The changes in ocular dimensions that occur between the ages of 6 and 14 years, and the components that are important in the development of the eye and maintaining emmetropia are well known. Over this age range, when the prevalence of myopia may increase rapidly, the major changes are an increase in vitreous chamber depth and a decrease in the power of the crystalline lens. Any imbalance between these two components will lead to a refractive error of the eye, primarily myopia.
One reason for conducting studies on eye growth during childhood is to provide insights as to how an eye that becomes myopic differs from an eye that remains essentially emmetropic. Identifying how aspects of the myopic eye differ from the emmetropic eye before the onset of the condition offers the possibility of predicting the refractive outcome of children. Sorsby approached the issue by examining correlations between refractive error and the various ocular components in children aged 3 to 13 years and concluded that there was no change in corneal power, crystalline lens power, or anterior chamber depth beyond 13 years of age. He did not identify differences between the growth of myopic and nonmyopic eyes other than to observe that myopia developed from a failure of the lens or cornea to compensate for an increase in axial length.
There are reports that in myopia, the cornea has a steeper radius of curvature, the lens power is reduced, the lens is thinner, and the axial length is greater than in nonmyopic eyes. However, there are few studies that have specifically examined the differences between eyes that become myopic and those that do not before the onset of the condition. Such a predictive approach would necessarily define the myopic eye as one that ultimately develops myopia and would require a different analysis of longitudinal data from that of previous work.
The Nepal Longitudinal Study of eye growth and development of refractive error was conducted from 1992 to 2000 when detailed biometric data were collected from children at the Srongtsen Bhrikuti Boarding School at Boudha on the outskirts of Katmandu in Nepal. The distribution of these children in terms of age at first examination and the number of examinations and the distribution of refractive error have been previously reported. The reason for conducting this study in Nepal was that the students at this school were predominantly of Tibetan origin with very few from other ethnic backgrounds. Additionally, children who entered the school at kindergarten age almost invariably completed their secondary schooling, leaving at approximately age 18 years. The school was well endowed and conducted a rigorous academic program. Some results from this project have been published previously.
DISCUSSION
Previous studies on ocular dimensions and refractive error have followed different lines of inquiry. Sorsby et al. examined the correlations between the various components and refractive error as a means of understanding the nature of the coordination shown in emmetropia and to give an explanation of why refractive errors occur. Longitudinal studies provide more information on changes that occur with age and usually compare the rate of change in ocular dimensions with refractive error to give a clue as to the ocular component contributing to the refractive error.
The analysis of our data was based on establishing two refractive error groups, myopic if the error was ever less than -0.50 D, irrespective of the age at which this occurred, and nonmyopic. Our groups were chosen on the basis of refractive error; there can therefore be no analysis using this variable such as how refractive error varies with age. Our decision to use this classification related to the question of how children who became myopic might differ from those that remained emmetropic or hypermetropic. Some children may have been placed into the myopia group based on measurements taken at an early age and subsequently developing higher degrees of myopia. A child we observed to develop say more than -0.50 D myopia for the first time at age 17 years would also have been placed into the myopia group. It is conceivable that some of the nonmyopic group may have become myopic at a time subsequent to our measurement period. In this case, a misclassification of these children would have occurred in our cohort. Any misclassification may result in the observed differences being smaller than the true differences. Nevertheless, we have demonstrated a statistically significant difference between our groups, and when this aspect is taken into consideration, our results are all the more compelling.
The major findings are discussed subsequently in terms of the various ocular components.
Cornea
We found that the radius of curvature of the cornea flattened by 0.08 mm for both groups. The corresponding decrease in corneal power amounted to 0.44 D, assuming a keratometer calibration refractive index of 1.3375. This flattening of the cornea occurred up to the age of approximately 15 years, and our model suggested little subsequent change. Whereas there was no significant difference in the rate of change in corneal radius of curvature between the two groups, there was a significant difference in the absolute radius values between the two groups. The myopia group demonstrated a steeper radius of curvature, by 0.09 mm, at all ages. Sorsby 1 concluded that a good correlation between corneal power and axial length existed for emmetropia, but that this broke down for refractive errors up to -4.00 D. The inference was that myopic eyes tended to have corneas of higher power. However, Sorsby admitted that the data on the cornea was equivocal for those beyond ages 10 to 12 years. Previous cross-sectional studies have generally failed to show any change in the cornea over this age range.
Friedman et al. reporting results from longitudinal data from the Orinda Longitudinal Study of Myopia gave a decrease in corneal power of 0.33 D over a 3-year period for subjects aged 8.8 to 14.5 years. Our reduction of 0.44 D over a 12-year period for children aged 6 to 18 years would tend to support their findings given that most of the change that we measured was apparent before 15 years of age. There was nothing in our results that suggested the rate of change was different in myopia; the cornea for subjects in the myopia group was always steeper than those in the nonmyopia group.
Anterior Chamber
There was a significant difference in the rate of increase in anterior chamber depth between the two groups, with the nonmyopia group increasing by 0.05 mm and the myopia group increasing by 0.19 mm. The increase in the anterior chamber depth may be attributed in the main to a decrease in lens thickness. Sorsby found an increase of 0.05 mm/year but did not find any correlation between anterior chamber depth and axial length or refractive error, and concluded that anterior chamber depth did not materially influence the development or degree of refractive error. This may well be correct with the increase in anterior chamber depth associated with the decrease in lens thickness involved in the emmetropization process. Larsen also found an increasing anterior chamber depth up to the age of 13 years. He further reported a negative correlation between chamber depth and refractive error, i.e., a deeper anterior chamber in myopia. These results concur with our findings.
Crystalline Lens
Thickness
We found a thinning of the crystalline lens with age of 0.20 mm for the myopia group and 0.14 mm for the nonmyopia group. These results are similar to those of Zadnik et al., who reported lens thinning of almost 0.20 mm for all refractive groups between 6 to 10 years and a largely constant thickness to age 14 years. They also reported a trend for children with myopia to have thinner lenses. Our results suggested that lens thinning continued to age 18 years, although the rate decreased with increasing age. Furthermore, our model suggested that the crystalline lens in the eye that developed myopia may be initially thicker than that in nonmyopia; a difference in the rate of thinning of -0.005 mm/year was apparent between the groups.
Equivalent Refractive Index
The equivalent refractive index increased with age with no significant difference in the rate of change between the two groups. At age 6 years, the index was 1.425 and for age 18 years, it had increased to 1.431 for the nonmyopia group. The method used to obtain the refractive index was an iterative procedure based on the Purkinje image from the posterior surface of the lens and the refractive error, a solution being based on the premise that only one refractive index will satisfy the other two measures. In an earlier report using this technique and based on cross-sectional data from this project, we reported a mean value of 1.4252, but as a result of the nature of the study, we could not show a change with age. Mutti et al. calculated a refractive index to produce agreement between the measured ocular components and the refractive error for 519 school children and obtained a similar value of 1.427. Because the posterior radius of curvature of the lens determined by phacometry is dependent on the refractive index of the lens, there is an inherent error in this method, and although they appreciated this interaction, no clarification of any corrections was offered.
In a later study Mutti et al. used an iterative procedure for determining equivalent refractive index and found a refractive index at age 6 years of 1.427, which reduced up to age 10 and then increased to 1.4305 by age 14 years. Our mean values were 1.425 at age 6 years, 1.429 at age 14 years, and 1.432 by age 18 years. Given the different populations and measurement techniques, the results are remarkably similar, although it must be said that small differences in refractive index have a marked effect on lens power.
Surface Radii of Curvatures
We found that the radius of curvature of the anterior surface increased from a mean of 9.09 mm at age 6 years to 11.90 mm at age 18 years for the nonmyopia group with corresponding values of 8.88 mm and 12.56 mm for the myopia group. The rate of flattening for the myopia group was significantly greater than for the nonmyopia group. These values are somewhat different from those obtained by Mutti et al. At age 6 years, they found an anterior radius of curvature of 10.51 mm increasing to 11.70 mm by age 14.5 years, an increase of 1.2 mm, which compares with our increase of 2.3 mm for the nonmyopia group over the same age range and an even greater change for the myopia group. Our results for the posterior lens surface are similar to Mutti et al. in which we found an increase from -5.50 mm at age 6 years to -6.19 mm at age 18 years for the nonmyopia group, a difference of 0.69 mm or a difference 0.60 mm to age 14 years. The results obtained by Mutti et al. were 6.05 mm at age 6 years increasing to 6.60 mm at age 14.5 years, a difference of 0.55 mm.
Equivalent Power
We found the lens power reduced in a regular manner up to age 18 years for both our groups, with possibly a greater rate of reduction in the myopia group. Given that the calculation of lens power is dependent on all the other measures, this is perhaps not unexpected. The reduction in power for the myopia group was 2.35 D compared with 1.64 D for the nonmyopia group, with the greater increase in the radius of curvature of the myopia group responsible for this difference. This suggests an attempt at compensation to increasing myopic defocus by an increased flattening of the anterior surface of the lens. Mutti et al. found a reduction in lens power of around 2.40 D from age 6 to 10 years with little change thereafter for all refractive error groups.
Normally, the smaller differences they report in surface radii of curvature would not be sufficient to account for the reduction in lens power with age without the reduction in refractive index over the age range 6 to 10 years, something we did not find. After age 10 years, Mutti et al. reported practically no increase in radius of curvature of the anterior surface and only a small increase in the posterior radius of curvature. Any subsequent decrease in lens power from the posterior surface was effectively nullified by the increase in refractive index after age 10 years, and little compensation by the lens was apparent after that age.
With the exception of the increase in refractive index, all the lens changes we measured tended to reduce the power of the lens in both groups with significantly greater increases in the anterior lens radius of curvature and lens thickness in those who became myopic. This suggests that the crystalline lens is involved in the emmetropization process. Mutti et al. proposed a passive mechanical model for maintaining emmetropia and to account for the observed lens changes based on a physical stretching of the lens in the equatorial direction. An alternative explanation lies in a proposed differential lens growth pattern for children that become myopic. It is known that there are many growth factors involved in the differentiation of epithelial cells beneath the lens capsule into lens fibers and that some factors originate in the retina and travel anteriorly in the eye. There are also reports that the development of the lens can be influenced by visual input. An increase in lens fiber production would lead to an increase in anterior lens surface radius, and hence a reduction in surface power, that would be partly offset by an increase in refractive index. Furthermore, such an increase in fiber production would be expected to increase the lens thickness. However, the increase in refractive index suggests a reduction in water content of the lens, which would be consistent with the observed thinning.
Our finding that the anterior surface of the lens becomes flatter in those who become myopic would suggest an attempt at maintaining emmetropia through lens fiber production rather than through a passive response of the lens to stretching in the equatorial plane. The idea of retinal control of lens growth as an emmetropization mechanism is not new. Sorsby proposed that the retina continued the function of the optic vesicle and was responsible for lens shape and eye size, and although this was in part a mechanical hypothesis proposed before our current knowledge of ocular growth factors, the concept was original.
The effect of the small increase in refractive index is to offset the reduction in equivalent power of the lens as a result of the increase in radius of curvature of the anterior and posterior surfaces of the lens. Schematic eye models such as the three-surface eye proposed by Rabbetts give relationships between lens power and vitreous chamber depth required to maintain emmetropia. A common relationship is that an increase of 1.00 mm in vitreous chamber depth requires a decrease in lens power of 2.7 D, sometimes approximated to 3 D. However, it is difficult to relate such a rule of thumb to the developing eye because it assumes that other parameters remain constant, when in fact there are concurrent changes in corneal radius of curvature, anterior chamber depth, lens thickness, and in equivalent refractive index. We found that the power of the crystalline lens reduced by 2.35 D for the nonmyopia group and 1.64 D for the myopia group, whereas the corresponding increases in mean vitreous chamber depth were 1.00 mm and 2.00 mm.
Vitreous Chamber
There were marked differences in the rate of change of the vitreous chamber depth between the two groups; we found a mean difference of 1.00 mm between the groups by age 18 years. This result is consistent with the many studies that have shown an association between axial length and refractive error. The changes in vitreous chamber depth have been reported earlier when we reported the merit of using the measurement of the rate of vitreous chamber elongation as a predictor for myopia development in children.
CONCLUSIONS
In summary, we found several differential growth patterns in the myopic group compared with those that were deemed nonmyopic. The students who became myopic had steeper corneas at all ages, greater increases in anterior chamber depth, and lenticular developmental differences involving greater lens flattening and thinning with age. These changes occurred despite the lens in the myopia group being initially thicker than the others. Furthermore, subjects in the myopia group initially had a shorter eye with greater optical power as a result of the cornea and lens. Subsequent ocular development in this group resulted in an increased rate of growth of the vitreous chamber and crystalline lens compared with those that were identified as nonmyopic.
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