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Research Papers

Three-Dimensional Strains in Human Posterior Sclera Using Ultrasound Speckle Tracking

[+] Author and Article Information
Elias Pavlatos

Department of Biomedical Engineering,
Ohio State University,
1080 Carmack Road,
Columbus, OH 43210
e-mail: pavlatos.2@osu.edu

Benjamin Cruz Perez

Department of Biomedical Engineering,
Ohio State University,
1080 Carmack Road,
Columbus, OH 43210
e-mail: b.cruz.perez@gmail.com

Hugh J. Morris

College of Optometry,
Ohio State University,
338 West 10th Avenue,
Columbus, OH 43210
e-mail: morris.1085@osu.edu

Hong Chen

Department of Biomedical Engineering,
Ohio State University,
1080 Carmack Road,
Columbus, OH 43210
e-mail: chenhong44@gmail.com

Joel R. Palko

Department of Biomedical Engineering,
Ohio State University,
1080 Carmack Road,
Columbus, OH 43210
e-mail: joel.palko@gmail.com

Xueliang Pan

Center for Biostatistics,
Ohio State University,
1800 Cannon Drive,
Columbus, OH 43210
e-mail: jeff.pan@osumc.edu

Paul A. Weber

Department of Ophthalmology,
Ohio State University,
915 Olentangy River Road,
Columbus, OH 43212
e-mail: paul.weber@osumc.edu

Richard T. Hart

Mem. ASME
Department of Biomedical Engineering,
Ohio State University,
1080 Carmack Road,
Columbus, OH 43210
e-mail: hart.322@osu.edu

Jun Liu

Department of Biomedical Engineering,
Ohio State University,
1080 Carmack Road,
Columbus, OH 43210
e-mail: liu.314@osu.edu

1Corresponding author.

Manuscript received August 12, 2015; final manuscript received November 13, 2015; published online January 27, 2016. Editor: Victor H. Barocas.

J Biomech Eng 138(2), 021015 (Jan 27, 2016) (9 pages) Paper No: BIO-15-1405; doi: 10.1115/1.4032124 History: Received August 12, 2015; Revised November 13, 2015

Intraocular pressure (IOP) induced strains in the peripapillary sclera may play a role in glaucoma progression. Using inflation testing and ultrasound speckle tracking, the 3D strains in the peripapillary sclera were measured in nine human donor globes. Our results showed that the peripapillary sclera experienced through-thickness compression and meridional stretch during inflation, while minimal circumferential dilation was observed when IOP was increased from 10 to 19 mmHg. The maximum shear was primarily oriented in the through-thickness, meridional cross sections and had a magnitude slightly larger than the first principal strain. The tissue volume had minimal overall change, confirming near-incompressibility of the sclera. Substantial strain heterogeneity was present in the peripapillary region, with local high strain areas likely corresponding to structural heterogeneity caused by traversing blood vessels. These 3D strain characteristics provide new insights into the biomechanical responses of the peripapillary sclera during physiological increases of IOP. Future studies are needed to confirm these findings and investigate the role of these biomechanical characteristics in ocular diseases.

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Figures

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Fig. 1

Experimental setup of the human donor scleral shell measured with the Vevo 660 high-frequency ultrasound system. ONH: optic nerve head. The shell was clamped near the corneoscleral junction, away from the measured posterior sclera; and immersed in PBS. The ultrasound probe was not in contact with the tissue during scanning.

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Fig. 2

Illustration of the scanned volume (white region) on nasal side of the ONH. Y is the axial direction (direction of sound propagation), X is the lateral direction (direction perpendicular to Y in the cross-sectional plane), and Z is the elevational direction (i.e., direction of step motor translation). S: superior, N: nasal, I: inferior, T: temporal.

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Fig. 3

(a) The reconstructed 3D volume of the nasal side of a donor eye, (b) a transverse cross section of the eye showing the span of the scanning into the ONH. Acoustic signals were poor inside ONH due to attenuation from the irregular surface of the optic nerve stub and the dural sheath. The tapering of the sclera (*) was often seen, (c) a coronal cross section of the eye showing the circular scleral canal.

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Fig. 4

Principal strains at different pressures in each donor eye ((a)–(c)) and averaged over all tested eyes (d). The legend shows donor age (y.o.: years old).

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Fig. 5

Maximum shear (a) and volume ratios (b) at different pressures in each donor eye. The legend shows donor age (y.o.: years old).

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Fig. 6

Serial strain maps at 13 mmHg at different depth from the posterior surface on the temporal side of a human eye (66 years male Caucasian). The strain map is overlaid on the scanned volume cropped at the plane of strain map. The small void in the scanned volume was caused by strong acoustic shadowing from tissue debris on the specimen surface.

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Fig. 7

Low acoustic scattering regions (white arrow heads) in ultrasound B-mode images (a) were co-localized with increased first principal strains (black arrow heads) in (b). The histology of this eye (c) showed the arterial circle of Zinn-Haller (white arrows).

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Fig. 8

Strain and volume ratio maps from three representative donors. The 71-year-old had the highest average strains. The 52-year-old had the lowest average strains. The 24-year-old, the youngest donor in the tested group, is also shown. The color bars are adjusted for each individual plot to show within-specimen heterogeneity.

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Fig. 9

Vector directions (green lines) at grid points for (a) first principal, (b) second principal, and (c) third principal strains. The large orange arrows indicate (a) meridional, (b) circumferential, and (c) through-thickness directions, which align with the predominant vector directions in each plot. The grid points were down-sampled for visual clarity.

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Fig. 10

The second principal vectors in three donor eyes, consistently showing the predominant circumferential orientation

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Fig. 11

The predominant orientation of the maximum shear in the peripapillary sclera. The red arrows represent the predominant directions of the maximum (ε1) and minimum (ε3) principal strains. The maximum shear is oriented 45 deg from the principal strain vectors.

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