How Do Most Young Moderate Hyperopes Avoid Strabismus?

Abstract

Purpose: Uncorrected hyperopic children must overcome an apparent conflict between accommodation and vergence demands to focus and align their retinal images. This study tested hypotheses about simultaneous accommodation and vergence performance of young hyperopes to gain insight into ocular motor strategies used to maintain eye alignment.

Methods: Simultaneous eccentric photorefraction and Purkinje image tracking were used to assess accommodative and vergence responses of 26 adult emmetropes (AE) and 94 children (0-13 years) viewing cartoons. Children were habitually uncorrected (CU) (spherical equivalent refractive error [SE] -0.5 to +4 D), corrected and aligned (CCA), or corrected with a history of refractive esotropia (CCS). Accommodative and vergence accuracy, dissociated heterophoria, and vergence/accommodation ratios in the absence of retinal disparity cues were measured for 33- and 80-cm viewing distances.

Results: In binocular viewing, median accommodative lags for 33 cm were 1.0 D (AE), 1.33 D (CU), 1.25 D (CCA), and 1.0 D (CCS). Median exophorias at 80 and 33 cm were 1.2 and 4.5 pd (AE), 0.8 and 2.5 pd (CU), and 0 and 1.2 pd (CCA), respectively. Without disparity cues, most response vergence/accommodation ratios were between 1 and 2 meter angle/D (∼5-10 pd/D) (69% of AE, 44% of CU, 60% of CCA, and 50% of CCS).

Conclusions: Despite apparent conflict in motor coupling, uncorrected hyperopes were typically exophoric and achieved adultlike accuracy of both vergence and accommodation simultaneously, indicating ability to compensate for conflicting demands rather than bias to accurate vergence while tolerating inaccurate accommodation. Large lags and esophoria are therefore atypical. This analysis provides normative guidelines for clinicians and a deeper mechanistic understanding of how hyperopes avoid strabismus.

Figure 1.

An illustration of the questions addressed in this study. An uncorrected child with nonstrabismic hyperopia could be predicted to have inaccurate accommodation (A), a large esophoria (B), a robust vergence adaptation system (C), a large fusional vergence range (D), and/or reduced proximal vergence and a low AC/A ratio (E) when they view a target.

Figure 2.

(A) A participant watching a movie through an aperture, while the horizontally mounted screen was moved back and forth along a motorized track in front of the PowerRef3 camera. The movie was presented using a beamsplitter mounted below the screen. The inset processed image collected by the camera demonstrates the principles of eccentric photorefraction and Purkinje image tracking. The equipment was covered with the lid during data collection and the room lights were dim to reduce distraction. (B) An illustration of the addition of a mirror for MEM retinoscopy.

Figure 3.

An example phoria measurement trial collected from a 5.5-year-old child with +4.00 D uncorrected hyperopia at a 33-cm viewing distance. Data were smoothed for illustration purposes. The top panel shows the refractive state for the right eye (RE) and left eye (LE), and the bottom panel shows the vergence alignment data. The white background indicates periods of binocular viewing (B), light shading indicates RE covered (R), and darker shading indicates LE covered (L). The covering of either eye elicits a latent convergent misalignment (esophoria) for this participant, with minimal change in accommodation. The accommodation data are separated vertically for clarity and merely represent change in response over time.

Figure 4.

Data from an example fusional divergence trial. A hyperopic child's responses to increasing and then decreasing steps of Base-In prism during a 140-second trial. Top panel: Refractive state of the right (RE) and left (LE) eyes, with upward indicating relaxation of accommodation. Bottom panel: Measured vergence position and magnitude of introduced prism (black step function), with upward indicating increased Base-In prism or apparent convergent alignment of the eyes. If the eyes realigned to overcome the prismatic demand, there was no change in the measured vergence position from the baseline value. When the participant was unable to overcome the prism driving divergence, the optical effect of the prism is visible in the apparently convergent vergence position data (gray shaded region). The accommodation data are vertically separated for clarity. The white background indicates periods when the eyes were aligned, and the participant was able to overcome the demand.

Figure 5.

The distribution of participants’ spherical equivalent refractive error as a function of age. CU (A), AE (B), CCA (C), and CCS (D). Open triangles represent the eye with less hyperopia (LHE), and filled dots represent the eye with more hyperopia (MHE).

Figure 6.

MEM accommodative lag of the less hyperopic (A) and more hyperopic (B) eye as a function of its spherical equivalent refractive error (cycloplegic refraction for children), for a 33-cm viewing distance. Positive values indicate accommodative lag and negative indicate accommodative lead.

Figure 7.

Mean-difference plots for the MEM retinoscopy and PowerRef 3 accommodative lag data for the less hyperopic eye, which was assumed to be used to view the target. (A) AE and CU. (B) CCA and CCS. The solid and dashed colored lines represent the mean and 95% limits of agreement for the group represented by each color.

Figure 8.

Dissociated heterophoria (A, B) and simultaneous accommodation changes between binocular and monocular viewing (C, D) during the 5-second measurements as a function of spherical equivalent refractive error of the less hyperopic eye for AE, CU, and CCA at 80-cm and 33-cm viewing distances. Positive values indicate exophoria and relaxation of accommodation. The lines in panels A and B represent the predicted amount of phoria, based on the median emmetropic adult phoria for each distance with a stable accommodative lag and a stimulus AC/A ratio of 3.5 pd/D (solid lines) or a response AC/A ratio of 8.6 pd/D (dashed lines).

Figure 9.

Dissociated heterophoria after 30 seconds of occlusion as a function of spherical equivalent refractive error of the less hyperopic eye for AE, CU, and CCA. The (A) 80-cm and (B) 33-cm viewing distances. Positive values indicate exophoria and hyperopia. The lines in panels A and B represent the predicted amount of phoria, based on the median emmetropic adult phoria for each distance with a stable accommodative lag and a stimulus AC/A ratio of 3.5 pd/D (solid lines) or a response AC/A ratio of 8.6 pd/D (dashed lines).

Figure 10.

The relationship between accommodative lag, phoria, and spherical equivalent refractive error in the adult emmetropes (A), uncorrected hyperopes of up to 4 D (B), and aligned hyperopes with correction (C) for the 33-cm viewing distance. The marker colors in each panel represent spherical equivalent refractive error as shown in the color bar. Positive values indicate hyperopia, accommodative lag, and exophoria.

Figure 11.

The relationship between accommodative lag and phoria in uncorrected hyperopes of up to 4 D for the 33-cm viewing distance. The children who have ≥3.0 D of hyperopia are shown as filled black circles, those who have anisometropia ≥1.0 D are shown with an additional circle around their data, and those with amblyopia are shown with a larger additional circle around them. Anyone with <3.0 D of hyperopia is represented by a small open circle. Positive values indicate accommodative lag and exophoria.

Figure 12.

Fusional vergence ranges around the dissociated heterophoria position and alignment of the eyes at the target (0 pd). (A) Adult emmetropes, (B) uncorrected children, (C) corrected and aligned children, and (D) corrected children with a history of esotropia. Each line represents the range of prismatic values over which an individual participant could realign their eyes (1 pd = 0.57 deg). Positive x-axis values represent divergent demand and exophoria. In each case, the asterisk represents the prism where the eyes have been stimulated to reach the position of their dissociated heterophoria. Currently strabismic participants have a diamond at their strabismic angle. The color scale represents the cycloplegic spherical equivalent refractive error of the less hyperopic eye in diopters.

Figure 13.

Change in accommodation during fusional range measurements for the AE, CU, CCA, and CCS groups. The change in accommodation is plotted as a function of the limit of the fusional range. Positive fusional range limits indicate divergence and positive accommodation changes indicate relaxation of accommodation toward hyperopic defocus.

Figure 14.

The relationship between change in vergence and accommodation responses when changing fixation from a target at an 80-cm to a 33-cm viewing distance in monocular viewing. The color scale represents the spherical equivalent refractive error of the less hyperopic eye in diopters. The diagonal black line represents a ratio of changes of 1 MA/D, the blue line represents 2 MA/D, and the red line indicates 0.5 MA/D. Positive values indicate increasing accommodation and convergence. The black dotted line indicates the demand of 1.75 MA of vergence. In the absence of a measurement of accommodation, all data on this line would be interpreted as a stimulus AC/A ratio of 1 MA/D (6 pd/D for an adult with a 6-cm interpupillary distance [IPD] and 4.5 pd/D for a child with a 4.5-cm IPD). The gray shaded area represents accommodation changes of <0.5 D that were excluded from summary analyses.