Direct measurements of collagen fiber recruitment in the posterior pole of the eye

DOI

10.1016/j.actbio.2023.11.013

Po-Yi Lee, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA, USA.
Gosia Fryc, Department of Chemistry, Dietrich School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA, USA.
John Gnalian, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.
Bingrui Wang, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.
Yi Hua, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA; Department of Biomedical Engineering, University of Mississippi, University, MS, USA; Department of Mechanical Engineering, University of Mississippi, University, MS, USA.
Susannah Waxman, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.
Fuqiang Zhong, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.
Bin Yang, Department of Engineering, Rangos School of Health Sciences, Duquesne University, Pittsburgh, PA, USA.
Ian A. Sigal, Department of Ophthalmology, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA, USA. Electronic address: ian@OcularBiomechanics.com.

Document Type

Journal Article

Publication Date

11-14-2023

Publication Title

Acta biomaterialia

Keywords

Collagen, Crimp, Polarized light microscopy, Posterior pole, Recruitment

Abstract

Collagen is the main load-bearing component of the peripapillary sclera (PPS) and lamina cribrosa (LC) in the eye. Whilst it has been shown that uncrimping and recruitment of the PPS and LC collagen fibers underlies the macro-scale nonlinear stiffening of both tissues with increased intraocular pressure (IOP), the uncrimping and recruitment as a function of local stretch have not been directly measured. This knowledge is crucial to understanding their functions in bearing loads and maintaining tissue integrity. In this project we measured local stretch-induced collagen fiber bundle uncrimping and recruitment curves of the PPS and LC. Thin coronal samples of PPS and LC of sheep eyes were mounted and stretched biaxially quasi-statically using a custom system. At each step, we imaged the PPS and LC with instant polarized light microscopy and quantified pixel-level (1.5 μm/pixel) collagen fiber orientations. We used digital image correlation to measure the local stretch and quantified collagen crimp by the circular standard deviation of fiber orientations, or waviness. Local stretch-recruitment curves of PPS and LC approximated sigmoid functions. PPS recruited more fibers than the LC at the low levels of stretch. At 10% stretch the curves crossed with 75% bundles recruited. The PPS had higher uncrimping rate and waviness remaining after recruitment than the LC: 0.9º vs. 0.6º and 3.1º vs. 2.7º. Altogether our findings support describing fiber recruitment of both PPS and LC with sigmoid curves, with the PPS recruiting faster and at lower stretch than the LC, consistent with a stiffer tissue. STATEMENT OF SIGNIFICANCE: Peripapillary sclera (PPS) and lamina cribrosa (LC) collagen recruitment behaviors are central to the nonlinear mechanical behavior of the posterior pole of the eye. How PPS and LC collagen fibers recruit under stretch is crucial to develop constitutive models of the tissues but remains unclear. We used image-based stretch testing to characterize PPS and LC collagen fiber bundle recruitment under local stretch. We found that fiber-level stretch-recruitment curves of PPS and LC approximated sigmoid functions. PPS recruited more fibers at a low stretch, but at 10% bundle stretch the two curves crossed with 75% bundles recruited. We also found that PPS and LC fibers had different uncrimping rates and non-zero waviness's when recruited.

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