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Novel method using 3-dimensional segmentation in spectral domain-optical coherence tomography imaging in the chick reveals defocus-induced regional and time-sensitive asymmetries in the choroidal thickness

Published online by Cambridge University Press:  01 August 2016

DIANE R. NAVA ,
BHAVNA ANTONY ,
LI ZHANG ,
MICHAEL D. ABRÀMOFF  and
CHRISTINE F. WILDSOET
DIANE R. NAVA*
Affiliation:
Vision Science Group, University of California Berkeley, Berkeley, California, United States of America
BHAVNA ANTONY
Affiliation:
Department of Engineering and Computer Science, University of Iowa, Iowa City, Iowa, United States of America
LI ZHANG
Affiliation:
Department of Engineering and Computer Science, University of Iowa, Iowa City, Iowa, United States of America
MICHAEL D. ABRÀMOFF
Affiliation:
Department of Engineering and Computer Science, University of Iowa, Iowa City, Iowa, United States of America Department of Ophthalmology and Visual Sciences, University of Iowa, Iowa City, Iowa, United States of America
CHRISTINE F. WILDSOET
Affiliation:
Vision Science Group, University of California Berkeley, Berkeley, California, United States of America School of Optometry, University of California Berkeley, Berkeley, California, United States of America
*
*Address correspondence to: Diane R. Nava, 17 Rue Moreau, 75012 Paris France. E-mail: diane.nava@gmail.com
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Abstract

Studies into the mechanisms underlying the active emmetropization process by which neonatal refractive errors are corrected, have described rapid, compensatory changes in the thickness of the choroidal layer in response to imposed optical defocus. While high frequency A-scan ultrasonography, as traditionally used to characterize such changes, offers good resolution of central (on-axis) changes, evidence of local retinal control mechanisms make it imperative that more peripheral, off-axis changes also be tracked. In this study, we used in vivo high resolution spectral domain-optical coherence tomography (SD-OCT) imaging in combination with the Iowa Reference Algorithms for 3-dimensional segmentation, to more fully characterize these changes, both spatially and temporally, in young, 7-day old chicks (n = 15), which were fitted with monocular +15 D defocusing lenses to induce choroidal thickening. With these tools, we were also able to localize the retinal area centralis, which was used as a landmark along with the ocular pectin in standardizing the location of scans and aligning them for subsequent analyses of choroidal thickness (CT) changes across time and between eyes. Values were derived for each of four quadrants, centered on the area centralis, and global CT values were also derived for all eyes. Data were compared with on-axis changes measured using ultrasonography. There were significant on-axis choroidal thickening that was detected after just one day of lens wear (∼190 µm), and regional (quadrant-related) differences in choroidal responses were also found, as well as global thickness changes 1 day after treatment. The ratio of global to on-axis choroidal thicknesses, used as an index of regional variability in responses, was also found to change significantly, reflecting the significant central changes. In summary, we demonstrated in vivo high resolution SD-OCT imaging, used in combination with segmentation algorithms, to be a viable and informative approach for characterizing regional (spatial), time-sensitive changes in CT in small animals such as the chick.

Keywords

ChoroidArea centralisSD-OCT imagingChickEmmetropizationEye growth
Type
Research Article
Information
Visual Neuroscience , Volume 33 , 2016 , E010
Copyright
Copyright © Cambridge University Press 2016 

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References

Abràmoff, M.D., Garvin, M.K. & Sonka, M. (2010). Retinal imaging and image analysis. IEEE Reviews in Biomedical Engineering 3, 169–208.Google Scholar
Agawa, T., Miura, M., Ikuno, Y., Makita, S., Fabritius, T., Iwasaki, T., Goto, H., Nishida, K. & Yasuno, Y. (2011). Choroidal thickness measurement in healthy Japanese subjects by three-dimensional high-penetration optical coherence tomography. Graefe’s Archive for Clinical and Experimental Ophthalmology 249, 1485–1492.CrossRefGoogle ScholarPubMed
Aller, T.A. & Wildsoet, C. (2008). Bifocal soft contact lenses as a possible myopia control treatment: A case report involving identical twins. Clinical and Experimental Optometry 91, 394–399.Google Scholar
Atchison, D.A., Jones, C.E., Schmid, K.L., Pritchard, N., Pope, J.M., Strugnell, W.E. & Riley, R.A. (2004). Eye shape in emmetropia and myopia. Investigative Opthalmology & Visual Science 45, 3380–3386.Google Scholar
Atchison, D.A., Pritchard, N., Schmid, K.L., Scott, D.H., Jones, C.E. & Pope, J.M. (2005). Shape of the retinal surface in emmetropia and myopia. Investigative Opthalmology & Visual Science 46, 2698–2707.Google Scholar
Bitzer, M. & Schaeffel, F. (2004). Effects of quisqualic acid on retinal ZENK expression induced by imposed defocus in the chick eye. Optometry and Vision Science 81, 127–136.Google Scholar
Diether, S. & Schaeffel, F. (1997). Local changes in eye growth induced by imposed local refractive error despite active accommodation. Vision Research 37, 659–668.CrossRefGoogle ScholarPubMed
Ehrlich, D. (1981). Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. The Journal of Comparative Neurology 195, 643–657.Google Scholar
Fitzgerald, M.E.C., Wildsoet, C.F. & Reiner, A. (2002). Temporal relationship of choroidal blood flow and thickness changes during recovery from form deprivation myopia in chicks. Experimental Eye Research 74, 561–570.Google Scholar
Garvin, M.K., Abràmoff, M.D., Wu, X., Russell, S.R., Burns, T.L. & Sonka, M. (2009). Automated 3-D intraretinal layer segmentation of macular spectral-domain optical coherence tomography images. IEEE Transactions on Medical Imaging 28, 1436–1447.Google Scholar
Guggenheim, J.A., Chen, Y.P., Yip, E., Hayet, H., Druel, V., Wang, L., Erichsen, J.T., Tumlinson, A.R., Povazay, B., Drexler, W. & Hocking, P.M. (2011). Pre-treatment choroidal thickness is not predictive of susceptibility to form-deprivation myopia in chickens. Ophthalmic and Physiological Optics 31, 516–528.Google Scholar
Howlett, M.H.C. & McFadden, S.A. (2009). Spectacle lens compensation in the pigmented guinea pig. Vision Research 49, 219–227.CrossRefGoogle ScholarPubMed
Jia, Y., Bailey, S.T., Hwang, T.S., McClintic, S.M., Gao, S.S., Pennesi, M.E., Flaxel, C.J., Lauer, A.K., Wilson, D.J., Hornegger, J., Fujimoto, J.G. & Huang, D. (2015). Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye. Proceedings of the National Academy of Sciences 112, E2395–E2402.Google Scholar
Junghans, B.M., Liang, H., Crewther, S.G. & Crewther, D.P. (1999). A role for choroidal lymphatics during recovery from form Deprivation myopia? Optometry and Vision Science 76, 796.Google Scholar
Kiernan, D.F., Mieler, W.F. & Hariprasad, S.M. (2010). Spectral-domain optical coherence tomography: A comparison of modern high-resolution retinal imaging systems. American Journal of Ophthalmology 149, 18–31.Google Scholar
Lan, W., Feldkaemper, M. & Schaeffel, F. (2013). Bright light induces choroidal thickening in chickens. Optometry and Vision Science 90, 1199–1206.Google Scholar
Lee, K., Niemeijer, M., Garvin, M.K., Kwon, Y.H., Sonka, M. & Abràmoff, M.D. (2009). Segmentation of the optic disc in 3D-OCT scans of the optic nerve head. IEEE Transactions on Image Processing 29, 159–168.Google Scholar
Liu, Y. & Wildsoet, C. (2011). The effect of two-zone concentric bifocal spectacle lenses on refractive error development and eye growth in young chicks. Investigative Opthalmology & Visual Science 52, 1078–1086.Google Scholar
Maier, F.M., Howland, H.C., Ohlendorf, A., Wahl, S. & Schaeffel, F. (2015). Lack of oblique astigmatism in the chicken eye. Vision Research 109, 68–76.Google Scholar
Margolis, R. & Spaide, R.F. (2009). A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. American Journal of Ophthalmology 147, 811–815.Google Scholar
Mcbrien, N.A., Young, T.L., Pang, C.P., Hammond, C., Baird, P., Saw, S., Morgan, I.G., Mutti, D.O., Rose, K.A., Wallman, J., Gentle, A., Wildsoet, C.F., Gwiazda, J., Schmid, K.L., Smith, E., Troilo, D., Summers-Rada, J., Norton, T., Schaeffel, F., Megaw, P., Beuerman, R.W., Mcfadden, S.A. & Rose, K.A. (2009). Myopia: Recent advances in molecular studies; prevalence, progression and risk factors; emmetropization; therapies; optical links; peripheral refraction; sclera and ocular growth; signalling cascades; and animal models. Optometry and Vision Science 86, 45–66.CrossRefGoogle Scholar
Moayed, A.A., Hariri, S., Song, E.S., Choh, V. & Bizheva, K. (2011). In vivo volumetric imaging of chicken retina with ultrahigh-resolution spectral domain optical coherence tomography. Biomedical Optics Express 2, 1268–1274.Google Scholar
Morris, V.B. (1982). An afoveate area centralis in the chick retina. The Journal of Comparative Neurology 210, 198–203.Google Scholar
Mutti, D.O., Hayes, J.R., Mitchell, G.L., Jones, L.A., Moeschberger, M.L., Cotter, S.A., Kleinstein, R.N., Manny, R.E., Twelker, J.D., Zadnik, K. & Study, C. (2007). Refractive error before and after the onset of myopia. Investigative Opthalmology & Visual Science, 48(6), 2510–2519.Google Scholar
Nava, D., Chang, A., Ostrin, L., Chen, Z. & Wildsoet, C. (2013). Neurochemical Ablation of Peripheral Glucagonergic Amacrine Cells in the Chick Retina and its Effects on Axial Eye Growth and Refractive Error. Investigative Ophthalmology & Visual Science e-abstract, 54(15), 4037.Google Scholar
Nava, D., Hammond, D.S. & Wildsoet, C.F. (2012). High Resolution Measurements of Quisqualate-induced Retinal and Ocular Growth Changes. Investigative Ophthalmology & Visual Science e-abstract, 53(14), 3438.Google Scholar
Nickla, D.L. & Wallman, J. (2010). The multifunctional choroid. Progress in Retinal and Eye Research 29, 144–168.CrossRefGoogle ScholarPubMed
Nickla, D.L., Wildsoet, C. & Wallman, J. (1998). Visual influences on diurnal rhythms in ocular length and choroidal thickness in chick eyes. Experimental Eye Research 66, 163–181.CrossRefGoogle ScholarPubMed
Norton, T.T., Essinger, J.A. & McBrien, N.A. (1994). Lid-suture myopia in tree shrews with retinal ganglion cell blockade. Visual Neuroscience 11, 143–153.Google Scholar
Read, S.A., Collins, M.J. & Sander, B.P. (2010). Human optical axial length and defocus. Investigative Opthalmology & Visual Science 51, 6262–6269.Google Scholar
Schaeffel, F., Glasser, A. & Howland, H.C. (1988). Accommodation, refractive error and eye growth in chickens. Vision Research 28, 639–657.Google Scholar
Schaeffel, F., Troilo, D., Wallman, J. & Howland, H.C. (1990). Developing eyes that lack accommodation grow to compensate for imposed defocus. Visual Neuroscience 4, 177–183.Google Scholar
Siegwart, J.T. & Norton, T.T. (1998). The susceptible period for deprivation-induced myopia in tree shrew. Vision Research 38, 3505–3515.Google Scholar
Smith, E.L. (2013). Optical treatment strategies to slow myopia progression: Effects of the visual extent of the optical treatment zone. Experimental Eye Research 114, 1–12.Google Scholar
Smith, E.L., Kee, C-S., Ramamirtham, R., Qiao-Grider, Y. & Hung, L-F. (2005). Peripheral vision can influence eye growth and refractive development in infant monkeys. Investigative Opthalmology & Visual Science 46, 3965–3972.Google Scholar
Smith, E.L., Ramamirtham, R., Qiao-Grider, Y., Hung, L-F., Huang, J., Kee, C., Coats, D. & Paysse, E. (2007). Effects of foveal ablation on emmetropization and form-deprivation myopia. Investigative Opthalmology & Visual Science 48, 3914–3922.Google Scholar
Troilo, D., Nickla, D.L. & Wildsoet, C.F. (2000). Choroidal thickness changes during altered eye growth and refractive state a primate. Investigative Opthalmology & Visual Science 41, 1249–1258.Google Scholar
Wallman, J. & Adams, J.I. (1987). Developmental aspects of experimental myopia in chicks: Susceptibility, recovery and relation to emmetropization. Vision Research 27, 1139–1163.CrossRefGoogle ScholarPubMed
Wallman, J., Gottlieb, M.D., Rajaram, V. & Fugate-Wentzek, L.A. (1987). Local retinal regions control local eye growth and myopia. Science 237, 73–77.Google Scholar
Wallman, J., Wildsoet, C., Xu, A., Gottlieb, M.D., Nickla, D.L., Marran, L., Krebs, W. & Christensen, A.M. (1995). Moving the retina: Choroidal modulation of refractive state. Vision Research 35, 37–50.Google Scholar
Wildsoet, C. (2003). Neural pathways subserving negative lens-induced emmetropization in chicks—Insights from selective lesions of the optic nerve and ciliary nerve. Current Eye Research 27, 371–385.Google Scholar
Wildsoet, C. & Wallman, J. (1995). Choroidal and scleral mechanisms of compensation for spectacle lenses in chicks. Vision Research 35, 1175–1194.Google Scholar
Wildsoet, C.F. & Pettigrew, J.D. (1988). Kainic acid-induced eye enlargement in chickens: Differential effects on anterior and posterior segments. Investigative Opthalmology & Visual Science 29, 311–319.Google Scholar
Zeng, G., Bowrey, H.E., Fang, J., Qi, Y. & McFadden, S.A. (2013). The development of eye shape and the origin of lower field myopia in the guinea pig eye. Vision Research 76, 77–88.Google Scholar
Zhang, L., Buitendijk, G.H.S., Lee, K., Sonka, M., Springelkamp, H., Hofman, A., Vingerling, J.R., Mullins, R.F., Klaver, C.C.W. & Abràmoff, M.D. (2015). Validity of automated choroidal segmentation in SS-OCT and SD-OCT. Investigative Opthalmology & Visual Science 56, 3202.Google Scholar
Zhang, L., Lee, K., Niemeijer, M., Mullins, R.F., Sonka, M. & Abràmoff, M.D. (2012). Automated segmentation of the choroid from clinical SD-OCT. Investigative Opthalmology & Visual Science 53, 7510–7519.Google Scholar
Zhang, L., Sonka, M., Folk, J.C., Russell, S.R. & Abràmoff, M.D. (2014). Quantifying disrupted outer retinal-subretinal layer in SD-OCT images in choroidal neovascularization. Investigative Opthalmology & Visual Science 55, 2329–2335.Google Scholar
Zhang, Y. & Wildsoet, C. (2015). RPE and choroid mechanisms underlying ocular growth and myopia. Progress in Molecular Biology and Translational Science 134, 219–240.Google ScholarPubMed
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