Top

Published in:

01-07-2018 | Original Communication

Auditory function in Pelizaeus–Merzbacher disease

Authors: Thierry Morlet, Kyoko Nagao, S. Charles Bean, Sara E. Mora, Sarah E. Hopkins, Grace M. Hobson

Published in: Journal of Neurology | Issue 7/2018

Abstract

Pelizaeus–Merzbacher disease (PMD; MIM 312080), an inherited defect of central nervous system myelin formation, affects individuals in many ways, including their hearing and language abilities. The aim of this study was to assess the auditory abilities in 18 patients with PMD by examining the functional processes along the central auditory pathways using auditory brainstem responses (ABR) and cortical auditory evoked potentials (CAEP) in response to speech sounds. The significant ABR anomalies confirm the existence of dyssynchrony previously described at the level of the brainstem in patients with PMD. Despite the significant auditory dyssynchrony observed at the level of the brainstem, CAEPs were present in most patients, albeit somehow abnormal in terms of morphology and latency, resembling a type of auditory neuropathy spectrum disorder.

Garbern JY, Cambi F, Lewis R, Shy M, Sima A, Kraft G, Vallat JM, Bosch EP, Hodes ME, Dlouhy S, Raskind W, Bird T, Macklin W, Kamholz J (1999) Peripheral neuropathy caused by proteolipid protein gene mutations. Ann N Y Acad Sci 883:351–365CrossRefPubMed

Shy ME, Hobson G, Jain M, Boespflug-Tanguy O, Garbern J, Sperle K, Li W, Gow A, Rodriguez D, Bertini E, Mancias P, Krajewski K, Lewis R, Kamholz J (2003) Schwann cell expression of PLP1 but not DM20 is necessary to prevent neuropathy. Ann Neurol 53:354–365. https://doi.org/10.1002/ana.10466 CrossRefPubMedPubMedCentral

Kuan CC, Sano M, Kaga K, Kodama M, Kodama K (2008) Hearing profile and MRI myelination of auditory pathway in Pelizaeus–Merzbacher disease. Acta Otolaryngol 128:539–546. https://doi.org/10.1080/00016480701258713 CrossRefPubMed

Garbern JY, Yool DA, Moore GJ, Wilds IB, Faulk MW, Klugmann M, Nave KA, Sistermans EA, van der Knaap MS, Bird TD, Shy ME, Kamholz JA, Griffiths IR (2002) Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain 125:551–561CrossRefPubMed

Sima AA, Pierson CR, Woltjer RL, Hobson GM, Golden JA, Kupsky WJ, Schauer GM, Bird TD, Skoff RP, Garbern JY (2009) Neuronal loss in Pelizaeus–Merzbacher disease differs in various mutations of the proteolipid protein 1. Acta Neuropathol 118:531–539. https://doi.org/10.1007/s00401-009-0562-8 CrossRefPubMed

Laukka JJ, Kamholz J, Bessert D, Skoff RP (2016) Novel pathologic findings in patients with Pelizaeus–Merzbacher disease. Neurosci Lett 627:222–232. https://doi.org/10.1016/j.neulet.2016.05.028 CrossRefPubMedPubMedCentral

Hobson GM, Garbern JY (2012) Pelizaeus–Merzbacher disease, Pelizaeus–Merzbacher-like disease 1, and related hypomyelinating disorders. Semin Neurol 32:62–67. https://doi.org/10.1055/s-0032-1306388 CrossRefPubMed

Hobson GM, Kamholz J. (1999) PLP1-related disorders. In: Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, Bird TD, Ledbetter N, Mefford HC, Smith RJH, Stephens K (eds) GeneReviews. University of Washington, Seattle, pp 1993–2017

Ochs R, Markand ON, DeMyer WE (1979) Brainstem auditory evoked responses in leukodystrophies. Neurology 29:1089–1093CrossRefPubMed

10.

Markand ON, Garg BP, DeMyer WE, Warren C, Worth RM (1982) Brain stem auditory, visual and somatosensory evoked potentials in leukodystrophies. Electroencephalogr Clin Neurophysiol 1982 54:39–48CrossRefPubMed

11.

Feldman JI, Kearns DB, Seid AB, Pransky SM, Jones MC (1990) The otolaryngologic manifestations of Pelizaeus–Merzbacher disease. Arch Otolaryngol Head Neck Surg 116:613–616CrossRefPubMed

12.

Garg BP, Markand ON, DeMyer WE (1983) Usefulness of BAER studies in the early diagnosis of Pelizaeus–Merzbacher disease. Neurology 33:955–956CrossRefPubMed

13.

Nezu A (1995) Neurophysiological study in Pelizaeus–Merzbacher disease. Brain Dev 17:175–181CrossRefPubMed

14.

Kon K, Inagaki M, Kaga M, Sasaki M, Hanaoka S (2000) Otoacoustic emission in patients with neurological disorders who have auditory brainstem response abnormality. Brain Dev 22:327–335CrossRefPubMed

15.

Kaga K, Tamai F, Kodama M, Kodama K (2005) Three young adult patients with Pelizaeus–Merzbacher disease who showed only waves I and II in auditory brainstem responses but had good auditory perception. Acta Otolaryngol 125:1018–1023CrossRefPubMed

16.

Tanaka M, Hamano S, Sakata H, Adachi N, Kaga K, Osaka H, Kurosawa K (2008) Discrepancy between auditory brainstem responses, auditory steady-state responses, and auditory behavior in two patients with Pelizaeus–Merzbacher disease. Auris Nasus Larynx 35:404–407CrossRefPubMed

17.

Henneke M, Gegner S, Hahn A, Plecko-Startinig B, Weschke B, Gärtner J, Brockmann K (2010) Clinical neurophysiology in GJA12-related hypomyelination vs Pelizaeus–Merzbacher disease. Neurology 74:1785–1789. https://doi.org/10.1212/WNL.0b013e3181e0f820 CrossRefPubMed

18.

Rikitake M, Kaga K (2012) Development of speech and hearing of two children with Pelizaeus–Merzbacher disease presenting only waves I and II of the auditory brainstem response. Acta Otolaryngol 132:563–569. https://doi.org/10.3109/00016489.2011.647362 CrossRefPubMed

19.

De Meirleir LJ, Taylor MJ, Logan WJ (1988) Multimodal evoked potential studies in leukodystrophies of children. Can J Neurol Sci 15:26–31CrossRefPubMed

20.

Schmutzhard J, Schwentner I, Glueckert R, Sergi C, Beckmann F, Abraham I, Riechelmann H, Schrott-Fischer A, Müller B (2009) Pelizaeus Merzbacher disease: morphological analysis of the vestibulo-cochlear system. Acta Otolaryngol 129:1395–1399. https://doi.org/10.3109/00016480802698866 CrossRefPubMed

21.

Beck CR, Carvalho CM, Banser L, Gambin T, Stubbolo D, Yuan B, Sperle K, McCahan SM, Henneke M, Seeman P, Garbern JY, Hobson GM, Lupski JR (2015) Complex genomic rearrangements at the PLP1 locus include triplication and quadruplication. PLoS Genet 6;11:e1005050. https://doi.org/10.1371/journal.pgen.1005050 CrossRef

22.

Fattal-Valevski A, DiMaio MS, Hisama FM, Hobson GM, Davis-Williams A, Garbern JY, Mahoney MJ, Kolodny EH, Pastores GM (2009) Variable expression of a novel PLP1 mutation in members of a family with Pelizaeus–Merzbacher disease. J Child Neurol 24:618–624. https://doi.org/10.1177/0883073808327833 CrossRefPubMed

23.

Woodward KJ, Cundall M, Sperle K, Sistermans EA, Ross M, Howell G, Gribble SM, Burford DC, Carter NP, Hobson DL, Garbern JY, Kamholz J, Heng H, Hodes ME, Malcolm S, Hobson GM (2005) Heterogeneous duplications in patients with Pelizaeus–Merzbacher disease suggest a mechanism of coupled homologous and nonhomologous recombination. Am J Hum Genet 77:966–987. https://doi.org/10.1086/498048 CrossRefPubMedPubMedCentral

24.

Laukka JJ, Stanley JA, Garbern JY, Trepanier A, Hobson G, Lafleur T, Gow A, Kamholz J (2013) Neuroradiologic correlates of clinical disability and progression in the X-linked leukodystrophy Pelizaeus–Merzbacher disease. J Neurol Sci 335:75–81. https://doi.org/10.1016/j.jns.2013.08.030 CrossRefPubMedPubMedCentral

25.

Biacabe B, Chevallier JM, Avan P, Bonfils P (2001) Functional anatomy of auditory brainstem nuclei: application to the anatomical basis of brainstem auditory evoked potentials. Auris Nasus Larynx 28:85–94CrossRefPubMed

26.

Seitelberger F (1995) Neuropathology and genetics of Pelizaeus–Merzbacher disease. Brain Pathol 5:267–273CrossRefPubMed

27.

McDonald WI (1980) Physiological consequences of demyelination. In: Sumner AJ (ed) The physiology of peripheral nerve disease. WB Saunders, Philadelphia, pp 265–286

28.

Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI (1996) Auditory neuropathy. Brain 119:741–753CrossRefPubMed

29.

Merchant SN, McKenna MJ, Nadol JB Jr, Kristiansen AG, Tropitzsch A, Lindal S, Tranebjaeizrg L (2001) Temporal bone histopathologic and genetic studies in Mohr-Tranebjaerg syndrome (DFN-1). Otol Neurotol 22:506–511CrossRefPubMed

30.

Ceranic B, Luxon LM (2004) Progressive auditory neuropathy in patients with Leber’s hereditary optic neuropathy. J Neurol Neurosurg Psychiatry 75:626–630CrossRefPubMedPubMedCentral

31.

Corley VM, Crabbe LS (1999) Auditory neuropathy and a mitochondrial disorder in a child: case study. J Am Acad Audiol 10:484–488PubMed

32.

Forli F, Mancuso M, Santoro A, Dotti MT, Siciliano G, Berrettini S (2006) Auditory neuropathy in a patient with mitochondrial myopathy and multiple mtDNA deletions. J Laryngol Otol 120:888–891. https://doi.org/10.1017/S0022215106001472 CrossRefPubMed

33.

Hood L, Morlet T (2012) Current issues in auditory neuropathy spectrum disorder. In: Tremblay K, Burkard R (eds) Translational perspectives in auditory neurosciences. Special topics. Plural Publishing, San Diego, pp 35–68

34.

Miyamoto RT, Kirk KI, Renshaw J, Hussain D (1999) Cochlear implantation in auditory neuropathy. Laryngoscope 109:181–185CrossRefPubMed

35.

Rance G, Fava R, Baldock H, Chong A, Barker E, Corben L, Delatycki MB (2008) Speech perception ability in individuals with Friedreich ataxia. Brain 131:2002–2012. https://doi.org/10.1093/brain/awn104 CrossRefPubMed

36.

Rance G, Corben L, Barker E, Carew P, Chisari D, Rogers M, Dowell R, Jamaluddin S, Bryson R, Delatycki MB (2010) Auditory perception in individuals with Friedreich’s ataxia. Audiol Neurotol 15:229–240. https://doi.org/10.1159/000255341 CrossRef

37.

Voordecker P, Brunko E, de Beyl Z (1988) Selective unilateral absence or attenuation of wave V of brain-stem auditory evoked potentials with intrinsic brain-stem lesions. Arch Neurol 45:1272–1276CrossRefPubMed

38.

Ceponiene R, Alku P, Westerfield M et al (2005) ERPs differentiate syllable and nonphonetic sound processing in children and adults. Psychophysiol 42:391–406CrossRef

39.

Hood LJ, Wilensky D, Li L, Berlin CI (2004) The role of FM technology in the management of patients with auditory neuropathy/dys-synchrony. In: Proceedings of the International Conference on FM Technology, Chicago, Illinois, November, 2003, pp 107–111

40.

Kraus N, Bradlow AR, Cheatham MA, Cunningham J, King CD, Koch DB, Nicol TG, McGee TJ, Stein LK, Wright BA (2000) Consequences of a neural asynchrony: a case of auditory neuropathy. J Assoc Res Otolaryngol 1:33–45CrossRefPubMedPubMedCentral

Title: Auditory function in Pelizaeus–Merzbacher disease
Authors: Thierry Morlet
Kyoko Nagao
S. Charles Bean
Sara E. Mora
Sarah E. Hopkins
Grace M. Hobson
Publication date: 01-07-2018
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue 7/2018
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-018-8884-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Auditory function in Pelizaeus–Merzbacher disease

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2018

The silver effect of admission glucose level on excellent outcome in thrombolysed stroke patients

Longitudinal diffusion tensor imaging changes in early Parkinson’s disease: ICICLE-PD study

A startling acoustic stimulus facilitates voluntary lower extremity movements and automatic postural responses in people with chronic stroke

Anti-NMDA receptor encephalitis triggered by epilepsy surgery

Proprioceptive muscle tendon stimulation reduces symptoms in primary orthostatic tremor

Adam Opalski (1897–1963)