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Translational Neurodegeneration
Published in: Translational Neurodegeneration 1/2019

Open Access 01-12-2019 | Blepharospasm | Review

How to spot ocular abnormalities in progressive supranuclear palsy? A practical review

Authors: Onanong Phokaewvarangkul, Roongroj Bhidayasiri

Published in: Translational Neurodegeneration | Issue 1/2019

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Abstract

Background

For parkinsonian disorders, progressive supranuclear palsy (PSP) continues to be significant for differential diagnosis. PSP presents a range of ocular abnormalities that have been suggested as optional tools for its early detection, apart from the principal characteristic of postural unsteadiness. Nonetheless, such symptoms may be difficult to identify, particularly during the early onset stage of the disorder. It may also be problematic to recognize these symptoms for general practitioners who lack the required experience or physicians who are not specifically educated and proficient in ophthalmology or neurology.

Main body

Thus, here, a methodical evaluation was carried out to identify seven oculomotor abnormalities occurring in PSP, comprising square wave jerks, the speed and range of saccades (slow saccades and vertical supranuclear gaze palsy), ‘round the houses’ sign, decreased blink rate, blepharospasm, and apraxia of eyelid opening. Inspections were conducted using direct visual observation. An approach to distinguish these signs during a bedside examination was also established. When presenting in a patient with parkinsonism or dementia, the existence of such ocular abnormalities could increase the risk of PSP. For the distinction between PSP and other parkinsonian disorders, these signs hold significant value for physicians.

Conclusion

The authors urge all concerned physicians to check for such abnormalities with the naked eye in patients with parkinsonism. This method has advantages, including ease of application, reduced time-consumption, and requirement of minimal resources. It will also help physicians to conduct efficient diagnoses since many patients with PSP could intially present with ocular symptoms in busy outpatient clinics.
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Literature
1.
Steele JC, Richardson JC, Olszewski J. Progressive supranuclear palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol. 1964;10:333–59.PubMedCrossRef
2.
Hughes AJ, Ben-Shlomo Y, Daniel SE, Lees AJ. What features improve the accuracy of clinical diagnosis in Parkinson’s disease: a clinicopathologic study. Neurology. 1992;42(6):1142–6.PubMedCrossRef
3.
Litvan I, Agid Y, Calne D, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology. 1996;47(1):1–9.PubMedCrossRef
4.
Litvan I, Mangone CA, McKee A, et al. Natural history of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. J Neurol Neurosurg Psychiatry. 1996;60(6):615–20.PubMedPubMedCentralCrossRef
5.
Williams DR, de Silva R, Paviour DC, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain. 2005;128(Pt 6):1247–58.PubMedCrossRef
6.
Hoglinger GU, Respondek G, Stamelou M, et al. Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord. 2017;32(6):853–64.PubMedPubMedCentralCrossRef
7.
Abdo WF, van de Warrenburg BP, Burn DJ, Quinn NP, Bloem BR. The clinical approach to movement disorders. Nat Rev Neurol. 2010;6(1):29–37.PubMedCrossRef
8.
Fahn S, Jankovic J, Hallett M. Atypical parkinsonism, parkinsonism-plus syndromes, and secondary parkinsonian disorders. In: Fahn S, Jankovic J, Hallett M, editors. Principles and practice of movement disorders. 2nd ed. United States: Saunders; 2011. p. 197–240.CrossRef
9.
Golbe LI, Ohman-Strickland PA. A clinical rating scale for progressive supranuclear palsy. Brain. 2007;130(Pt 6):1552–65.PubMedCrossRef
10.
Nath U, Ben-Shlomo Y, Thomson RG, Lees AJ, Burn DJ. Clinical features and natural history of progressive supranuclear palsy: a clinical cohort study. Neurology. 2003;60(6):910–6.PubMedCrossRef
11.
Respondek G, Roeber S, Kretzschmar H, et al. Accuracy of the National Institute for Neurological Disorders and Stroke/Society for Progressive Supranuclear Palsy and neuroprotection and natural history in Parkinson plus syndromes criteria for the diagnosis of progressive supranuclear palsy. Mov Disord. 2013;28(4):504–9.PubMedCrossRef
12.
Lopez OL, Litvan I, Catt KE, et al. Accuracy of four clinical diagnostic criteria for the diagnosis of neurodegenerative dementias. Neurology. 1999;53(6):1292–9.PubMedCrossRef
13.
Osaki Y, Ben-Shlomo Y, Lees AJ, et al. Accuracy of clinical diagnosis of progressive supranuclear palsy. Mov Disord. 2004;19(2):181–9.PubMedCrossRef
14.
Lopez G, Bayulkem K, Hallett M. Progressive supranuclear palsy (PSP): Richardson syndrome and other PSP variants. Acta Neurol Scand. 2016;134(4):242-9.PubMedCrossRefPubMedCentral
15.
Respondek G, Stamelou M, Kurz C, et al. The phenotypic spectrum of progressive supranuclear palsy: a retrospective multicenter study of 100 definite cases. Mov Disord. 2014;29(14):1758–66.PubMedCrossRef
16.
Williams DR, Lees AJ. Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol. 2009;8(3):270–9.PubMedCrossRef
17.
dell’Aquila C, Zoccolella S, Cardinali V, et al. Predictors of survival in a series of clinically diagnosed progressive supranuclear palsy patients. Parkinsonism Relat Disord. 2013;19(11):980–5.PubMedCrossRef
18.
Collins SJ, Ahlskog JE, Parisi JE, Maraganore DM. Progressive supranuclear palsy: neuropathologically based diagnostic clinical criteria. J Neurol Neurosurg Psychiatry. 1995;58(2):167–73.PubMedPubMedCentralCrossRef
19.
Chen AL, Riley DE, King SA, et al. The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis. Front Neurol. 2010;1:147.PubMedPubMedCentral
20.
Hauw JJ, Daniel SE, Dickson D, et al. Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology. 1994;44(11):2015–9.PubMedCrossRef
21.
Lantos PL. The neuropathology of progressive supranuclear palsy. J Neural Transm Suppl. 1994;42:137–52.PubMedCrossRef
22.
Bhidayasiri R, Plant GT, Leigh RJ. A hypothetical scheme for the brainstem control of vertical gaze. Neurology. 2000;54(10):1985–93.PubMedCrossRef
23.
Bhidayasiri R, Riley DE, Somers JT, Lerner AJ, Buttner-Ennever JA, Leigh RJ. Pathophysiology of slow vertical saccades in progressive supranuclear palsy. Neurology. 2001;57(11):2070–7.PubMedCrossRef
24.
Averbuch-Heller L, Helmchen C, Horn AK, Leigh RJ, Buttner-Ennerver JA. Slow vertical saccades in motor neuron disease: correlation of structure and function. Ann Neurol. 1998;44(4):641–8.PubMedCrossRef
25.
Leigh RJ, Zee DS. The neurology of eye movements. 5th ed. Oxford: Oxford University Press; 2015.CrossRef
26.
Otero-Millan J, Serra A, Leigh RJ, Troncoso XG, Macknik SL, Martinez-Conde S. Distinctive features of saccadic intrusions and microsaccades in progressive supranuclear palsy. J Neurosci. 2011;31(12):4379–87.PubMedPubMedCentralCrossRef
27.
Martinez-Conde S, Macknik SL, Troncoso XG, Dyar TA. Microsaccades counteract visual fading during fixation. Neuron. 2006;49(2):297–305.PubMedCrossRef
28.
Martinez-Conde S, Macknik SL, Troncoso XG, Hubel DH. Microsaccades: a neurophysiological analysis. Trends Neurosci. 2009;32(9):463–75.PubMedCrossRef
29.
Otero-Millan J, Schneider R, Leigh RJ, Macknik SL, Martinez-Conde S. Saccades during attempted fixation in parkinsonian disorders and recessive ataxia: from microsaccades to square-wave jerks. PLoS One. 2013;8(3):e58535.PubMedPubMedCentralCrossRef
30.
31.
32.
Herishanu YO, Sharpe JA. Normal square wave jerks. Invest Ophthalmol Vis Sci. 1981;20(2):268–72.PubMed
33.
Shallo-Hoffmann J, Petersen J, Muhlendyck H. How normal are “normal” square wave jerks? Invest Ophthalmol Vis Sci. 1989;30(5):1009–11.PubMed
34.
Rascol O, Sabatini U, Simonetta-Moreau M, Montastruc JL, Rascol A, Clanet M. Square wave jerks in parkinsonian syndromes. J Neurol Neurosurg Psychiatry. 1991;54(7):599–602.PubMedPubMedCentralCrossRef
35.
Fahey MC, Cremer PD, Aw ST, et al. Vestibular, saccadic and fixation abnormalities in genetically confirmed Friedreich ataxia. Brain. 2008;131(Pt 4):1035–45.PubMedCrossRef
36.
Vidailhet M, Rivaud S, Gouider-Khouja N, et al. Eye movements in parkinsonian syndromes. Ann Neurol. 1994;35(4):420–6.PubMedCrossRef
37.
Friedman DI, Jankovic J, McCrary JA 3rd. Neuro-ophthalmic findings in progressive supranuclear palsy. J Clin Neuroophthalmol. 1992;12(2):104–9.PubMed
38.
Gironell A, Kulisevsky J, Roig C, Pascual-Sedano B, Rodriguez-Fornells A, Otermin P. Diagnostic potential of acoustic startle reflex, acoustic blink reflex, and electro-oculography in progressive supranuclear palsy: a prospective study. Mov Disord. 2003;18(11):1273–9.PubMedCrossRef
39.
Pinnock RA, McGivern RC, Forbes R, Gibson JM. An exploration of ocular fixation in Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. J Neurol. 2010;257(4):533–9.PubMedCrossRef
40.
Rottach KG, Riley DE, DiScenna AO, Zivotofsky AZ, Leigh RJ. Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes. Ann Neurol. 1996;39(3):368–77.PubMedCrossRef
41.
Troost BT, Daroff RB. The ocular motor defects in progressive supranuclear palsy. Ann Neurol. 1977;2(5):397–403.PubMedCrossRef
42.
Garbutt S, Riley DE, Kumar AN, Han Y, Harwood MR, Leigh RJ. Abnormalities of optokinetic nystagmus in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry. 2004;75(10):1386–94.PubMedPubMedCentralCrossRef
43.
Zee DS, Robinson DA. A hypothetical explanation of saccadic oscillations. Ann Neurol. 1979;5(5):405–14.PubMedCrossRef
44.
Dickson DW, Ahmed Z, Algom AA, Tsuboi Y, Josephs KA. Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol. 2010;23(4):394–400.PubMedCrossRef
45.
46.
Fisk JD, Goodale MA, Burkhart G, Barnett HJ. Progressive supranuclear palsy: the relationship between ocular motor dysfunction and psychological test performance. Neurology. 1982;32(7):698–705.PubMedCrossRef
47.
Wray SH. Eye movement disorders in clinical practice. New York: Oxford University Press; 2014.CrossRef
48.
Antoniades C, Ettinger U, Gaymard B, et al. An internationally standardised antisaccade protocol. Vis Res. 2013;84:1–5.PubMedCrossRef
49.
Schmidt D, Abel LA, Dell’Osso LF, Daroff RB. Saccadic velocity characteristics: intrinsic variability and fatigue. Aviat Space Environ Med. 1979;50(4):393–5.PubMed
50.
Munoz DP, Broughton JR, Goldring JE, Armstrong IT. Age-related performance of human subjects on saccadic eye movement tasks. Exp Brain Res. 1998;121(4):391–400.PubMedCrossRef
51.
Termsarasab P, Thammongkolchai T, Rucker JC, Frucht SJ. The diagnostic value of saccades in movement disorder patients: a practical guide and review. J Clin Mov Disord. 2015;2:14.PubMedPubMedCentralCrossRef
52.
Danchaivijitr C, Kennard C. Diplopia and eye movement disorders. J Neurol Neurosurg Psychiatry. 2004;75(Suppl 4):iv24–31.PubMedPubMedCentral
53.
Oguro H, Okada K, Suyama N, Yamashita K, Yamaguchi S, Kobayashi S. Decline of vertical gaze and convergence with aging. Gerontology. 2004;50(3):177–81.PubMedCrossRef
54.
Terao Y, Fukuda H, Shirota Y, et al. Deterioration of horizontal saccades in progressive supranuclear palsy. Clin Neurophysiol. 2013;124(2):354–63.PubMedCrossRef
55.
Garbutt S, Harwood MR, Kumar AN, Han YH, Leigh RJ. Evaluating small eye movements in patients with saccadic palsies. Ann N Y Acad Sci. 2003;1004:337–46.PubMedCrossRef
56.
Pierrot-Deseilligny C, Rivaud S, Pillon B, Fournier E, Agid Y. Lateral visually-guided saccades in progressive supranuclear palsy. Brain. 1989;112(Pt 2):471–87.PubMedCrossRef
57.
Shaikh AG, Factor SA, Juncos J. Saccades in progressive supranuclear palsy - maladapted, irregular, curved, and slow. Mov Disord Clin Pract. 2017;4(5):671–81.PubMedPubMedCentralCrossRef
58.
Verny M, Jellinger KA, Hauw JJ, Bancher C, Litvan I, Agid Y. Progressive supranuclear palsy: a clinicopathological study of 21 cases. Acta Neuropathol. 1996;91(4):427–31.PubMedCrossRef
59.
De Bruin VM, Lees AJ. Subcortical neurofibrillary degeneration presenting as Steele-Richardson-Olszewski and other related syndromes: a review of 90 pathologically verified cases. Mov Disord. 1994;9(4):381–9.PubMedCrossRef
60.
Birdi S, Rajput AH, Fenton M, et al. Progressive supranuclear palsy diagnosis and confounding features: report on 16 autopsied cases. Mov Disord. 2002;17(6):1255–64.PubMedCrossRef
61.
Diroma C, Dell’Aquila C, Fraddosio A, et al. Natural history and clinical features of progressive supranuclear palsy: a clinical study. Neurol Sci. 2003;24(3):176–7.PubMedCrossRef
62.
Marra M, Toni V, Trianni G, Coppola G. Progressive supranuclear palsy: analysis of six cases. Neurol Sci. 2003;24(3):186–7.PubMedCrossRef
63.
Kanazawa M, Tada M, Onodera O, Takahashi H, Nishizawa M, Shimohata T. Early clinical features of patients with progressive supranuclear palsy with predominant cerebellar ataxia. Parkinsonism Relat Disord. 2013;19(12):1149–51.PubMedCrossRef
64.
Pinhas I, Pinhas A, Goldhammer Y, Braham J. Progressive supranuclear palsy: electomyographic examinations of eye muscles. Acta Neurol Scand. 1978;58(5):304–8.PubMedCrossRef
65.
66.
Kanazawa M, Shimohata T, Toyoshima Y, et al. Cerebellar involvement in progressive supranuclear palsy: a clinicopathological study. Mov Disord. 2009;24(9):1312–8.PubMedCrossRef
67.
Anderson TJ, MacAskill MR. Eye movements in patients with neurodegenerative disorders. Nat Rev Neurol. 2013;9(2):74–85.PubMedCrossRef
68.
Riley DE, Lang AE, Lewis A, et al. Cortical-basal ganglionic degeneration. Neurology. 1990;40(8):1203–12.PubMedCrossRef
69.
Lewis AJ, Gawel MJ. Diffuse Lewy body disease with dementia and oculomotor dysfunction. Mov Disord. 1990;5(2):143–7.PubMedCrossRef
70.
Fearnley JM, Lees AJ. Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain. 1991;114(Pt 5):2283–301.PubMedCrossRef
71.
Williams DR, Lees AJ. What features improve the accuracy of the clinical diagnosis of progressive supranuclear palsy-parkinsonism (PSP-P)? Mov Disord. 2010;25(3):357–62.PubMedCrossRef
72.
Nuwer MR. Progressive supranuclear palsy despite normal eye movements. Arch Neurol. 1981;38(12):784.PubMedCrossRef
73.
Williams DR, Holton JL, Strand K, Revesz T, Lees AJ. Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord. 2007;22(15):2235–41.PubMedCrossRef
74.
Cordato NJ, Halliday GM, McCann H, et al. Corticobasal syndrome with tau pathology. Mov Disord. 2001;16(4):656–67.PubMedCrossRef
75.
Wakabayashi K, Takahashi H. Pathological heterogeneity in progressive supranuclear palsy and corticobasal degeneration. Neuropathology. 2004;24(1):79–86.PubMedCrossRef
76.
Daniel SE, de Bruin VM, Lees AJ. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain. 1995;118(Pt 3):759–70.PubMedCrossRef
77.
Tsuboi Y, Josephs KA, Boeve BF, et al. Increased tau burden in the cortices of progressive supranuclear palsy presenting with corticobasal syndrome. Mov Disord. 2005;20(8):982–8.PubMedCrossRef
78.
Ling H, O'Sullivan SS, Holton JL, et al. Does corticobasal degeneration exist? A clinicopathological re-evaluation. Brain. 2010;133(Pt 7):2045–57.PubMedCrossRef
79.
Josephs KA, Katsuse O, Beccano-Kelly DA, et al. Atypical progressive supranuclear palsy with corticospinal tract degeneration. J Neuropathol Exp Neurol. 2006;65(4):396–405.PubMedCrossRef
80.
Josephs KA, Duffy JR. Apraxia of speech and nonfluent aphasia: a new clinical marker for corticobasal degeneration and progressive supranuclear palsy. Curr Opin Neurol. 2008;21(6):688–92.PubMedCrossRef
81.
Nagao S, Yokota O, Nanba R, et al. Progressive supranuclear palsy presenting as primary lateral sclerosis but lacking parkinsonism, gaze palsy, aphasia, or dementia. J Neurol Sci. 2012;323(1–2):147–53.PubMedCrossRef
82.
Boeve B, Dickson D, Duffy J, Bartleson J, Trenerry M, Petersen R. Progressive nonfluent aphasia and subsequent aphasic dementia associated with atypical progressive supranuclear palsy pathology. Eur Neurol. 2003;49(2):72–8.PubMedCrossRef
83.
Halliday GM, Hardman CD, Cordato NJ, Hely MA, Morris JG. A role for the substantia nigra pars reticulata in the gaze palsy of progressive supranuclear palsy. Brain. 2000;123(Pt 4):724–32.PubMedCrossRef
84.
Rivaud-Pechoux S, Vidailhet M, Gallouedec G, Litvan I, Gaymard B, Pierrot-Deseilligny C. Longitudinal ocular motor study in corticobasal degeneration and progressive supranuclear palsy. Neurology. 2000;54(5):1029–32.PubMedCrossRef
85.
Quinn N. The “round the houses” sign in progressive supranuclear palsy. Ann Neurol. 1996;40(6):951.PubMedCrossRef
86.
Bhattacharjee S, Ng KL. “Round the houses” sign and apraxia of eyelid opening in a 62-year old man. Neurol India. 2017;65(5):1157.PubMedCrossRef
87.
Crespi J, Brathen G, Quist-Paulsen P, Pagonabarraga J, Roig-Arnall C. Facial dystonia with facial grimacing and vertical gaze palsy with “round the houses” sign in a 29-year-old woman. Neuroophthalmology. 2016;40(1):31–4.PubMedPubMedCentralCrossRef
88.
Eggink H, Brandsma R, van der Hoeven JH, Lange F, de Koning TJ, Tijssen MA. Teaching video NeuroImages: the “round the houses” sign as a clinical clue for Niemann-Pick disease type C. Neurology. 2016;86(19):e202.PubMedCrossRef
89.
Davson H. The protective mechanism. In: Davson H, editor. Physiology of the eye fourth edition. United States: Academic; 1980. p. 492.
90.
VanderWerf F, Brassinga P, Reits D, Aramideh M, Ongerboer de Visser B. Eyelid movements: behavioral studies of blinking in humans under different stimulus conditions. J Neurophysiol. 2003;89(5):2784–96.PubMedCrossRef
91.
Reddy VC, Patel SV, Hodge DO, Leavitt JA. Corneal sensitivity, blink rate, and corneal nerve density in progressive supranuclear palsy and Parkinson disease. Cornea. 2013;32(5):631–5.PubMedCrossRef
92.
Fitzpatrick E, Hohl N, Silburn P, O’Gorman C, Broadley SA. Case-control study of blink rate in Parkinson’s disease under different conditions. J Neurol. 2012;259(4):739–44.PubMedCrossRef
93.
Sommer M, Grafman J, Litvan I, Hallett M. Impairment of eyeblink classical conditioning in progressive supranuclear palsy. Mov Disord. 2001;16(2):240–51.PubMedCrossRef
94.
Golbe LI, Davis PH, Lepore FE. Eyelid movement abnormalities in progressive supranuclear palsy. Mov Disord. 1989;4(4):297–302.PubMedCrossRef
95.
Bologna M, Agostino R, Gregori B, et al. Voluntary, spontaneous and reflex blinking in patients with clinically probable progressive supranuclear palsy. Brain. 2009;132(Pt 2):502–10.PubMed
96.
Sciacca G, Nicoletti A, Mostile G, et al. Blink reflex recovery cycle to differentiate progressive supranuclear palsy from corticobasal syndrome. Eur J Neurol. 2018;25(8):1100–e1185.PubMedCrossRef
97.
Sandyk R. The significance of eye blink rate in parkinsonism: a hypothesis. Int J Neurosci. 1990;51(1–2):99–103.PubMedCrossRef
98.
Karson CN, Burns RS, LeWitt PA, Foster NL, Newman RP. Blink rates and disorders of movement. Neurology. 1984;34(5):677–8.PubMedCrossRef
99.
Tamer C, Melek IM, Duman T, Oksuz H. Tear film tests in Parkinson’s disease patients. Ophthalmology. 2005;112(10):1795.PubMedCrossRef
100.
101.
102.
Rana AQ, Kabir A, Dogu O, Patel A, Khondker S. Prevalence of blepharospasm and apraxia of eyelid opening in patients with parkinsonism, cervical dystonia and essential tremor. Eur Neurol. 2012;68(5):318–21.PubMedCrossRef
103.
Janati A. Progressive supranuclear palsy: report of a case with torticollis, blepharospasm, and dysfluency. Am J Med Sci. 1986;292(6):391–2.PubMedCrossRef
104.
Hallett M, Evinger C, Jankovic J, Stacy M, Workshop BI. Update on blepharospasm: report from the BEBRF international workshop. Neurology. 2008;71(16):1275–82.PubMedPubMedCentralCrossRef
105.
106.
Lepore FE, Duvoisin RC. “Apraxia” of eyelid opening: an involuntary levator inhibition. Neurology. 1985;35(3):423–7.PubMedCrossRef
107.
108.
Krack P, Marion MH. “Apraxia of lid opening”, a focal eyelid dystonia: clinical study of 32 patients. Mov Disord. 1994;9(6):610–5.PubMedCrossRef
109.
Yoon WT, Chung EJ, Lee SH, Kim BJ, Lee WY. Clinical analysis of blepharospasm and apraxia of eyelid opening in patients with parkinsonism. J Clin Neurol. 2005;1(2):159–65.PubMedPubMedCentralCrossRef
110.
Rana AQ, Shah R. Combination of blepharospasm and apraxia of eyelid opening: a condition resistant to treatment. Acta Neurol Belg. 2012;112(1):95–6.PubMedCrossRef
111.
Esteban A, Gimenez-Roldan S. Involuntary closure of eyelids in parkinsonism. Electrophysiological evidence for prolonged inhibition of the levator palpebrae muscles. J Neurol Sci. 1988;85(3):333–45.PubMedCrossRef
112.
Aramideh M, Ongerboer de Visser BW, Koelman JH, Speelman JD. Motor persistence of orbicularis oculi muscle in eyelid-opening disorders. Neurology. 1995;45(5):897–902.PubMedCrossRef
113.
Piccione F, Mancini E, Tonin P, Bizzarini M. Botulinum toxin treatment of apraxia of eyelid opening in progressive supranuclear palsy: report of two cases. Arch Phys Med Rehabil. 1997;78(5):525–9.PubMedCrossRef
114.
Lamberti P, De Mari M, Zenzola A, Aniello MS, Defazio G. Frequency of apraxia of eyelid opening in the general population and in patients with extrapyramidal disorders. Neurol Sci. 2002;23(Suppl 2):S81–2.PubMedCrossRef
115.
Defazio G, De Mari M, De Salvia R, Lamberti P, Giorelli M, Livrea P. “Apraxia of eyelid opening” induced by levodopa therapy and apomorphine in atypical parkinsonism (possible progressive supranuclear palsy): a case report. Clin Neuropharmacol. 1999;22(5):292–4.PubMed
Metadata
Title
How to spot ocular abnormalities in progressive supranuclear palsy? A practical review
Authors
Onanong Phokaewvarangkul
Roongroj Bhidayasiri
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Translational Neurodegeneration / Issue 1/2019
Electronic ISSN: 2047-9158
DOI
https://doi.org/10.1186/s40035-019-0160-1

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