Polarization microscopy for characterizing fiber orientation of ocular tissues

Jan, Ning-Jiun; Grimm, J.; Tran, Hoang; Lathrop, Kira L.; Wollstein, Gadi; Bilonick, Richard A.; Ishikawa, Hiroshi; Kagemann, Larry; Schuman, Joel S.; Sigal, Ian A.

doi:10.1364/boe.6.004705

Cited by 85 publications

(155 citation statements)

References 56 publications

(68 reference statements)

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“…This non-linearity in the response to IOP is largely due to the mechanics of the collagen fibers within the ocular tissues of the sclera and cornea, a result of their microstructure (Jan et al, 2015; Sigal and Ethier, 2009). Much effort within the ocular biomechanics community has gone into measuring the non-linear material properties of the eye in order to better characterize how various parts of the eye, particularly the optic nerve head and lamina cribrosa, deform both under small deviations from physiological IOP and large deviations (Coudrillier et al, 2013; Girard et al, 2009; Grytz et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Whole-globe biomechanics using high-field MRI

Voorhees

Jan

et al. 2017

Experimental Eye Research

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The eye is a complex structure composed of several interconnected tissues acting together, across the whole globe, to resist deformation due to intraocular pressure (IOP). However, most work in the ocular biomechanics field only examines the response to IOP over smaller regions of the eye. We used high-field MRI to measure IOP induced ocular displacements and deformations over the whole globe. Seven sheep eyes were obtained from a local abattoir and imaged within 48 hours using MRI at multiple levels of IOP. IOP was controlled with a gravity perfusion system and a cannula inserted into the anterior chamber. T2-weighted imaging was performed to the eyes serially at 0 mmHg, 10 mmHg, 20 mmHg and 40 mmHg of IOP using a 9.4 Tesla MRI scanner. Manual morphometry was conducted using 3D visualization software to quantify IOP-induced effects at the globe scale (e.g. axial length and equatorial diameters) or optic nerve head scale (e.g. canal diameter, peripapillary sclera bowing). Measurement sensitivity analysis was conducted to determine measurement precision. High-field MRI revealed an outward bowing of the posterior sclera and anterior bulging of the cornea due to IOP elevation. Increments in IOP from 10 to 40 mmHg caused measurable increases in axial length in 6 of 7 eyes of 7.9±5.7% (mean±SD). Changes in equatorial diameter were minimal, 0.4±1.2% between 10 and 40 mmHg, and in all cases less than the measurement sensitivity. The effects were nonlinear, with larger deformations at normal IOPs (10–20mmHg) than at elevated IOPs (20–40mmHg). IOP also caused measurable increases in the nasal-temporal scleral canal diameter of 13.4±9.7% between 0 and 20 mmHg, but not in the superior-inferior diameter. This study demonstrates that high-field MRI can be used to visualize and measure simultaneously the effects of IOP over the whole globe, including the effects on axial length and equatorial diameter, posterior sclera displacement and bowing, and even changes in scleral canal diameter. The fact that the equatorial diameter did not change with IOP, in agreement with previous studies, indicates that a fixed boundary condition is a reasonable assumption for half globe inflation tests and computational models. Our results demonstrate the potential of high-field MRI to contribute to understanding ocular biomechanics, and specifically of the effects of IOP in large animal models.

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Section: Discussionmentioning

confidence: 99%

Whole-globe biomechanics using high-field MRI

Voorhees

Jan

et al. 2017

Experimental Eye Research

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“…Fibrillar collagens are highly bright second harmonic generator, and can be considered as periodic and ordered nanostructures able to altering the propagation of polarized light by exhibiting nonlinear optical properties [43]. Many polarized light-based techniques are disponible to studying collagen fibers, including polarizing microscopy [44].…”

Section: Discussionmentioning

confidence: 99%

Supra-organization and optical anisotropies of the extracellular matrix in the amniotic membrane and limbal stroma before and after explant culture

Valdetaro¹,

Aldrovani²,

Padua³

et al. 2016

Biomed. Opt. Express

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Abstract:In this research we evaluated the supramolecular organizations and the optical anisotropical properties of the de-epithelialized human amniotic membrane and rabbit limbal stroma, before and after explant culture. Birefringence, monochromatic light spectral absorption and linear dichroism of the main extracellular matrix biopolymers, that is, the fibrillar collagens and proteoglycans, were investigated by polarized light microscopy combined with image analysis. Our results demonstrated that the culture procedure-induced stimuli altered the supra-organizational characteristics (in terms of collagens/proteoglycans spatial orientation and ordered-aggregational state) of the amniotic and limbal extracellular matrix, which led to changes in optical anisotropical properties. and extracellular matrix alignment on human mesenchymal stem cells invasion into decellularized engineered tissues," J. Tissue Eng. Regen. Med. 9(5), 605-618 (2015). 10. E. Mattia and S. Otto, "Supramolecular systems chemistry," Nat. Nanotechnol. 10(2), 111-119 (2015). 11. P. Rifes and S. Thorsteinsdóttir, "Extracellular matrix assembly and 3D organization during paraxial mesoderm development in the chick embryo," Dev. Biol. 368(2), 370-381 (2012). 12. K. Burridge and M. Chrzanowska-Wodnicka, "Focal adhesions, contractility, and signaling," Annu. Rev. Cell Dev. Biol. 12(1), 463-519 (1996).

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“…All histological methodology has been described elsewhere [21, 22]. Briefly, eyes were pressure fixed via cannulation through the anterior chamber at 5 mmHg with a gravity column and bath of 10% formalin overnight.…”

Section: Methodsmentioning

confidence: 99%

“…It should be noted that the tissue was neither stained nor dehydrated. We have demonstrated our tissue processing protocol including formalin fixation and sectioning generally preserves both the shape and size of ocular tissues [21]. …”

Section: Methodsmentioning

confidence: 99%

Effects of collagen microstructure and material properties on the deformation of the neural tissues of the lamina cribrosa

2017

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It is widely considered that intraocular pressure (IOP)-induced deformation within the neural tissue pores of the lamina cribrosa (LC) contributes to neurodegeneration and glaucoma. Our goal was to study how the LC microstructure and mechanical properties determine the mechanical insult to the neural tissues within the pores of the LC. Polarized light microscopy was used to measure the collagen density and orientation in histology sections of three sheep optic nerve heads (ONH) at both mesoscale (4.4 µm) and microscale (0.73 µm) resolutions. Mesoscale fiber-aware FE models were first used to calculate ONH deformations at an IOP of 30 mmHg. The results were then used as boundary conditions for microscale models of LC regions. Models predicted large insult to the LC neural tissues, with 95th percentile 1st principal strains ranging from 7–12%. Pores near the scleral boundary suffered significantly higher stretch compared to pores in more central regions (10.0 ± 1.4% vs. 7.2 ± 0.4%; p=0.014; mean ± SD). Variations in material properties altered the minimum, median, and maximum levels of neural tissue insult but largely did not alter the patterns of pore-to-pore variation, suggesting these patterns are determined by the underlying structure and geometry of the LC beams and pores. To the best of our knowledge, this is the first computational model that reproduces the highly heterogeneous neural tissue strain fields observed experimentally.

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Polarization microscopy for characterizing fiber orientation of ocular tissues

Cited by 85 publications

References 56 publications

Whole-globe biomechanics using high-field MRI

Whole-globe biomechanics using high-field MRI

Supra-organization and optical anisotropies of the extracellular matrix in the amniotic membrane and limbal stroma before and after explant culture

Effects of collagen microstructure and material properties on the deformation of the neural tissues of the lamina cribrosa

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