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Supranuclear gaze palsy and eyelid apraxia in postencephalitic parkinsonism

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Summary

We describe six patients with clinicopathologically confirmed postencephalitic parkinsonism (PEP) in whom oculomotor abnormalities developed several years after suffering the initial episode of encephalitis lethargica. Four of the cases had vertical supranuclear gaze palsy and two eyelid apraxia, features typically associated with progressive supranuclear palsy (PSP). Our findings indicate that the presence of gaze palsy alone may not be a reliable clinical discriminator between PEP and PSP. Involvement of the dorsal central gray nucleus, nucleus centralis pontis oralis, nucleus dorsal raphe interpositus, rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), nucleus interstitialis of Cajal, nucleus of the posterior commissure, pedunculopontine nuclei and frontal cortex was observed in several of our PEP cases and may contribute to the oculomotor abnormalities in this disorder. Whether the dorsal tegmental nucleus, caudal to the supratrochlear nucleus, severely affected in all our PEP cases, has a role in vertical gaze needs to be further studied.

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Abbreviations

PSP :

progressive supranuclear palsy

NFTs :

neurofibrillary tangles

NPTs :

neuropil threads

riMLF :

rostral interstitial nucleus of the medial longitudinal fasciculus

References

  • Albert ML, Feldman RG, Willis AL (1974) The “subcortical dementia” of progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 37: 121–130

    PubMed  Google Scholar 

  • Barletta L, Simonetti F, Karau J, Manni R, Uggetti C, Poloni TE, et al (1995) Encephalitis lethargica. Nervenarzt 66: 781–784

    PubMed  Google Scholar 

  • Blin J, Baron JC, Dubois B, Pillon B, Cambon H, Cambier J, Agid Y (1990) Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch Neurol 47: 747–752

    PubMed  Google Scholar 

  • Buttner-Ennever JA, Buttner U (1978) A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res 151: 31–47

    PubMed  Google Scholar 

  • Buttner-Ennever JA, Buttner U, Cohen B, Baumgartner G (1982) Vertical gaze paralysis and the rostral interstitial nucleus of the medial longitudinal fasciculus. Brain 105: 125–149

    PubMed  Google Scholar 

  • Calne DB, Lees AJ (1988) Late progression of post-encephalitic Parkinson's syndrome. Can J Neurol Sci 15: 135–138

    PubMed  Google Scholar 

  • Calne DB, Stern GM, Laurence DR, Sharkey J, Armitage P (1969) L-dopa in postencephalitic parkinsonism. Lancet i: 744–746

    Google Scholar 

  • Cambier J, Masson M, Viader F, Limodin J, Strube A (1985) Frontal syndrome of progressive supranuclear palsy. Rev Neurol (Paris) 141: 528–536

    Google Scholar 

  • Chu FC, Reingold DB, Cogan DG, Williams AC (1979) The eye movement disorders of progressive supranuclear palsy. Ophthalmology 86: 422–428

    PubMed  Google Scholar 

  • Clough CG, Plaitakis A, Yahr MD (1983) Oculogyric crises and parkinsonism. A case of recent onset. Arch Neurol 40: 36–37

    PubMed  Google Scholar 

  • Cogan DC (1974) Paralysis of down-gaze. Arch Ophthalmol 91: 192–199

    PubMed  Google Scholar 

  • Crawford JP (1970) Side-effects of L-dopa in postencephalitic parkinsonism. Lancet ii: 660

    Google Scholar 

  • Crow J (1949) A note on certain ocular phenomena of postencephalitic parkinsonism. Glasgow Med J 30: 29–34

    Google Scholar 

  • Daniel SE, de Bruin VMS, Lees AJ (1995) The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain 118: 759–770

    PubMed  Google Scholar 

  • Dehaene I (1984) Apraxia of eyelid opening in progressive supranuclear palsy. Ann Neurol 15: 115–116

    PubMed  Google Scholar 

  • Dimsdale H (1946) Changes in Parkinson syndrome in the 20th century. Quart J Med 15: 155–170

    Google Scholar 

  • Dix MR, Harrison MJG, Lewis PD (1971) Progressive supranuclear palsy (the Steele-Richardson-Olszewski syndrome). J Neurol Sci 13: 237–256

    PubMed  Google Scholar 

  • Dubas F, Gray F, Escourolle R (1983) Steele-Richardson-Olszewski disease without ophthalmoplegia. 6 clinico-anatomic cases. Rev Neurol 139: 407–416

    PubMed  Google Scholar 

  • Duvernoy HM (1995) The human brain stem and cerebellum. Surface, structure, vascularization, and three-dimensional sectional anatomy with MRI. Springer, Wien New York

    Google Scholar 

  • Duvoisin RC (1994) Differential diagnosis of PSP. In: Tolosa E, Duvoisin R, Cruz-Sanchez F (eds) Progressive supranuclear palsy: diagnosis, pathology, and therapy. Springer, Wien New York, pp 51–67

    Google Scholar 

  • Duvoisin RC, Yahr MD (1965) Encephalitis and parkinsonism. Arch Neurol 12: 227–239

    PubMed  Google Scholar 

  • Duvoisin RC, Lobo-Antunes J, Yahr MD (1972) Response of patients with postencephalitic Parkinsonism to levodopa. J Neurol Neurosurg Psychiatry 35: 487–495

    PubMed  Google Scholar 

  • Elizan TS, Casals J (1991) Astrogliosis in von Economo's and postencephalitic parkinson's disease supports probable viral etiology. J Neurol Sci 105: 131–134

    PubMed  Google Scholar 

  • Elizan TS, Casals J, Swash M (1989) No viral antigens detected in brain tissue from a case of acute encephalitis lethargica and another case of post-encephalitic parkinsonism (Letter). J Neurol Neurosurg Psychiatry 52: 800–801

    PubMed  Google Scholar 

  • Esiri MM, Swash M (1984) Absence of herpes simplex virus antigen in brain in encephalitis lethargica [Letter]. J Neurol Neurosurg Psychiatry 47: 1049–1050

    PubMed  Google Scholar 

  • Feany MB, Mattiace LA, Dickson DW (1996) Neuropathologic overlap of progressive supranuclear palsy, Pick's disease and corticobasal degeneration. J Neuropathol Exp Neurol 55: 53–67

    PubMed  Google Scholar 

  • Geddes JF, Hughes AJ, Lees AJ, Daniel SE (1993) Pathological overlap in cases of parkinsonism associated with neurofibrillary tangles. A study of recent cases of postencephalitic parkinsonism and comparison with progressive supranuclear palsy and Guamanian parkinsonism-dementia complex. Brain 116: 281–302

    PubMed  Google Scholar 

  • Golbe LI, Davis PH, Lepore FE (1989) Eyelid movement abnormalities in progressive supranuclear palsy. Mov Disord 4: 297–302

    PubMed  Google Scholar 

  • Grandas F, Esteban A (1994) Eyelid motor abnormalities in progressive supranuclear palsy. In: Tolosa E, Duvoisin R, Cruz-Sanchez F (eds) Progressive supranuclear palsy: diagnosis, pathology, and therapy. Springer, Wien New York, pp 33–41

    Google Scholar 

  • Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, et al (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44: 2015–2019

    PubMed  Google Scholar 

  • Howard RS, Lees AJ (1987) Encephalitis lethargica. A report of four recent cases. Brain 110: 19–33

    PubMed  Google Scholar 

  • Hunter KR, Stern GM, Sharkey J (1970) Levodopa in postencephalitic parkinsonism. Lancet ii: 1366–1367

    Google Scholar 

  • Jankovic J, Friedman DI, Pirozzolo FJ, McCrary JA (1990) Progressive supranuclear palsy: motor, neurobehavioural, and neuro-ophthalmic findings. Adv Neurol 53: 294–304

    Google Scholar 

  • Jellinger KA (1996) Differential diagnosis: progressive supranuclear palsy vs postencephalitic parkinsonism [Abstract]. Neurobiol Aging 17 [Suppl]: S13

    Google Scholar 

  • Jellinger KA, Bancher C (1992) Neuropathology. In: Litvan I, Agid Y (eds) Progressive supranuclear palsy. Clinical and research approaches. Oxford University Press, New York, pp 44–88

    Google Scholar 

  • Juncos JL, Hirsch EC, Malessa S, Duyckaerts C, Hersh LB, Agid Y (1991) Mesencephalic cholinergic nuclei in progressive supranuclear palsy. Neurology 41: 25–30

    PubMed  Google Scholar 

  • Krusz JC, Koller WC, Ziegler DK (1987) Historical review: abnormal movements associated with epidemic encephalitis lethargica. Mov Disord 2: 137–141

    PubMed  Google Scholar 

  • Leigh JR, Zee DS (1991) The neurology of eye movements, 2nd edn. FA Davis, Philadelphia

    Google Scholar 

  • Lees AJ (1987) The Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). In: Marsden CD, Fahn S (eds) Movement disorders 2. Butterworths, London, pp 272–287

    Google Scholar 

  • Litvan I, Agid Y, Jankovic J, Goetz C, Brandel JP, Lai EC, et al (1996a) Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 46: 922–930

    PubMed  Google Scholar 

  • Litvan I, Hauw JJ, Bartko JJ, Lantos PL, Daniel SE, Horoupian DS, et al (1996b) Validity and reliability of the preliminary NINDS neuropathologic criteria for progressive supranuclear palsy and related disorders. J Neuropathol Exp Neurol 55: 97–103

    PubMed  Google Scholar 

  • Litvan I, Mega MS, Cummings JL, Fairbanks L (1996c) Neuropsychiatric aspects of progressive supranuclear palsy. Neurology 47: 1184–1189

    PubMed  Google Scholar 

  • Litvan I, DeLeo JM, Hauw JJ, Daniel SE, Jellinger K, McKee A, et al (1996d) What can artificial neural networks teach us about neurodegenerative disorders with extrapyramidal features? Brain 119: 831–839

    PubMed  Google Scholar 

  • Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al (1996e) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 47: 1–9

    PubMed  Google Scholar 

  • Malessa S, Hirsch E, Cervera P, Javoy-Agid F, Duyckaerts C, Hauw JJ, et al (1991) Progressive supranuclear palsy: loss of choline acetyltransferase-like immunoreactive neurons in the pontine reticular formation. Neurology 41: 1593–1597

    PubMed  Google Scholar 

  • Malessa S, Gaymard B, Rivaud S, Cervera P, Hirsch E, Verny M, et al (1994) Role of pontine nuclei damage in smooth pursuit impairment of progressive supranuclear palsy: a clinical-pathologic. Neurology 44: 716–721

    PubMed  Google Scholar 

  • Martin PJ (1983). Old photographs: postencephalitic parkinsonism in two small boys. J Neurol Neurosurg Psychiatry 46: 953–955

    PubMed  Google Scholar 

  • Marttila RJ, Halonen P, Rinne UK (1977) Influenza virus antibodies in Parkinsonism. Comparison of postencephalic and idiopathic Parkinson patients and matched controls. Arch Neurol 34: 99–100

    PubMed  Google Scholar 

  • Nuwer M (1981) Progressive supranuclear palsy despite normal eye movements. Arch Neurol 38: 784

    Google Scholar 

  • Olszewski J (1966) Heterogenous system degeneration. Progressive supranuclear palsy: ocular, facial, bulbar. J Neurosurg [Suppl]: 250–263

    Google Scholar 

  • Olszewski J, Baxter D (1982) Cytoarchitecture of the human brain stem, 2nd edn. Karger, Basel

    Google Scholar 

  • Paxinos G (1980) The human nervous system. Academic Press, San Diego

    Google Scholar 

  • Perkin GD, Lees AJ, Stern GM, Kocen RS (1978) Problems in the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Can J Neurol Sci 5: 167–173

    Google Scholar 

  • Pfaffenbach DD, Layton DD, Kearns TP (1972) Ocular manifestation in progressive supranuclear palsy. Am J Ophthalmol 74: 1179–1184

    PubMed  Google Scholar 

  • Pierrot-Deseilligny Ch (1994) Saccade and smooth-pursuit impairment after cerebral hemispheric lesions. Eur Neurol 34: 121–134

    PubMed  Google Scholar 

  • Pierrot-Deseilligny Ch, Rivaud S, Pillon E, Agid Y (1989) Lateral visually-guided saccades in progressive supranuclear palsy. Brain 112: 471–487

    PubMed  Google Scholar 

  • Pierrot-Deseilligny Ch, Rivaud S, Gaymard B, Muri R, Vermersch AI (1995) Cortical control of saccades. Ann Neurol 37: 557–567

    PubMed  Google Scholar 

  • Pillon B, Dubois B, Lhermitte F, Agid Y (1986) Heterogeneity of cognitive impairment in progressive supranuclear palsy, Parkinson's disease, and Alzheimer's disease. Neurology 36: 1179–1185

    PubMed  Google Scholar 

  • Pillon B, Dubois B, Ploska A, Agid Y (1991) Severity and specificity of cognitive impairment in Alzheimer's, Huntington's, and Parkinson's diseases and progressive supranuclear palsy. Neurology 41: 634–643

    PubMed  Google Scholar 

  • Pramstaller PP, Lees AJ, Luxon LM (1996) Possible clinical overlap between postencephalitic parkinsonism and progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 60: 589–590

    PubMed  Google Scholar 

  • Rail D, Scholtz C, Swash M (1981) Post-encephalitic parkinsonism: current experience. J Neurol Neurosurg Psychiatry 4: 670–676

    Google Scholar 

  • Revesz T, Sangha H, Daniel SE (1996) The nucleus raphe interpositus in the Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Brain 119: 1137–1143

    PubMed  Google Scholar 

  • Rinne JO, Lee MS, Thompson PD, Marsden CD (1994) Corticobasal degeneration. A clinical study of 36 cases. Brain 117: 1183–1196

    PubMed  Google Scholar 

  • Schmidtke K, Buttner-Ennever JA (1992) Nervous control of eyelid function. A review of clinical, experimental and pathological data. Brain 115: 227–247

    PubMed  Google Scholar 

  • Troost BT (1992) Neuro-ophthalmological aspects. In: Litvan I, Agid Y (eds) Progressive supranuclear palsy. Clinical and research approaches. Oxford University Press, New York, pp 184–203

    Google Scholar 

  • Troost BT, Daroff RB (1977) The ocular motor defects in progressive supranuclear palsy. Ann Neurol 2: 397–403

    PubMed  Google Scholar 

  • Verny M, Duyckaerts C, Agid Y, Hauw JJ (1996) The significance of cortical pathology in progressive supranuclear palsy. Clinicopathological data in 10 cases. Brain 119: 1123–1136

    PubMed  Google Scholar 

  • Von Economo C (1929) Die Encephalitis lethargica. Urban und Schwarzenberg, Wien

    Google Scholar 

  • Wenning GK, Ben Shlomo Y, Magalhaes M, Daniel SE, Quinn NP (1994) Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain 117: 835–845

    PubMed  Google Scholar 

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Wenning, G.K., Jellinger, K. & Litvan, I. Supranuclear gaze palsy and eyelid apraxia in postencephalitic parkinsonism. J. Neural Transmission 104, 845–865 (1997). https://doi.org/10.1007/BF01285553

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