Quantitative mapping of collagen fiber orientation in non-glaucoma and glaucoma posterior human sclerae

Jacek K. Pijanka, Baptiste Coudrillier, Kimberly Ziegler, Thomas Sorensen, Keith M. Meek, Thao D. Nguyen, Harry A Quigley, Craig Boote

Research output: Contribution to journalArticle

Abstract

Purpose. The posterior sclera has a major biomechanical influence on the optic nerve head, and may therefore be important in glaucoma. Scleral material properties are influenced significantly by collagen fiber architecture. Here we quantitatively map fiber orientation in non-glaucoma and glaucoma posterior human sclerae. Methods. Wide-angle x-ray scattering quantified fiber orientation at 0.5-mm intervals across seven non-glaucoma post-mortem human sclerae, and five sclerae with glaucoma history and confirmed axon loss. Multiphoton microscopy provided semiquantitative depth-profiling in the peripapillary sclera. Results. Midposterior fiber orientation was either uniaxial (one preferred direction) or biaxial (two directions). The peripapillary sclera was characterized by a ring of fibers located mainly in the mid-/outer stromal depth and encompassing ~50% of the total tissue thickness. Fiber anisotropy was 37% higher in the peripapillary sclera compared with midposterior, varied up to 4-fold with position around the scleral canal, and was consistently lowest in the superior-nasal quadrant. Mean fiber anisotropy was significantly lower in the superior-temporal (P <0.01) and inferior-nasal (P <0.05) peripapillary scleral quadrants in glaucoma compared with non-glaucoma eyes. Conclusions. The collagen fiber architecture of the posterior human sclera is highly anisotropic and inhomogeneous. Regional differences in peripapillary fiber anisotropy between non-glaucoma and glaucoma eyes may represent adaptive changes in response to elevated IOP and/or glaucoma, or baseline structural properties that associate with predisposition to glaucomatous axon damage. Quantitative fiber orientation data will benefit numerical eye models aimed at predicting the sclera's influence on nerve head biomechanics, and thereby its possible role in glaucoma.

Original languageEnglish (US)
Pages (from-to)5258-5270
Number of pages13
JournalInvestigative Ophthalmology and Visual Science
Volume53
Issue number9
DOIs
StatePublished - Aug 2012

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Sclera
Glaucoma
Collagen
Anisotropy
Nose
Axons
Optic Disk
Biomechanical Phenomena
Microscopy
X-Rays

ASJC Scopus subject areas

  • Ophthalmology
  • Sensory Systems
  • Cellular and Molecular Neuroscience
  • Medicine(all)

Cite this

Pijanka, J. K., Coudrillier, B., Ziegler, K., Sorensen, T., Meek, K. M., Nguyen, T. D., ... Boote, C. (2012). Quantitative mapping of collagen fiber orientation in non-glaucoma and glaucoma posterior human sclerae. Investigative Ophthalmology and Visual Science, 53(9), 5258-5270. https://doi.org/10.1167/iovs.12-9705

Quantitative mapping of collagen fiber orientation in non-glaucoma and glaucoma posterior human sclerae. / Pijanka, Jacek K.; Coudrillier, Baptiste; Ziegler, Kimberly; Sorensen, Thomas; Meek, Keith M.; Nguyen, Thao D.; Quigley, Harry A; Boote, Craig.

In: Investigative Ophthalmology and Visual Science, Vol. 53, No. 9, 08.2012, p. 5258-5270.

Research output: Contribution to journalArticle

Pijanka, Jacek K. ; Coudrillier, Baptiste ; Ziegler, Kimberly ; Sorensen, Thomas ; Meek, Keith M. ; Nguyen, Thao D. ; Quigley, Harry A ; Boote, Craig. / Quantitative mapping of collagen fiber orientation in non-glaucoma and glaucoma posterior human sclerae. In: Investigative Ophthalmology and Visual Science. 2012 ; Vol. 53, No. 9. pp. 5258-5270.
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abstract = "Purpose. The posterior sclera has a major biomechanical influence on the optic nerve head, and may therefore be important in glaucoma. Scleral material properties are influenced significantly by collagen fiber architecture. Here we quantitatively map fiber orientation in non-glaucoma and glaucoma posterior human sclerae. Methods. Wide-angle x-ray scattering quantified fiber orientation at 0.5-mm intervals across seven non-glaucoma post-mortem human sclerae, and five sclerae with glaucoma history and confirmed axon loss. Multiphoton microscopy provided semiquantitative depth-profiling in the peripapillary sclera. Results. Midposterior fiber orientation was either uniaxial (one preferred direction) or biaxial (two directions). The peripapillary sclera was characterized by a ring of fibers located mainly in the mid-/outer stromal depth and encompassing ~50{\%} of the total tissue thickness. Fiber anisotropy was 37{\%} higher in the peripapillary sclera compared with midposterior, varied up to 4-fold with position around the scleral canal, and was consistently lowest in the superior-nasal quadrant. Mean fiber anisotropy was significantly lower in the superior-temporal (P <0.01) and inferior-nasal (P <0.05) peripapillary scleral quadrants in glaucoma compared with non-glaucoma eyes. Conclusions. The collagen fiber architecture of the posterior human sclera is highly anisotropic and inhomogeneous. Regional differences in peripapillary fiber anisotropy between non-glaucoma and glaucoma eyes may represent adaptive changes in response to elevated IOP and/or glaucoma, or baseline structural properties that associate with predisposition to glaucomatous axon damage. Quantitative fiber orientation data will benefit numerical eye models aimed at predicting the sclera's influence on nerve head biomechanics, and thereby its possible role in glaucoma.",
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AU - Meek, Keith M.

AU - Nguyen, Thao D.

AU - Quigley, Harry A

AU - Boote, Craig

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N2 - Purpose. The posterior sclera has a major biomechanical influence on the optic nerve head, and may therefore be important in glaucoma. Scleral material properties are influenced significantly by collagen fiber architecture. Here we quantitatively map fiber orientation in non-glaucoma and glaucoma posterior human sclerae. Methods. Wide-angle x-ray scattering quantified fiber orientation at 0.5-mm intervals across seven non-glaucoma post-mortem human sclerae, and five sclerae with glaucoma history and confirmed axon loss. Multiphoton microscopy provided semiquantitative depth-profiling in the peripapillary sclera. Results. Midposterior fiber orientation was either uniaxial (one preferred direction) or biaxial (two directions). The peripapillary sclera was characterized by a ring of fibers located mainly in the mid-/outer stromal depth and encompassing ~50% of the total tissue thickness. Fiber anisotropy was 37% higher in the peripapillary sclera compared with midposterior, varied up to 4-fold with position around the scleral canal, and was consistently lowest in the superior-nasal quadrant. Mean fiber anisotropy was significantly lower in the superior-temporal (P <0.01) and inferior-nasal (P <0.05) peripapillary scleral quadrants in glaucoma compared with non-glaucoma eyes. Conclusions. The collagen fiber architecture of the posterior human sclera is highly anisotropic and inhomogeneous. Regional differences in peripapillary fiber anisotropy between non-glaucoma and glaucoma eyes may represent adaptive changes in response to elevated IOP and/or glaucoma, or baseline structural properties that associate with predisposition to glaucomatous axon damage. Quantitative fiber orientation data will benefit numerical eye models aimed at predicting the sclera's influence on nerve head biomechanics, and thereby its possible role in glaucoma.

AB - Purpose. The posterior sclera has a major biomechanical influence on the optic nerve head, and may therefore be important in glaucoma. Scleral material properties are influenced significantly by collagen fiber architecture. Here we quantitatively map fiber orientation in non-glaucoma and glaucoma posterior human sclerae. Methods. Wide-angle x-ray scattering quantified fiber orientation at 0.5-mm intervals across seven non-glaucoma post-mortem human sclerae, and five sclerae with glaucoma history and confirmed axon loss. Multiphoton microscopy provided semiquantitative depth-profiling in the peripapillary sclera. Results. Midposterior fiber orientation was either uniaxial (one preferred direction) or biaxial (two directions). The peripapillary sclera was characterized by a ring of fibers located mainly in the mid-/outer stromal depth and encompassing ~50% of the total tissue thickness. Fiber anisotropy was 37% higher in the peripapillary sclera compared with midposterior, varied up to 4-fold with position around the scleral canal, and was consistently lowest in the superior-nasal quadrant. Mean fiber anisotropy was significantly lower in the superior-temporal (P <0.01) and inferior-nasal (P <0.05) peripapillary scleral quadrants in glaucoma compared with non-glaucoma eyes. Conclusions. The collagen fiber architecture of the posterior human sclera is highly anisotropic and inhomogeneous. Regional differences in peripapillary fiber anisotropy between non-glaucoma and glaucoma eyes may represent adaptive changes in response to elevated IOP and/or glaucoma, or baseline structural properties that associate with predisposition to glaucomatous axon damage. Quantitative fiber orientation data will benefit numerical eye models aimed at predicting the sclera's influence on nerve head biomechanics, and thereby its possible role in glaucoma.

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