Myopia and Myopic Progression Among Schoolchildren: A Three-Year Follow-Up Study

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1 Myopia and Myopic Progression Among Schoolchildren: A Three-Year Follow-Up Study Olavi Pcirssinen* and Anna-Liisa Lyyraf Purpose. To discuss the factors that might explain the rate of myopic progression and the degree of myopia after a 3-year follow-up among schoolchildren with myopia. Methods. Myopic progression among 238 schoolchildren was followed up in a randomized clinical trial of myopia treatment. The associations between the explanatory factors and myopic progression and thefinalvalue of the spherical equivalent after the follow-up were studied by analysis of variance and regression analysis. Results. Myopia progressed faster among girls than boys. According to the regression models for the boys, 25% of the variation of myopic progression and 57% of the final spherical equivalent could be explained by initial spherical equivalent, age at receiving first spectacles, time spent on sports and outdoor activities, and on reading and close work. Among the girls, 30% of myopic progression could be explained by age at receiving first spectacles, time spent on reading and close work, and reading distance. Similarly, 49% of the final spherical equivalent could be explained by age at receiving first spectacles, initial spherical equivalent, time spent on reading and close work, and reading distance. The rest of the variations could not be explained by the variables measured in this study. Conclusions. The factors with the most significant relationships to myopic progression were sex, age of onset, and degree of myopia at the beginning of the follow-up. Myopic progression and final myopia were related to time spent on reading and close work and to reading distance but not, however, to accommodation stimulus. Invest Ophthalmol Vis Sci 993; 34: JMyopia is a common refractive error in the literate countries. It is clear that there is a hereditary influence on the different components of the refractive elements of the eye. However, the influence of various external factors on myopia and on its progression is still under discussion. 23 That myopia is related to education and the higher.occupational groups would seem to be clearly established. 45 Accommodation, 6 conver- Frtnn the * Department of Ophthalmology, Central Hospital of Central Finland, and the ^Department of Statistics, University ofjyvaskyla, Jyviiskyla, Finland. This study was supported by a grant from the Academy of Finland. We thank also the instrnvientarium Corporation for sharing the costs of bifocal lenses. Submitted for publication October 23, 992; accepted January 2, 993. Propriety interest category: N. Reprint requests: Olavi Pdrssinen, Kannaksenkatu 5, SF-40600, Jyviiskyla, Finland. gence, 7 or both have most often been advanced as the reasons for these relationships. Our previous report on a 3-year follow-up study of myopia treatment showed that myopic progression among schoolchildren could not be prevented with the use of bifocals or by avoiding spectacles in reading and close work. 8 The same report showed a relationship between myopic progression and time spent on reading and close work, and also between myopia and reading distance. Progression was also faster among the girls than among the boys. This article deals with the factors that might explain the rate of myopic progression as well as the degree of myopia after a 3-year follow-up among myopic schoolchildren by using multivariate statistical 2794 Investigative Ophthalmology & Visual Science, August 993, Vol. 34, No. 9 Copyright Association for Research in Vision and Ophthalmology

2 Myopic Progression 2795 methods. We also attempted to identify those factors that would discriminate the fastest and slowest rates of myopic progression. The possible relationships between reading and myopia are also discussed. MATERIALS AND METHODS Myopic progression (final spherical equivalent [SFE] initial SFE) among myopic schoolchildren was followed for a 3-year period as a part of a clinical trial of myopia treatment. 8 Schoolchildren from the third and fifth grades of lower comprehensive school (mean age 0.9 years), with no previously prescribed spectacles for myopia, were considered for inclusion in the study. Two hundred forty children were randomly allocated to one of three treatment groups: full corrected spectacles to be used continuously, only for distant vision, or in the form of bifocals with +.75 D add. Before randomization the children were invited to participate in a follow-up study of myopia and all agreed. The research followed the tenets of the Declaration of Helsinki. Informed consent was obtained after the nature and the possible consequences of the study were explained to the participants. The research was approved by the institutional human experimentation committee. The 3-year follow-up proved possible for 238 children. Cycloplegic refraction was performed annually. Reading distance was measured during each annual examination using a Clement Clark accommodometer. The average value of the accommodation stimulus was calculated from annual measurements of reading distances and the refraction values. Myopic progression and the way of wearing spectacles were accounted for in these calculations. The following formulae were used to calculate accommodation stimulus between two control visits: Continuous use: ACC = (00/Rj + 00/R 2 ):2 + (SFD 2 - SFD,):2 Distant use: ACC = (00/R, + 00/R 2 ):2 + (SFD 2 + SFD,):2 : ACC = (00/R, + 00/R 2 ):2 + (SFD 2 - SFD,):2-.75, where ACC = accommodation stimulus, Rj and R 2 = reading distances in two consecutive visits, SFDj and SFD 2 = spherical equivalents of the right eye in two consecutive visits. The average reading distance and accommodation stimulus for the whole follow-up period was calculated from the consecutive values for annual reading distance and accommodation stimulus. Intraocular pressure was measured annually using Haag Streit applanation tonometry. Keratometry readings were measured at the beginning and at the end of the study using a Wesley Jessen System 2000 PEK camera. 9 At the end of the follow-up period the axial dimensions were measured by a Storz a-scan with a soft probe. A questionnaire was used to determine the use of spectacles by the children's parents. The children were divided into two groups according to whether one or both parents or neither parent had spectacles for distant vision. The questionnaire at the end of the followup asked for the average, amount of time spent daily to the nearest half hour separately on reading and on other types of close work outside school, separately for both school days and weekends. The mean number of hours spent daily on close work was calculated from those four estimates so that the values for school days were multiplied by five and those for weekends by two, and the different types of near work added together and divided by seven. The mean number of hours spent daily on outdoor activities was calculated likewise. In this report only the refraction values of the right eye are used. Because the differences between the treatment groups in myopic progression and in the final SFE (spherical equivalent at the end of the follow-up) of the right eye were statistically non-significant, the treatment groups are mainly treated as a whole. Materials and methods have been published in earlier reports. 80 Statistical Methods The comparisons of means for myopic progression and final SFE between the sexes, between treatment groups and between parent groups (according to whether parents wore spectacles for distant vision) were made using analysis of variance. Analysis of variance was also used to make the comparisons of the mean values of myopic progression with regard to sex and to different groups concerning time spent on reading and close work, reading distance, and time spent outdoors. The degree of myopic progression and final SFE were explained by age, initial SFE, time spent on reading and close work, time spent on outdoor activities, and average reading distance. These relationships were examined by constructing regression models separately for boys and girls. These models were estimated and tested using the LISREL 7 software program (Scientific Software, Mooresville, IN). Comparisons of the refraction-related variables and selected background variables between the slowest and the fastest progressing groups were made by Student's tf-test. Comparisons of the relative proportions of the sex, treatment, and parent groups between the slowest and the fastest progressing groups were made using x 2 -test. For the longitudinal examination of myopic progression at the four measurement points the growth curves were constructed for boys and girls separately using Generalized Multivariate Analysis of Vari-

3 2796 Investigative Ophthalmology & Visual Science, August 993, Vol. 34, No. 9 TABLE l. Comparisons of the Means for Myopic Progression and Final Spherical Equivalent (SFE) Sex Parents Group One or both Neither One or both Neither Source of Variation Main Effects Sex Parent group Treatment group Treatment Group Continuously Only distant Continuously Only distant Continuously Only distant Continuously Only distant F df 4 2 Mean Myopic Progression SD P (n) (9) (2) (22) (8) (6) (5) (25) (23) (20) (4) (3) (6) F Mean Final SFE df 4 2 SD (n) (9) (2) (22) (8) (6) (5) (25) (23) (20) (4) (3) (6) P Comparisons were performed by three-way analysis of variance among boys and girls in two groups of parents regarding their wearing of spectacles for distant vision and in the three treatment groups. ance (GMANOVA) model. 2 The estimation and testing of hypotheses for the growth curves and the calculations of confidence intervals were also computed using the GMANOVA program. 3 RESULTS The differences in myopic progression and final SFE between the boys and girls, between the treatment groups, and between the two groups according to parents' use of spectacles were studied by analysis of variance (Table ). Myopic progression was significantly slower among boys, and among those whose parents did not have spectacles for distant vision. The differences between the treatment groups (in the right eye) were not significant. No interaction among these three explanatory factors was found. TABLE 2. Regression Models of Myopic Progression and Final SFE for and Myopic Progression Final SFE Explanatory Age Initial SFE Close work Outdoors Reading distance N R * 0.25f f (SE) P 0.40* -0.8J 0.8J (SE) (-09) (.08) 0.24* 0.67* J (SE) (.07) (.07) (.07) (.07) 0.34* 0.5* -0.6J 0.5f (SE) (0.07) (0.07) (0.07) (0.07) The explanatory variables used were: age at commencement of study (Age); initial spherical equivalent (SFE); daily time spent on reading and close work (Close work); time spent on outdoor activities (Outdoors), and average reading distance during the follow up (Reading distance). Only effective variables were included in the models. Estimates for regression coefficients /3 and their standard errors are in parentheses. N, number of observations. R 2, determination coefficients. * P< fp<0.0. %P < 0.05.

4 Myopic Progression n MYOPIC PROGRESSION (D) f >. ' n n nrn s i GIRLS p = BOYS TIME SPENT ON READING AND CLOSE WORK (h) MYOPIC PROGRESSIONJ (D) - B _ MYOPIC i a n n nn? READING DISTANCE (cm) PROGRESSION (D) i " GIRLS \ p= BOYS > The correlations among the different explanatory factors about certain living habits and myopic progression and the final SFE were analyzed by constructing regression models for boys and girls separately, including age at the start of the study (age of receiving the first spectacles for myopia) and the initial SFE as control variables (Table 2). The age of receiving first spectacles for myopia was significantly related to myopic progression and final myopia among both boys and girls. Similarly SFE on receiving the first spectacles had a significant relationship with final SFE and with myopic progression among the boys. Time spent on reading and close work was associated with a faster rate of myopic progression and a higher degree of myopia at the end of the study, although the association was slightly weaker among the boys. The amount of time spent outdoors was clearly connected with myopic progression and final SFE among the boys, so that the greater the amount of time spent outdoors, the lower was the rate of myopic progression and the degree of myopia at the end of the follow-up. A shorter reading distance was clearly connected with a faster rate of myopic progression and higher myopia at the end of the follow-up among the girls. According to the regression models these factors explained 25% of the variation in myopic progression among the boys and 30% among the girls, and 57% and 49% of the variation in final SFE, among the boys and the girls, respectively. We also compared the mean values of myopic progression with the factors characterizing habits of reading and outdoor activities classified in four groups (Figure ). Figure la shows that when more time was spent on reading and close work, myopia progressed faster (P = 0.003). Progression was significantly faster among the girls than among the boys (P = 0.004). The figures MYOPIC PROGRESSION (D) - - BOYS GIRLS s >4.0 TIME SPENT ON SPORTS AND OUTDOOR ACTIVITIES (h) FIGURE l. Comparisons of the mean values of myopic progression with regard to sex and to (A) time spent on reading and close work; (B) reading distance and (C) time spent outdoors. Results of two-way analysis of variance: P values for differences among four groups on x-axis and between sex. Bars represent standard deviations BEGINNING FIRST yr SECOND yr THIRD yr FIGURE 2. Curves showing final spherical equivalent changes for boys and girls.

5 2798 Investigative Ophthalmology & Visual Science, August 993, Vol. 34, No. 9 TABLE 3. Comparisons of Annual Myopic Progression in Dioptes (D) Between and Using Two-Tailed t-test First year Second year Third year Mean (D) SD(n) 0.4 (9) 0.36(9) 0.44(9) Mean (D) SD(n) 0.5 (20) 0.47(8) 0.42(9) t-test (P Value) < were virtually the same when reading time only was taken into account. Myopic progression was also faster among children with a shorter reading distance (P = 0.002; Fig lb). The difference between boys and girls was also significant (P = 0.003). Myopic progression was slightly slower when more time was spent on outdoor activities, but the relationship was nonsignificant (Fig lc). Nevertheless, the difference between the boys and the girls was significant. The differences in the data in Figure were tested using the two-way analysis of variance. There were no interactions between sex and these three explanatory variables. The longitudinal investigation of myopic progression during the 3-year period was carried out by fitting the growth curve model for the SFE of the right eye through the four time points separately for both sexes using the GMANOVA model. The second-order polynomials were obtained as the growth curve models for the SFE; for the boys SFE t = t t 2, t = 0,,2,3, and for the girls SFE t = t t 2, t = 0,,2,3, where SFE is the expectation of the spherical equivalent of the right eye, t = 0 at the beginning of the study and t = 3 at the final examination 3 years later. The hypotheses suggesting identical and parallel curves for both sexes were both rejected (P < 0.00), and the myopic progression among the girls was found to be clearly faster. The graphs of the growth curves of SFE are shown in Figure 2. There was a divergent trend between the boys and the girls as well as a slight decrease in the rate of myopic progression. The annual progression among the girls was faster than that among the boys during the first 2 follow-up years but not thereafter (Table 3). The amount of time spent on reading and close work was somewhat greater among the girls and the amount of time spent outdoors was correspondingly shorter. However, the differences in these variables could not fully explain the divergence in myopic progression between the sexes. Different profiles of myopic progression emerged. Among six boys and six girls myopic progression during the follow-up was 0.25 D or less. Conversely, seven boys and seventeen girls had a myopic progression of TABLE 4. Comparisons of s Connected With Refraction Between the Slowest and Fastest Progressing Groups Using Two-Tailed t-test Age at entering the study (yr) Initial spherical equivalent (D) Myopic progression (D) Initial corneal refraction (D) Final corneal refraction (D) Final anterior chamber depth (mm) Final lens thickness (mm) Final axial length (mm) Slow Fast Mean SD(n) Mean SD (n) (60) 0.6 (60) 0.3 (60).3(55).3(35) 0.38 (33) 0.4(32) 0.74 (38) (60) 0.7 (60) 0.6 (60).4(55).3(39) 0.35 (44) 0.20 (44) 0.77 (46) t-test (P Value) < < <0.00

6 Myopic Progression 2799 TABLE 5. Comparisons of Selected Background s Between the Slowest and Fastest Progressing Groups Using x 2 -test Sex Treatment group Wearing spectacles continuously Wearing spectacles only for distant vision Parents' spectacles for distant vision One or both Neither Slow (%) Fast (%) n X 2 -test (P Value) more than 3 D. There was considerable variation in SFE at beginning of the follow-up in both the stable (-0.38 D to D) and the fastest progressing cases (-0.38 D to D). On the basis of the initial SFE we could not discriminate the stable from the fastest progressing cases. We then tried to ascertain which of the different variables would discriminate between the fastest and slowest progressing quartiles in this myopic child population. The comparison groups consisted of the 60 slowest and the 60 fastest progressing cases (Table 4). The fastest progressing group received their first spectacles approximately year earlier than those with the slowest progression. At the beginning of the follow-up there were no significant differences between the groups in SFE although myopic progression was about 2.4 D more in the fastest progressing quartile. There were no significant differences between the groups in corneal refraction at the beginning or at the end of the follow-up. Of the axial dimensions at the end of the follow-up only a greater total axial length was observed in the faster progressing group. Table 5 shows the other comparisons between the slowest and the fastest progressing groups. The faster progressing group contained more girls, and the parents of the children in this group more often had spectacles for distant vision. The comparison did not show any significant differences between the treatment groups. The faster progressing group had a shorter reading distance, but despite this their accommodation stimulus in reading was less than in the slowest progressing group (Table 6). Intraocular pressure seemed to be slightly higher in the faster progressing quartile, although this difference was not statistically significant. Furthermore, the time spent on reading or on both reading and close work was longer, and the time spent outdoors shorter in the faster progressing group. DISCUSSION The subjects selected for this study consisted of a rather visually homogenous group of schoolchildren receiving their first spectacles for myopia at beginning of the study. The age of the children on entering the study was also within narrow limits (mean 0.9 years, range years), thus imposing certain limitations on interpretation of the results. Had the study included hyperopic and emmetropic cases, the variation in the different explanatory factors used here would perhaps have been wider. However, even in the design of this study of myopic schoolchildren many variables were found to be related to myopia and to its progression. TABLE 6. Comparisons of Selected Background s Between the Slowest and Fastest Progressing Groups Using Two-tailed t-test Slow Fast Mean SD(n) Mean SD (n) t-test (P Value) Reading distance (cm) Accommodation stimulus (D) Intraocular pressure (mm Hg) At commencement to the study At the end of the study Time spent on reading (hours/day) Time spent on reading and close work (hours/day) Time spent outdoors (hours/day) (56) 0.9 (55) 2.8 (58) 2.2 (59) 0.3 (58) 0.8 (58).4(60) (58).2 (58) 2.6 (60) 2.5 (58) 0.4 (60) 0.9 (60). (60) <

7 2800 Investigative Ophthalmology & Visual Science, August 993, Vol. 34, No. 9 Heredity That heredity has an influence on refraction is obvious. In a recent study of 09 pairs of twins by Teikari et al, the heritability of myopia was 0.58 when myopia was considered a dichotomous variable. 4 It can be assumed that the effect of heredity on refraction is similar to that of many other physiologic phenomena, both in terms of direct influence and influence on susceptibility to external factors. In a previous Finnish study the percentage of myopes among those adults who wore spectacles for poor distant vision was 66%. 5 Thus a higher frequency of myopia can be assumed in the case of those parents of the children in the current study who had spectacles for poor distant vision compared to those who did not have spectacles for this purpose. Although this variable was apparently a rather weak variable in the heredity of myopia, it nevertheless had a relationship both with myopic progression and final myopia in this study. - Myopic progression was significantly faster among the girls than the boys. Interestingly, the difference in the rate of progression was significant only during the first 2 years of the follow-up and remained approximately the same thereafter. In the data studied by Goss, sex did not have a great effect on the rate of progression of childhood myopia. 6 Perhaps this difference between the sexes is evident only at the beginning of myopia and when the onset of myopia is early. The variables used in this study could not fully explain the difference in myopic progression between boys and girls. It has been proposed that the progression of myopia in children is related to the rate of their rate of growth. 7 Some of the difference in myopic progression between the sexes might be explained by the faster maturation of girls at the ages studied. Age of Onset and Degree of Myopia Earlier studies have shown that myopic progression is faster in the younger age groups. For example, in the study by Mantyjarvi myopic progression was 0.93 D/yr in 8-year-olds and 0.52 D/yr in 3-year-olds. 8 In the Houston myopia control study there was also a more rapid rate of progression among those who entered the study at an early age with a large amount of myopia. 9 In the current study the rate of myopic progression was also related to the age of onset of myopia and also independently to the degree of myopia at the beginning of the study. Thus the greater amount of myopia in adulthood among those whose myopia begins earlier is not at least solely dependent on more years of progression but also on faster progression when younger. Although the degree of myopia at the beginning was, on average, related to the rate of myopic progression, this did not hold true in individual cases. In this study there were stable cases of myopia varying from D to D. The distant vision of these children had been tested by school nurses at - or 2-year intervals at least twice before the commencement of the study. Thus it can be supposed that their myopia had developed during a few years and then stabilized. What halted their myopic progression remains to be answered. The relationship between faster myopic progression and earlier onset of myopia may depend on a stronger hereditary influence and/or a stronger susceptibility to external influences. Living Habits It is known that myopia is common among school children and educated people, 5 and less common among nonliterate populations. 20 Myopia has also been shown to be rare among occupational groups such as farmers and fishermen. 4 Further, restricted spaces have been shown to increases myopia in animal experiments. 2 In our previous study of men aged between 33 and 37 years, 77% of the subjects were correctly assignable as myopic by means of discriminant analysis taking into account interest in reading, length of education, occupational status, and body mass index. 22 Richler and Bear, respectively, using multiple regression coefficients, found an age-related relationship between myopia and near work. 23 In this study the amount of time spent on reading and on reading and close work and reading distance were related to myopic progression and final SFE, although there were clear differences between the boys and the girls. In this study there was also a slight negative correlation among the boys between myopic progression and the amount of time spent on sports and outdoor activities. It cannot be said whether the relationship between slower progression rate and longer amounts of time spent outdoors was attributable to some effect of distant gazing or simply to being away from reading and close work. Accommodation, Convergence, and Eye Movements What then might link myopia and reading and close work? Accommodation 6 and convergence 7 have been suggested as the reasons sons for the development of myopia. If accommodation played a significant role in myopic progression the feedback mechanism would

8 Myopic Progression 280 probably halt the process when reading with undercorrected glasses or without glasses. The results obtained in the earlier report 8 and from this study did not support the hypothesis of accommodation as a significant cause of myopia. As the matter of fact, in this study the accommodation stimulus was smaller among the fastest progressing quartile than among the slowest progressing quartile. The overall low accommodation stimulus values found here can be explained by the study design as one third of the children were recommended to do close work without spectacles and a second one third were prescribed bifocals. However, when a person with myopia reads without spectacles small changes in reading distance cause a greater percentage of changes in the amplitude of accommodation than when reading with spectacles, and we do not exactly know the effects of these changes. The relationships between short reading distance and myopic progression and final myopia found in this study could support the hypothesis that convergence is one factor inducing myopia. Greene has supposed convergence, and specially the stress between the oblique muscles, to be an important factor in myopic progression. 7 However, in a previous Finnish study of 26- and 46-year-olds it was shown that education increased the prevalence of myopia more than doing other kinds of precision close work. 5 It can be suggested that the use of eyes in close work like sewing, watch-repairing, and assembling electronic equipment is different from that in reading. A fact that has been largely neglected when discussing the possible relationships between reading and myopia is the physiologic nature of the reading process. Skilled readers move their eyes, on average, every quarter of a second when reading. 24 Thus, there are constant saccadic back-and-forth movements of the eye during reading. These eye movements clearly cause repeated pressure and stretch pulses on the eye during reading. It is obvious that there are fewer eye movements, although the working distance is the same, when doing many other kinds of close work. It seems feasible to assume that the structure as well as the thickness of collagen is influenced by heredity. The width of the eye muscle attachments and their strength can also vary because of heredity. The same is obviously true of axial length prior to any significant external influences. Hence, there are many variables influenced by heredity, and in a multiplicity of combinations, all of which can cause different affinities of the eye in response to various external factors. CONCLUSION Several variables in this study were related to myopia and myopic progression among schoolchildren, and also discriminated the fastest and slowest progressing myopes. The factors that had the most significant relationships to myopic progression were sex, age of onset, and degree of myopia at the beginning of the follow-up. In addition to having parents who had spectacles for poor distant vision, more time spent on reading and close work, and short reading distance but not high accommodation stimulus were all related to myopic progression. Of the refractive elements of the eye, greater axial length was related to higher myopia. It remains to be answered what, in addition to hereditary factors, could be the reason for greater axial length and myopia, but we suggest that studies of myopia should be addressed in part to determine the mechanical forces affecting the eye and sclera during close work and especially when reading. Key Words myopia, progression, reading distance, accommodation, convergence References. Sorsby A, Benjamin B, Sheridan M. Refraction and its components during the growth of the eye from the age of three. 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