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Relationship between Reduced Accommodative Lag and Myopia Progression

Koomson, Nana Yaa; Amedo, Angela Ofeibea; Opoku-Baah, Collins; Ampeh, Percy Boateng; Ankamah, Emmanuel; Bonsu, Kwaku

Optometry and Vision Science: July 2016 - Volume 93 - Issue 7 - p 683–691
doi: 10.1097/OPX.0000000000000867
Original Articles

Purpose To determine the relationship between accommodative lag and rate of myopia progression when Ghanaian myopic school children are either undercorrected or fully corrected with single vision lenses.

Methods A 2-year single masked randomized control trial was conducted using 150 Ghanaian myopic children aged 10 to 15 years with mean baseline myopia of −1.98 ± 0.50D. The children were randomly assigned to wear either a full correction (n = 75) or +0.50D undercorrection (UC) (n = 75) single vision lenses. Repeated measurements which included refractive error and accommodative response at 33 and 28.6 cm for FC and UC, respectively, were performed using Open-Field Autorefractor whereas ocular biometry results were obtained using A-Scan ultrasonography. Results were based on the right eye and analyzed using STATA 11.

Results After 24 months, the mean myopia progression of children in the FC group (−0.54 ± 0.26D) was not significantly different from that of the children in the UC group (−0.5 ± 0.22D) (p = 0.31). There was no significant difference between the mean values of the initial near lag and the average lag measured 24 months later in both groups (FC: initial lag −0.74 ± 0.17D, average lag −0.72 ± 0.15D, p = 0.44; UC: initial lag −0.57 ± 0.14D, average lag −0.58 ± 0.15D; p = 0.67). Also, there was no significant correlation between refractive change seen in 24 months and either the first near lag for both FC (r = −0.05, p = 0.43) and UC (r = −0.08, p = 0.43) or the average near lag of accommodation for both FC (r = −0.02, p = 0.49) and UC (r = −0.04, p = 0.49).

Conclusions This study showed no relationship between lag of accommodation and rate of myopia progression in children with progressing myopia. Different ethnic groups may respond differently to the same size of hyperopic blur.

*OD, MS

OD, PhD

OD

Department of Optometry and Visual Science, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana (NYK, AOA, PBA, EA, KB); Department of Psychological Sciences, Vanderbilt University, Nashville, TN (CO-B).

Collins Opoku-Baah Department of Psychological Sciences Vanderbilt University Nashville, TN e-mail: copokubaah@gmail.com

Myopia is a common eye defect and a major cause of blindness among children worldwide.1 About 84% of children between 16 and 18 years and 80% of young adult Asians are myopic2,3 compared to about a third of the adult population in the United States.1 The prevalence of myopia is shown to be lowest among white4 and black children.5–8 In Ghana, 54% of people who self-report to eye care facilities are myopic with 69% of them between the ages of 10 and 29 years.9

Typically, myopia is managed with negative lenses, and as myopia progresses, the optical power of the negative lens is increased so that a good foveal image is maintained. However, about 48% of myopic school children in developing countries are not privileged to change their lenses when myopia progresses and, thus, wear lenses that have powers less than optimal.10–12

There is evidence that fully corrected myopes accommodate less than is required to bring the prints at near into focus.13,14 This underaccommodation also known as lag of accommodation is quantified as the difference between accommodative demand and accommodative response. Increased lag of accommodation in myopes may cause prolonged periods of hyperopic defocus that may eventually result in axial elongation and myopia progression.15,16 When myopic children were fitted with progressive addition lenses (PALs), there was a small statistically significant reduction in myopia progression.17–21 The rational for fitting children with PALs was to reduce hyperopic defocus and consequently myopia progression. It is expected that this action of PAL on reducing myopic progression could be performed by single vision lenses.

Meanwhile, previous studies that investigated the effect of undercorrecting and fully correcting myopia with single vision lenses on myopia progression have found equivocal results.22–24 In a 24-month clinical trial involving 94 children aged 9 to 14 years, Chung et al.22 showed a faster rate of myopia progression in children who were undercorrected by 0.75D than those who wore full correction. Conversely, Adler and Millodot23 found no difference in the rate of myopia progression between undercorrected and fully corrected Israeli school children aged 6 to 15 years. In 2014, Vasudevan et al.24 confirmed reports of Chung et al.22 in a study in which they compared the rate of myopia progression among children who were either undercorrected by 0.25D, 0.37D, or 0.50D and fully corrected children in a retrospective study. They showed that the rate of myopia progression was fastest among children and adults who were undercorrected by 0.50D than in the other groups.

In literature, near phoria status has been related to myopia progression. Several studies have consistently shown that in subjects wearing single-vision refractive corrections, the rate of progression of myopia is slightly higher in the esophoric group than in the orthophoric and exophoric groups.25,26 A simulation study using an accommodation-convergence control model suggested that accommodative lag is increased by esophoria and uncorrected hyperopia, and decreased by exophoria and uncorrected myopia under a binocular fused condition.27 Thus, near phoria has been implicated to have a linkage with both lag of accommodation and myopia progression.

Although these previous clinical trials appropriately evaluated the effect of undercorrecting myopia with single vision lenses on myopia progression, none of them included subjects who were Africans or African Americans. Past studies have shown a significant relationship between myopia progression and ethnic variations.28,29 During the review of literature, little information was found on undercorrecting myopia with single vision lenses among African cohorts. Also, those clinical trials failed to consider the amounts of accommodative lag of the children.

Owing to the aforementioned, this randomized control trial investigated the relationship between accommodative lag and the rate of myopia progression when myopic Ghanaian children are either fully corrected or undercorrected with single vision lenses.

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METHODS

Ethical Consideration

The Committee on Human Research, Publications and Ethics of the School of Medical Sciences, Kwame Nkrumah University of Science and Technology and Komfo Anokye Teaching Hospital reviewed and approved the study. Approval was also obtained from the Regional Directorate and the Regional Education Service, Ashanti Region. In addition, informed consent and verbal assent were received from the parents and the children, respectively. The study was conducted in accordance with the tenets of the Declaration of Helsinki.

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Subjects

Verbal and written advertisements were made in eight purposively chosen high socioeconomic schools in the Kumasi metropolis. Children who voluntarily responded and submitted their informed consent forms were examined and allowed to further participate in the study upon meeting the inclusion criteria: healthy children aged from 10 to 15 years with visual acuity (VA) of 0.20 log MAR or worse with habitual spectacles, spherical equivalent refraction (SER) of −1.25 to −4.50D in each meridian as measured by cycloplegic refraction, VA of log MAR 0.00 or better with full correction spectacles, astigmatism ≤ −1.25D, anisometropia ≤1.00D, agree to wear study spectacles only and to wear them during waking hours, and no parental myopia. Exclusion criteria were amblyopia, strabismus, allergy to the cycloplegic agents, controlling myopia with either multifocal optical lenses or pharmacological agents, and history of contact lens wear. The study took place between September 13, 2010 and March 5, 2011.

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Procedures

After enrolling a child in the study, she/he was randomly assigned to either a FC, which is the control group, or an UC, the treatment group. Subjects for the study were matched in cells derived by using randomized block design based on three criteria (age, sex, and school) as suggested by Chung et al.22 The study design comprised three age groups (10–11, 12–13, and 14–15 years), created from the ages of the subjects recorded at baseline; two gender categories; and four schools. In total, 24 different cells of at most 10 members (due to the matched design, cells had even number of members starting from 4 to 10) were formed. In each block, numbers generated from random tables and placed in sealed envelopes with sequential patient identification numbers were used to pair the children. A coin was then tossed to separate each pair into either a control group (FC) or the treatment group (UC). After tossing the coin, if a head came up, the first subject in the pair was assigned to UC and the second to FC. On the contrary, if a tail came up, the first subject was allocated to FC and the second to UC.

Cycloplegic refraction was used to determine myopia progression which was the primary outcome measure. The Shin-Nippon NVision K50001 autorefractor (marketed as Grand Seiko WR-5100K, Japan) was used for measuring accommodative response and cycloplegic refractive error. Non-cycloplegic autorefraction and subjective refraction were carried out on each child before cycloplegic refraction was performed to determine distant prescriptions at enrollment. Subjective refraction was reached using the endpoint maximum plus for best acuity, after which visual acuities were measured after dispensing glasses. Dispensed glasses were adjusted for the UC group if vision was better than +0.2 log MAR. The open-field autorefractor allowed targets to be viewed at any viewing distance. Children were instructed to fixate binocularly on a target placed at near and keep it in focus. The FC and UC groups fixated on targets at 33 and 28.6 cm, respectively, to provide equal magnitude of accommodative stimulus. The fixation target was a 4 × 4 standard E letter with N10 size. Fixation target were viewed binocularly and the unmeasured left eye was not covered. Measurement was done under ambient room lighting conditions between 120 and 130 lux. Axial length and vitreous chamber depth were measured under cycloplegia using the Opto US 1000 A-scan.

Distance and near lateral phorias were measured by the alternating cover test using target that were two lines above the threshold on the Early Treatment Diabetic Retinopathy Study (ETDRS) distance chart and a crowded N10 standard letter E at 33 or 28.6 cm. Children who showed five or more prism diopter of exophoria were classified as exophores, those exhibiting less than five prism diopters of exophoria were orthophoric, whereas those with any amount of esophoria were classified as esophores.23

Children received their study spectacles 2 days after examination and were instructed to wear their study spectacles all the time except during bathing and sleeping. Parents and guardians were asked to ensure that the children complied and also to return every 6 months for a follow-up examination which included subjective refraction, near lateral alternating cover test, and cycloplegic autorefraction.

During all examinations, the optometrist who took all measurements was not aware of the treatment group the child belonged and no child was supposed to discuss any problem on the spectacles with the optometrist. Children were given written instructions on the use and care of study spectacles. The instruction sheet had the phone numbers of a second optometrist they could call in the event of missing spectacles, broken spectacle, or intolerance of spectacle prescription. The second optometrist was unmasked to children’s lens assignment and was responsible for subjective refraction, children’s frame selection and dispensing of children’s spectacles, taking aided VAs, and determining the correction after the measures made by the masked optometrist.

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Compliance

At each 6-month visit, parent(s) and child were to indicate the number of times the child wore the spectacles in a day to read and also to do outdoor activities by providing answers to a survey which was originally developed by Gwiazda et al.17

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Frame Selection and Dispensing

Children selected a frame each from a number of fashionable ones. Both frame and photochromic lenses (CR-39) were free and the spectacles were fitted to a vertex distance of 12 mm. Children in the FC group received new spectacles when there was at least 0.50D change in the subjective finding of one or both eyes. In the UC group, a child’s lens was changed by adding a plus power to blur vision and maintained to give vision of about 0.20 log MAR in both eyes.22,23 The lens was changed if the cycloplegic autorefraction had changed by at least 0.50D spherical equivalent or was clinically indicated.

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Statistical Analysis

Results were analyzed with Microsoft Office Excel 2010 and STATA 11. The sample size was calculated as 150 children (75 per group) for a predetermined statistical power of 90% and a type 1 error rate of 5% so that a difference in the 24-month myopia progression between FC and UC treatment groups would be detected if the difference was at least 0.25D, assuming a 0.38D standard deviation in each treatment group23 and allowing 20% loss to follow-up. Follow-up data were analyzed using an intent-to-treat principle according to the child’s original lens assignment and the last measured value of the outcome measures. Due to the high Pearson correlation coefficient (0.9) between the two eyes after 2 years and the mean spherical equivalent refractive error (SER) between the two eyes which was <0.25D (p = 0.89), results for this study were based on the right eye only.

The average of five readings from the open-field autorefractor was used to calculate the accommodative lag as the difference between the measured accommodative response and accommodative demand.30

M = spherical equivalent of the subjective refraction lens. R = mean refractive value given by autorefractor, DTE = distance between the accommodative target and the corneal apex (m), DLE = distance between the correcting lens and the corneal apex (0.012 m), LENS = spherical equivalent of the spectacles worn.

The primary outcome, which was progression of myopia, was defined as the change in SER relative to the baseline as a continuous measure. An average measure of SER was calculated from five autorefraction measurements made for the right eye. Secondary outcome was defined as the change in axial length at the end of the 24 months to baseline. Linear regression was used to model the 24-month change in myopia progression and axial length and also determine the unadjusted difference between the mean myopia progressions of both groups. The relationship between lag of accommodation and myopia progression was evaluated using linear regression to determine the correlation between (1) baseline accommodative lag and SER changes seen after 24 months and (2) average lag (average of the 6th, 12th, 18th, and 24th months near lags) and SER changes seen after 24 months. Interaction analyses were performed to identify whether treatment affected the children differently if they had smaller or larger lag.

Two-sample t-test was used to determine the difference between the mean baseline myopia of children under larger and smaller lag groups in both FC and UC. Also, difference in mean accommodative lag between FC and UC at baseline and at the 24-month period was determined using two-sample t-test. Comparisons of the relative proportions of sex and phoria between the two groups were made using chi-square tests. ANOVA analysis was done to compare the significant difference in rate of myopia progression over time between FC and UC. Tests of significance were two tailed and the level of significance was set at 5%.

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RESULTS

Compliance

Parents of children in FC and UC groups reported that their children wore the study spectacles 98 and 96% of the time, respectively, after school and also on weekends and holidays. Children in the FC and UC reported that they wore their spectacles 96 and 97% of the time, respectively, at school, after school, and also on weekends and holidays. The wearing times reported by parents and children in both groups were comparable (p ≥ 0.34).

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Baseline Characteristics of Children

Out of the 261 children who voluntarily responded to written and verbal advertisements done in eight purposively chosen high socioeconomic schools in the Kumasi metropolis, 253 returned the signed consent forms and were allowed to further partake in the study. The first 150 children to meet the inclusion criteria were enrolled in the study. Out of the 150 myopic children who enrolled in the study, one girl dropped out after 18 months. The remaining 149 participated and completed the 24-month study. Seventy-five children remained undercorrected (left slightly myopic) whereas seventy-four were fully corrected. The ages of children enrolled in the study ranged from 10 to 15 years with a mean age of 12.39 ± 1.27 years. The study sample consisted of 60% female. The overall mean baseline SER myopia measured by cycloplegic autorefraction and mean lag of accommodation were −2.00 ± 0.54D (ranging from −1.25 to −4D) and 0.65 ± 0.18D (ranging from 0.35 to 1.05D), respectively. The overall mean baseline axial length was 23.24 ± 0.41 mm. Before study prescriptions were given to the children, the lags of accommodation among the two groups were similar at enrollment (FC −0.55 ± 0.23D, UC −0.56 ± 0.21D, p = 0.78) whereas with study spectacles, the baseline lags of accommodation were significantly different among the two groups (FC −0.74 ± 0.17D, UC −0.57 ± 0.14D, p = 0.0001). The baseline characteristics between FC and UC groups are shown in Table 1 below. The two groups showed no statistically significant difference in mean age, baseline myopia, period of wearing spectacles, baseline phoria, baseline level of myopia, axial length, and vitreous chamber depth.

TABLE 1

TABLE 1

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Accommodative Lag when Wearing Study Spectacles

The mean and standard deviation of baseline lag measured at 28.6 cm were 0.57 ± 0. 14D with UC and 0.74 ± 0.17D when those who wore FC were measured at 33 cm (p = 0.0001). The amount of myopia at baseline in the FC and UC child by lag of accommodation is presented in Table 2 below.31 The children were divided into high and low lag subgroups depending on greater or smaller than the mean lag (0.65D). The mean myopia values observed between full correction and undercorrection children for both high and low lag subgroups were not significantly different.

TABLE 2

TABLE 2

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Primary Outcome

Fig. 1 below shows mean changes in refractive errors for children in the FC and UC groups within a 24-month period. At the end of 24 months, the mean myopia progression in the UC and FC was −0.5 ± 0.22D and −0.54 ± 0.26D, respectively. The unadjusted difference of −0.04 between FC and UC was not statistically significant (p = 0.31). There was no significant difference in rate of myopia progression over time between FC and UC (repeated measure ANOVA, two treatments, F = 0.44, p = 0.78).

FIGURE 1

FIGURE 1

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Secondary Outcomes

Fig. 2 below shows the changes in axial length for UC and FC groups over the 24-month period of the study. There was no significant difference in axial length between the two groups. The unadjusted mean changes in axial length at 24th month were 0.24 ± 0.17 (n = 75) and 0.21 ± 0.14 mm (n = 75) for FC and UC groups, respectively. There was no statistical difference between the two groups (p > 0.05).

FIGURE 2

FIGURE 2

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Lag of Accommodation and Myopia Progression

Fig. 3A and 3B below show a comparison between the scatter diagrams of refractive change seen in 24 months and baseline lag while wearing either a FC or UC, respectively. The correlation between them was (r = −0.05, p = 0.43) and (r = −0.08, p = 0.43) when lag was measured with FC and UC, respectively. The overall mean of the average of the 6th, 12th, 18th, and 24th months near lags was 0.66 ± 0.12D ranging from 0.37 to 0.93D whereas FC and UC had means of 0.72 ± 0.15D and 0.58 ± 0.15D, respectively. Fig. 4A and 4B below represent scatter diagrams that show change in refraction error versus the average near lag of accommodation with FC or UC, respectively. The correlation between them was (r = −0.02, p = 0.49) and (r = −0.04, p = 0.49) when lag was measured with FC and UC, respectively. There was no interaction between treatment whether the child had smaller or larger lag (p = 0.13) as shown in Table 3 below. The treatment effect had no interaction effect on children with esophoria compared to exophoric (p = 0.24) and orthophoric (p = 0.31) subgroups.

TABLE 3

TABLE 3

FIGURE 3

FIGURE 3

FIGURE 4

FIGURE 4

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DISCUSSION

This present study showed that whether accommodative lag is large or small, there seems to be no association between lag of accommodation and myopia progression. This result is in agreement with that found by Weizhong et al.32 and Berntsen et al.33 In a 1-year longitudinal study, Weizhong et al.27 followed 62 Chinese myopic children aged 7 to 13 years and found no relationship between lag of accommodation and myopia progression. The team also found no correlation between baseline accommodative lag and myopia progression or the average of the baseline and the 12th month lag and myopia progression. In an independent study, Berntsen et al.34 found that neither lag of accommodation at the beginning nor at the end of a yearly progression interval was associated with yearly myopia progression in 592 myopic children. The relationship between accommodative lag and annual myopia progression was investigated using linear models in fully corrected children who were enrolled in the Collaborative Longitudinal Evaluation of Ethnicity and Refractive Error (CLEERE) Study.

In our study, undercorrection of myopia by +0.50D significantly decreased accommodative lag at near compared to full correction (p = 0.0001); however, the rate of myopia progression between the groups was not different as shown in Figs. 1 and 2 (p = 0.31). There was also no association between myopia progression and either the first lag or the average lag measured at the 6th, 12th, 18th, and 24th months as shown in Figs. 3A and B, and 4A and B, respectively. This present study also found no interaction between lag of accommodation and assigned group. This data suggests that whether fully corrected or undercorrected, the spectacle treatment that a child wears does not contribute to the rate of myopia progression. This result is in agreement with that by Ong et al.35 who showed no difference in myopia progression in children who either wore their full correction all the time, none of the time, or on part-time basis.

Meanwhile, Allen and O’Leary36 reported results that conflicted that of this present study and that by Weizhong et al.37 and Berntsen et al.38 Allen and O’Leary39 worked on adults aged 18 to 22 years and found an association between higher accommodative lag and increased progression rates.

It has been hypothesized that increased accommodative lag caused by hyperopic defocus increases myopia progression, and Rosenfield et al.40 found results that contradict this hypothesis. Although Rosenfield et al.41 also worked on adults, the team found that myopia progressed faster when lag of accommodation was smaller. Considering the age range of children in this present study, the results of Weizhong et al.42 and Berntsen et al.33 are similar and no association between lag of accommodation and myopia progression was found; it could be that an association might be found later when children grow to become adults.

Although undercorrection could cause myopic defocus and reduce distance vision, it is the normal condition under which about 48% myopic school children in developing countries read the board.10–12 Chung et al.22 suggested that both hyperopic and myopic blur could cause myopia progression. However, in our study, which used Ghanaian children who wore undercorrected spectacles, we found that undercorrection did not result in any greater myopia progression than that shown in the full correction group. It could be then suggested that if the magnitude of hyperopic or myopic blur was the only factor used in determining the rate of myopia progression, then undercorrected myopic children would eventually suffer extremely high levels of myopia and its associated blinding conditions.22 Chung et al.22 investigated the rate of myopia progression between fully corrected and undercorrected Hong Kong Chinese children aged 9 to 14 years in a 24-month clinical trial. The rate of myopia progression significantly increased by 0.23D in the undercorrected group compared to the fully corrected group. Chung et al.22 speculated that the presence of blurred vision at any distance could stimulate myopia progression. Conversely, in an 18-month clinical trial, Adler and Millodot23 found that the rate of myopia progression between fully corrected and undercorrected Israeli schoolchildren aged 6 to 15 years was not different. The different rates of myopic progression among different ethnic groups could result from different thresholds to the same size of hyperopic blur, but this is yet to be demonstrated.

The mean baseline values of lag at 28.6 cm and 33 cm target distances were 0.57 ± 0.14D with UC and 0.74 ± 0.17D with FC. Undercorrected myopic children require less accommodation to read at near, and the lag measured with UC was significantly lower than that measured with FC (p = 0.0001). However, there was no difference in the rate of myopia progression between the fully corrected and undercorrected. The hypothesis is that a larger lag of accommodation in association with near work13,37,38 increases myopia progression.14,39 In contrast to this present study, the Correction of Myopia Evaluation Trial (COMET) suggested that COMET children were at risk of increased myopia progression if they had a larger accommodative lag with a combination of esophoria and wore full correction single vision lenses. COMET was a prospective, randomized clinical trial that evaluated the effect of PALs compared to single vision lenses on the progression of juvenile-onset myopia. The COMET study enrolled 469 ethnically diverse children aged 6 to11 years with baseline myopia equivalent between −1.25 and −4.50D and found a statistically significant PAL treatment effect of 0.20D after 3 years.17 However, 2 years later, the PAL treatment effect of 0.13D was found to be not different from SVL.40 Children enrolled in this present study and COMET children had similar baseline spherical equivalent of −1.25 to −4.50D. There was a significant reduction in myopia progression in the PAL group compared to the group that wore full correction single vision lenses in the COMET children; however, no difference in progression was seen between the undercorrected and fully corrected in this current study possibly due to the large difference in sample size. Lag of accommodation and amount of myopia were the two variables that interacted significantly with treatment in the COMET child. The treatment effect of PALs in the COMET children was significantly larger in children with larger lag than those with smaller lag. In this study, no interaction was seen between lag of accommodation and assigned group.

Although the optical treatments in this study had no interaction effect on children with near point esophoria, orthophoria (0.31), or exophoria (0.24), Adler and Millodot23 found a slight interaction effect (0.06D) on children with esophoria compared to the combined orthophoric and exophoric group.

It has been hypothesized that hyperopic blur in the peripheral retina of human eyes results in increased axial elongation and that optical treatments that decrease or remove hyperopic retinal defocus slow myopia progression. A limitation of this present study is that the peripheral refraction of enrolled children with and without spectacles was not measured. It could be that some aspects of single vision lenses other than its effect on lag of accommodation might be the alternate explanation for increased myopia progression in undercorrected myopic schoolchildren seen in previous studies. Several optical treatments that change peripheral refraction of myopic eyes are at present being investigated, and they include novel lens designs, orthokeratology lenses, various bifocal lenses, and novel soft contact lens designs.42–47 Meanwhile, previous studies have reported that single vision lenses cause a hyperopic shift in the peripheral retina of the horizontal meridian of the myopic eye.48–50

This study was limited by the fact that some of the participants recruited wore habitual undercorrected spectacles (with best corrected visual acuities of worse than 0.20 log MAR) and, therefore, could have had an effect on myopia progression and the overall study.

In conclusion, our results failed to support the evidence found in previous studies that undercorrecting juvenile-onset myopia increases myopia progression. This study showed that the rate of myopia progression was not altered by manipulating lag of accommodation. Although we found that UC did alter the lag of accommodation in this group of subjects, it is not clear whether UC would alter the lag of accommodation in other subjects. Lag of accommodation does change with viewing distance, and lag was measured at two different viewing distances in this study, so it is possible that the difference in lag found between the groups could have been due to other factors. It is also important to note that the blur at distance created by the UC did not result in faster progression. Therefore, the relationship between different magnitudes of hyperopic blur and rate of myopia progression in different ethnic groups requires further investigation.

Collins Opoku-Baah

Department of Psychological Sciences

Vanderbilt University

Nashville, TN

e-mail: copokubaah@gmail.com

Received January 29, 2015; accepted January 7, 2016.

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Keywords:

hyperopic defocus; lag of accommodation; children; undercorrection; myopia progression

© 2016 American Academy of Optometry