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01-11-2016 | Original Communication

Vestibular function in patients with Niemann-Pick type C disease

Authors: Tatiana Bremova, Siegbert Krafczyk, Stanislavs Bardins, Jörg Reinke, Michael Strupp

Published in: Journal of Neurology | Issue 11/2016

Abstract

We investigated whether vestibular dysfunction may cause or contribute to postural imbalance and falls in patients with Niemann-Pick type C disease (NP-C). Eight patients with NP-C disease and 20 healthy controls were examined using the video-based head impulse test (vHIT) and caloric irrigation to investigate horizontal canal function as well as ocular- and cervical vestibular evoked myogenic potentials (o- and cVEMP), and binocular subjective visual vertical estimation (SVV) for otolith function, and static posturography. There were no significant differences in vestibulo-ocular gain, caloric excitability, o-/cVEMP measures or SVV between the two groups. Posturographic total sway path (tSP) and root mean square (RMS) were significantly higher in NP-C than in controls in 3 out of 4 conditions. The Romberg quotient (RQ) to assess the amount of visual stabilization was significantly lower in the NP-C than in the HC group. In contrast to other inherited metabolic disorders, such as Morbus Gaucher type 3, we did not find any evidence for an impairment of canal or otolith function in patients with NP-C as their cause of postural imbalance. Since RQ was low in NP-C patients, indicating proper sensory input, the observed increased postural sway is most likely due to a cerebellar dysfunction in NP-C, which may therefore, explain postural imbalance.

Vanier MT (2013) Niemann-Pick diseases. Handb Clin Neurol 113:1717–1721. doi:10.1016/B978-0-444-59565-2.00041-1 CrossRefPubMed

Patterson MC, Mengel E, Wijburg FA et al (2013) Disease and patient characteristics in NP-C patients: findings from an international disease registry. Orphanet J Rare Dis 8:12. doi:10.1186/1750-1172-8-12 CrossRefPubMedPubMedCentral

Abel LA, Walterfang M, Fietz M et al (2009) Saccades in adult Niemann-Pick disease type C reflect frontal, brainstem, and biochemical deficits. Neurology 72:1083–1086. doi:10.1212/01.wnl.0000345040.01917.9d CrossRefPubMed

Rottach KG, von Maydell RD, Das VE et al (1997) Evidence for independent feedback control of horizontal and vertical saccades from Niemann-Pick type C disease. Vision Res 37:3627–3638. doi:10.1016/S0042-6989(96)00066-1 CrossRefPubMed

Chen L, Halmagyi GM, Todd MJ, Aw ST (2014) Vestibular and saccadic abnormalities in Gaucher’s disease. JIMD Rep 13:111–118. doi:10.1007/8904_2013_264 CrossRefPubMed

Ritchie AE, Griffiths PG, Chinnery PF, Davidson AW (2010) Eye movement recordings to investigate a supranuclear component in chronic progressive external ophthalmoplegia: a cross-sectional study. Br J Ophthalmol 94:1165–1168. doi:10.1136/bjo.2009.165639 CrossRefPubMedPubMedCentral

Kirchner H, Kremmyda O, Hufner K et al (2011) Clinical, electrophysiological, and MRI findings in patients with cerebellar ataxia and a bilaterally pathological head-impulse test. Ann N Y Acad Sci 1233:127–138. doi:10.1111/j.1749-6632.2011.06175.x CrossRefPubMed

Szmulewicz DJ, Waterston JA, Halmagyi GM et al (2011) Sensory neuropathy as part of the cerebellar ataxia neuropathy vestibular areflexia syndrome. Neurology 76:1903–1910. doi:10.1212/WNL.0b013e31821d746e/WNL.0b013e31821d746e CrossRefPubMedPubMedCentral

King KA, Gordon-Salant S, Yanjanin N et al (2014) Auditory phenotype of Niemann-Pick disease, type C1. Ear Hear 35:110–117. doi:10.1097/AUD.0b013e3182a362b8 CrossRefPubMedPubMedCentral

10.

Lengyel D, Weissert M, Schmid L, Gottlob I (1999) Eye movement abnormalities as a sign for the diagnosis in Niemann-Pick disease type C. Klin Monbl Augenheilkd 214:50–52. doi:10.1055/s-2008-1034748 CrossRefPubMed

11.

Solomon D, Winkelman AC, Zee DS et al (2005) Niemann-Pick type C disease in two affected sisters: ocular motor recordings and brain-stem neuropathology. Ann N Y Acad Sci 1039:436–445. doi:10.1196/annals.1325.041 CrossRefPubMed

12.

Krafczyk S, Tietze S, Swoboda W et al (2006) Artificial neural network: a new diagnostic posturographic tool for disorders of stance. Clin Neurophysiol 117:1692–1698CrossRefPubMed

13.

Diener HC, Dichgans J, Bacher M, Gompf B (1984) Quantification of postural sway in normals and patients with cerebellar diseases. Electroencephalogr Clin Neurophysiol 57:134–142CrossRefPubMed

14.

Agrawal Y, Schubert MC, Migliaccio AA et al (2014) Evaluation of quantitative head impulse testing using search coils versus video-oculography in older individuals. Otol Neurotol 35:283–288. doi:10.1097/MAO.0b013e3182995227 CrossRefPubMedPubMedCentral

15.

Halmagyi GM, Cremer PD, Anderson J et al (2000) Isolated directional preponderance of caloric nystagmus: I. Clinical significance. Am J Otol 21:559–567PubMed

16.

Curthoys IS, Vulovic V, Manzari L (2012) Ocular vestibular-evoked myogenic potential (oVEMP) to test utricular function: neural and oculomotor evidence. Acta Otorhinolaryngol Ital 32:41–45PubMedPubMedCentral

17.

Rosengren SM, Kingma H (2013) New perspectives on vestibular evoked myogenic potentials. Curr Opin Neurol 26:74–80. doi:10.1097/WCO.0b013e32835c5ef3 CrossRefPubMed

18.

Zwergal A, Rettinger N, Frenzel C et al (2009) A bucket of static vestibular function. Neurology 72:1689–1692CrossRefPubMed

19.

Bremova T, Malinová V, Amraoui Y et al (2015) Acetyl-dl-leucine in Niemann-Pick type C: a case series. Neurology 85:1368–1375. doi:10.1212/WNL.0000000000002041 CrossRefPubMed

20.

Iturriaga C, Pineda M, Fernández-Valero EM et al (2006) Niemann-Pick C disease in Spain: clinical spectrum and development of a disability scale. J Neurol Sci 249:1–6. doi:10.1016/j.jns.2006.05.054 CrossRefPubMed

21.

Pineda M, Wraith JE, Mengel E et al (2009) Miglustat in patients with Niemann-Pick disease Type C (NP-C): a multicenter observational retrospective cohort study. Mol Genet Metab 98:243–249. doi:10.1016/j.ymgme.2009.07.003 CrossRefPubMed

22.

Subramony SH (2007) SARA–a new clinical scale for the assessment and rating of ataxia. Nat Clin Pract Neurol 3:136–137. doi:10.1038/ncpneuro0426 CrossRefPubMed

23.

Weyer A, Abele M, Schmitz-Hübsch T et al (2007) Reliability and validity of the scale for the assessment and rating of ataxia: a study in 64 ataxia patients. Mov Disord 22:1633–1637. doi:10.1002/mds.21544 CrossRefPubMed

24.

Nasreddine ZS, Phillips NA, Bédirian V et al (2005) The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699. doi:10.1111/j.1532-5415.2005.53221.x CrossRefPubMed

25.

Agrawal Y, Bremova T, Kremmyda O, Strupp M (2013) Semicircular canal, saccular and utricular function in patients with bilateral vestibulopathy: analysis based on etiology. J Neurol 260:876–883. doi:10.1007/s00415-012-6724-y CrossRefPubMed

26.

Bremova T, Bayer O, Agrawal Y et al (2013) Ocular VEMPs indicate repositioning of otoconia to the utricle after successful liberatory maneuvers in benign paroxysmal positioning vertigo. Acta Otolaryngol 133:1297–1303. doi:10.3109/00016489.2013.829922 CrossRefPubMedPubMedCentral

27.

Jongkees LB, Maas JP, Philipszoon AJ (1962) Clinical electronystagmography: a detailed study of electronystagmography in 341 patients with vertigo. Pract Otorhinolaryngol Basel 24:65–93PubMed

28.

Aw ST, Haslwanter T, Halmagyi GM et al (1996) Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects. J Neurophysiol 76:4009–4020PubMed

29.

Schneider E, Villgrattner T, Vockeroth J et al (2009) EyeSeeCam: an eye movement-driven head camera for the examination of natural visual exploration. Ann N Y Acad Sci 1164:461–467. doi:10.1111/j.1749-6632.2009.03858.x CrossRefPubMed

30.

Bartl K, Lehnen N, Kohlbecher S, Schneider E (2009) Head impulse testing using video-oculography. Ann N Y Acad Sci 1164:331–333. doi:10.1111/j.1749-6632.2009.03850.x CrossRefPubMed

31.

Njiokiktjien CJ, Van Parys JA (1976) Romberg’s sign expressed in a quotient. II. Pathology. Agressologie 17:19–23PubMed

32.

Shaikh AG, Marti S, Tarnutzer AA et al (2011) Ataxia telangiectasia: a “disease model” to understand the cerebellar control of vestibular reflexes. J Neurophysiol 105:3034–3041. doi:10.1152/jn.00721.2010 CrossRefPubMed

33.

Strupp M, Kremmyda O, Adamczyk C et al (2014) Central ocular motor disorders, including gaze palsy and nystagmus. J Neurol 261(Suppl 2):542–558. doi:10.1007/s00415-014-7385-9 CrossRefPubMedCentral

34.

Choi J-Y, Kim J-S, Jung J-M et al (2013) Reversed corrective saccades during head impulse test in acute cerebellar dysfunction. Cerebellum 13:243–247. doi:10.1007/s12311-013-0535-2 CrossRef

35.

Choi SY, Lee S-H, Kim HJ, Kim J-S (2014) Impaired modulation of the otolithic function in acute unilateral cerebellar infarction. Cerebellum 13:362–371. doi:10.1007/s12311-013-0544-1 CrossRefPubMed

36.

Solomon D, Winkelman AC, Zee DS et al (2005) Niemann-pick type C disease in two affected sisters: ocular motor recordings and brain-stem neuropathology. Ann N Y Acad Sci 1039:436–445. doi:10.1196/annals.1325.041 CrossRefPubMed

37.

Che Ngwa E, Zeeh C, Messoudi A et al (2014) Delineation of motoneuron subgroups supplying individual eye muscles in the human oculomotor nucleus. Front Neuroanat 8:2. doi:10.3389/fnana.2014.00002 CrossRefPubMedPubMedCentral

38.

Zeeh C, Hess BJ, Horn AKE (2013) Calretinin inputs are confined to motoneurons for upward eye movements in monkey. J Comp Neurol 521:3154–3166. doi:10.1002/cne.23337 CrossRefPubMed

39.

Zeeh C, Mustari MJ, Hess BJM, Horn AKE (2015) Transmitter inputs to different motoneuron subgroups in the oculomotor and trochlear nucleus in monkey. Front Neuroanat 9:95. doi:10.3389/fnana.2015.00095 CrossRefPubMedPubMedCentral

40.

Lloyd-Evans E, Morgan AJ, He X et al (2008) Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 14:1247–1255. doi:10.1038/nm.1876 CrossRefPubMed

41.

Adamczyk C, Strupp M, Jahn K, Horn AKE (2015) Calretinin as a marker for premotor neurons involved in Upgaze in human brainstem. Front Neuroanat 14(9):153. doi:10.3389/fnana.2015.00153

42.

Nashner LM, Black FO, Wall CI (1982) Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci 2:536–544PubMed

43.

Huang J-Y, Peng S-F, Yang C-C et al (2011) Neuroimaging findings in a brain with Niemann-Pick type C disease. J Formos Med Assoc 110:537–542. doi:10.1016/S0929-6646(11)60080-6 CrossRefPubMed

44.

Fusco C, Russo A, Galla D et al (2013) New Niemann-Pick Type C1 gene mutation associated with very severe disease course and marked early cerebellar vermis atrophy. J Child Neurol 28:1694–1697. doi:10.1177/0883073812462765 CrossRefPubMed

45.

Schwesig R, Becker S, Lauenroth A, Kluttig A, Leuchte S, Esperer HD (2009) A novel posturographic method to differentiate sway patterns of patients with Parkinson’s disease from patients with cerebellar ataxia. Biomed Tech 54:347–356. doi:10.1515/BMT.2009.041 CrossRef

46.

Sarna JR, Larouche M, Marzban H et al (2003) Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J Comp Neurol 456:279–291. doi:10.1002/cne.10522 CrossRefPubMed

47.

Günther L, Beck R, Xiong G et al (2015) N-acetyl-L-leucine accelerates vestibular compensation after unilateral labyrinthectomy by action in the cerebellum and thalamus 10(3):e0120891. doi:10.1371/journal.pone.0120891

48.

Vibert N, Vidal PP (2001) In vitro effects of acetyl-DL-leucine (tanganil) on central vestibular neurons and vestibulo-ocular networks of the guinea-pig. Eur J Neurosci 13:735–748CrossRefPubMed

49.

Ertl M, Boegle R, Kirsch V, Dieterich M (2016) On the impact of examiners on latencies and amplitudes in cervical and ocular vestibular-evoked myogenic potentials evaluated over a large sample (N = 1,038). Eur Arch Oto Rhino Laryngol 273:317–323CrossRef

Title: Vestibular function in patients with Niemann-Pick type C disease
Authors: Tatiana Bremova
Siegbert Krafczyk
Stanislavs Bardins
Jörg Reinke
Michael Strupp
Publication date: 01-11-2016
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue 11/2016
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-016-8247-4

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Vestibular function in patients with Niemann-Pick type C disease

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