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Multi-system neurological disease is common in patients with OPA1 mutations

Multi-system neurological disease is common in patients with OPA1 mutations
Multi-system neurological disease is common in patients with OPA1 mutations
Additional neurological features have recently been described in seven families transmitting pathogenic mutations in OPA1, the most common cause of autosomal dominant optic atrophy. However, the frequency of these syndromal 'dominant optic atrophy plus' variants and the extent of neurological involvement have not been established. In this large multi-centre study of 104 patients from 45 independent families, including 60 new cases, we show that extra-ocular neurological complications are common in OPA1 disease, and affect up to 20% of all mutational carriers. Bilateral sensorineural deafness beginning in late childhood and early adulthood was a prominent manifestation, followed by a combination of ataxia, myopathy, peripheral neuropathy and progressive external ophthalmoplegia from the third decade of life onwards. We also identified novel clinical presentations with spastic paraparesis mimicking hereditary spastic paraplegia, and a multiple sclerosis-like illness. In contrast to initial reports, multi-system neurological disease was associated with all mutational subtypes, although there was an increased risk with missense mutations [odds ratio = 3.06, 95% confidence interval = 1.44-6.49; P = 0.0027], and mutations located within the guanosine triphosphate-ase region (odds ratio = 2.29, 95% confidence interval = 1.08-4.82; P = 0.0271). Histochemical and molecular characterization of skeletal muscle biopsies revealed the presence of cytochrome c oxidase-deficient fibres and multiple mitochondrial DNA deletions in the majority of patients harbouring OPA1 mutations, even in those with isolated optic nerve involvement. However, the cytochrome c oxidase-deficient load was over four times higher in the dominant optic atrophy + group compared to the pure optic neuropathy group, implicating a causal role for these secondary mitochondrial DNA defects in disease pathophysiology. Individuals with dominant optic atrophy plus phenotypes also had significantly worse visual outcomes, and careful surveillance is therefore mandatory to optimize the detection and management of neurological disability in a group of patients who already have significant visual impairment.
0006-8950
771-786
Yu-Wai-Man, P.
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Griffiths, P. G.
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Gorman, G. S.
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Lourenco, C. M.
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Caporali, L.
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Lamperti, C.
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Tallaksen, C. M.
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Duffey, P.
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Clarke, M. P.
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Dhillon, B.
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Czermin, B.
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Bonneau, D.
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Marques, W.
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Lenaers, G.
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McFarland, R.
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Carelli, V.
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Bindoff, L .A.
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Horvath, R.
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Amati-Bonneau, P.
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Yu-Wai-Man, P.
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Gorman, G. S.
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Duffey, P.
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Czermin, B.
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Votruba, M.
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Zeviani, M.
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Bindoff, L .A.
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Horvath, R.
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Amati-Bonneau, P.
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Chinnery, P. F.
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Yu-Wai-Man, P., Griffiths, P. G., Gorman, G. S., Lourenco, C. M., Wright, A. F., Auer-Grumbach, M., Toscano, A., Musumeci, O., Valentino, M. L., Caporali, L., Lamperti, C., Tallaksen, C. M., Duffey, P., Miller, J., Whittaker, R. G., Baker, M. R., Jackson, M. J., Clarke, M. P., Dhillon, B., Czermin, B., Stewart, J. D., Hudson, G., Reynier, P., Bonneau, D., Marques, W., Lenaers, G., McFarland, R., Taylor, R .W., Turnbull, D. M., Votruba, M., Zeviani, M., Carelli, V., Bindoff, L .A., Horvath, R., Amati-Bonneau, P. and Chinnery, P. F. (2010) Multi-system neurological disease is common in patients with OPA1 mutations. Brain, 133 (3), 771-786. (doi:10.1093/brain/awq007). (PMID:21646330)

Record type: Article

Abstract

Additional neurological features have recently been described in seven families transmitting pathogenic mutations in OPA1, the most common cause of autosomal dominant optic atrophy. However, the frequency of these syndromal 'dominant optic atrophy plus' variants and the extent of neurological involvement have not been established. In this large multi-centre study of 104 patients from 45 independent families, including 60 new cases, we show that extra-ocular neurological complications are common in OPA1 disease, and affect up to 20% of all mutational carriers. Bilateral sensorineural deafness beginning in late childhood and early adulthood was a prominent manifestation, followed by a combination of ataxia, myopathy, peripheral neuropathy and progressive external ophthalmoplegia from the third decade of life onwards. We also identified novel clinical presentations with spastic paraparesis mimicking hereditary spastic paraplegia, and a multiple sclerosis-like illness. In contrast to initial reports, multi-system neurological disease was associated with all mutational subtypes, although there was an increased risk with missense mutations [odds ratio = 3.06, 95% confidence interval = 1.44-6.49; P = 0.0027], and mutations located within the guanosine triphosphate-ase region (odds ratio = 2.29, 95% confidence interval = 1.08-4.82; P = 0.0271). Histochemical and molecular characterization of skeletal muscle biopsies revealed the presence of cytochrome c oxidase-deficient fibres and multiple mitochondrial DNA deletions in the majority of patients harbouring OPA1 mutations, even in those with isolated optic nerve involvement. However, the cytochrome c oxidase-deficient load was over four times higher in the dominant optic atrophy + group compared to the pure optic neuropathy group, implicating a causal role for these secondary mitochondrial DNA defects in disease pathophysiology. Individuals with dominant optic atrophy plus phenotypes also had significantly worse visual outcomes, and careful surveillance is therefore mandatory to optimize the detection and management of neurological disability in a group of patients who already have significant visual impairment.

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Published date: March 2010
Organisations: Centre for Biological Sciences

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Local EPrints ID: 355910
URI: http://eprints.soton.ac.uk/id/eprint/355910
ISSN: 0006-8950
PURE UUID: 5f655468-0c9d-4d38-a069-337294f33de6
ORCID for J. D. Stewart: ORCID iD orcid.org/0000-0002-2608-1967

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Date deposited: 04 Sep 2013 16:55
Last modified: 14 Mar 2024 14:39

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Contributors

Author: P. Yu-Wai-Man
Author: P. G. Griffiths
Author: G. S. Gorman
Author: C. M. Lourenco
Author: A. F. Wright
Author: M. Auer-Grumbach
Author: A. Toscano
Author: O. Musumeci
Author: M. L. Valentino
Author: L. Caporali
Author: C. Lamperti
Author: C. M. Tallaksen
Author: P. Duffey
Author: J. Miller
Author: R. G. Whittaker
Author: M. R. Baker
Author: M. J. Jackson
Author: M. P. Clarke
Author: B. Dhillon
Author: B. Czermin
Author: J. D. Stewart ORCID iD
Author: G. Hudson
Author: P. Reynier
Author: D. Bonneau
Author: W. Marques
Author: G. Lenaers
Author: R. McFarland
Author: R .W. Taylor
Author: D. M. Turnbull
Author: M. Votruba
Author: M. Zeviani
Author: V. Carelli
Author: L .A. Bindoff
Author: R. Horvath
Author: P. Amati-Bonneau
Author: P. F. Chinnery

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