Eye–Hand Coordination Impairment in Glaucoma Patients
Abstract
:1. Introduction
2. Materials and Methods
2.1. Clinical Tests
2.2. Measurement of Eye–Hand Coordination
- (1)
- Aiming. The pen was used to touch 20 sensors placed in a row on the board as quickly as possible. The time to perform the test (t) in seconds (s) and number of hits (n) were measured. The aiming index (ai), defined as the ratio of the number of targeted hits to the time taken to perform the test, was calculated, ai = n/t (s−1).
- (2)
- Linear tracking. The pen was used to follow a groove with several bends, angles, and curves without touching the sides or bottom of the baseplate. The number of errors (n; i.e., scored by the number of times the pen touches the surface), error duration (s), and time taken to perform the task (t) in seconds (s) were measured. The linear tracking index (ti) was calculated as the number of target errors to the time taken to perform the test, ti = n/t (s−1)
- (3)
- Tremor test (steadiness). The task involved keeping the pen inside a hole (inner diameter of 5 mm) on the board without touching the walls for a specified time (32 s). The task was assessed based on the number of errors (n; i.e., scored by the number of times the pen touches the wall) and the average error duration (s).
- (4)
- Tapping test. The pen was used to strike a special 40 × 40 mm square surface as many times as possible within a specified time (32 s). The number of accurate hits (n) was used to determine the wrist–finger speed of untargeted movements with maximal frequency.
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Mariotti, S.P. Global Data on Visual Impairment, 2010; Switzerland World Health Organisation: Geneva, Switzerland, 2012. [Google Scholar]
- Waugh, D.T. The contribution of fluoride to the pathogenesis of eye diseases: Molecular mechanisms and implications for public health. Int. J. Environ. Res. Public Health 2019, 16, 856. [Google Scholar] [CrossRef]
- Quigley, H.A. Glaucoma. Lancet 2011, 377, 1367–1377. [Google Scholar] [CrossRef]
- Tham, Y.C.; Li, X.; Wong, T.Y.; Quigley, H.A.; Aung, T.; Cheng, C.Y. Global prevalence of glaucoma and projections of glaucoma burden through 2040: A systematic review and meta-analysis. Ophthalmology 2014, 121, 2081–2090. [Google Scholar] [CrossRef] [PubMed]
- Ehrlich, J.R.; Moroi, S.E. Glaucoma, Cognitive Decline, and Healthy Aging. JAMA Ophthalmol. 2017, 135, 740–741. [Google Scholar] [CrossRef] [PubMed]
- Quaranta, L.; Riva, I.; Gerardi, C.; Oddone, F.; Floriani, I.; Konstas, A.G. Quality of life in glaucoma: A review of the literature. Adv. Ther. 2016, 33, 959–981. [Google Scholar] [CrossRef] [PubMed]
- Chun, Y.S.; Sung, K.R.; Park, C.K.; Kim, H.K.; Yoo, C.; Kim, Y.Y.; Park, K.H.; Kim, C.Y.; Choi, K.R.; Lee, K.W.; et al. Vision-Related quality of life according to location of visual field loss in patients with glaucoma. Acta Ophthalmol. 2019, 97, e772–e779. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.Y.; Rousseau, J.; Boisjoly, H.; Schmaltz, H.; Kergoat, M.J.; Moghadaszadeh, S.; Djafari, F.; Freeman, E.E. Activity limitation due to a fear of falling in older adults with eye disease. Investig. Ophthalmol. Vis. Sci. 2012, 53, 7967–7972. [Google Scholar] [CrossRef]
- Friedman, D.S.; Freeman, E.; Munoz, B.; Jampel, H.D.; West, S.K. Glaucoma and mobility performance: The salisbury eye evaluation project. Ophthalmology 2007, 114, 2232–2237. [Google Scholar] [CrossRef]
- Gomes, H.A.; Moreira, B.S.; Sampaio, R.F.; Furtado, S.R.C.; Cronemberger, S.; Gomes, R.A.; Kirkwood, R.N. Gait parameters, functional mobility and fall risk in individuals with early to moderate primary open angle glaucoma: A cross-sectional study. Braz. J. Phys. Ther. 2018, 22, 376–382. [Google Scholar] [CrossRef]
- Tatham, A.J.; Boer, E.R.; Gracitelli, C.P.; Rosen, P.N.; Medeiros, F.A. Relationship between motor vehicle collisions and results of perimetry, useful field of view, and driving simulation in drivers with glaucoma. Transl. Vis. Sci. Technol. 2015, 4, 5. [Google Scholar] [CrossRef]
- Lee, S.S.; Black, A.A.; Wood, J.M. Scanning behavior and daytime driving performance of older adults with glaucoma. J. Glaucoma 2018, 27, 558–565. [Google Scholar] [PubMed]
- Alkarmo, W.; Ouhib, F.; Aqil, A.; Thomassin, J.M.; Yuan, J.; Gong, J.; Vertruyen, B.; Detrembleur, C.; Jérôme, C. Poly(ionic liquid)-Derived N-Doped Carbons with Hierarchical Porosity for Lithium- and Sodium-Ion Batteries. Macromol. Rapid. Commun. 2019, 40, e1800545. [Google Scholar] [CrossRef] [PubMed]
- Kasneci, E.; Sippel, K.; Aehling, K.; Heister, M.; Rosenstiel, W.; Schiefer, U.; Papageorgiou, E. Driving with binocular visual field loss? A study on a supervised on-road parcours with simultaneous eye and head tracking. PLoS ONE 2014, 9, e87470. [Google Scholar] [CrossRef] [PubMed]
- Rolle, T.; Dallorto, L.; Cafasso, R.; Mazzocca, R.; Curto, D.; Nuzzi, R. Reading ability in primary open-angle glaucoma: Evaluation with radner reading charts. Optom. Vis. Sci. 2019, 96, 55–61. [Google Scholar] [CrossRef] [PubMed]
- Glen, F.C.; Crabb, D.P.; Smith, N.D.; Burton, R.; Garway-Heath, D.F. Do patients with glaucoma have difficulty recognizing faces? Investig. Ophthalmol. Vis. Sci. 2012, 53, 3629–3637. [Google Scholar] [CrossRef]
- Daveckaite, A.; Grusauskiene, E.; Petrikonis, K.; Vaitkus, A.; Siaudvytyte, L.; Januleviciene, I. Cognitive functions and normal tension glaucoma. Indian J. Ophthalmol. 2017, 65, 974–978. [Google Scholar]
- Bulut, M.; Yaman, A.; Erol, M.K.; Kurtulus, F.; Toslak, D.; Coban, D.T.; Başar, E.K. Cognitive performance of primary open-angle glaucoma and normal-tension glaucoma patients. Arq. Bras. Oftalmol. 2016, 79, 100–104. [Google Scholar] [CrossRef] [Green Version]
- Ogata, N.G.; Daga, F.B.; Jammal, A.A.; Boer, E.R.; Hill, L.L.; Stringham, J.M.; Susanna, R., Jr.; Medeiros, F.A. Mobile telephone use and reaction time in drivers with glaucoma. JAMA Netw. Open 2019, 2, e192169. [Google Scholar] [CrossRef]
- Miller, A.B.; Lajoie, K.; Strath, R.A.; Neima, D.R.; Marigold, D.S. Coordination of gaze behavior and foot placement during walking in persons with glaucoma. J. Glaucoma. 2018, 27, 55–63. [Google Scholar] [CrossRef]
- Smith, N.D.; Glen, F.C.; Crabb, D.P. Eye movements during visual search in patients with glaucoma. BMC Ophthalmol. 2012, 12, 45. [Google Scholar] [CrossRef]
- Abrams, R.A.; Meyer, D.E.; Kornblum, S. Eye-hand coordination: Oculomotor control in rapid aimed limb movements. J. Exp. Psychol. Hum. Percept. Perform. 1990, 16, 248–267. [Google Scholar] [CrossRef] [PubMed]
- Shadmehr, R.; Smith, M.A.; Krakauer, J.W. Error correction, sensory prediction, and adaptation in motor control. Annu. Rev. Neurosci. 2010, 33, 89–108. [Google Scholar] [CrossRef] [PubMed]
- Bard, C.; Fleuy, M.; Hay, L. Development of Eye Hand Coordination across the Life Span; University of South Carolina Press: Columbia, SC, USA, 1990. [Google Scholar]
- Crawford, J.D.; Medendorp, W.P.; Marotta, J.J. Spatial transformations for eye-hand coordination. J. Neurophysiol. 2004, 92, 10–19. [Google Scholar] [CrossRef] [PubMed]
- Coats, R.O.; Fath, A.J.; Astill, S.L.; Wann, J.P. Eye and hand movement strategies in older adults during a complex reaching task. Exp. Brain Res. 2016, 234, 533–547. [Google Scholar] [CrossRef] [PubMed]
- Ketcham, C.J.; Seidler, R.D.; Van Gemmert, A.W.; Stelmach, G.E. Age-related kinematic differences as influenced by task difficulty, target size, and movement amplitude. J. Gerontol. B Psychol. Sci. Soc. Sci. 2002, 57, P54–P64. [Google Scholar] [CrossRef] [PubMed]
- Kotecha, A.; O’Leary, N.; Melmoth, D.; Grant, S.; Crabb, D.P. The functional consequences of glaucoma for eye-hand coordination. Investig. Ophthalmol. Vis. Sci. 2009, 50, 203–213. [Google Scholar] [CrossRef] [PubMed]
- Pardhan, S.; Scarfe, A.; Bourne, R.; Timmis, M. A comparison of reach-to-grasp and transport-to-place performance in participants with age-related macular degeneration and glaucoma. Investig. Ophthalmol. Vis. Sci. 2017, 58, 1560–1569. [Google Scholar] [CrossRef]
- Cohen, J. Statistical Power Analysis for the Behavioral Sciences; Routledge Academic: New York, NY, USA, 1988. [Google Scholar]
- Fritz, C.O.; Morris, P.E.; Richler, J.J. Effect size estimates: Current use, calculations, and interpretation. J. Exp. Psychol. Gen. 2012, 141, 2–18. [Google Scholar] [CrossRef]
- Noe, G.; Ferraro, J.; Lamoureux, E.; Rait, J.; Keeffe, J.E. Associations between glaucomatous visual field loss and participation in activities of daily living. Clin. Exp. Ophthalmol. 2003, 31, 482–486. [Google Scholar] [CrossRef]
- McKean-Cowdin, R.; Varma, R.; Wu, J.; Hays, R.D.; Azen, S.P.; Los Angeles Latino Eye Study Group. Severity of visual field loss and health-related quality of life. Am. J. Ophthalmol. 2007, 143, 1013–1023. [Google Scholar] [CrossRef]
- Lombardi, M.; Zenouda, A.; Azoulay-Sebban, L.; Lebrisse, M.; Gutman, E.; Brasnu, E.; Hamard, P.; Sahel, J.A.; Baudouin, C.; Labbé, A. Correlation between visual function and performance of simulated daily living activities in glaucomatous patients. J. Glaucoma 2018, 27, 1017–1024. [Google Scholar] [CrossRef] [PubMed]
- Ayala, M. Comparison of the monocular humphrey visual field and the binocular Humphrey Esterman visual field test for driver licensing in glaucoma subjects in Sweden. BMC Ophthalmol. 2012, 12, 35. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Lu, P.; Dai, M.; Huang, W.; Lin, J.; Huang, J. The relationship between binocular visual field loss and various stages of monocular visual field damage in glaucoma patients. J. Glaucoma 2019, 28, 42–50. [Google Scholar] [CrossRef] [PubMed]
- Shandiz, J.H.; Riazi, A.; Khorasani, A.A.; Yazdani, N.; Torab Mostaedi, M.; Zohourian, B. Impact of vision therapy on eye‑hand coordination skills in students with visual impairment. J. Ophthalmic. Vis. Res. 2018, 13, 301–306. [Google Scholar]
- Leung, C.K.; Chong, K.K.; Chan, W.M.; Yiu, C.K.; Tso, M.Y.; Woo, J.; Tsang, M.K.; Tse, K.K.; Yung, W.H. Comparative study of retinal nerve fiber layer measurement by StratusOCT and GDx VCC, II: Structure/function regression analysis in glaucoma. Investig. Ophthalmol. Vis. Sci. 2005, 46, 3702–3711. [Google Scholar] [CrossRef]
- Kim, J.H.; Lee, H.S.; Kim, N.R.; Seong, G.J.; Kim, C.Y. Relationship between visual acuity and retinal structures measured by spectral domain optical coherence tomography in patients with open-angle glaucoma. Investig. Ophthalmol. Vis. Sci. 2014, 55, 4801–4810. [Google Scholar] [CrossRef]
- Shaikh, A.G.; Otero-Millan, J.; Kumar, P.; Ghasia, F.F. Abnormal fixational eye movements in amblyopia. PLoS ONE 2016, 11, e0149953. [Google Scholar] [CrossRef]
- Chung, S.T.; Kumar, G.; Li, R.W.; Levi, D.M. Characteristics of fixational eye movements in amblyopia: Limitations on fixation stability and acuity? Vis. Res. 2015, 114, 87–99. [Google Scholar] [CrossRef]
- Schmetterer, L. Vascular optic neuropathies versus glaucomatous optic neuropathy. Acta Ophthalmol. 2014, 92, e4722. [Google Scholar] [CrossRef]
- Kothari, R.; Bokariya, P.; Singh, S.; Singh, R. A comprehensive review on methodologies employed for visual evoked potentials. Scientifica 2016, 2016, e9852194. [Google Scholar] [CrossRef]
- Jha, M.K.; Thakur, D.; Limbu, N.; Badhu, B.P.; Paudel, B.H. Visual Evoked Potentials in primary open angle glaucoma. J. Neurodegener. Dis. 2017, 2017, e9540609. [Google Scholar] [CrossRef] [PubMed]
- Parisi, V.; Miglior, S.; Manni, G.; Centofanti, M.; Bucci, M.G. Clinical ability of pattern electroretinograms and visual evoked potentials in detecting visual dysfunction in ocular hypertension and glaucoma. Ophthalmology 2006, 113, 216–228. [Google Scholar] [CrossRef] [PubMed]
- Geruschat, D.R.; Turano, K.A. Estimating the amount of mental effort required for independent mobility: Persons with glaucoma. Investig. Ophthalmol. Vis. Sci. 2007, 48, 3988–3994. [Google Scholar] [CrossRef] [PubMed]
- Guan, J.; Wade, M.G. The effect of aging on adaptive eye-hand coordination. J. Gerontol. B Psychol. Sci. Soc. Sci. 2000, 55, P151–P162. [Google Scholar] [CrossRef]
- Boisseau, E.; Scherzer, P.; Cohen, H. Eye-hand coordination in aging and in Parkinson’s Disease. Aging Neuropsychol. Cogn. 2002, 9, 266–275. [Google Scholar] [CrossRef]
- Van Halewyck, F.; Lavrysen, A.; Levin, O.; Boisgontier, M.P.; Elliott, D.; Helsen, W.F. Both age and physical activity level impact on eye-hand coordination. Hum. Mov. Sci. 2014, 36, 80–96. [Google Scholar] [CrossRef]
- Rand, M.K.; Stelmach, G.E. Effects of hand termination and accuracy requirements on eye-hand coordination in older adults. Behav. Brain Res. 2011, 219, 39–46. [Google Scholar] [CrossRef]
- Rand, M.K.; Stelmach, G.E. Effect of aging on coordinated eye and hand movements with two-segment sequence. Motor Control 2012, 16, 447–465. [Google Scholar] [CrossRef]
- Han, A.; Bokshan, S.L.; Marcaccio, S.E.; DePasse, J.M.; Daniels, A.H. Diagnostic criteria and clinical outcomes in sarcopenia research: A literature review. J. Clin. Med. 2018, 7, 70. [Google Scholar] [CrossRef]
- Yochim, B.P.; Mueller, A.E.; Kane, K.D.; Kahook, M.Y. Prevalence of cognitive impairment, depression, and anxiety symptoms among older adults with glaucoma. J. Glaucoma 2012, 21, 250–254. [Google Scholar] [CrossRef]
Parameters | Glaucoma Patients, n = 28 Mean ± SD (Range/n [%]) | Controls, n = 28 Mean ± SD (Range/n [%]) | p |
---|---|---|---|
Age (year) | 66.82 ± 6.52 (51–76) | 65.54 ± 5.12 (51–73) | 0.212 |
Women (%) | 13 (46.43%) | 14 (50%) | 0.789 |
Left-handed (%) | 1 (3.57%) | 0 (0%) | 0.313 |
Snellen BCVA | |||
Better eye (dB) | 0.853 ± 0.147 (0.7–1.0) | 1.021 ± 0.078 (0.9–1.2) | <0.001 |
Worse eye (dB) | 0.671 ± 0.225 (0.1–1.0) | 0.982 ± 0.061 (0.9–1.1) | <0.001 |
Monocular VF | |||
MD better eye (dB) | −5.848 ± 5.145 (−20.5–1.3) | 0.720 ± 0.948 (−1.42–2.18) | <0.001 |
MD worse eye (dB) | −16.944 ± 8.224 (−32.4–6.4) | 0.292 ± 0.941 (−1.45–1.78 | <0.001 |
Binocular VF | |||
Defect scores (n) | 25.821 ± 18.387 (0–75) | 0.464 ± 0.999 (0–4) | <0.001 |
Esterman coefficient score (%) | 78.482 ± 15.322 (37.5–100) | 99.613 ± 0.833 (96.6–100) | <0.001 |
Parameters | Group | Mean ± SD | 25th | Median | 75th | p | Effect Size |
---|---|---|---|---|---|---|---|
Aiming | |||||||
Number of hits (n) | G | 19.214 ± 1.134 | 19.000 | 19.000 | 20.000 | 0.491 | - |
C | 19.643 ± 0.621 | 19.000 | 20.000 | 20.000 | |||
Total time (s) | G | 9.801 ± 2.052 | 8.470 | 9.655 | 11.020 | <0.001 | 0.46 |
C | 7.982 ± 1.596 | 7.170 | 7.635 | 8.735 | |||
Aiming index (s−1) | G | 2.029 ± 0.356 | 1.783 | 2.007 | 2.286 | <0.001 | 0.47 |
C | 2.550 ± 0.490 | 2.172 | 2.542 | 2.721 | |||
Linear tracking | |||||||
Number of errors (n) | G | 31.610 ± 11.100 | 24.500 | 29.000 | 37.500 | 0.020 | 0.31 |
C | 24.286 ± 8.059 | 18.000 | 23.500 | 29.500 | |||
Time of error (s) | G | 2.929 ± 1.438 | 2.110 | 2.660 | 3.630 | 0.006 | 0.37 |
C | 2.046 ± 0.812 | 1.485 | 1.990 | 2.525 | |||
Total time (s) | G | 25.574 ± 11.006 | 18.110 | 22.025 | 33.945 | 0.724 | - |
C | 25.329 ± 12.651 | 15.170 | 20.855 | 32.170 | |||
Tracking index (s−1) | G | 0.168 ± 0.099 | 0.088 | 0.160 | 0.205 | 0.035 | 0.28 |
C | 0.214 ± 0.091 | 0.158 | 0.199 | 0.278 | |||
Tremor | |||||||
Number of errors (n) | G | 3.964 ± 7.280 | 0.000 | 3.000 | 5.000 | 0.011 | 0.34 |
C | 1.107 ± 2.671 | 0.000 | 0.000 | 1.000 | |||
Time of error (s) | G | 0.219 ± 0.286 | 0.000 | 0.095 | 0.325 | 0.014 | 0.33 |
C | 0.066 ± 0.205 | 0.000 | 0.000 | 0.045 | |||
Tapping | |||||||
Number of hits (n) | G | 183.036 ± 19.416 | 169.500 | 186.000 | 198.500 | 0.003 | 0.40 |
C | 199.929 ± 14.934 | 187.000 | 199.500 | 209.500 |
Parameters | Age | BCVA Better Eye | BCVA Worse Eye | MD Better Eye | MD Worse Eye | MD Asymmetry | VF Binocular |
---|---|---|---|---|---|---|---|
Aiming | |||||||
Number of hits (n) | 0.111 | −0.151 | −0.077 | 0.043 | 0.065 | −0.184 | 0.072 |
Total time (s) | 0.357 | −0.467 * | 0.029 | −0.017 | −0.290 | 0.369 | 0.120 |
Aiming index (s−1) | −0.374 * | 0.507 * | −0.055 | 0.084 | −0.155 | −0.337 | −0.092 |
Linear tracking | |||||||
Number of errors (n) | 0.171 | −0.297 | −0.366 | −0.081 | 0.170 | −0.167 | 0.219 |
Error duration (s) | 0.151 | −0.300 | −0.432* | −0.126 | −0.441 * | 0.405 * | −0.212 |
Total time (s) | −0.021 | −0.023 | 0.028 | −0.112 | 0.112 | −0.230 | 0.125 |
Tracking index (s−1) | −0.062 | 0.149 | 0.165 | 0.122 | −0.184 | 0.197 | −0.195 |
Tremor | |||||||
Number of errors (n) | 0.419 * | −0.444 * | 0.003 | −0.181 | 0.101 | −0.017 | −0.001 |
Error duration (s) | 0.391 * | −0.465 * | −0.016 | −0.232 | 0.075 | −0.056 | 0.015 |
Tapping | |||||||
Number of hits (n) | −0.172 | 0.302 | 0.107 | 0.176 | −0.085 | 0.254 | 0.120 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zwierko, T.; Jedziniak, W.; Lesiakowski, P.; Śliwiak, M.; Kirkiewicz, M.; Lubiński, W. Eye–Hand Coordination Impairment in Glaucoma Patients. Int. J. Environ. Res. Public Health 2019, 16, 4332. https://doi.org/10.3390/ijerph16224332
Zwierko T, Jedziniak W, Lesiakowski P, Śliwiak M, Kirkiewicz M, Lubiński W. Eye–Hand Coordination Impairment in Glaucoma Patients. International Journal of Environmental Research and Public Health. 2019; 16(22):4332. https://doi.org/10.3390/ijerph16224332
Chicago/Turabian StyleZwierko, Teresa, Wojciech Jedziniak, Piotr Lesiakowski, Marta Śliwiak, Marta Kirkiewicz, and Wojciech Lubiński. 2019. "Eye–Hand Coordination Impairment in Glaucoma Patients" International Journal of Environmental Research and Public Health 16, no. 22: 4332. https://doi.org/10.3390/ijerph16224332