Journal of Elasticity

, Volume 129, Issue 1–2, pp 171–195 | Cite as

Multi-scale Modeling of Vision-Guided Remodeling and Age-Dependent Growth of the Tree Shrew Sclera During Eye Development and Lens-Induced Myopia

  • Rafael GrytzEmail author
  • Mustapha El Hamdaoui


The sclera uses unknown mechanisms to match the eye’s axial length to its optics during development, producing eyes with good focus (emmetropia). A myopic eye is too long for its own optics. We propose a multi-scale computational model to simulate eye development based on the assumption that scleral growth is controlled by genetic factors while scleral remodeling is driven by genetic factors and the eye’s refractive error. We define growth as a mechanism that changes the tissue volume and mass while remodeling involves internal micro-deformations that are volume-preserving at the macro-scale. The model was fitted against longitudinal refractive measurements in tree shrews of different ages and exposed to three different visual conditions: (i) normal development; (ii) negative lens wear to induce myopia; and (iii) recovery from myopia by removing the negative lens. The model was able to replicate the age- and vision-dependent response of the tree shrew experiments. Scleral growth ceased at younger age than scleral remodeling. The remodeling rate decreased as the eye emmetropized but increased at any age when a negative lens was put on. The predictive power of the model was investigated by calculating the susceptibility to scleral remodeling and the response to form deprivation myopia in tree shrews. Both predictions were in good agreement with experimental data that were not used to fit the model. We propose the first model that distinguishes scleral growth from remodeling. The good agreement of our results with experimental data supports the notion that scleral growth and scleral remodeling are two independently controlled mechanisms during eye development.


Myopia Growth Remodeling Emmetropization Multi-scale modeling Finite element method 

Mathematics Subject Classification

74L15 92C10 74B20 74S05 



This work was supported by the National Institutes of Health Grants R01-EY026588 (RG) and P30-EY003039 (Bethesda, Maryland); Eye Sight Foundation of Alabama (Birmingham, Alabama); and Research to Prevent Blindness (New York, New York). The authors would like to give special thanks to Dr. Thomas T. Norton for sharing his experimental data.


  1. 1.
    Dolgin, E.: The myopia boom. Nature 519(7543), 276–278 (2015) ADSCrossRefGoogle Scholar
  2. 2.
    Vitale, S., Sperduto, R.D., Ferris, F.L. III: Increased prevalence of myopia in the United States between 1971–1972 and 1999–2004. Arch. Ophthalmol. 127(12), 1632–1639 (2009) CrossRefGoogle Scholar
  3. 3.
    Lin, L.L.K., Shih, Y.F., Hsiao, C.K., Chen, C.J.: Prevalence of myopia in Taiwanese schoolchildren: 1983 to 2000. Ann. Acad. Med. Singap. 33(1), 27–33 (2000) Google Scholar
  4. 4.
    Morgan, I., Rose, K.: How genetic is school myopia? Prog. Retin. Eye Res. 24(1), 1–38 (2005) CrossRefGoogle Scholar
  5. 5.
    Heine, L.: Beitrage zur anatomie des myopischen auges. Arch. Augenheilkd. 38, 277–290 (1899) Google Scholar
  6. 6.
    Saw, S.-M., Gazzard, G., Shih-Yen, E.C., Chua, W.-H.: Myopia and associated pathological complications. Ophthalmic Physiol. Opt. 25(5), 381–391 (2005) CrossRefGoogle Scholar
  7. 7.
    Mitchell, P., Hourihan, F., Sandbach, J., Wang, J.J.: The relationship between glaucoma and myopia: the blue mountains eye study. Ophthalmology 106(10), 2010–2015 (1999) CrossRefGoogle Scholar
  8. 8.
    Xu, L., Wang, Y., Wang, S., Wang, Y., Jonas, J.B.: High myopia and glaucoma susceptibility: the Beijing eye study. Ophthalmology 114(2), 216–220 (2007) CrossRefGoogle Scholar
  9. 9.
    Qiu, M., Wang, S.Y., Singh, K., Lin, S.C.: Association between myopia and glaucoma in the United States populationmyopia and glaucoma in the us population. Investig. Ophthalmol. Vis. Sci. 54(1), 830 (2013) CrossRefGoogle Scholar
  10. 10.
    Summers Rada, J.A., Shelton, S., Norton, T.T.: The sclera and myopia. Exp. Eye Res. 82(2), 185–200 (2006) CrossRefGoogle Scholar
  11. 11.
    McBrien, N.A., Gentle, A.: Role of the sclera in the development and pathological complications of myopia. Prog. Retin. Eye Res. 22(3), 307–338 (2003) CrossRefGoogle Scholar
  12. 12.
    Norton, T.T., Siegwart, J.T.: Animal models of emmetropization: matching axial length to the focal plane. J. Am. Optom. Assoc. 66(7), 405–414 (1995) Google Scholar
  13. 13.
    Wallman, J., Winawer, J.: Homeostasis of eye growth and the question of myopia. Neuron 43(4), 447–468 (2004) CrossRefGoogle Scholar
  14. 14.
    Walls, G.L.: The Vertebrate Eye and Its Adaptive Radiation. Cranbrook Institute of Science, New York (1942) CrossRefGoogle Scholar
  15. 15.
    Torczynski, E.: Normal and abnormal ocular development in man. Prog. Clin. Biol. Res. 82, 35–51 (1982) Google Scholar
  16. 16.
    Norton, T.T., Rada, J.A.: Reduced extracellular matrix in mammalian sclera with induced myopia. Vis. Res. 35(9), 1271–1281 (1995) CrossRefGoogle Scholar
  17. 17.
    Rada, J.A., Achen, V.R., Perry, C.A., Fox, P.W.: Proteoglycans in the human sclera. Evidence for the presence of aggrecan. Investig. Ophthalmol. Vis. Sci. 38(9), 1740–1751 (1997) Google Scholar
  18. 18.
    Norton, T.T.: Experimental myopia in tree shrews. Ciba Found. Symp. 155, 178–194, discussion 194-9 (1990) Google Scholar
  19. 19.
    McBrien, N.A., Lawlor, P., Gentle, A.: Scleral remodeling during the development of and recovery from axial myopia in the tree shrew. Investig. Ophthalmol. Vis. Sci. 41(12), 3713 (2000) Google Scholar
  20. 20.
    Moring, A.G., Baker, J.R., Norton, T.T.: Modulation of glycosaminoglycan levels in tree shrew sclera during lens-induced myopia development and recovery. Investig. Ophthalmol. Vis. Sci. 48(7), 2947 (2007) CrossRefGoogle Scholar
  21. 21.
    Guo, L., Frost, M.R., He, L., Siegwart, J.T. Jr., Norton, T.T.: Gene expression signatures in tree shrew sclera in response to three myopiagenic conditionsgene expression signatures in myopic sclera. Investig. Ophthalmol. Vis. Sci. 54(10), 6806 (2013) CrossRefGoogle Scholar
  22. 22.
    Gao, H., Frost, M.R., Siegwart, J.T., Norton, T.T.: Patterns of mRNA and protein expression during minus-lens compensation and recovery in tree shrew sclera. Mol. Vis. 17, 903–919 (2011) Google Scholar
  23. 23.
    Siegwart, J.T., Norton, T.T.: Selective regulation of MMP and timp mRNA levels in tree shrew sclera during minus lens compensation and recovery. Investig. Ophthalmol. Vis. Sci. 46(10), 3484–3492 (2005) CrossRefGoogle Scholar
  24. 24.
    Siegwart, J.T. Jr., Norton, T.T.: The time course of changes in mRNA levels in tree shrew sclera during induced myopia and recovery. Investig. Ophthalmol. Vis. Sci. 43(7), 2067 (2002) Google Scholar
  25. 25.
    Gentle, A., Liu, Y., Martin, J.E., Conti, G.L., McBrien, N.A.: Collagen gene expression and the altered accumulation of scleral collagen during the development of high myopia. J. Biol. Chem. 278(19), 16587–16594 (2003) CrossRefGoogle Scholar
  26. 26.
    Siegwart, J.T., Norton, T.T.: Regulation of the mechanical properties of tree shrew sclera by the visual environment. Vis. Res. 39(2), 387–407 (1999) CrossRefGoogle Scholar
  27. 27.
    Phillips, J.R., Khalaj, M., McBrien, N.A.: Induced myopia associated with increased scleral creep in chick and tree shrew eyes. Investig. Ophthalmol. Vis. Sci. 41(8), 2028–2034 (2000) Google Scholar
  28. 28.
    McBrien, N.A., Jobling, A.I., Gentle, A.: Biomechanics of the sclera in myopia: extracellular and cellular factors. Optom. Vis. Sci. 86(1), E23–E30 (2009) CrossRefGoogle Scholar
  29. 29.
    Grytz, R., Siegwart, J.T. Jr.: Changing material properties of the tree shrew sclera during minus lens compensation and recovery scleral material properties in myopia. Investig. Ophthalmol. Vis. Sci. 56(3), 2065 (2015) CrossRefGoogle Scholar
  30. 30.
    Zhu, X., McBrien, N.A., Smith, E.L. III, Troilo, D., Wallman, J.: Eyes in various species can shorten to compensate for myopic defocus. Investig. Ophthalmol. Vis. Sci. 54(4), 2634 (2013) CrossRefGoogle Scholar
  31. 31.
    Bryant, M.R., McDonnell, P.J.: Optical feedback-controlled scleral remodeling as a mechanism for myopic eye growth. J. Theor. Biol. 193(4), 613–622 (1998) CrossRefGoogle Scholar
  32. 32.
    Norton, T.T., Amedo, A.O., Siegwart, J.T. Jr.: The effect of age on compensation for a negative lens and recovery from lens-induced myopia in tree shrews (Tupaia glis belangeri). Vis. Res. 50(6), 564–576 (2010) CrossRefGoogle Scholar
  33. 33.
    Siegwart, J.T. Jr., Norton, T.T.: The susceptible period for deprivation-induced myopia in tree shrew. Vis. Res. 38(22), 3505–3515 (1998) CrossRefGoogle Scholar
  34. 34.
    Grytz, R., Sigal, I.A., Ruberti, J.W., Meschke, G., Downs, J.C.: Lamina cribrosa thickening in early glaucoma predicted by a microstructure motivated growth and remodeling approach. Mech. Mater. 44, 99–109 (2011) CrossRefGoogle Scholar
  35. 35.
    Guggenheim, J.A., McBrien, N.A.: Form-deprivation myopia induces activation of scleral matrix metalloproteinase-2 in tree shrew. Investig. Ophthalmol. Vis. Sci. 37(7), 1380–1395 (1996) Google Scholar
  36. 36.
    Diether, S., Schaeffel, F.: Local changes in eye growth induced by imposed local refractive error despite active accommodation. Vis. Res. 37(6), 659–668 (1997) CrossRefGoogle Scholar
  37. 37.
    Hodos, W., Kuenzel, W.J.: Retinal-image degradation produces ocular enlargement in chicks. Investig. Ophthalmol. Vis. Sci. 25(6), 652–659 (1984) Google Scholar
  38. 38.
    Kang, R.N., Norton, T.T.: Alteration of scleral morphology in tree shrews with induced myopia. Investig. Ophthalmol. Vis. Sci. 34, ARVO Abstract 1209 (1993) Google Scholar
  39. 39.
    Rodriguez, E.K., Hoger, A., McCulloch, A.D.: Stress-dependent finite growth in soft elastic tissues. J. Biomech. 27(4), 455–467 (1994) CrossRefGoogle Scholar
  40. 40.
    Grytz, R., Meschke, G.: Constitutive modeling of crimped collagen fibrils in soft tissues. J. Mech. Behav. Biomed. Mater. 2(5), 522–533 (2009) CrossRefGoogle Scholar
  41. 41.
    Grytz, R., Meschke, G.: A computational remodeling approach to predict the physiological architecture of the collagen fibril network in corneo-scleral shells. Biomech. Model. Mechanobiol. 9(2), 225–235 (2009) CrossRefGoogle Scholar
  42. 42.
    Grytz, R., Fazio, M.A., Girard, M.J.A., Libertiaux, V., Bruno, L., Gardiner, S., Girkin, C.A., Downs, J.C.: Material properties of the posterior human sclera. J. Mech. Behav. Biomed. Mater. 29, 602–617 (2014) CrossRefGoogle Scholar
  43. 43.
    Girard, M.J., Crawford Downs, J., Burgoyne, C.F., Suh, J.F.: Peripapillary and posterior scleral mechanics–part I: development of an anisotropic hyperelastic constitutive model. J. Biomech. Eng. 131(5), 051011 (2009) CrossRefGoogle Scholar
  44. 44.
    Suheimat, M., Verkicharla, P.K., Mallen, E.A.H., Rozema, J.J., Atchison, D.A.: Refractive indices used by the Haag-Streit Lenstar to calculate axial biometric dimensions. Ophthalmic Physiol. Opt. 35(1), 90–96 (2015) CrossRefGoogle Scholar
  45. 45.
    Gann, D.: Comparison of the Lenstar biometer and A-scan ultrasonography to measure ocular components. Master’s thesis, University of Alabama at Birmingham (2013) Google Scholar
  46. 46.
    Norton, T.T., McBrien, N.A.: Normal development of refractive state and ocular component dimensions in the tree shrew (tupaia belangeri). Vis. Res. 32(5), 833–842 (1992) CrossRefGoogle Scholar
  47. 47.
    Marsh-Tootle, W.L., Norton, T.T.: Refractive and structural measures of lid-suture myopia in tree shrew. Investig. Ophthalmol. Vis. Sci. 30(10), 2245–2257 (1989) Google Scholar
  48. 48.
    Kang, R.N.: A light and electronmicroscopic study of tree shrew sclera during normal development, induced myopia, and recovery. Ph.D. thesis, University of Alabama at Birmingham (1994) Google Scholar
  49. 49.
    Dhondt, G.: The Finite Element Method for Three-Dimensional Thermomechanical Applications. Wiley Online Library (2004) CrossRefzbMATHGoogle Scholar
  50. 50.
    Grytz, R., Downs, J.C.: A forward incremental prestressing method with application to inverse parameter estimations and eye-specific simulations of posterior scleral shells. Comput. Methods Biomech. Biomed. Eng. 16(7), 768–780 (2013) CrossRefGoogle Scholar
  51. 51.
    Park, T.W., Winawer, J., Wallman, J.: Further evidence that chick eyes use the sign of blur in spectacle lens compensation. Vis. Res. 43(14), 1519–1531 (2003) CrossRefGoogle Scholar
  52. 52.
    Norton, T.T., Amedo, A.O., Siegwart, J.T. Jr.: Darkness causes myopia in visually experienced tree shrews. Investig. Ophthalmol. Vis. Sci. 47(11), 4700–4707 (2006) CrossRefGoogle Scholar
  53. 53.
    Loman, J., Quinn, G.E., Kamoun, L., Ying, G.-S., Maguire, M.G., Hudesman, D., Stone, R.A.: Darkness and near work: myopia and its progression in third-year law students. Ophthalmology 109(5), 1032–1038 (2002) CrossRefGoogle Scholar
  54. 54.
    Schmid, K.L., Brinkworth, D.R., Wallace, K.M., Hess, R.: The effect of manipulations to target contrast on emmetropization in chick. Vis. Res. 46(6–7), 1099–1107 (2006) CrossRefGoogle Scholar
  55. 55.
    Diether, S., Gekeler, F., Schaeffel, F.: Changes in contrast sensitivity induced by defocus and their possible relations to emmetropization in the chicken. Investig. Ophthalmol. Vis. Sci. 42(12), 3072–3079 (2001) Google Scholar
  56. 56.
    Ohlendorf, A., Schaeffel, F.: Contrast adaptation induced by defocus—a possible error signal for emmetropization? Vis. Res. 49(2), 249–256 (2009) CrossRefGoogle Scholar
  57. 57.
    Narayanan, R., Metha, A.: Enhanced contrast sensitivity confirms active compensation in blur adaptation. Investig. Ophthalmol. Vis. Sci. 51(2), 1242–1246 (2010) CrossRefGoogle Scholar
  58. 58.
    Ashby, R., Ohlendorf, A., Schaeffel, F.: The effect of ambient illuminance on the development of deprivation myopia in chicks. Investig. Ophthalmol. Vis. Sci. 50(11), 5348–5354 (2009) CrossRefGoogle Scholar
  59. 59.
    Ashby, R.S., Schaeffel, F.: The effect of bright light on lens compensation in chicks. Investig. Ophthalmol. Vis. Sci. 51(10), 5247–5253 (2010) CrossRefGoogle Scholar
  60. 60.
    Siegwart, J.T., Ward, A.H., Norton, T.T.: Moderately elevated fluorescent light levels slow form deprivation and minus lens-induced myopia development in tree shrews. Investig. Ophthalmol. Vis. Sci. 53, ARVO E-Abstract 3457 (2012) Google Scholar
  61. 61.
    Smith, E.L., Hung, L.-F., Huang, J.: Protective effects of high ambient lighting on the development of form-deprivation myopia in rhesus monkeys. Investig. Ophthalmol. Vis. Sci. 53(1), 421–428 (2012) CrossRefGoogle Scholar
  62. 62.
    Karouta, C., Ashby, R.S.: Correlation between light levels and the development of deprivation myopia. Investig. Ophthalmol. Vis. Sci. 56(1), 299–309 (2015) CrossRefGoogle Scholar
  63. 63.
    Long, Q., Chen, D., Chu, R.: Illumination with monochromatic long-wavelength light promotes myopic shift and ocular elongation in newborn pigmented Guinea pigs. Cutan. Ocul. Toxicol. 28(4), 176–180 (2009) CrossRefGoogle Scholar
  64. 64.
    Rucker, F.J., Wallman, J.: Chicks use changes in luminance and chromatic contrast as indicators of the sign of defocus. J. Vis. 12(6), 23 (2012) CrossRefGoogle Scholar
  65. 65.
    Rucker, F.J.: The role of luminance and chromatic cues in emmetropisation. Ophthalmic Physiol. Opt. 33(3), 196–214 (2013) CrossRefGoogle Scholar
  66. 66.
    Smith, E.L., Hung, L.-F., Arumugam, B., Holden, B.A., Neitz, M., Neitz, J.: Effects of long-wavelength lighting on refractive development in infant rhesus monkeys. Investig. Ophthalmol. Vis. Sci. 56(11), 6490–6500 (2015) CrossRefGoogle Scholar
  67. 67.
    Rucker, F., Britton, S., Spatcher, M., Hanowsky, S.: Blue light protects against temporal frequency sensitive refractive changes the role of blue light in the development of myopia. Investig. Ophthalmol. Vis. Sci. 56(10), 6121–6131 (2015) CrossRefGoogle Scholar
  68. 68.
    Meek, K.M., Tuft, S.J., Huang, Y., Gill, P.S., Hayes, S., Newton, R.H., Bron, A.J.: Changes in collagen orientation and distribution in keratoconus corneas. Investig. Ophthalmol. Vis. Sci. 46(6), 1948–1956 (2005) CrossRefGoogle Scholar
  69. 69.
    Humphrey, J.D., Rajagopal, K.R.: A constrained mixture model for growth and remodeling of soft tissues. Math. Models Methods Appl. Sci. 12(3), 407–430 (2002) MathSciNetCrossRefzbMATHGoogle Scholar
  70. 70.
    Gleason, R.L., Humphrey, J.D.: A mixture model of arterial growth and remodeling in hypertension: altered muscle tone and tissue turnover. J. Vasc. Res. 41(4), 352–363 (2004) CrossRefGoogle Scholar
  71. 71.
    Machyshyn, I.M., Bovendeerd, P.H.M., Ven, A.A.F., Rongen, P.M.J., Vosse, F.N.: A model for arterial adaptation combining microstructural collagen remodeling and 3D tissue growth. Biomech. Model. Mechanobiol. 9(6), 671–687 (2010) CrossRefzbMATHGoogle Scholar
  72. 72.
    Ambrosi, D., Ateshian, G.A., Arruda, E.M., Cowin, S.C., Dumais, J., Goriely, A., Holzapfel, G.A., Humphrey, J.D., Kemkemer, R., Kuhl, E., Olberding, J.E., Taber, L.A., Garikipati, K.: Perspectives on biological growth and remodeling. J. Mech. Phys. Solids 59(4), 863–883 (2011) ADSMathSciNetCrossRefzbMATHGoogle Scholar
  73. 73.
    Kuhl, E.: Growing matter: a review of growth in living systems. J. Mech. Behav. Biomed. Mater. 29, 529–543 (2014) CrossRefGoogle Scholar
  74. 74.
    Cyron, C.J., Humphrey, J.D.: Growth and remodeling of load-bearing biological soft tissues. Meccanica (2016). doi: 10.1007/s11012-016-0472-5 Google Scholar
  75. 75.
    Cyron, C.J., Humphrey, J.D.: Vascular homeostasis and the concept of mechanobiological stability. Int. J. Eng. Sci. 85, 203–223 (2014). doi: 10.1016/j.ijengsci.2014.08.003 CrossRefGoogle Scholar
  76. 76.
    Pluijmert, M., Kroon, W., Delhaas, T., Bovendeerd, P.H.M.: Adaptive reorientation of cardiac myofibers: the long-term effect of initial and boundary conditions. Mech. Res. Commun. 42, 60–67 (2012) CrossRefGoogle Scholar
  77. 77.
    Kroon, M.: Modeling of fibroblast-controlled strengthening and remodeling of uniaxially constrained collagen gels. J. Biomech. Eng. 132(11), 111008 (2010) CrossRefGoogle Scholar
  78. 78.
    McBrien, N.A., Norton, T.T.: Prevention of collagen crosslinking increases form-deprivation myopia in tree shrew. Exp. Eye Res. 59(4), 475–486 (1994) CrossRefGoogle Scholar
  79. 79.
    Wang, M., Corpuz, C.C.C.: Effects of scleral cross-linking using genipin on the process of form-deprivation myopia in the Guinea pig: a randomized controlled experimental study. BMC Ophthalmol. 15(1), 1–7 (2015) CrossRefGoogle Scholar
  80. 80.
    Grytz, R., Girkin, C.A., Libertiaux, V., Downs, J.C.: Perspectives on biomechanical growth and remodeling mechanisms in glaucoma. Mech. Res. Commun. 42, 92–106 (2012) CrossRefGoogle Scholar
  81. 81.
    Roberts, M.D., Grau, V., Grimm, J., Reynaud, J., Bellezza, A.J., Burgoyne, C.F., Downs, J.C.: Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma. Investig. Ophthalmol. Vis. Sci. 50(2), 681–690 (2009) CrossRefGoogle Scholar
  82. 82.
    Siegwart, J.T., Norton, T.T.: Binocular lens treatment in tree shrews: effect of age and comparison of plus lens wear with recovery from minus lens-induced myopia. Exp. Eye Res. 91(5), 660–669 (2010) CrossRefGoogle Scholar
  83. 83.
    Metlapally, S., McBrien, N.A.: The effect of positive lens defocus on ocular growth and emmetropization in the tree shrew. J. Vis. 8(3), 1.1–112 (2008) CrossRefGoogle Scholar
  84. 84.
    He, L., Frost, M.R., Siegwart, J.T. Jr., Norton, T.T.: Gene expression signatures in tree shrew choroid in response to three myopiagenic conditions. Vis. Res. 102, 52–63 (2014) CrossRefGoogle Scholar
  85. 85.
    Summers Rada, J.A., Palmer, L.: Choroidal regulation of scleral glycosaminoglycan synthesis during recovery from induced myopia. Investig. Ophthalmol. Vis. Sci. 48(7), 2957–2966 (2007) CrossRefGoogle Scholar
  86. 86.
    Li, H., Wu, J., Cui, D., Zeng, J.: Retinal and choroidal expression of BMP-2 in lens-induced myopia and recovery from myopia in guinea pigs. Mol. Med. Rep. 13(3), 2671–2676 (2016) CrossRefGoogle Scholar
  87. 87.
    Summers, J.A.: The choroid as a sclera growth regulator. Exp. Eye Res. 114, 120–127 (2013) CrossRefGoogle Scholar
  88. 88.
    Howlett, M.H.C., McFadden, S.A.: Emmetropization and schematic eye models in developing pigmented Guinea pigs. Vis. Res. 47(9), 1178–1190 (2007) CrossRefGoogle Scholar
  89. 89.
    Summers Rada, J.A., Wiechmann, A.F., Hollaway, L.R., Baggenstoss, B.A., Weigel, P.H.: Increased hyaluronan synthase-2 mRNA expression and hyaluronan accumulation with choroidal thickening: response during recovery from induced myopia. Investig. Ophthalmol. Vis. Sci. 51(12), 6172–6179 (2010) CrossRefGoogle Scholar
  90. 90.
    Troilo, D., Nickla, D.L., Wildsoet, C.F.: Choroidal thickness changes during altered eye growth and refractive state in a primate. Investig. Ophthalmol. Vis. Sci. 41(6), 1249–1258 (2000) Google Scholar
  91. 91.
    Smith, E.L. 3rd, Hung, L.-F., Huang, J., Blasdel, T.L., Humbird, T.L., Bockhorst, K.H.: Effects of optical defocus on refractive development in monkeys: evidence for local, regionally selective mechanisms. Investig. Ophthalmol. Vis. Sci. 51(8), 3864–3873 (2010) CrossRefGoogle Scholar
  92. 92.
    Backhouse, S., Fox, S., Ibrahim, B., Phillips, J.R.: Peripheral refraction in myopia corrected with spectacles versus contact lenses. Ophthalmic Physiol. Opt. 32(4), 294–303 (2012) CrossRefGoogle Scholar
  93. 93.
    Fedtke, C., Ehrmann, K., Holden, B.A.: A review of peripheral refraction techniques. Optom. Vis. Sci. 86(5), 429–446 (2009) CrossRefGoogle Scholar
  94. 94.
    Benavente-Pérez, A., Nour, A., Troilo, D.: Axial eye growth and refractive error development can be modified by exposing the peripheral retina to relative myopic or hyperopic defocus. Investig. Ophthalmol. Vis. Sci. 55(10), 6765–6773 (2014) CrossRefGoogle Scholar
  95. 95.
    Faria-Ribeiro, M., Queirós, A., Lopes-Ferreira, D., Jorge, J., González-Méijome, J.M.: Peripheral refraction and retinal contour in stable and progressive myopia. Optom. Vis. Sci. 90(1), 9–15 (2013) CrossRefGoogle Scholar
  96. 96.
    Mutti, D.O., Sholtz, R.I., Friedman, N.E., Zadnik, K.: Peripheral refraction and ocular shape in children. Investig. Ophthalmol. Vis. Sci. 41(5), 1022–1030 (2000) Google Scholar
  97. 97.
    Radhakrishnan, H., Allen, P.M., Calver, R.I., Theagarayan, B., Price, H., Rae, S., Sailoganathan, A., O’Leary, D.J.: Peripheral refractive changes associated with myopia progression. Investig. Ophthalmol. Vis. Sci. 54(2), 1573–1581 (2013) CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of OphthalmologyUniversity of Alabama at BirminghamBirminghamUSA

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