Falls are a significant cause of injury, health care utilization, morbidity, and mortality among older adults.1,2 Importantly, older adults with visual impairment are more likely to experience falls compared with their normally sighted counterparts, as shown in population studies3,4 and in cohorts with specific ocular diseases, such as age-related macular degeneration5,6 and glaucoma.7 This increased risk of falls may partially arise from the reduced ability of older adults with visual impairment to extract relevant visual information from the environment to guide safe walking.
The visual impairment from refractive blur, associated with wearing presbyopic multifocal spectacle corrections, including bifocals and progressive lenses, may also contribute to the increased fall risk among older adults because of the resultant blurring of the lower portion of the field of view. Lord et al.8 found that multifocal wearers were more than twice as likely to fall compared with nonmultifocal wearers, particularly when precision stepping tasks were involved, such as stair negotiation. Even in adapted wearers, multifocal corrections have been demonstrated to increase the number of contacts with ground-level obstacles9 and increase the risk of tripping through greater variability in toe clearance and foot placement when negotiating raised surfaces10,11 compared with single-vision lens corrections. Furthermore, adaptive gait changes have been reported in inexperienced multifocal wearers for stepping tasks, including slower stepping speeds and increased toe clearance.12 Optical blur, of a similar magnitude to that resulting from multifocal corrections, has recently been shown to increase stepping errors.13 A randomized controlled trial found that the provision of single-vision distance spectacles for multifocal wearers significantly reduced the rate of falls among older adults who took part in regular outdoor activities.14
Coordinated visuomotor stepping control is required to walk safely through the environment, where accurate visual identification of potential hazards guides appropriate planning and execution of the lower limb trajectory and foot placement.15 In uncluttered environments where there are no constraints on foot placement for safety, such as an unobstructed level footpath, gaze is generally directed several steps ahead and visual information is used in a feed-forward manner for path planning.16 However, in challenging or cluttered environments where precise foot placement is crucial for safety, such as stair negotiation, gaze is directed downward toward the area of the stepping location, facilitating accurate visual localization of the stepping location and optimizing the accuracy of the endpoint foot placement.16,17 In these precision stepping situations, vision is used in a feedback, or online, manner to continuously adjust foot trajectory during the step action to improve stepping accuracy, followed by a gaze transfer away from the stepping location as the foot contacts the ground.18,19 Importantly, poor stepping accuracy has been identified as a potential indicator of fall risk among older adults.19,20
Age-related differences in stepping gaze behaviors, where some older adults prematurely transfer their gaze away from the foot landing locations before placing their foot on the ground, have also been demonstrated.19 This strategy may assist in planning of future stepping actions in challenging visual environments but at the cost of reduced stepping accuracy and precision.19 Indeed, there is evidence that older adults can improve stepping accuracy by altering their gaze behavior to maintain fixation on stepping targets until heel contact is made.21 Importantly, prematurely transferring gaze farther ahead from a stepping target relies on the use of the inferior visual field to guide the final foot placement. The use of nonfoveal visual information has been shown to reduce stepping placement accuracy in young participants, when laterally viewing a stepping target (about 10 deg to the right and left) compared with directly viewing the target.22
Previous research thus highlights the importance of using visual information to guide spatial planning of stepping location and the impact of visual impairment from blur. The aim of the present study was to investigate the impact of optical blur, similar to that resulting from commonly prescribed presbyopic multifocal corrections, and the location of gaze on the stepping accuracy of older adults during a precision stepping task to better understand potential mechanisms underlying the increased fall risk seen with these corrections. Participants included current multifocal wearers and nonwearers to also assess whether existing multifocal wearers would exhibit less problems with blur given that they should have already been adapted to blur at ground level.
Nineteen community-dwelling older adults (11 women, 8 men; mean age, 71.6 ± 8.8 years; range, 53 to 85 years) were recruited from the QUT Optometry Clinic. Participants were independently mobile and were excluded if they had any significant ocular disease or any neurological or musculoskeletal disorders, which could affect their balance or gait. Participants were excluded if best-corrected visual acuity was worse than 0.1 logMAR in either eye (6/7.5, 20/25 Snellen equivalent) or had any significant cataracts (graded 4.0 or worse as defined by the Lens Opacities Classification System23). The research followed the tenets of the Declaration of Helsinki, and informed consent was obtained before participant assessment. The study was approved by the Queensland University of Technology Human Research Ethics Committee.
Visual Function Assessment
Binocular visual acuity and contrast sensitivity were measured with the best-corrected refractive correction, which was determined subjectively at the time of the study. Visual acuity was measured with a high-contrast logMAR chart using a letter-by-letter scoring system at 5 m with a chart luminance of 125 cd/m2. Contrast sensitivity was measured binocularly using the paper version of the Melbourne Edge Test at a working distance of 40 cm using an appropriate near correction and an average luminance of 65 cd/m2. The Melbourne Edge Test is a 4-alternative forced-choice edge detection test, where participants are asked to identify the orientation of the edge within each circular patch until two consecutive incorrect responses are made, and the lowest contrast edge correctly identified recorded as the participant’s contrast sensitivity in decibels. Monocular visual fields were assessed using a 40-point screening test (Model HFA-II 750 m; Carl Zeiss Meditec; www.zeiss.com) to ensure participants had no visual field defects. The habitual spectacle correction design worn by participants was recorded.
For the precision stepping task, participants were instructed to take a single step forward on the same level at a self-selected pace, from a stationary standing position, leading with their dominant foot and placing this foot as accurately as possible onto a stepping target located directly in front of them, as shown in Fig. 1. The stepping target comprised a contour of each participant’s stepping foot, which had been previously drawn using a white marker onto the gray floor surface (Weber contrast 8%) and was positioned 30 cm in front of the starting position, which approximated an average step length.22 Foot dominance was determined according to participants’ reported preference for kicking a ball.
Before each stepping trial, participants were instructed to fixate on one of three gaze positions: (1) on the stepping target (aligned with the toe position), (2) 30 cm farther forward or away from the stepping target (30 cm gaze position), or (3) 60 cm farther forward or away from the stepping target (60 cm gaze position). The gaze positions were indicated by yellow dots on the floor. The angular difference between each of the gaze positions was about 10 deg based on an average person’s height of 160 cm.
Participants completed the stepping tasks under two visual conditions using their best-spherocylinder spectacle correction and with an additional +2.50DS blur to reflect the blur resulting from commonly prescribed multifocal lens additions for patients aged 70 years and older, who are those older adults most at risk of falling. For each visual condition, standard single-vision trial lenses (38-mm diameter) were mounted into Halberg trial lens clips fitted into the eye-tracker goggles. Participants performed 10 trials for each combination of gaze position and visual condition, resulting in a total of 60 (10 by 3 by 2) stepping trials. The conditions were presented in randomized blocks for each vision and gaze position combination. Participants were provided with several practice trials before testing.
Participants wore socks for all stepping trials, onto which three retroreflective markers were mounted (Fig. 2). Five fixed floor-mounted retroreflective markers were also located under the small perforations (about 0.5 mm in diameter) of the gray flooring, which were inconspicuous to participants. After each step, the final foot position was recorded using a flash high-resolution digital camera (Nikon D3000; Nikon; www.nikon.com; 10 megapixels, 3872 by 2592 pixels) mounted on a tripod above the stepping target, which captured the reflected light from the foot and floor-mounted retroreflective markers. A reference step was generated from a photo of each participant’s foot positioned directly in the center of the stepping target before experimental testing. Photographs were taken of a standard ruler before testing each participant to calibrate the pixel-to-length ratio. For each trial photograph, the center pixel coordinates of the foot and floor markers (which subtended about 5 pixels in diameter) were determined by a single-masked grader. Analysis of localization errors for the fixed floor-based markers for the 60 trials across participants showed low variability, with a standard deviation of less than 1 pixel (∼0.2 mm).
A head-mounted eye tracker (ASL MobileEye; Applied Science Laboratories; www.asleyetracking.com) was used to monitor gaze position in real time during each step. For the 30- and 60-cm gaze position trials, participants were instructed to view the stepping target before directing their fixation to the appropriate gaze position. Trials were repeated if gaze was not maintained at the appropriate position for the complete stepping action.
Data and Statistical Analysis
For each stepping trial, the midpoint of the foot in the landing position was calculated as the mean position of the two lateral foot markers. Absolute foot placement error was calculated as the Euclidean distance between the midpoint of each step and the midpoint of the reference step. Anteroposterior and mediolateral foot placement errors were calculated in a similar fashion using the anteroposterior and mediolateral distances between the midpoints of each step and the reference step. Within-subject foot placement variability was quantified using the standard deviations for the respective absolute, anteroposterior, and mediolateral foot placement errors.
For this repeated-measures design, a series of random intercept linear mixed models was fitted to assess changes in stepping parameters for the blur and gaze conditions using the maximum likelihood procedure in SPSS (Version 21.0; http://www-01.ibm.com/software/analytics/spss/). The covariance structure used was autoregressive, to account for the correlation among repeated measures, based on the Akaike Information Criterion.24 Separate analyses were conducted for each of the stepping measures, with each model incorporating a random intercept for participants, and fixed effects of gaze position (three levels: on-target, 30 cm, and 60 cm), visual condition (two levels: best-corrected, +2.50DS blur), and an interaction term. Stepping sequence and condition order were also included in the models as fixed effects, as they significantly improved the model fits and adjusted for potential learning effect with repeated stepping trials. Any significant main effects or interactions were examined using Bonferroni-adjusted post hoc comparisons.
To further explore whether habitual spectacle correction influenced the stepping measures, a variable for habitual spectacle type (nonmultifocal vs. multifocal correction) was also included in these models to test our hypotheses that existing multifocal wearers would exhibit better stepping accuracy and less variability under the blur conditions than nonmultifocal wearers given that they should already be adapted to blur at ground level.
For the best-corrected vision condition, mean binocular visual acuity was −0.04 ± 0.07 logMAR and Melbourne Edge Test contrast sensitivity was 21.7 ± 1.1 dB. The +2.50DS blurring lenses reduced binocular visual acuity to 0.54 ± 0.13 logMAR. Participants regularly wore a range of spectacle corrections when walking: 9 did not wear any multifocal correction (eight no correction, one single-vision distance), and 10 wore a multifocal correction (five bifocals, five progressives). Means and standard deviations of the stepping outcome measures are presented in Table 1.
Stepping Accuracy: Foot Placement Errors
There were significant main effects of gaze position (F2,298 = 53.8, p < 0.001) and visual condition (F1,411 = 13.8, p < 0.001) on absolute foot placement error. There was also a significant gaze position by visual condition interaction on absolute foot placement error (F2,356 = 5.6, p = 0.004; Fig. 3). For both visual conditions, post hoc comparisons revealed that absolute stepping errors were significantly larger with increasing gaze eccentricity from the target (p < 0.05). Furthermore, absolute stepping errors were significantly larger with +2.50DS blur at the 60-cm gaze position compared with best-corrected vision (p = 0.001).
In the anteroposterior direction, there was a significant main effect of visual condition on foot placement errors (F1,420 = 16.2, p < 0.001), but no significant main effect of gaze position (F2,271 = 2.0, p = 0.13). However, there was a significant gaze position by visual condition interaction (F2,347 = 5.4, p = 0.005). With best-corrected vision, post hoc comparisons revealed that participants overstepped onto the target (more anterior foot placement) when viewing the 60-cm gaze position compared with the on-target and 30-cm positions (p = 0.025). With +2.50DS blur, participants significantly understepped onto the target (more posterior foot placement) at the 30- and 60-cm gaze positions compared with the on-target position (p < 0.027), but this was not evident when directly viewing the target (p = 0.67). Furthermore, the +2.50DS blur resulted in significantly more understepping errors onto the target for both the 30- and 60-cm gaze positions compared with best-corrected vision (p < 0.026).
In the mediolateral direction, there were no significant main or interaction effects of gaze position or visual condition on foot placement errors (p > 0.05).
Stepping Precision: Within-Subject Foot Placement Variability
There were significant main effects of gaze position (F2,48 = 31.3, p < 0.001) and visual condition (F1,32 = 10.3, p = 0.003) on absolute foot placement variability, as well as a significant gaze position by visual condition interaction (F2,85 = 5.7, p = 0.005; Fig. 4). With best-corrected vision, variability was significantly larger when viewing the 30- and 60-cm gaze positions than the on-target position (p < 0.048). With +2.50DS blur, variability was significantly larger with increasing gaze eccentricity from the target (p < 0.019). Furthermore, absolute stepping variability was significantly larger with +2.50DS blur at the 60-cm gaze position than with best-corrected vision (p = 0.001).
In the anteroposterior direction, there were significant main effects of gaze position (F2,48 = 16.0, p < 0.001) and visual condition (F1,37 = 9.3, p = 0.004) on foot placement variability, as well as a significant gaze position by vision condition interaction (F2,85 = 4.0, p = 0.022). With best-corrected vision, post hoc comparisons revealed a difference in anteroposterior stepping variability only between the 60-cm and on-target gaze positions (p = 0.04). With the +2.50DS blur, significantly larger variability was found between the 60-cm gaze position compared with the on-target and 30-cm positions (p < 0.001). Furthermore, anteroposterior stepping variability was significantly larger with +2.50DS blur at the 60-cm gaze position than with best-corrected vision (p = 0.005).
In the mediolateral direction, there was a significant main effect of gaze position on foot placement variability (F2,52 = 10.2, p < 0.001), showing greater variability for the 30- and 60-cm gaze positions compared with the on-target position. There was no main effect of visual condition (F1,41 = 0.6, p = 0.43) or an interaction effect (F2,87 = 0.5, p = 0.63) for mediolateral foot placement variability.
When habitual spectacle correction was also included in the analyses, no significant differences were found between multifocal and nonmultifocal wearers across all of the stepping measures (p = 0.23 to 0.77); however, post hoc power analysis indicated that the sample size provided only 19% power to detect differences across stepping outcomes between the groups at a level of α = 0.05.
The results of this study indicate that stepping accuracy and precision are reduced among healthy normally sighted older adults when gaze is directed farther ahead from the immediate stepping location, as shown by increased foot placement errors and variability. Furthermore, optical blur reduced stepping accuracy and precision and compounded the effect of gaze position particularly when gaze was positioned 60 cm farther forward of the stepping target. These findings are important given that many older adults wear multifocal spectacle corrections when walking and the feed-forward nature of visual control when walking means that their gaze is generally directed about two steps ahead of the target.25
Precision stepping tasks require gaze fixations toward a stepping target before initiation of the foot swing to step onto a target, using vision in an online manner to adjust foot trajectory during the step action to optimize stepping accuracy, followed by saccadic eye movements away from a stepping target as the heel of the foot contacts the target.16,18,19 Importantly, some older adults demonstrate premature gaze transfer before foot placement to the detriment of their stepping accuracy.19 Our study supports these previous findings, highlighting the importance of maintaining gaze position on the stepping targets to maximize stepping accuracy and precision. When gaze is directed ahead of the stepping target, the inferior peripheral visual field is used to modulate limb trajectory and guide foot placement, and our findings indicate that this does not provide the level of visual information required for a precision stepping task. Our findings also support the benefits of gaze training to maintain gaze position on stepping locations when undertaking precision stepping tasks and to improve stepping accuracy and minimize the risk of trips or slips, particularly in older adults at high risk of falls.21 Although the observed magnitude of stepping errors in this study is not high, as measured using a simple stepping task under controlled conditions, there are many challenging environments in the natural environment where foot placement position is crucial for safety, such as when negotiating stairs or uneven pavements, where even small errors in foot position may be enough to instigate a trip or fall.
The findings of the present study agree with recent research that demonstrated that viewing targets laterally, about 10 degrees to the left and right of a stepping target, resulted in greater stepping errors and variability compared with on-target viewing in a group of young healthy participants.22 However, a lateral gaze position is unlikely to reflect natural gaze position when walking because individuals tend to look farther forward along the travel path when walking.25
Blur also significantly increased stepping errors and variability, which is consistent with previous research showing reductions in stepping accuracy with greater levels of refractive blur.13 Importantly, blur significantly interacted with gaze position, where stepping errors and variability were greatest under the blur condition, particularly when gaze was directed 60 cm ahead of the stepping target. Furthermore, blur resulted in significant understepping errors in the anteroposterior direction at the 30- and 60-cm gaze positions, most likely from the spectacle magnification effect of the +2.50 lenses26; however, no understepping errors were found when gaze was directed at the stepping target. Thus, older adults at a high risk of falls might benefit from single-vision glasses to improve stepping accuracy in addition to training to maintain gaze position on stepping locations until heel contact.21
There was no evidence in the current study to suggest that older adults regularly wearing multifocal corrections differed in their precision stepping behaviors under any of the visual conditions compared with nonmultifocal wearers. This suggests that habituation to blur from regular multifocal wear may not lead to improvements in stepping accuracy and supports the benefits of prescribing single-vision lenses, particularly in active older adults.14 However, our findings must be interpreted with caution given the small sample size (post hoc power analyses of all group comparisons were <80%). In addition, the single-vision lenses used in the present study do not incorporate any peripheral distortion or image jump effects, which are present in multifocal lenses, which may also impact stepping accuracy. Further research with larger samples is needed to explore these effects for both single-vision and multifocal corrections on visuomotor control.
The present study provides novel information pertaining to the contribution of vision to precision stepping in a well-controlled repeated-measures design using eye-tracking technology to ensure accurate gaze position for all trials. The novel approach using high-resolution still photography provided robust estimates of stepping position, but further research is warranted to compare our findings with those derived using standard motion capture technology. The study was also limited by its sample size, which was not powered to detect between-group differences for multifocal and nonmultifocal wearers. In addition, the stepping task, although having the advantage of providing a controlled and repeatable task, may not completely represent gaze and stepping within natural environments, where gaze might be redirected toward the stepping location during the swing phase of the leg to make corrections. Furthermore, the set stepping length used in this study may not have corresponded to participants’ preferred step length, and future work should consider scaling of this length according to participants’ height. Lastly, healthy active participants were included, so the results cannot be generalized to frailer, less independent, older populations. Therefore, further research is needed to examine how stepping precision is affected among older adults at a higher risk of falling, including those with vision impairment from ocular disease.
In conclusion, this study provides important insights into the contribution of vision to the spatial planning of precision steps, highlighting the detrimental effects of increasing gaze position away from imminent stepping locations and visual impairment from optical blur. These findings indicate that blur, similar to that used in multifocal corrections, has the potential to increase the risk of trips and falls among older populations when negotiating challenging environments where precision stepping is required, particularly as gaze is directed farther ahead from stepping locations when walking.
School of Optometry and Vision Science
Queensland University of Technology
Victoria Park Rd
Kelvin Grove Queensland 4059
e-mail: [email protected]
We thank Mr. James Urquhart for his valuable assistance with the image analysis as well as the participants who gave so generously of their time.
Received June 30, 2015; accepted December 2, 2015.
1. Tinetti ME, Speechley M, Ginter SF. Risk factors for falls among elderly persons living in the community. N Engl J Med 1988; 319: 1701–7.
2. Bradley C. Hospitalisations Due to Falls by Older People, Australia 2009–2010. Injury Research and Statistics Series No. 70 (INJCAT 146). Canberra: Australian Institute of Health and Welfare; 2013.
3. Coleman AL, Cummings SR, Yu F, Kodjebacheva G, Ensrud KE, Gutierrez P, Stone KL, Cauley JA, Pedula KL, Hochberg MC, Mangione CM. Binocular visual-field loss increases the risk of future falls in older white women. J Am Geriatr Soc 2007; 55: 357–64.
4. Patino CM, McKean-Cowdin R, Azen SP, Allison JC, Choudhury F, Varma R. Central and peripheral visual impairment and the risk of falls and falls with injury. Ophthalmology 2010; 117: 199–206.
5. Szabo SM, Janssen PA, Khan K, Lord SR, Potter MJ. Neovascular AMD: an overlooked risk factor for injurious falls. Osteoporos Int 2010; 21: 855–62.
6. Wood JM, Lacherez P, Black AA, Cole MH, Boon MY, Kerr GK. Risk of falls, injurious falls, and other injuries resulting from visual impairment among older adults
with age-related macular degeneration. Invest Ophthalmol Vis Sci 2011; 52: 5088–92.
7. Black AA, Wood JM, Lovie-Kitchin JE. Inferior field loss increases rate of falls in older adults
with glaucoma. Optom Vis Sci 2011; 88: 1275–82.
8. Lord SR, Dayhew J, Howland A. Multifocal glasses impair edge-contrast sensitivity and depth perception and increase the risk of falls in older people. J Am Geriatr Soc 2002; 50: 1760–6.
9. Menant JC, St George RJ, Sandery B, Fitzpatrick RC, Lord SR. Older people contact more obstacles when wearing multifocal glasses and performing a secondary visual task. J Am Geriatr Soc 2009; 57: 1833–8.
10. Johnson L, Buckley JG, Scally AJ, Elliott DB. Multifocal spectacles increase variability in toe clearance and risk of tripping in the elderly. Invest Ophthalmol Vis Sci 2007; 48: 1466–71.
11. Johnson L, Buckley JG, Harley C, Elliott DB. Use of single-vision eyeglasses improves stepping precision and safety when elderly habitual multifocal wearers negotiate a raised surface. J Am Geriatr Soc 2008; 56: 178–80.
12. Beschorner KE, Milanowski A, Tomashek D, Smith RO. Effect of multifocal lens glasses on the stepping patterns of novice wearers. Gait Posture 2013; 38: 1015–20.
13. Black AA, Kimlin JA, Wood JM. Stepping accuracy
and visuomotor control
among older adults
: effect of target contrast and refractive blur
. Ophthalmic Physiol Opt 2014; 34: 470–8.
14. Haran MJ, Cameron ID, Ivers RQ, Simpson JM, Lee BB, Tanzer M, Porwal M, Kwan MMS, Severino C, Lord SR. Effect on falls of providing single lens distance vision glasses to multifocal glasses wearers: VISIBLE randomised controlled trial. BMJ 2010; 340: c2265.
15. Patla AE. Understanding the roles of vision in the control of human locomotion. Gait Posture 1997; 5: 54–69.
16. Marigold DS. Role of peripheral visual cues in online visual guidance of locomotion. Exerc Sport Sci Rev 2008; 36: 145–51.
17. Reynolds RF, Day BL. Visual guidance of the human foot during a step. J Physiol 2005; 569: 677–84.
18. Chapman GJ, Hollands MA. Evidence for a link between changes to gaze behaviour and risk of falling in older adults
during adaptive locomotion. Gait Posture 2006; 24: 288–94.
19. Chapman GJ, Hollands MA. Evidence that older adult fallers prioritise the planning of future stepping actions over the accurate execution of ongoing steps during complex locomotor tasks. Gait Posture 2007; 26: 59–67.
20. Yamada M, Higuchi T, Tanaka B, Nagai K, Uemura K, Aoyama T, Ichihashi N. Measurements of stepping accuracy
in a multitarget stepping task as a potential indicator of fall risk in elderly individuals. J Gerontol A Biol Sci Med Sci 2011; 66: 994–1000.
21. Young WR, Hollands MA. Can telling older adults
where to look reduce falls? Evidence for a causal link between inappropriate visual sampling and suboptimal stepping performance. Exp Brain Res 2010; 204: 103–13.
22. Smid KA, den Otter AR. Why you need to look where you step for precise foot placement: the effects of gaze eccentricity on stepping errors. Gait Posture 2013; 38: 242–6.
23. Chylack LT Jr., Wolfe JK, Singer DM, Leske MC, Bullimore MA, Bailey IL, Friend J, McCarthy D, Wu SY. The Lens Opacities Classification System III. The Longitudinal Study of Cataract Study Group. Arch Ophthalmol 1993; 111: 831–6.
24. Field A. Discovering Statistics Using IBM SPSS Statistics, 4th ed. Los Angeles: Sage; 2013.
25. Patla AE, Vickers JN. How far ahead do we look when required to step on specific locations in the travel path during locomotion? Exp Brain Res 2003; 148: 133–8.
26. Elliott DB, Chapman GJ. Adaptive gait changes due to spectacle magnification and dioptric blur
in older people. Invest Ophthalmol Vis Sci 2010; 51: 718–22.