamann, K.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[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]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

Plotz, P.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Pols, H. A.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Popov, K.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Poundarik, A. A.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

Prockop, D. J.

D. J. Prockop and K. I. Kivirikko, “Collagens: molecular biology, diseases, and potentials for therapy,” Annu. Rev. Biochem. 64(1), 403–434 (1995).
[Crossref]

Qian, D.

Z. Zhou, D. Qian, and M. Minary-Jolandan, “Molecular mechanism of polarization and piezoelectric effect in super-twisted collagen,” ACS Biomater. Sci. Eng. 2(6), 929–936 (2016).
[Crossref]

Raben, N.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Raff, M.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

Rahman, H.

W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
[Crossref]

Ralston, E.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Ramunno, L.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

Ranjit, S.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Redford-Badwal, D.

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

Reiser, K. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(6), 3330–3342 (2002).
[Crossref]

Rho, J. Y.

J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, “Mechanical properties and the hierarchical structure of bone,” Med. Eng. Phys. 20(2), 92–102 (1998).
[Crossref]

Ritchie, R. O.

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

Roberts, K.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

Rodrigues, A.

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

Rubenchik, A. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(6), 3330–3342 (2002).
[Crossref]

Rubin, M.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

Saito, M.

M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
[Crossref]

M. Saito and K. Marumo, “Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus,” Osteoporosis Int. 21(2), 195–214 (2010).
[Crossref]

Sakaguchi, S.

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

Schaffler, M. B.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Schanne-Klein, M. C.

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref]

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved second harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref]

Schanne-Klein, M.-C.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

C. Teulon, I. Gusachenko, G. Latour, and M.-C. Schanne-Klein, “Theoretical, numerical and experimental study of geometrical parameters that affect anisotropy measurements in polarization-resolved SHG microscopy,” Opt. Express 23(7), 9313–9328 (2015).
[Crossref]

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

Schuit, S. C.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Schwartz, O.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Seeman, E.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Sereysky, J. B.

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Shane, E.

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

Shen, P.

Shigdel, R.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Sims, T. J.

A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
[Crossref]

Skarantavos, G.

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

Slemenda, C. W.

S. L. Hui, C. W. Slemenda, and C. C. Johnston, “Age and bone mass as predictors of fracture in a prospective study,” J. Clin. Invest. 81(6), 1804–1809 (1988).
[Crossref]

Sroga, G. E.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

Stadelmann, V. A.

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

Stakic, M.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

Stock, S. R.

S. R. Stock, “The mineral–collagen interface in bone,” Calcif. Tissue Int. 97(3), 262–280 (2015).
[Crossref]

Stoller, P.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(6), 3330–3342 (2002).
[Crossref]

Studd, J. W.

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

Sun, W.

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

Swaim, B.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

Tang, J.

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U. S. A. 109(22), 8434–8439 (2012).
[Crossref]

Tang, T.

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Tehrani, K. F.

K. F. Tehrani, P. Kner, and L. J. Mortensen, “Characterization of wavefront errors in mouse cranial bone using second-harmonic generation,” J. Biomed. Opt. 22(3), 036012 (2017).
[Crossref]

K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (ao-storm) using a genetic algorithm,” Opt. Express 23(10), 13677–13692 (2015).
[Crossref]

Terasaki, M.

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

Teulon, C.

Thompson, P. W.

A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
[Crossref]

Tilbury, K.

K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
[Crossref]

C.-H. Lien, K. Tilbury, S.-J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in second harmonic generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[Crossref]

Tohno, Y.

Toms, A.

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

Toussaint Jr., K. C.

W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
[Crossref]

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

Traub, W.

S. Weiner, W. Traub, and H. D. Wagner, “Lamellar bone: structure-function relations,” J. Struct. Biol. 126(3), 241–255 (1999).
[Crossref]

Turcotte, R.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

Uitterlinden, A. G.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Ural, A.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

van der Klift, M.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Van der Kolk, J.

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

van Leeuwen, J. P.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Vashishth, D.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

Vaz, M. F.

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

Vial, J.-C.

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Wagner, H. D.

S. Weiner, W. Traub, and H. D. Wagner, “Lamellar bone: structure-function relations,” J. Struct. Biol. 126(3), 241–255 (1999).
[Crossref]

Walter, P.

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

Wang, R.

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Weel, A. E.

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

Weiner, S.

S. Weiner, W. Traub, and H. D. Wagner, “Lamellar bone: structure-function relations,” J. Struct. Biol. 126(3), 241–255 (1999).
[Crossref]

Winlove, C. P.

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

Wotton, S. F.

A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
[Crossref]

Wu, J. W.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

Wu, P. C.

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

Xu, J.

Yasui, T.

Zebaze, R.

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

Zhang, B.

Zhang, Y.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (ao-storm) using a genetic algorithm,” Opt. Express 23(10), 13677–13692 (2015).
[Crossref]

Zhou, Z.

Z. Zhou, D. Qian, and M. Minary-Jolandan, “Molecular mechanism of polarization and piezoelectric effect in super-twisted collagen,” ACS Biomater. Sci. Eng. 2(6), 929–936 (2016).
[Crossref]

Zioupos, P.

J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, “Mechanical properties and the hierarchical structure of bone,” Med. Eng. Phys. 20(2), 92–102 (1998).
[Crossref]

ACS Biomater. Sci. Eng. (1)

Z. Zhou, D. Qian, and M. Minary-Jolandan, “Molecular mechanism of polarization and piezoelectric effect in super-twisted collagen,” ACS Biomater. Sci. Eng. 2(6), 929–936 (2016).
[Crossref]

Anal. Chem. (1)

P. Campagnola, “Second harmonic generation imaging microscopy: Applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
[Crossref]

Ann. Biomed. Eng. (1)

D. T. Fung, J. B. Sereysky, J. Basta-Pljakic, D. M. Laudier, R. Huq, K. J. Jepsen, M. B. Schaffler, and E. L. Flatow, “Second harmonic generation imaging and fourier transform spectral analysis reveal damage in fatigue-loaded tendons,” Ann. Biomed. Eng. 38(5), 1741–1751 (2010).
[Crossref]

Annu. Rev. Biochem. (1)

D. J. Prockop and K. I. Kivirikko, “Collagens: molecular biology, diseases, and potentials for therapy,” Annu. Rev. Biochem. 64(1), 403–434 (1995).
[Crossref]

Appl. Opt. (2)

Arthritis Res. Ther. (1)

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

Biomed. Opt. Express (1)

Biophys. J. (6)

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref]

K. Tilbury, C.-H. Lien, S.-J. Chen, and P. J. Campagnola, “Differentiation of col i and col iii isoforms in stromal models of ovarian cancer by analysis of second harmonic generation polarization and emission directionality,” Biophys. J. 106(2), 354–365 (2014).
[Crossref]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008).
[Crossref]

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

I. Jager and P. Fratzl, “Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles,” Biophys. J. 79(4), 1737–1746 (2000).
[Crossref]

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(6), 3330–3342 (2002).
[Crossref]

Bone (4)

S. C. Schuit, M. van der Klift, A. E. Weel, C. E. de Laet, H. Burger, E. Seeman, A. Hofman, A. G. Uitterlinden, J. P. van Leeuwen, and H. A. Pols, “Fracture incidence and association with bone mineral density in elderly men and women: the rotterdam study,” Bone 34(1), 195–202 (2004).
[Crossref]

R. Shigdel, M. Osima, L. A. Ahmed, R. M. Joakimsen, E. F. Eriksen, R. Zebaze, and A. Bjornerem, “Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures,” Bone 81, 1–6 (2015).
[Crossref]

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

T. Tang, V. Ebacher, P. Cripton, P. Guy, H. McKay, and R. Wang, “Shear deformation and fracture of human cortical bone,” Bone 71, 25–35 (2015).
[Crossref]

Calcif. Tissue Int. (2)

S. R. Stock, “The mineral–collagen interface in bone,” Calcif. Tissue Int. 97(3), 262–280 (2015).
[Crossref]

P. Garnero, “The role of collagen organization on the properties of bone,” Calcif. Tissue Int. 97(3), 229–240 (2015).
[Crossref]

Connect. Tissue Res. (1)

A. J. Bailey, S. F. Wotton, T. J. Sims, and P. W. Thompson, “Biochemical changes in the collagen of human osteoporotic bone matrix,” Connect. Tissue Res. 29(2), 119–132 (1993).
[Crossref]

Curr. Osteoporos Rep. (1)

M. Saito, Y. Kida, S. Kato, and K. Marumo, “Diabetes, collagen, and bone quality,” Curr. Osteoporos Rep. 12(2), 181–188 (2014).
[Crossref]

Invest. Ophthalmol. Visual Sci. (1)

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Visual Sci. 51(5), 2459–2465 (2010).
[Crossref]

J. Biomech. (1)

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref]

J. Biomed. Opt. (3)

K. F. Tehrani, P. Kner, and L. J. Mortensen, “Characterization of wavefront errors in mouse cranial bone using second-harmonic generation,” J. Biomed. Opt. 22(3), 036012 (2017).
[Crossref]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref]

W. Lee, H. Rahman, M. E. Kersh, and K. C. Toussaint Jr., “Application of quantitative second-harmonic generation microscopy to posterior cruciate ligament for crimp analysis studies,” J. Biomed. Opt. 22(4), 046009 (2017).
[Crossref]

J. Biophotonics (1)

M. A. Houle, C. A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Legare, “Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref]

J. Bone Miner. Res. (1)

E. P. Paschalis, E. Shane, G. Lyritis, G. Skarantavos, R. Mendelsohn, and A. L. Boskey, “Bone fragility and collagen cross-links,” J. Bone Miner. Res. 19(12), 2000–2004 (2004).
[Crossref]

J. Clin. Invest. (1)

S. L. Hui, C. W. Slemenda, and C. C. Johnston, “Age and bone mass as predictors of fracture in a prospective study,” J. Clin. Invest. 81(6), 1804–1809 (1988).
[Crossref]

J. Mech. Behav. Biomed. Mater. (1)

A. A. Poundarik, P. C. Wu, Z. Evis, G. E. Sroga, A. Ural, M. Rubin, and D. Vashishth, “A direct role of collagen glycation in bone fracture,” J. Mech. Behav. Biomed. Mater. 52, 120–130 (2015).
[Crossref]

J. R. Soc., Interface (1)

J. C. Mansfield, V. Mandalia, A. Toms, C. P. Winlove, and S. Brasselet, “Collagen reorganization in cartilage under strain probed by polarization sensitive second harmonic generation microscopy,” J. R. Soc., Interface 16(150), 20180611 (2019).
[Crossref]

J. Struct. Biol. (4)

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref]

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

R. C. Paietta, E. L. Burger, and V. L. Ferguson, “Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine,” J. Struct. Biol. 184(2), 310–320 (2013).
[Crossref]

S. Weiner, W. Traub, and H. D. Wagner, “Lamellar bone: structure-function relations,” J. Struct. Biol. 126(3), 241–255 (1999).
[Crossref]

Lancet (1)

A. Forlino and J. C. Marini, “Osteogenesis imperfecta,” Lancet 387(10028), 1657–1671 (2016).
[Crossref]

Med. Eng. Phys. (1)

J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, “Mechanical properties and the hierarchical structure of bone,” Med. Eng. Phys. 20(2), 92–102 (1998).
[Crossref]

Nat. Biomed. Eng. (1)

C. Acevedo, V. A. Stadelmann, D. P. Pioletti, T. Alliston, and R. O. Ritchie, “Fatigue as the missing link between bone fragility and fracture,” Nat. Biomed. Eng. 2(2), 62–71 (2018).
[Crossref]

Nat. Biotechnol. (1)

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

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]

Obstet Gynecol. (1)

E. F. Holland, J. W. Studd, J. P. Mansell, A. T. Leather, and A. J. Bailey, “Changes in collagen composition and cross-links in bone and skin of osteoporotic postmenopausal women treated with percutaneous estradiol implants,” Obstet Gynecol. 83, 180–183 (1994).

Opt. Express (5)

Osteoporosis Int. (1)

M. Saito and K. Marumo, “Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus,” Osteoporosis Int. 21(2), 195–214 (2010).
[Crossref]

Proc. Natl. Acad. Sci. U. S. A. (2)

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U. S. A. 109(22), 8434–8439 (2012).
[Crossref]

Sci. Rep. (2)

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging fibrosis and separating collagens using second harmonic generation and phasor approach to fluorescence lifetime imaging,” Sci. Rep. 5(1), 13378 (2015).
[Crossref]

R. Genthial, E. Beaurepaire, M.-C. Schanne-Klein, F. Peyrin, D. Farlay, C. Olivier, Y. Bala, G. Boivin, J.-C. Vial, D. Débarre, and A. Gourrier, “Label-free imaging of bone multiscale porosity and interfaces using third-harmonic generation microscopy,” Sci. Rep. 7(1), 3419 (2017).
[Crossref]

Other (3)

B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, 2002).

R. Christensen, Mechanics of Composite Materials (Krieger, 1991).

C. P. Adler, Bone Diseases: Macroscopic, Histological, and Radiological Diagnosis of Structural Changes in the Skeleton (Springer Science and Business Media, 2013).

Cited By

OSA participates in Crossref's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (7)

Fig. 1.
Fig. 1. The strength of the second harmonic signal is dependent on the orientation of collagen relative to the polarized light. (A) SHG signal will change with the angle of polarized light when collagen fibers are aligned but not when there is variable orientation. (B) When the light is parallel to the dominant orientation of collagen fibers, here at 90°, these fibers will generate strong second harmonic signal. The SHG signal is dimmest when it is perpendicular to the dominant orientation of collagen fibers (180°). At intermediate angles, 40° and 130°, collagen fibers of different orientations create second harmonic signal. Scale bar: $20\ \mu$m.
Fig. 2.
Fig. 2. Optical setup of the two-photon microscope. The red path is the excitation light and the blue path is the SHG emission. Mrm: motorized rotational mount, DiM: Dichroic mirror, BiBo: Bismuth triborate, PMT: Photon multiplier tube, L: Lens, F: Filter, PBS: Polarizing Beam Splitter. Detection path (A) was used unless otherwise noted. A PBS was added to the detection path (B) to evaluate polarization contrast through depth in sections 3.5 and 4.1.2.
Fig. 3.
Fig. 3. Loss of resolution and maintenance of polarization through full thickness bone. (A) The detected spot size in bone gradually gets larger with depth while maintaining a Gaussian beam through the first mean-free-path of bone. (B) The bandwidth decreases with depth through $70\ \mu$m of adult bone. Significantly lower bandwidth than what is detected at $0\ \mu$m (p <0.05) is denoted by (*). (C) The average collagen fiber width does not change over the first $20\ \mu$m of depth. (D) The amount of collagen fiber content that we are able to detect decreases with depth. Significantly less (p <0.05) collagen fiber content than what is detected at $0\ \mu$m is denoted by (*). Each color represents a different calvarial bone sample with colors in (B) and (D) coordinating with each other. (E) The polarization contrast remains constant through $70\ \mu$m of adult bone. The standard deviation of all polarization stacks averaged 19.5% of the stack mean. Inset: Example normalized intensity values over angles of polarized light for images acquired at the surface (dark line) and $70\ \mu$m deep (light line).
Fig. 4.
Fig. 4. Polarization is retained with depth while resolution diminishes. At $5\ \mu$m from the periosteum (A and B) in whole bone, more collagen fibers are visible than when bone is evaluated $60\ \mu$m from the periosteum (C and D). Polarized light selectively excites collagen fibers of a single orientation, here 30° to the vertical axis, regardless of depth in whole bone using SHG (A and C). When all angles of polarized light are used, collagen fibers of all orientations are more equally excited with SHG signal (B and D). Scale Bar: $20\ \mu$m.
Fig. 5.
Fig. 5. Lamella sheet formation is observed through depth. (A) Freeze fractured cross sections of bone were analyzed with SEM to directly visualize lamella sheets. (B) An x,z profile of a single polarization of excitation light allows for visualization of lamella sheets in intact bone. Scale Bars: $20\ \mu$m. (C) Intensity profile of green line in (B) shows oscillatory patterns demonstrating alternating angles of lamella sheets.
Fig. 6.
Fig. 6. Scattering properties of bone have little impact on polarization retention through the first mean-free-path. (A) The polarization angle of the excitation light is scattered similarly regardless of the angle of polarized light. (B) $\rho$, the ratio of the two main tensorial components, remains relatively constant through the depth of intact bone, though elevated by 70 $\mu$m of depth. (C) $\Delta$ is the combined effect of birefringence and polarization cross-talk; the combined effect exhibits small fluctuations through the depth of bone. (D) Linearly polarized light was rotated and the signal was collected through the depth of bone. (E) To examine the effects of birefringence and polarization cross-talk, our data was fitted using Eq. (13). (F) and (G) show similar trends in the normalized intensity and fit, respectively, across stacks acquired in 3 individual mice (each color represents one mouse). The data and fit are offset to allow for simultaneous viewing of the trends in each biological replicate.
Fig. 7.
Fig. 7. SHG polarized imaging of collagen orientation in whole bone. (A) The frontal bones of wild type mice were imaged dorsal to the jugum limitans (i) and lateral to the sagittal suture (ii). (B) Polarized light was rotated using a motorized half-wave plate, images were collected every 10°, and pixels containing collagen fiber information were assigned colors based on orientation angle. Images were collected at $5\ \mu$m (C-F), $10\ \mu$m (G-J), $15\ \mu$m (K-N), and $60\ \mu$m (O-R) from the surface of the periosteum. The asterisk in N denotes an osteocyte lacunae. Scale Bar: $20\ \mu$m. (S-U) Average intensity profiles were plotted, fitted, and 95% confidence intervals were established to demonstrate the intensity signature of each orientation. (V) The same technique can be used to create a 3-D reconstruction of intact lamellar bone.

Equations (25)

Equations on this page are rendered with MathJax. Learn more.

I 2 ω = X i j k 2 E 2
X i j k 2 E 2 = N s < β >
I x 2 ω ρ c o s 2 ( α φ ) + s i n 2 ( α φ )
I y 2 ω 2 c o s ( α φ ) s i n ( α φ )
I x 2 ω = A c o s ( 4 α ) + B c o s ( 2 α ) + C
I y 2 ω = K 2 ( c o s ( 4 α ) + 1 )
A = K 2 ( ρ 1 2 ) 2
B = 2 K ( ρ 1 2 ) ( ρ + 1 2 )
C = K 2 ( ρ 1 2 ) 2 + ( ρ + 1 2 ) 2
ρ 2 = X x x x ( 2 ) X x y y ( 2 ) = A + B + C A B + C
I x 2 ω ( z ) = K e 2 z l a 0 ( | ρ e z Δ l a c o s 2 α e i Δ ϕ + s i n 2 α | 2 + η e z Δ l a | s i n 2 α | 2 )
Δ = C 3 A ( A + C ) 2 B 2 2 ( A B + C )
I 2 ω ( α ) = β [ A c o s ( 4 α 4 φ ) + B c o s ( 2 α 2 φ ) + 1 ]
μ r = μ cos ϕ ν sin ϕ
ν r = μ sin ϕ + ν cos ϕ
ϵ μ r = ϵ μ cos ϕ ϵ ν sin ϕ
ϵ ν r = ϵ μ sin ϕ + ϵ ν cos ϕ
F = A e x p ( ( ( μ r ϵ μ r ) 2 2 σ μ   2 + ( ν r ϵ ν r ) 2 2 σ ν   2 ) )
σ = m a x ( [ σ μ , σ ν ] ) 1 1 n x d x
I ( μ , ν ) = F { i ( x , y ) } ,
F C = μ , ν ( G ( μ , ν ) | I ( μ , ν ) | M ( μ , ν ) ) 2 μ , ν | I ( μ , ν ) | M ( μ , ν ) 2 ,
G ( μ , ν ) = 1 e x p ( μ 2 + ν 2 2 σ 2 ) ,
M ( μ , ν ) = { 1 μ 2 + ν 2 < f c o 0 otherwise ,
o ( x , y ) = 1 N p 1 Σ P ( i ( x , y , p ) μ p ( x , y ) ) 2 μ p ( x , y )
μ p ( x , y ) = 1 N p Σ   i ( x , y , p )

Metrics