The anterior surface of the eye is its most powerful refractive component and, as such, subtle changes in corneal shape can cause substantial changes in its optical characteristics. Monocular diplopia has been linked to corneal distortion after nearwork in various studies dating back over 35 years. 1–9 The corneal distortions that have been observed in these studies have been explained by sustained 1–4 or abnormal lid pressure, 6 lid position, 5,7 and tear film interactions with the corneal surface during sustained close work. 7,9 During routine topography measurements, lid pressure effects on corneal topography have been observed in the central and peripheral corneal shape. 10,11
There has been conjecture that lid pressure may cause corneal astigmatism. 12,13 Vihlen and Wilson 14 found no significant association between the tension of the eyelids and the amount of corneal toricity. Grey and Yap 13 measured ocular astigmatism in subjects with three deliberately narrowed lid positions and found a statistically significant increase of ocular with-the-rule astigmatism when the lid aperture was narrowed. There is also evidence that astigmatism can be induced by chalazion, 15,16 lid-loading procedures used in the treatment of lagophthalmos, 17–19 and after ptosis surgery. 20
Some researchers have hypothesized that uncorrected astigmatism may play a role in the development of school-age myopia 21–23 and it has been associated with faster myopic progression rates in children with against-the-rule astigmatism. 24–26 Although there is general agreement that axial elongation is the most obvious cause of school-age myopia progression, myopes have steeper corneas, 27–29 and myopia progression has been shown to correlate with steepening of the principal meridian nearest to vertical. 30
In this study, we have investigated the effect of 1 hour of reading on corneal topography. The position of eyelids during reading, relative to the location and size of the pupil, was measured and compared with corneal topography changes. We have analyzed the optical consequences of the changes that were observed using traditional spherocylinder and corneal higher-order aberrations.
Twenty subjects (age range, 20 to 37 years; mean, 27) with healthy eyes were recruited for the experiment, and one eye was randomly chosen for analysis. Informed consent was obtained for all subjects. The 20 eyes had a range of refractive errors (mean, −1.6 D; range +0.25 to −6.00 D): five were emmetropic (i.e., ≤0.5 D in the worst meridian), five were primarily astigmatic (i.e., ≤0.5 D of spherical component and >0.5 D of astigmatic component), five had simple myopia (i.e., ≤0.5 D of astigmatism and >0.5 D of myopic component), and five had myopic astigmatism (i.e., >0.5 D of myopic and astigmatic component).
The experiment was always conducted early in the morning, approximately 2 to 3 hours after the subjects woke. All subjects were given the instruction not to perform any sustained reading (e.g., newspaper) before the experiment. For each subject, six baseline videokeratographs were taken before reading and six videokeratographs were again taken immediately after the 60-min reading task.
The Keratron videokeratoscope (EyeQuip Division, Alliance Medical Marketing, Jacksonville, FL) was used for all corneal topography measurements. The Keratron has been shown to have high accuracy and precision performance for inanimate test objects. 31,32 Before the study, the instrument calibration was checked according to the manufacturer’s instructions. The videokeratoscope is based on the placido-disk principle and enables the capture of six consecutive videokeratographs without the requirement for immediate data processing.
The subjects were seated and asked to read from a novel for 60 min. During this time, the subjects were allowed to adopt whatever head posture was comfortable. Photopic lighting conditions were used during the reading task. The subjects’ pupil size was measured in the photopic room condition with the subjects focused at a distance of 33 cm.
Before the reading experiment, digital photography was used to document the external ocular features using a high-resolution digital camera (Kodak DC260). Photography was conducted with (1) the eyes in reading gaze posture and (2) the subject positioned in a head rest with eyes in primary gaze. A ruler with millimeter increments was placed in the peripheral field of the captured images to allow calibration of subsequent measurements.
To determine the approximate position of the eyelids during reading in relation to the corneal topography, we identified iris features in the digital photographs of the eye taken during both reading and in the head rest. We then assumed that the relative position of the eye during videokeratoscopy was the same as that photographed when the subject was in the head rest. This allowed us to superimpose the approximate position of the eyelids during reading onto the corneal topography measurements taken after reading (Fig. 1). In this way, we could investigate the potential association between lid position during reading and changes in topography.
After 30 min of reading, the subjects’ blink frequency was measured over a time period of 3 min, and mean blink rate per minute was later calculated. The subjects were not informed that blink frequency was being monitored because this may cause a change in blink characteristics. 33,34
Corneal instantaneous power, height data, and refractive power were exported from the videokeratoscope for analysis. The instantaneous power maps were chosen to compare corneal topography with the subject’s natural lid position during reading because the instantaneous power maps are most sensitive to local power changes caused by slight variations in slope.
To study the potential effect of reading on topography, height-difference maps were calculated. For each set of six baseline measurements and six postreading measurements, the effect of ocular microfluctuations were minimized using the method described by Buehren et al. 35 The methodology repositions a given videokeratograph map to best approximate an “average” videokeratograph based on a set of multiple measurements of the same cornea. This procedure involves interpolating (bilinear) the topography data to a common grid format (256 meridians and point spacing along the meridian of 0.15 mm) and subsequent calculation of an average height map for each set of maps (i.e., before and after reading).
From the six refractive power maps for each condition (i.e., pre- and postreading), we calculated the average, standard deviation, and the number of valid measurements at each grid location within the map. Difference maps of pre- vs. postreading topography were calculated along with the t-test maps showing significant areas of change. 11 The root mean square error (RMSE) between corneal refractive power and best-fit spherocylinder before and after reading was calculated and t-tests were applied to measure the significance of changes in refractive power between the averages of the two conditions. This was performed for each individual’s photopic pupil size and also for fixed pupil sizes of 2.5, 3, 4, 5, and 6 mm. For the 4-mm fixed pupil size, power matrices 36 were used to average individual best-fit spherocylinders for each condition and again to calculate the corneal changes in sphere, cylinder, and astigmatic axis pre- vs. postreading. A multivariate test (Hotelling’s T2) representing a generalization of the t statistic was used to test the significance of overall change in corneal spherocylinder.
The anterior surface of the cornea was modeled as a single surface optical system to derive the corneal wavefront error using a method similar to that described by Guirao and Artal. 37 Optical path distance for each point on the surface was calculated using three-dimensional ray tracing, and the wavefront was fitted using a set Zernike terms of up to the fourth-order polynomial expansion according to the Optical Society of America convention 38 for pupil sizes of 2.5, 4, and 6 mm (image plane at circle of least confusion, wavefront error scaled by λ = 555 nm, and midline symmetry taken into account 39). All wavefront coefficients were normalized to a unit circle to enable quantitative comparison between different pupil sizes. The wavefront was centered on the line of sight. To achieve this, we calculated the average pupil offset derived from the pupil detection system provided by the Keratron videokeratoscope for each subject and used this offset as the new principle axis reference point. A full three-dimensional ray-trace technique was applied to calculate the wavefront error along the line of sight. Statistically significant changes in corneal wavefront Zernike coefficients after reading were identified using t-tests.
In 12 of the 20 subjects we studied, the instantaneous power maps after reading showed distinct band-like distortions in the superior region of the maps, which correlated closely with the subject’s natural lid position during reading. In Fig. 2, two examples of videokeratograph comparisons before and after reading for subjects 1 and 15 are shown, with the overlay of the subject’s lid position during reading. These topography changes were often encroaching within the boundary of the subject’s upper pupil margin. Topography changes were also often evident in the inferior cornea associated with the position of the lower lid margin during reading (see subject 1, Fig. 2). However, these inferior distorted regions generally did not encroach within the pupil zone.
Analysis of the corneal wavefronts revealed that seven wavefront coefficients were significantly changed after 1 hour of reading (Fig. 3). The terms that changed significantly for all pupil sizes were Z 2 2 primary astigmatism (p < 0.05 at 2.5 mm, and p < 0.01 at 4 and 6 mm), Z 3 −1 primary vertical coma (p < 0.01 at 2.5 mm, and p < 0.001 at 4 and 6 mm), and Z 3 −3 trefoil 30° (p < 0.05 at 6 mm, and p < 0.01 at 2.5 and 4 mm). The change of the primary astigmatism terms was in the direction of against-the-rule (i.e., with-the-rule astigmatism decreased or against-the-rule astigmatism increased).
Other changes in Zernike terms were limited to certain pupil sizes (i.e., corneal regions). For the 2.5-mm pupil size, the term Z 3 1 primary horizontal coma (p < 0.05) changed significantly. The defocus term Z 2 0 changed for the 4- and 6-mm pupil sizes (p < 0.01 at 4 and 6 mm). The vertical prism term Z 1 −1 changed for the 6-mm pupil size (p < 0.05), and the secondary astigmatism component Z 4 2 changed for the 4-mm pupil size (p < 0.05).
There was a significant association between changes occurring in the wavefront for the Z 3 −1 vertical coma and the Z 3 −3 trefoil 30° terms after reading. Most subjects (15 of 20) showed positive vertical coma and negative trefoil 30° or negative vertical coma and positive trefoil 30° in the baseline (prereading) measurements; this trend increased after reading (18 of 20). Both of these combinations of coma and trefoil terms represent a wave-like shape (Fig. 4, bottom) but they are opposite in direction. After reading, there was a trend for the vertical coma term to shift in the positive direction, whereas the trefoil 30° term generally shifted in the negative direction. The changes in the vertical coma and trefoil 30° coefficients after reading are shown in Fig. 4, top. These wave-like shape changes in the wavefront are consistent with the changes in instantaneous power maps associated with the effect of the upper lid margin.
An example of the optical changes in corneal refractive power after reading is presented for subject 8 in Fig. 5. In the difference map (pre- vs. postreading refractive power), the superior semimeridian shows values of up to −1.34 D change. These changes are highly statistically significant as shown by the p values of the t-test map (Fig. 5). Within a 4-mm pupil, 13 of the 20 subjects showed statistically significant (p < 0.001) areas of change in refractive power (Table 1, last column). These significant regions of change were mostly located in the upper and/or the lower pupil areas. Some subjects showed small randomly distributed points of statistically significant change, however these areas were considered to be nonsystematic and probably related to local tear instabilities rather than true changes in corneal topography and, thus, were not classified as representing statistically significant change (Table 1, last column).
The group mean RMSE deviation from the best-fit spherocylinder was slightly larger for the postreading corneas (Table 1). This difference was statistically significant when calculated for the individuals’ photopic pupil size (prereading 0.23 D vs. postreading 0.28 D, p = 0.013) as well as for fixed pupils of 5 and 6 mm (prereading 0.31 D vs. postreading 0.35 D, p = 0.036; prereading 0.38 D vs. postreading 0.42 D, p = 0.022, respectively). The increased RMSE was not statistically significant for the 2.5-, 3-, and 4-mm pupils (p = 0.66, p = 0.28, and p = 0.09, respectively).
Individual subject data for various refractive power changes after reading are summarized in Table 1. This includes the total refractive error, corneal best-fit spherocylinder power pre- and postreading, and the change in corneal spherocylinder for the 20 subjects.
Across the group, lid fissure width decreased from a mean of 9.4 mm (SD ±0.9) in primary gaze to 6.8 mm (SD ±1.0) in the reading position. Average pupil size of the subject group during reading in the photopic condition was 3.3 mm (SD ±0.7). Blink frequency showed large variability between individuals, with an average value of 8.3 blinks/min (range, 2 to 26 blinks/min). There was no significant correlation between blink rate and corneal RMSE differences (R2 = 0.10).
The changes in corneal aberrations that we measured after reading were clearly associated with forces applied by the eyelid margin to the surface of the eye. However the role of eye movements during reading was unknown. To investigate this, we recruited one subject (subject 9) who showed obvious corneal topography changes after the reading trial. The subject was retested on a separate morning, but this time the subject had to stare (fixed gaze) at a single word on a page for 60 min in normal reading gaze. The changes in refractive power after the fixed gaze trial along with the results from the initial reading trial of the same subject are shown in Fig. 6. The corneal changes after 60 min of staring are less pronounced, with values approximately half those found after 60 min of reading. The locations of changes shown after both trials indicate that a similar lid position was adapted during the two experiments. These results suggest that eye movements during reading contribute to the forces applied to the cornea.
We have shown that some individuals have significant changes in the topographical and optical characteristics of the cornea after 1 hour of reading. The topographical changes showed a clear association with the position of the eyelids during the reading task. The upper eyelid in particular, caused a wave-like distortion that was evident in the topography and corneal wavefront postreading.
Corneal distortions have been previously reported in cases associated with monocular diplopia after reading. 1–7, 9 Most of these studies have reported that subjects perceive vertical doubling of images. The wave-like aberration change that we found in many subjects, related to the vertical coma and trefoil Zernike terms (Fig. 4), is the likely optical explanation for this perception of vertical doubling. The significant wave-like aberration changes we found after reading were oriented vertically and would have the effect of smearing the retinal image along the vertical axis.
The time course of remission of corneal changes after reading is probably influenced by various factors such as the time spent reading, the visual tasks undertaken after reading, the subject’s blink frequency, and individual corneal tissue characteristics. To gain an impression of this time course, we continued to measure corneal topography after the 60-min reading task for one subject (subject 9). A large proportion of the corneal changes had disappeared at 10 min postreading, however it required 120 min before the topography was approaching prereading shape. Knoll 2 found that the perception of double images caused by corneal distortions after reading can last several hours as long as no further nearwork is done. Golnik and Eggenberger 9 have recently reported that 30 to 60 min is needed to resolve visual symptoms after cessation of reading. Because the time period of the experimental reading task in this experiment extended over only 60 min, longer periods of reading may intensify the degree of corneal changes that occur, and the recovery of normal topography may take substantial time.
The changes we observed in the corneal topography after reading are probably the result of displacement of epithelial tissue, although this assumption needs to be confirmed by pachometry of the epithelium. The magnitude of the height changes observed in postreading topography were in the order of 4 μm (range, 3 to 7), which would suggest that only a few superficial epithelial cells would need to be displaced for this topographical change to occur.
Because reading in some individuals can significantly change the corneal shape, this raises the question of the true refractive error of these eyes. It could be argued that a refractive correction for reading/close work might be best derived after a period of reading in these individuals. In terms of the best-fit spherocylinder to corneal topography, this result changed by up to 0.37 D in spherical component, up to 0.41 D in cylinder component, and up to 30° in cylinder axis when comparing pre- to postreading topography.
In another scenario, the question of the appropriate refractive correction of an individual arises in corneal refractive surgery. The appropriate spherocylinder correction in procedures such as laser in situ keratomileusis and photorefractive keratectomy may be altered if the individual has undertaken significant reading before corneal topography measurement. Potentially more problematic is the case of customized laser in situ keratomileusis, where the higher-order wavefront aberrations of the eye are also corrected by a corneal ablation. 40–42 We have shown that a number of higher-order Zernike aberration terms of the corneal wavefront are significantly changed by 60 min of reading.
The anterior corneal surface is the most powerful refractive component of the eye and, therefore, is a major contributor to the total wavefront aberrations of the eye. In general, third-order (coma and coma-like) aberrations are the dominant aberrations for most eyes. 43, 44 In this study, corneal coma and trefoil changed substantially in both magnitude and direction after reading. Our results suggest that studies of total aberrations of the eye should account for the visual tasks undertaken before total wavefront aberration measurement. Various studies of total wavefront aberrations of the eye have found that higher-order aberrations change with increasing levels of accommodation. 45, 46 Because the changes we observed in the corneal wavefront after reading were related to lid position, we expect that previous studies of aberrations and accommodation have been measuring the effects of changes in the optical characteristics of the crystalline lens and not the cornea because wavefront sensors typically induce accommodation with the subject in primary gaze (not downward reading gaze). To fully understand the optical characteristics of the eye during reading, it would be necessary to measure the total wavefront of the eye during reading (or downgaze).
The results of studies that have measured accommodation (refractive status) of the eye pre- vs. postreading tasks may have been influenced by the temporary optical changes that we have found to occur in the corneas of some subjects. The exact effect of these corneal changes on total refractive error (accommodative status) is difficult to predict, but would depend on the method of refractive measurement used by the optometer. 47
It is generally accepted that the risk factors for myopia development can be broadly classed as genetic and environmental factors. 48 One of the major environmental factors that has been shown to have an association with myopia development is reading and nearwork, 49–51 and there has been considerable speculation about the role of retinal image quality in myopia development. 52 The results of our study suggest that in some individuals, the corneal optics change during reading in a variety of ways that influence retinal image quality. Corneal spherocylinder can change, individual aberrations change (e.g., vertical coma and trefoil), and the total corneal RMSE (i.e., variation from a perfect spherocylinder) can change.
When we studied the interaction between corneal RMSE (i.e., variation from a perfect spherocylinder) and pupil size, we found that the group mean RMSE became significantly higher after reading for pupil sizes of 5 and 6 mm, showed borderline significance for a 4-mm pupil, and was not statistically significant for pupil sizes of 2.5 and 3 mm. For many individuals within the group, this increased RMSE was significant at all pupil sizes, and if we analyzed the increase in RMSE postreading for each individual’s photopic pupil size, the effect was again significant. This suggests that there is a small but significant overall loss in retinal image quality for some individuals during reading.
Studies of myopia development in various animals show that the overall sign of defocus can regulate eye growth. 53–55 In our subjects, the optical changes induced by the eyelids during reading did not typically have a rotationally symmetrical form. We described the most common change in shape of the corneal wavefront as “wave-like” accompanied by an astigmatic shift in direction of against-the-rule. When we examined the group mean change in the corneal wavefront defocus, there was a small change indicating slight central flattening of the cornea for pupil sizes of 4 and 6 mm.
Lid-related forces could play a role in refractive error development. O’Leary and Millodot 56 reported that subjects with ptosis were more likely to develop myopia and speculated that palpebral aperture may be a factor in the etiology of myopia. Many Asian populations are reported to have significantly higher rates of myopia than Western populations. 57–60 Compared with Western populations, it is well known that Asian eyes have smaller vertical palpebral apertures 61 and different anatomical characteristics, resulting in a thickened upper eyelid and overlying fold of skin, 62 all of which may serve to increase the optical effects of lid forces during reading. A number of studies have reported that rigid contact lenses may slow the progression of myopia in some children. 25, 63 We expect that rigid contact lenses might absorb much of the force of the eyelids during reading. These potential interactions are speculative, but we believe that they are worthy of further investigation.
During reading, corneal topography can change, and this effect appears to be directly related to the force exerted by the eyelids. As a consequence, the optical characteristics of the eye can be significantly altered during and after reading. This leads to questions of how we define the refractive status of the cornea and eye, which may need to be qualified in terms of the visual tasks undertaken before the refractive and corneal topography measurements. Our findings may also lead to a better understanding of the relationship between reading and the development of refractive errors.
We thank Robert Iskander, Mark Morelande, and Brett Davis for their advice and assistance with various aspects of the data analysis.
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Keywords:© 2003 American Academy of Optometry
corneal topography; reading; lid forces; aberrations; refractive error