Seeing ophthalmologic problems in Parkinson disease: Results of a visual impairment questionnaire

Carlijn D J M Borm, Femke Visser, Mario Werkmann, Debbie de Graaf, Diana Putz, Klaus Seppi, Werner Poewe, Annemarie M M Vlaar, Carel Hoyng, Bastiaan R Bloem, Thomas Theelen, Nienke M de Vries, Carlijn D J M Borm, Femke Visser, Mario Werkmann, Debbie de Graaf, Diana Putz, Klaus Seppi, Werner Poewe, Annemarie M M Vlaar, Carel Hoyng, Bastiaan R Bloem, Thomas Theelen, Nienke M de Vries

Abstract

Objective: To determine the prevalence and clinical effect of ophthalmologic symptoms in patients with Parkinson disease (PD), compared with controls, using a standardized questionnaire.

Methods: In this observational, cross-sectional, multicenter study, 848 patients with PD and 250 healthy controls completed the Visual Impairment in Parkinson's Disease Questionnaire (VIPD-Q). The VIPD-Q addressed 4 domains according to structures: (1) ocular surface; (2) intraocular; (3) oculomotor; and (4) optic nerve. The questionnaire also assessed the effect of ophthalmologic symptoms on daily activities.

Results: One or more ophthalmologic symptoms were reported by 82% (95% confidence interval [CI], 80-85) of patients, compared with 48% (95% CI, 42-54) of controls (p < 0.001). Patients with PD experienced more ophthalmologic symptoms across all domains than controls (p < 0.001), as reflected by a higher VIPD-Q total score among patients (median 10 [interquartile range (IQR) 13]) than controls (median 2 [IQR 5]; p < 0.001). Ophthalmologic symptoms interfered with daily activities in 68% (95% CI, 65-71) of patients, compared with 35% (95% CI, 29-41) of controls (p < 0.001).

Conclusion: Patients with PD have a higher prevalence of ophthalmologic symptoms than controls. Moreover, these frequently interfere with daily activities. A screening questionnaire such as the VIPD-Q may help with identifying ophthalmologic symptoms in PD, thereby enabling more timely treatment.

Copyright © 2020 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

Figures

Figure 1. Boxplot of the total Visual…
Figure 1. Boxplot of the total Visual Impairment in Parkinson's Disease Questionnaire (VIPD-Q) score
Boxplot of the median total score of the VIPD-Q in Parkinson disease (PD) and the control group (n = 773, PD group; n = 224, control group). ***p < 0.05.
Figure 2. Number of ophthalmologic symptoms reported…
Figure 2. Number of ophthalmologic symptoms reported per domain compared between patients with Parkinson disease (PD) and controls
Each pair of bars represents patients with PD and healthy controls. The bars are divided into the cumulative percentages of participants reporting no ophthalmologic symptoms, 1 ophthalmologic symptom, 2 ophthalmologic symptoms, 3 ophthalmologic symptoms, or 4 ophthalmologic symptoms. For example, in the domain of the ophthalmologic surface, only 37% of the patients with PD reported no symptoms, compared with 76% in the control group. In the control group in the domains intraocular, oculomotor, and optic nerve the option “4 symptoms” is 0%. In the control group in the domains oculomotor and optic nerve the option “3 symptoms” is 0%. ***p < 0.001.
Figure 3. Effect of ophthalmologic symptoms: Interference…
Figure 3. Effect of ophthalmologic symptoms: Interference with daily activities
Reported interference with daily activities due to ophthalmologic symptoms in the Parkinson disease (PD) group (n = 848) compared with controls (n = 250). Each pair of bars represents patients with PD compared with healthy controls. ***p < 0.001.

References

    1. Ekker MS, Janssen S, Seppi K, et al. . Ocular and visual disorders in Parkinson's disease: common but frequently overlooked. Parkinsonism Relat Disord 2017;40:1–10.
    1. Archibald NK, Clarke MP, Mosimann UP, Burn DJ. The retina in Parkinson's disease. Brain 2009;132:1128–1145.
    1. Biousse V, Skibell BC, Watts RL, Loupe DN, Drews-Botsch C, Newman NJ. Ophthalmologic features of Parkinson's disease. Neurology 2004;62:177–180.
    1. Pascolini D, Mariotti SP. Global estimates of visual impairment: 2010. Br J Ophthalmol 2012;96:614–618.
    1. Miljanovic B, Dana R, Sullivan DA, Schaumberg DA. Impact of dry eye syndrome on vision-related quality of life. Am J Ophthalmol 2007;143:409–415.
    1. Amick MM, Grace J, Ott BR. Visual and cognitive predictors of driving safety in Parkinson's disease patients. Arch Clin Neuropsychol 2007;22:957–967.
    1. Wood BH, Bilclough JA, Bowron A, Walker RW. Incidence and prediction of falls in Parkinson's disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 2002;72:721–725.
    1. Azulay JP, Mesure S, Amblard B, Pouget J. Increased visual dependence in Parkinson's disease. Perceptual Mot Skills 2002;95:1106–1114.
    1. McDowell SA, Harris JP. Visual problems in Parkinson's disease: a questionnaire survey. Behav Neurol 1997;10:77–81.
    1. Urwyler P, Nef T, Killen A, et al. . Visual complaints and visual hallucinations in Parkinson's disease. Parkinsonism Relat Disord 2014;20:318–322.
    1. Davidsdottir S, Cronin-Golomb A, Lee A. Visual and spatial symptoms in Parkinson's disease. Vis Res 2005;45:1285–1296.
    1. Sauerbier A, Ray Chaudhuri K. Parkinson's disease and vision. Basal Ganglia 2013;3:159–163.
    1. Borm C, Werkmann M, Visser F, et al. . Towards seeing the visual impairments in Parkinson's disease: protocol for a multicentre observational, cross-sectional study. BMC Neurol 2019;19:141.
    1. Nowacka B, Lubinski W, Honczarenko K, Potemkowski A, Safranow K. Ophthalmological features of Parkinson disease. Med Sci Monit 2014;20:2243–2249.
    1. Muller T, Kuhn W, Buttner T, Przuntek H. Distorted colour discrimination in Parkinson's disease is related to severity of the disease. Acta Neurol Scand 1997;96:293–296.
    1. Pieri V, Diederich NJ, Raman R, Goetz CG. Decreased color discrimination and contrast sensitivity in Parkinson's disease. J Neurol Sci 2000;172:7–11.
    1. Hutton JT, Morris JL. Vision in Parkinson's disease. Adv Neurol 2001;86:279–288.
    1. Muller T, Woitalla D, Peters S, Kohla K, Przuntek H. Progress of visual dysfunction in Parkinson's disease. Acta Neurol Scand 2002;105:256–260.
    1. Tamer C, Melek IM, Duman T, Oksuz H. Tear film tests in Parkinson's disease patients. Ophthalmology 2005;112:1795.
    1. Matsui H, Udaka F, Tamura A, et al. . Impaired visual acuity as a risk factor for visual hallucinations in Parkinson's disease. J Geriatr Psychiatry Neurol 2006;19:36–40.
    1. Diederich NJ, Fenelon G, Stebbins G, Goetz CG. Hallucinations in Parkinson disease. Nat Rev Neurol 2009;5:331–342.
    1. Seichepine DR, Neargarder S, Miller IN, Riedel TM, Gilmore GC, Cronin-Golomb A. Relation of Parkinson's disease subtypes to visual activities of daily living. J Int Neuropsychol Soc 2011;17:841–852.
    1. Armstrong RA. Oculo-visual dysfunction in Parkinson's disease. J Parkinsons Dis 2015;5:715–726.
    1. Lin TP, Rigby H, Adler JS, et al. . Abnormal visual contrast acuity in Parkinson's disease. J Parkinsons Dis 2015;5:125–130.
    1. Matlach J, Wagner M, Malzahn U, et al. . Retinal changes in Parkinson's disease and glaucoma. Parkinsonism Relat Disord 2018;56:41–46.
    1. Weil RS, Schrag AE, Warren JD, Crutch SJ, Lees AJ, Morris HR. Visual dysfunction in Parkinson's disease. Brain 2016;139:2827–2843.
    1. Huang FC, Tseng SH, Shih MH, Chen FK. Effect of artificial tears on corneal surface regularity, contrast sensitivity, and glare disability in dry eyes. Ophthalmology 2002;109:1934–1940.
    1. The management of dry eye. BMJ 2016;353:i2333.
    1. Milner MS, Beckman KA, Luchs JI, et al. . Dysfunctional tear syndrome: dry eye disease and associated tear film disorders: new strategies for diagnosis and treatment. Curr Opin Ophthalmol 2017;27(suppl 1):3–47.
    1. Ding J, Sullivan DA. Aging and dry eye disease. Exp Gerontol 2012;47:483–490.
    1. Klettner A, Richert E, Kuhlenbaumer G, et al. . Alpha synuclein and crystallin expression in human lens in Parkinson's disease. Mov Disord 2016;31:600–601.
    1. Ortuno-Lizaran I, Beach TG, Serrano GE, Walker DG, Adler CH, Cuenca N. Phosphorylated alpha-synuclein in the retina is a biomarker of Parkinson's disease pathology severity. Mov Disord 2018;33:1315–1324.
    1. Chung SD, Ho JD, Hu CC, Lin HC, Sheu JJ. Increased risk of Parkinson disease following a diagnosis of neovascular age-related macular degeneration: a retrospective cohort study. Am J Ophthalmol 2014;157:464–469.e461.
    1. Etminan M, Samii A, He B. Risk of Parkinson's disease in patients with neovascular age-related macular degeneration. J Curr Ophthalmol 2018;30:365–367.
    1. Yenice O, Onal S, Midi I, Ozcan E, Temel A, I-Gunal D. Visual field analysis in patients with Parkinson's disease. Parkinsonism Relat Disord 2008;14:193–198.
    1. Guo L, Normando EM, Shah PA, De Groef L, Cordeiro MF. Oculo-visual abnormalities in Parkinson's disease: possible value as biomarkers. Mov Disord 2018;33:1390–1406.
    1. Chaudhuri KR, Martinez-Martin P, Schapira AH, et al. . International multicenter pilot study of the first comprehensive self-completed nonmotor symptoms questionnaire for Parkinson's disease: the NMSQuest study. Mov Disord 2006;21:916–923.
    1. Terao Y, Fukuda H, Ugawa Y, Hikosaka O. New perspectives on the pathophysiology of Parkinson's disease as assessed by saccade performance: a clinical review. Clin Neurophysiol 2013;124:1491–1506.
    1. Barrell K, Bureau B, Turcano P, et al. . High-order visual processing, visual symptoms, and visual hallucinations: a possible symptomatic progression of Parkinson's disease. Front Neurol 2018;9:999.
    1. Visser F, Vlaar AMM, Borm C, et al. . Diplopia in Parkinson's disease: visual illusion or oculomotor impairment? J Neurol 2019;266:2457–2464.
    1. Goetz CG, Leurgans S, Pappert EJ, Raman R, Stemer AB. Prospective longitudinal assessment of hallucinations in Parkinson's disease. Neurology 2001;57:2078–2082.
    1. Ffytche DH, Blom JD, Catani M. Disorders of visual perception. J Neurol Neurosurg Psychiatry 2010;81:1280–1287.
    1. Aarsland D, Larsen JP, Tandberg E, Laake K. Predictors of nursing home placement in Parkinson's disease: a population-based, prospective study. J Am Geriatr Soc 2000;48:938–942.
    1. Archibald NK, Clarke MP, Mosimann UP, Burn DJ. Visual symptoms in Parkinson's disease and Parkinson's disease dementia. Mov Disord 2011;26:2387–2395.
    1. Caudron S, Guerraz M, Eusebio A, Gros JP, Azulay JP, Vaugoyeau M. Evaluation of a visual biofeedback on the postural control in Parkinson's disease. Neurophysiol Clin 2014;44:77–86.
    1. Ivers RQ, Cumming RG, Mitchell P, Attebo K. Visual impairment and falls in older adults: the blue mountains eye study. J Am Geriatr Soc 1998;46:58–64.
    1. Uc EY, Rizzo M, Anderson SW, Sparks J, Rodnitzky RL, Dawson JD. Impaired visual search in drivers with Parkinson's disease. Ann Neurol 2006;60:407–413.
    1. Worringham CJ, Wood JM, Kerr GK, Silburn PA. Predictors of driving assessment outcome in Parkinson's disease. Mov Disord 2006;21:230–235.
    1. Diederich NJ, Raman R, Leurgans S, Goetz CG. Progressive worsening of spatial and chromatic processing deficits in Parkinson disease. Arch Neurol 2002;59:1249–1252.
    1. Law C, Chriqui E, Kergoat MJ, et al. . Prevalence of convergence insufficiency-type symptomatology in Parkinson's disease. Can J Neurol Sci 2017;44:562–566.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe