Abstract

Assessing the biomechanical properties of the crystalline lens can provide crucial information for diagnosing disease and guiding precision therapeutic interventions. Existing noninvasive methods have been limited to global measurements. Here, we demonstrate the quantitative assessment of the elasticity of crystalline lens with a multimodal optical elastography technique, which combines dynamic wave-based optical coherence elastography (OCE) and Brillouin microscopy to overcome the drawbacks of individual modalities. OCE can provide direct measurements of tissue elasticity rapidly and quantitatively, but it is a challenge to image transparent samples such as the lens because this technique relies on backscattered light. On the other hand, Brillouin microscopy can map the longitudinal modulus with micro-scale resolution in transparent samples. However, the relationship between Brillouin-deduced modulus and Young’s modulus is not straightforward and sample dependent. By combining these two techniques, we can calibrate Brillouin measurements with OCE, based on the same sample, allowing us to completely map the Young’s modulus of the crystalline lens. The combined system was first validated with tissue-mimicking gelatin phantoms of varying elasticities (N = 9). The OCE data was used to calibrate the Brillouin shift measurements and subsequently map the Young’s modulus of the phantoms. After validation, OCE and Brillouin measurements were performed on ex-vivo porcine lenses (N = 6), and the Young’s modulus of the lenses was spatially mapped. The results show a strong correlation between Young’s moduli measured by OCE and longitudinal moduli measured by Brillouin microscopy. The correlation coefficient R was 0.98 for the phantoms and 0.94 for the lenses, respectively. The mean Young’s modulus of the anterior and posterior lens was 1.98 ± 0.74 kPa and 2.93 ± 1.13 kPa, respectively, and the Young’s modulus of the lens nucleus was 11.90 ± 2.94 kPa. The results presented in this manuscript open a new way for truly quantitative biomechanical mapping of optically transparent (or low scattering) tissues in 3D.

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

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References

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2020 (1)

S. Kling, “Optical coherence elastography by ambient pressure modulation for high-resolution strain mapping applied to patterned cross-linking,” J. R. Soc., Interface 17(162), 20190786 (2020).
[Crossref]

2019 (7)

F. Zvietcovich, P. Pongchalee, P. Meemon, J. P. Rolland, and K. J. Parker, “Reverberant 3D optical coherence elastography maps the elasticity of individual corneal layers,” Nat. Commun. 10(1), 4895 (2019).
[Crossref]

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, O. I. Baum, A. I. Omelchenko, D. V. Shabanov, A. A. Sovetsky, A. V. Yuzhakov, and A. A. Fedorov, “Revealing structural modifications in thermomechanical reshaping of collagenous tissues using optical coherence elastography,” J. Biophotonics 12(3), e201800250 (2019).
[Crossref]

A. Jiménez-villar, E. Mączyńska, A. Cichański, M. Wojtkowski, B. J. Kałużny, and I. Grulkowski, “High-speed OCT-based ocular biometer combined with an air-puff system for determination of induced retraction-free eye dynamics,” Biomed. Opt. Express 10(7), 3663–3680 (2019).
[Crossref]

H. Zhang, C. Wu, M. Singh, A. Nair, S. Aglyamov, and K. Larin, “Optical coherence elastography of cold cataract in porcine lens,” J. Biomed. Opt. 24(03), 1–7 (2019).
[Crossref]

C. Wu, S. R. Aglyamov, H. Zhang, and K. V. Larin, “Measuring the elastic wave velocity in the lens of the eye as a function of intraocular pressure using optical coherent elastography,” Quantum Electron. 49(1), 20–24 (2019).
[Crossref]

Y. Li, J. Zhu, J. J. Chen, J. Yu, Z. Jin, Y. Miao, A. W. Browne, Q. Zhou, and Z. Chen, “Simultaneously imaging and quantifying in vivo mechanical properties of crystalline lens and cornea using optical coherence elastography with acoustic radiation force excitation,” APL Photonics 4(10), 106104 (2019).
[Crossref]

M. Nikolic and G. Scarcelli, “Long-term Brillouin imaging of live cells with reduced absorption-mediated damage at 660 nm wavelength,” Biomed. Opt. Express 10(4), 1567–1580 (2019).
[Crossref]

2018 (5)

X. Y. Zhang, Q. M. Wang, Z. Lyu, X. H. Gao, P. P. Zhang, H. M. Lin, Y. R. Guo, T. F. Wang, S. P. Chen, and X. Chen, “Noninvasive assessment of age-related stiffness of crystalline lenses in a rabbit model using ultrasound elastography,” Biomed. Eng. Online 17(1), 75 (2018).
[Crossref]

C. Wu, S. R. Aglyamov, Z. Han, M. Singh, C. H. Liu, and K. V. Larin, “Assessing the biomechanical properties of the porcine crystalline lens as a function of intraocular pressure with optical coherence elastography,” Biomed. Opt. Express 9(12), 6455–6466 (2018).
[Crossref]

V. S. De Stefano, M. R. Ford, I. Seven, and W. J. Dupps, “Live human assessment of depth-dependent corneal displacements with swept-source optical coherence elastography,” PLoS One 13(12), e0209480 (2018).
[Crossref]

J. Fernandez, M. Rodriguez-Vallejo, J. Martinez, A. Tauste, and D. P. Pinero, “From Presbyopia to Cataracts: A Critical Review on Dysfunctional Lens Syndrome,” J. Ophthalmol. 2018, 1–10 (2018).
[Crossref]

K. H. Wang, D. T. Venetsanos, J. Wang, and B. K. Pierscionek, “Combined Use of Parallel-Plate Compression and Finite Element Modeling to Analyze the Mechanical Properties of Intact Porcine Lens,” J. Mech. Med. Biol. 18(07), 1840013 (2018).
[Crossref]

2017 (5)

B. F. Kennedy, P. Wijesinghe, and D. D. Sampson, “The emergence of optical elastography in biomedicine,” Nat. Photonics 11(4), 215–221 (2017).
[Crossref]

K. V. Larin and D. D. Sampson, “Optical coherence elastography - OCT at work in tissue biomechanics [Invited],” Biomed. Opt. Express 8(2), 1172–1202 (2017).
[Crossref]

M. A. Kirby, I. Pelivanov, S. Song, L. Ambrozinski, S. J. Yoon, L. Gao, D. Li, T. T. Shen, R. K. Wang, and M. O’Donnell, “Optical coherence elastography in ophthalmology,” J. Biomed. Opt. 22(12), 1 (2017).
[Crossref]

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, A. I. Omelchenko, O. I. Baum, S. E. Avetisov, A. V. Bolshunov, V. I. Siplivy, and D. V. Shabanov, “Optical coherence elastography for strain dynamics measurements in laser correction of cornea shape,” J. Biophotonics 10(11), 1450–1463 (2017).
[Crossref]

S. Park, H. Yoon, K. V. Larin, S. Y. Emelianov, and S. R. Aglyamov, “The impact of intraocular pressure on elastic wave velocity estimates in the crystalline lens,” Phys. Med. Biol. 62(3), N45–N57 (2017).
[Crossref]

2016 (5)

S. Besner, G. Scarcelli, R. Pineda, and S. H. Yun, “In Vivo Brillouin Analysis of the Aging Crystalline Lens,” Invest. Ophthalmol. Visual Sci. 57(13), 5093–5100 (2016).
[Crossref]

M. Singh, J. Li, S. Vantipalli, S. Wang, Z. Han, A. Nair, S. R. Aglyamov, M. D. Twa, and K. V. Larin, “Noncontact Elastic Wave Imaging Optical Coherence Elastography for Evaluating Changes in Corneal Elasticity Due to Crosslinking,” IEEE J. Sel. Top. Quantum Electron. 22(3), 266–276 (2016).
[Crossref]

Z. Han, M. Singh, S. R. Aglyamov, C.-H. Liu, A. Nair, R. Raghunathan, C. Wu, J. Li, and K. V. Larin, “Quantifying tissue viscoelasticity using optical coherence elastography and the Rayleigh wave model,” J. Biomed. Opt. 21(9), 090504 (2016).
[Crossref]

B. Y. Hsieh, S. Song, T. M. Nguyen, S. J. Yoon, T. T. Shen, R. K. Wang, and M. O’Donnell, “Moving-source elastic wave reconstruction for high-resolution optical coherence elastography,” J. Biomed. Opt. 21(11), 116006 (2016).
[Crossref]

C. H. Liu, A. Schill, C. Wu, M. Singh, and K. V. Larin, “Non-contact single shot elastography using line field low coherence holography,” Biomed. Opt. Express 7(8), 3021–3031 (2016).
[Crossref]

2015 (2)

G. Scarcelli, W. J. Polacheck, H. T. Nia, K. Patel, A. J. Grodzinsky, R. D. Kamm, and S. H. Yun, “Noncontact three-dimensional mapping of intracellular hydromechanical properties by Brillouin microscopy,” Nat. Methods 12(12), 1132–1134 (2015).
[Crossref]

C. Wu, Z. Han, S. Wang, J. Li, M. Singh, C. H. Liu, S. Aglyamov, S. Emelianov, F. Manns, and K. V. Larin, “Assessing age-related changes in the biomechanical properties of rabbit lens using a coaligned ultrasound and optical coherence elastography system,” Invest. Ophthalmol. Visual Sci. 56(2), 1292–1300 (2015).
[Crossref]

2014 (2)

2013 (2)

S. Yoon, S. Aglyamov, A. Karpiouk, and S. Emelianov, “The mechanical properties of ex vivo bovine and porcine crystalline lenses: age-related changes and location-dependent variations,” Ultrasound Med. Biol. 39(6), 1120–1127 (2013).
[Crossref]

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett. 10(7), 075605 (2013).
[Crossref]

2012 (3)

G. Scarcelli and S. H. Yun, “In vivo Brillouin optical microscopy of the human eye,” Opt. Express 20(8), 9197–9202 (2012).
[Crossref]

K. D. Mohan and A. L. Oldenburg, “Elastography of soft materials and tissues by holographic imaging of surface acoustic waves,” Opt. Express 20(17), 18887–18897 (2012).
[Crossref]

S. Choi, H. J. Lee, Y. Cheong, J. H. Shin, K. H. Jin, H. K. Park, and Y. G. Park, “AFM study for morphological characteristics and biomechanical properties of human cataract anterior lens capsules,” Scanning 34(4), 247–256 (2012).
[Crossref]

2011 (5)

S. Reiss, G. Burau, O. Stachs, R. Guthoff, and H. Stolz, “Spatially resolved Brillouin spectroscopy to determine the rheological properties of the eye lens,” Biomed. Opt. Express 2(8), 2144–2159 (2011).
[Crossref]

G. Scarcelli, P. Kim, and S. H. Yun, “In vivo measurement of age-related stiffening in the crystalline lens by Brillouin optical microscopy,” Biophys. J. 101(6), 1539–1545 (2011).
[Crossref]

G. Scarcelli and S. H. Yun, “Multistage VIPA etalons for high-extinction parallel Brillouin spectroscopy,” Opt. Express 19(11), 10913–10922 (2011).
[Crossref]

I. Z. Nenadic, M. W. Urban, S. Aristizabal, S. A. Mitchell, T. C. Humphrey, and J. F. Greenleaf, “On Lamb and Rayleigh wave convergence in viscoelastic tissues,” Phys. Med. Biol. 56(20), 6723–6738 (2011).
[Crossref]

Q. Ye, J. Wang, Z.-C. Deng, W.-Y. Zhou, C.-P. Zhang, and J.-G. Tian, “Measurement of the complex refractive index of tissue-mimicking phantoms and biotissue by extended differential total reflection method,” J. Biomed. Opt. 16(9), 097001 (2011).
[Crossref]

2010 (2)

J. Kwon and G. Subhash, “Compressive strain rate sensitivity of ballistic gelatin,” J. Biomech. 43(3), 420–425 (2010).
[Crossref]

H. Baradia, N. Nikahd, and A. Glasser, “Mouse lens stiffness measurements,” Exp. Eye Res. 91(2), 300–307 (2010).
[Crossref]

2008 (3)

K. R. Heys and R. J. Truscott, “The stiffness of human cataract lenses is a function of both age and the type of cataract,” Exp. Eye Res. 86(4), 701–703 (2008).
[Crossref]

G. Scarcelli and S. H. Yun, “Confocal Brillouin microscopy for three-dimensional mechanical imaging,” Nat. Photonics 2(1), 39–43 (2008).
[Crossref]

R. K. Manapuram, V. G. R. Manne, and K. V. Larin, “Development of phase-stabilized swept-source OCT for the ultrasensitive quantification of microbubbles,” Laser Phys. 18(9), 1080–1086 (2008).
[Crossref]

2007 (2)

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton Microscopy,” Biophys. J. 92(6), 2212–2222 (2007).
[Crossref]

H. A. Weeber, G. Eckert, W. Pechhold, and R. G. van der Heijde, “Stiffness gradient in the crystalline lens,” Graefe’s Arch. Clin. Exp. Ophthalmol. 245(9), 1357–1366 (2007).
[Crossref]

2005 (1)

B. Pierscionek, A. Belaidi, and H. Bruun, “Refractive index distribution in the porcine eye lens for 532 nm and 633 nm light,” Eye 19(4), 375–381 (2005).
[Crossref]

2004 (1)

K. R. Heys, S. L. Cram, and R. J. Truscott, “Massive increase in the stiffness of the human lens nucleus with age: the basis for presbyopia?” Mol. Vis. 10(114), 956–963 (2004).

2001 (1)

A. S. Vilupuru and A. Glasser, “Optical and biometric relationships of the isolated pig crystalline lens,” Oph. Physl. Opt. 21(4), 296–311 (2001).
[Crossref]

1998 (2)

A. Glasser and M. C. Campbell, “Presbyopia and the optical changes in the human crystalline lens with age,” Vision Res. 38(2), 209–229 (1998).
[Crossref]

J. Schmitt, “OCT elastography: imaging microscopic deformation and strain of tissue,” Opt. Express 3(6), 199–211 (1998).
[Crossref]

1997 (1)

T. J. Hall, M. Bilgen, M. F. Insana, and T. A. Krouskop, “Phantom materials for elastography,” IEEE Trans. Sonics Ultrason. 44(6), 1355–1365 (1997).
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1996 (1)

E. Soczkiewicz, “The penetration depth of Rayleigh surface waves,” Acustica 82, 380–382 (1996).

1995 (1)

R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman, “Magnetic-Resonance Elastography by Direct Visualization of Propagating Acoustic Strain Waves,” Science 269(5232), 1854–1857 (1995).
[Crossref]

1994 (2)

H. Tabandeh, G. M. Thompson, P. Heyworth, S. Dorey, A. J. Woods, and D. Lynch, “Water content, lens hardness and cataract appearance,” Eye 8(1), 125–129 (1994).
[Crossref]

C. De Korte, A. Van Der Steen, J. Thijssen, J. Duindam, C. Otto, and G. Puppels, “Relation between local acoustic parameters and protein distribution in human and porcine eye lenses,” Exp. Eye Res. 59(5), 617–627 (1994).
[Crossref]

1991 (2)

H. Pau and J. Kranz, “The increasing sclerosis of the human lens with age and its relevance to accommodation and presbyopia,” Graefe’s Arch. Clin. Exp. Ophthalmol. 229(3), 294–296 (1991).
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J. Ophir, I. Cespedes, H. Ponnekanti, Y. Yazdi, and X. Li, “Elastography: a quantitative method for imaging the elasticity of biological tissues,” Ultrason. Imaging 13(2), 111–134 (1991).
[Crossref]

1982 (1)

J. G. Dil, “Brillouin-Scattering in Condensed Matter,” Rep. Prog. Phys. 45(3), 285–334 (1982).
[Crossref]

1980 (1)

J. M. Vaughan and J. T. Randall, “Brillouin scattering, density and elastic properties of the lens and cornea of the eye,” Nature 284(5755), 489–491 (1980).
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Aglyamov, S.

H. Zhang, C. Wu, M. Singh, A. Nair, S. Aglyamov, and K. Larin, “Optical coherence elastography of cold cataract in porcine lens,” J. Biomed. Opt. 24(03), 1–7 (2019).
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C. Wu, Z. Han, S. Wang, J. Li, M. Singh, C. H. Liu, S. Aglyamov, S. Emelianov, F. Manns, and K. V. Larin, “Assessing age-related changes in the biomechanical properties of rabbit lens using a coaligned ultrasound and optical coherence elastography system,” Invest. Ophthalmol. Visual Sci. 56(2), 1292–1300 (2015).
[Crossref]

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett. 10(7), 075605 (2013).
[Crossref]

S. Yoon, S. Aglyamov, A. Karpiouk, and S. Emelianov, “The mechanical properties of ex vivo bovine and porcine crystalline lenses: age-related changes and location-dependent variations,” Ultrasound Med. Biol. 39(6), 1120–1127 (2013).
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Aglyamov, S. R.

C. Wu, S. R. Aglyamov, H. Zhang, and K. V. Larin, “Measuring the elastic wave velocity in the lens of the eye as a function of intraocular pressure using optical coherent elastography,” Quantum Electron. 49(1), 20–24 (2019).
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C. Wu, S. R. Aglyamov, Z. Han, M. Singh, C. H. Liu, and K. V. Larin, “Assessing the biomechanical properties of the porcine crystalline lens as a function of intraocular pressure with optical coherence elastography,” Biomed. Opt. Express 9(12), 6455–6466 (2018).
[Crossref]

S. Park, H. Yoon, K. V. Larin, S. Y. Emelianov, and S. R. Aglyamov, “The impact of intraocular pressure on elastic wave velocity estimates in the crystalline lens,” Phys. Med. Biol. 62(3), N45–N57 (2017).
[Crossref]

Z. Han, M. Singh, S. R. Aglyamov, C.-H. Liu, A. Nair, R. Raghunathan, C. Wu, J. Li, and K. V. Larin, “Quantifying tissue viscoelasticity using optical coherence elastography and the Rayleigh wave model,” J. Biomed. Opt. 21(9), 090504 (2016).
[Crossref]

M. Singh, J. Li, S. Vantipalli, S. Wang, Z. Han, A. Nair, S. R. Aglyamov, M. D. Twa, and K. V. Larin, “Noncontact Elastic Wave Imaging Optical Coherence Elastography for Evaluating Changes in Corneal Elasticity Due to Crosslinking,” IEEE J. Sel. Top. Quantum Electron. 22(3), 266–276 (2016).
[Crossref]

Ambrozinski, L.

M. A. Kirby, I. Pelivanov, S. Song, L. Ambrozinski, S. J. Yoon, L. Gao, D. Li, T. T. Shen, R. K. Wang, and M. O’Donnell, “Optical coherence elastography in ophthalmology,” J. Biomed. Opt. 22(12), 1 (2017).
[Crossref]

Aristizabal, S.

I. Z. Nenadic, M. W. Urban, S. Aristizabal, S. A. Mitchell, T. C. Humphrey, and J. F. Greenleaf, “On Lamb and Rayleigh wave convergence in viscoelastic tissues,” Phys. Med. Biol. 56(20), 6723–6738 (2011).
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Avetisov, S. E.

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, A. I. Omelchenko, O. I. Baum, S. E. Avetisov, A. V. Bolshunov, V. I. Siplivy, and D. V. Shabanov, “Optical coherence elastography for strain dynamics measurements in laser correction of cornea shape,” J. Biophotonics 10(11), 1450–1463 (2017).
[Crossref]

Baradia, H.

H. Baradia, N. Nikahd, and A. Glasser, “Mouse lens stiffness measurements,” Exp. Eye Res. 91(2), 300–307 (2010).
[Crossref]

Baum, O. I.

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, O. I. Baum, A. I. Omelchenko, D. V. Shabanov, A. A. Sovetsky, A. V. Yuzhakov, and A. A. Fedorov, “Revealing structural modifications in thermomechanical reshaping of collagenous tissues using optical coherence elastography,” J. Biophotonics 12(3), e201800250 (2019).
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V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, A. I. Omelchenko, O. I. Baum, S. E. Avetisov, A. V. Bolshunov, V. I. Siplivy, and D. V. Shabanov, “Optical coherence elastography for strain dynamics measurements in laser correction of cornea shape,” J. Biophotonics 10(11), 1450–1463 (2017).
[Crossref]

Belaidi, A.

B. Pierscionek, A. Belaidi, and H. Bruun, “Refractive index distribution in the porcine eye lens for 532 nm and 633 nm light,” Eye 19(4), 375–381 (2005).
[Crossref]

Besner, S.

S. Besner, G. Scarcelli, R. Pineda, and S. H. Yun, “In Vivo Brillouin Analysis of the Aging Crystalline Lens,” Invest. Ophthalmol. Visual Sci. 57(13), 5093–5100 (2016).
[Crossref]

Bilgen, M.

T. J. Hall, M. Bilgen, M. F. Insana, and T. A. Krouskop, “Phantom materials for elastography,” IEEE Trans. Sonics Ultrason. 44(6), 1355–1365 (1997).
[Crossref]

Bolshunov, A. V.

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, A. I. Omelchenko, O. I. Baum, S. E. Avetisov, A. V. Bolshunov, V. I. Siplivy, and D. V. Shabanov, “Optical coherence elastography for strain dynamics measurements in laser correction of cornea shape,” J. Biophotonics 10(11), 1450–1463 (2017).
[Crossref]

Browne, A. W.

Y. Li, J. Zhu, J. J. Chen, J. Yu, Z. Jin, Y. Miao, A. W. Browne, Q. Zhou, and Z. Chen, “Simultaneously imaging and quantifying in vivo mechanical properties of crystalline lens and cornea using optical coherence elastography with acoustic radiation force excitation,” APL Photonics 4(10), 106104 (2019).
[Crossref]

Bruun, H.

B. Pierscionek, A. Belaidi, and H. Bruun, “Refractive index distribution in the porcine eye lens for 532 nm and 633 nm light,” Eye 19(4), 375–381 (2005).
[Crossref]

Burau, G.

Campbell, M. C.

A. Glasser and M. C. Campbell, “Presbyopia and the optical changes in the human crystalline lens with age,” Vision Res. 38(2), 209–229 (1998).
[Crossref]

Cespedes, I.

J. Ophir, I. Cespedes, H. Ponnekanti, Y. Yazdi, and X. Li, “Elastography: a quantitative method for imaging the elasticity of biological tissues,” Ultrason. Imaging 13(2), 111–134 (1991).
[Crossref]

Chen, J. J.

Y. Li, J. Zhu, J. J. Chen, J. Yu, Z. Jin, Y. Miao, A. W. Browne, Q. Zhou, and Z. Chen, “Simultaneously imaging and quantifying in vivo mechanical properties of crystalline lens and cornea using optical coherence elastography with acoustic radiation force excitation,” APL Photonics 4(10), 106104 (2019).
[Crossref]

Chen, S. P.

X. Y. Zhang, Q. M. Wang, Z. Lyu, X. H. Gao, P. P. Zhang, H. M. Lin, Y. R. Guo, T. F. Wang, S. P. Chen, and X. Chen, “Noninvasive assessment of age-related stiffness of crystalline lenses in a rabbit model using ultrasound elastography,” Biomed. Eng. Online 17(1), 75 (2018).
[Crossref]

Chen, X.

X. Y. Zhang, Q. M. Wang, Z. Lyu, X. H. Gao, P. P. Zhang, H. M. Lin, Y. R. Guo, T. F. Wang, S. P. Chen, and X. Chen, “Noninvasive assessment of age-related stiffness of crystalline lenses in a rabbit model using ultrasound elastography,” Biomed. Eng. Online 17(1), 75 (2018).
[Crossref]

Chen, Z.

Y. Li, J. Zhu, J. J. Chen, J. Yu, Z. Jin, Y. Miao, A. W. Browne, Q. Zhou, and Z. Chen, “Simultaneously imaging and quantifying in vivo mechanical properties of crystalline lens and cornea using optical coherence elastography with acoustic radiation force excitation,” APL Photonics 4(10), 106104 (2019).
[Crossref]

Cheong, Y.

S. Choi, H. J. Lee, Y. Cheong, J. H. Shin, K. H. Jin, H. K. Park, and Y. G. Park, “AFM study for morphological characteristics and biomechanical properties of human cataract anterior lens capsules,” Scanning 34(4), 247–256 (2012).
[Crossref]

Choi, S.

S. Choi, H. J. Lee, Y. Cheong, J. H. Shin, K. H. Jin, H. K. Park, and Y. G. Park, “AFM study for morphological characteristics and biomechanical properties of human cataract anterior lens capsules,” Scanning 34(4), 247–256 (2012).
[Crossref]

Cichanski, A.

Cram, S. L.

K. R. Heys, S. L. Cram, and R. J. Truscott, “Massive increase in the stiffness of the human lens nucleus with age: the basis for presbyopia?” Mol. Vis. 10(114), 956–963 (2004).

De Korte, C.

C. De Korte, A. Van Der Steen, J. Thijssen, J. Duindam, C. Otto, and G. Puppels, “Relation between local acoustic parameters and protein distribution in human and porcine eye lenses,” Exp. Eye Res. 59(5), 617–627 (1994).
[Crossref]

De Stefano, V. S.

V. S. De Stefano, M. R. Ford, I. Seven, and W. J. Dupps, “Live human assessment of depth-dependent corneal displacements with swept-source optical coherence elastography,” PLoS One 13(12), e0209480 (2018).
[Crossref]

Deng, Z.-C.

Q. Ye, J. Wang, Z.-C. Deng, W.-Y. Zhou, C.-P. Zhang, and J.-G. Tian, “Measurement of the complex refractive index of tissue-mimicking phantoms and biotissue by extended differential total reflection method,” J. Biomed. Opt. 16(9), 097001 (2011).
[Crossref]

Dil, J. G.

J. G. Dil, “Brillouin-Scattering in Condensed Matter,” Rep. Prog. Phys. 45(3), 285–334 (1982).
[Crossref]

Dorey, S.

H. Tabandeh, G. M. Thompson, P. Heyworth, S. Dorey, A. J. Woods, and D. Lynch, “Water content, lens hardness and cataract appearance,” Eye 8(1), 125–129 (1994).
[Crossref]

Duindam, J.

C. De Korte, A. Van Der Steen, J. Thijssen, J. Duindam, C. Otto, and G. Puppels, “Relation between local acoustic parameters and protein distribution in human and porcine eye lenses,” Exp. Eye Res. 59(5), 617–627 (1994).
[Crossref]

Dupps, W. J.

V. S. De Stefano, M. R. Ford, I. Seven, and W. J. Dupps, “Live human assessment of depth-dependent corneal displacements with swept-source optical coherence elastography,” PLoS One 13(12), e0209480 (2018).
[Crossref]

Eckert, G.

H. A. Weeber, G. Eckert, W. Pechhold, and R. G. van der Heijde, “Stiffness gradient in the crystalline lens,” Graefe’s Arch. Clin. Exp. Ophthalmol. 245(9), 1357–1366 (2007).
[Crossref]

Ehman, R. L.

R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman, “Magnetic-Resonance Elastography by Direct Visualization of Propagating Acoustic Strain Waves,” Science 269(5232), 1854–1857 (1995).
[Crossref]

Emelianov, S.

C. Wu, Z. Han, S. Wang, J. Li, M. Singh, C. H. Liu, S. Aglyamov, S. Emelianov, F. Manns, and K. V. Larin, “Assessing age-related changes in the biomechanical properties of rabbit lens using a coaligned ultrasound and optical coherence elastography system,” Invest. Ophthalmol. Visual Sci. 56(2), 1292–1300 (2015).
[Crossref]

S. Yoon, S. Aglyamov, A. Karpiouk, and S. Emelianov, “The mechanical properties of ex vivo bovine and porcine crystalline lenses: age-related changes and location-dependent variations,” Ultrasound Med. Biol. 39(6), 1120–1127 (2013).
[Crossref]

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett. 10(7), 075605 (2013).
[Crossref]

Emelianov, S. Y.

S. Park, H. Yoon, K. V. Larin, S. Y. Emelianov, and S. R. Aglyamov, “The impact of intraocular pressure on elastic wave velocity estimates in the crystalline lens,” Phys. Med. Biol. 62(3), N45–N57 (2017).
[Crossref]

Fatt, I.

I. Fatt and B. A. Weissman, “The Lens,” in Physiology of the Eye, I. Fatt and B. A. Weissman, eds. (Butterworth-Heinemann, 1992), pp. 85–95.

Fedorov, A. A.

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, O. I. Baum, A. I. Omelchenko, D. V. Shabanov, A. A. Sovetsky, A. V. Yuzhakov, and A. A. Fedorov, “Revealing structural modifications in thermomechanical reshaping of collagenous tissues using optical coherence elastography,” J. Biophotonics 12(3), e201800250 (2019).
[Crossref]

Fernandez, J.

J. Fernandez, M. Rodriguez-Vallejo, J. Martinez, A. Tauste, and D. P. Pinero, “From Presbyopia to Cataracts: A Critical Review on Dysfunctional Lens Syndrome,” J. Ophthalmol. 2018, 1–10 (2018).
[Crossref]

Ford, M. R.

V. S. De Stefano, M. R. Ford, I. Seven, and W. J. Dupps, “Live human assessment of depth-dependent corneal displacements with swept-source optical coherence elastography,” PLoS One 13(12), e0209480 (2018).
[Crossref]

Gao, L.

M. A. Kirby, I. Pelivanov, S. Song, L. Ambrozinski, S. J. Yoon, L. Gao, D. Li, T. T. Shen, R. K. Wang, and M. O’Donnell, “Optical coherence elastography in ophthalmology,” J. Biomed. Opt. 22(12), 1 (2017).
[Crossref]

Gao, X. H.

X. Y. Zhang, Q. M. Wang, Z. Lyu, X. H. Gao, P. P. Zhang, H. M. Lin, Y. R. Guo, T. F. Wang, S. P. Chen, and X. Chen, “Noninvasive assessment of age-related stiffness of crystalline lenses in a rabbit model using ultrasound elastography,” Biomed. Eng. Online 17(1), 75 (2018).
[Crossref]

Gelikonov, G. V.

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, O. I. Baum, A. I. Omelchenko, D. V. Shabanov, A. A. Sovetsky, A. V. Yuzhakov, and A. A. Fedorov, “Revealing structural modifications in thermomechanical reshaping of collagenous tissues using optical coherence elastography,” J. Biophotonics 12(3), e201800250 (2019).
[Crossref]

V. Y. Zaitsev, A. L. Matveyev, L. A. Matveev, G. V. Gelikonov, A. I. Omelchenko, O. I. Baum, S. E. Avetisov, A. V. Bolshunov, V. I. Siplivy, and D. V. Shabanov, “Optical coherence elastography for strain dynamics measurements in laser correction of cornea shape,” J. Biophotonics 10(11), 1450–1463 (2017).
[Crossref]

George, S. C.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton Microscopy,” Biophys. J. 92(6), 2212–2222 (2007).
[Crossref]

Glasser, A.

H. Baradia, N. Nikahd, and A. Glasser, “Mouse lens stiffness measurements,” Exp. Eye Res. 91(2), 300–307 (2010).
[Crossref]

A. S. Vilupuru and A. Glasser, “Optical and biometric relationships of the isolated pig crystalline lens,” Oph. Physl. Opt. 21(4), 296–311 (2001).
[Crossref]

A. Glasser and M. C. Campbell, “Presbyopia and the optical changes in the human crystalline lens with age,” Vision Res. 38(2), 209–229 (1998).
[Crossref]

Graff, K. F.

K. F. Graff, Wave motion in elastic solids (Courier Corporation, 2012).

Greenleaf, J. F.

I. Z. Nenadic, M. W. Urban, S. Aristizabal, S. A. Mitchell, T. C. Humphrey, and J. F. Greenleaf, “On Lamb and Rayleigh wave convergence in viscoelastic tissues,” Phys. Med. Biol. 56(20), 6723–6738 (2011).
[Crossref]

R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman, “Magnetic-Resonance Elastography by Direct Visualization of Propagating Acoustic Strain Waves,” Science 269(5232), 1854–1857 (1995).
[Crossref]

Grodzinsky, A. J.

G. Scarcelli, W. J. Polacheck, H. T. Nia, K. Patel, A. J. Grodzinsky, R. D. Kamm, and S. H. Yun, “Noncontact three-dimensional mapping of intracellular hydromechanical properties by Brillouin microscopy,” Nat. Methods 12(12), 1132–1134 (2015).
[Crossref]

Grulkowski, I.

Guo, Y. R.

X. Y. Zhang, Q. M. Wang, Z. Lyu, X. H. Gao, P. P. Zhang, H. M. Lin, Y. R. Guo, T. F. Wang, S. P. Chen, and X. Chen, “Noninvasive assessment of age-related stiffness of crystalline lenses in a rabbit model using ultrasound elastography,” Biomed. Eng. Online 17(1), 75 (2018).
[Crossref]

Guthoff, R.

Hall, T. J.

T. J. Hall, M. Bilgen, M. F. Insana, and T. A. Krouskop, “Phantom materials for elastography,” IEEE Trans. Sonics Ultrason. 44(6), 1355–1365 (1997).
[Crossref]

Han, Z.

C. Wu, S. R. Aglyamov, Z. Han, M. Singh, C. H. Liu, and K. V. Larin, “Assessing the biomechanical properties of the porcine crystalline lens as a function of intraocular pressure with optical coherence elastography,” Biomed. Opt. Express 9(12), 6455–6466 (2018).
[Crossref]

Z. Han, M. Singh, S. R. Aglyamov, C.-H. Liu, A. Nair, R. Raghunathan, C. Wu, J. Li, and K. V. Larin, “Quantifying tissue viscoelasticity using optical coherence elastography and the Rayleigh wave model,” J. Biomed. Opt. 21(9), 090504 (2016).
[Crossref]

M. Singh, J. Li, S. Vantipalli, S. Wang, Z. Han, A. Nair, S. R. Aglyamov, M. D. Twa, and K. V. Larin, “Noncontact Elastic Wave Imaging Optical Coherence Elastography for Evaluating Changes in Corneal Elasticity Due to Crosslinking,” IEEE J. Sel. Top. Quantum Electron. 22(3), 266–276 (2016).
[Crossref]

C. Wu, Z. Han, S. Wang, J. Li, M. Singh, C. H. Liu, S. Aglyamov, S. Emelianov, F. Manns, and K. V. Larin, “Assessing age-related changes in the biomechanical properties of rabbit lens using a coaligned ultrasound and optical coherence elastography system,” Invest. Ophthalmol. Visual Sci. 56(2), 1292–1300 (2015).
[Crossref]

Heys, K. R.

K. R. Heys and R. J. Truscott, “The stiffness of human cataract lenses is a function of both age and the type of cataract,” Exp. Eye Res. 86(4), 701–703 (2008).
[Crossref]

K. R. Heys, S. L. Cram, and R. J. Truscott, “Massive increase in the stiffness of the human lens nucleus with age: the basis for presbyopia?” Mol. Vis. 10(114), 956–963 (2004).

Heyworth, P.

H. Tabandeh, G. M. Thompson, P. Heyworth, S. Dorey, A. J. Woods, and D. Lynch, “Water content, lens hardness and cataract appearance,” Eye 8(1), 125–129 (1994).
[Crossref]

Hsieh, B. Y.

B. Y. Hsieh, S. Song, T. M. Nguyen, S. J. Yoon, T. T. Shen, R. K. Wang, and M. O’Donnell, “Moving-source elastic wave reconstruction for high-resolution optical coherence elastography,” J. Biomed. Opt. 21(11), 116006 (2016).
[Crossref]

Humphrey, T. C.

I. Z. Nenadic, M. W. Urban, S. Aristizabal, S. A. Mitchell, T. C. Humphrey, and J. F. Greenleaf, “On Lamb and Rayleigh wave convergence in viscoelastic tissues,” Phys. Med. Biol. 56(20), 6723–6738 (2011).
[Crossref]

Insana, M. F.

T. J. Hall, M. Bilgen, M. F. Insana, and T. A. Krouskop, “Phantom materials for elastography,” IEEE Trans. Sonics Ultrason. 44(6), 1355–1365 (1997).
[Crossref]

Jiménez-villar, A.

Jin, K. H.

S. Choi, H. J. Lee, Y. Cheong, J. H. Shin, K. H. Jin, H. K. Park, and Y. G. Park, “AFM study for morphological characteristics and biomechanical properties of human cataract anterior lens capsules,” Scanning 34(4), 247–256 (2012).
[Crossref]

Jin, Z.

Y. Li, J. Zhu, J. J. Chen, J. Yu, Z. Jin, Y. Miao, A. W. Browne, Q. Zhou, and Z. Chen, “Simultaneously imaging and quantifying in vivo mechanical properties of crystalline lens and cornea using optical coherence elastography with acoustic radiation force excitation,” APL Photonics 4(10), 106104 (2019).
[Crossref]

Kaluzny, B. J.

Kamm, R. D.

G. Scarcelli, W. J. Polacheck, H. T. Nia, K. Patel, A. J. Grodzinsky, R. D. Kamm, and S. H. Yun, “Noncontact three-dimensional mapping of intracellular hydromechanical properties by Brillouin microscopy,” Nat. Methods 12(12), 1132–1134 (2015).
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Figures (5)

Fig. 1.
Fig. 1. Schematic of the Brillouin microscopy system. PBS: polarization beam splitter; λ/4: quarter wave plate; VIPA: VIPA spectrometer.
Fig. 2.
Fig. 2. Schematic of the OCE setup.
Fig. 3.
Fig. 3. (a) Young’s moduli of gelatin phantoms of varying concentrations (N = 3 of each concentration) obtained from mechanical testing and OCE. (b) Young’s moduli and Brillouin moduli of the gelatin phantoms as measured by OCE and Brillouin microscopy, respectively. (c) Log-log scaled correlation between the Brillouin modulus and OCE-measured Young’s modulus of the (red: 6%, green: 10%, and blue: 12%; same color dots represent different phantoms) gelatin phantoms. The slope and 95% confidence intervals are plotted as the dashed line and gray area, respectively, and are noted in the legend along with the correlation coefficient and statistical significance of the slope. Error bars represent inter-sample standard deviation in (a) and (b) and intra-sample standard deviation in (c)..
Fig. 4.
Fig. 4. (a) OCE-measured Young’s modulus and Brillouin modulus of the ex vivo porcine lenses. (b) Correlation between the Brillouin modulus and OCE-measured Young’s modulus of the porcine lenses. Data are represented as the intra-sample average, and the error bars are the intra-sample standard deviation.
Fig. 5.
Fig. 5. (a) Distribution of the derived Young’s modulus from the correlation between Brillouin and Young’s modulus along the optical axis of lens 3 from Fig. 4(a). (b) Distribution of the Young’s modulus along the optical axis of a typical lens where the error bar is the average over the local 1 mm region of (a). (c) The derived Young’s modulus of anterior, posterior and central parts averaged for all 6 lenses used in the study.

Equations (3)

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M = ρ λ 2 ω 2 4 n 2 s i n 2 ( θ 2 ) ,
E = 2 ρ ( 1 + v ) 3 ( 0.87 + 1.12 v ) 2 c g 2 ,
f a v g = i N f i w i i N w i ,