The Cerebellum

, Volume 13, Issue 2, pp 215–221 | Cite as

Recessive Spinocerebellar Ataxia with Paroxysmal Cough Attacks: A Report of Five Cases

  • Luis Velázquez-Pérez
  • Rigoberto González-Piña
  • Roberto Rodríguez-Labrada
  • Raul Aguilera-Rodríguez
  • Lourdes Galicia-Polo
  • Yaimeé Vázquez-Mojena
  • Ana M. Cortés-Rubio
  • Marla R. Trujillo-Bracamontes
  • Cesar M. Cerecedo-Zapata
  • Oscar Hernández-Hernández
  • Bulmaro Cisneros
  • Jonathan J. Magaña
Original Paper

Abstract

Hereditary ataxias are a heterogeneous group of neurological diseases characterized by progressive cerebellar syndrome and numerous other features, which result in great diversity of ataxia subtypes. Despite the characterization of a number of both autosomal dominant and autosomal recessive ataxias, it is thought that a large group of these conditions remains to be identified. In this study, we report the characterization of five patients (three Mexicans and two Italians) who exhibit a peculiar form of recessive ataxia associated with coughing. The main clinical and neurophysiological features of these patients include cerebellar ataxia, paroxysmal cough, restless legs syndrome (RLS), choreic movements, atrophy of distal muscles, and oculomotor disorders. Brain magnetic resonance imaging (MRI) revealed cerebellar atrophy, while video polysomnography (VPSG) studies showed a severe pattern of breathing-related sleep disorder, including sleep apnea, snoring, and significant oxygen saturation in the absence of risk factors. All patients share clinical features in the peripheral nervous system, including reduction of amplitude and prolonged latency of sensory potentials in median and sural nerves. Altogether, clinical criteria as well as molecular genetic testing that was negative for different autosomal dominant and autosomal recessive ataxias suggest the presence of a new form of recessive ataxia. This ataxia, in which cerebellar signs are preceded by paroxysmal cough, affects not only the cerebellum and its fiber connections, but also the sensory peripheral nervous system and extracerebellar central pathways.

Keywords

Ataxia Autosomal recessive ataxia Autosomal dominant ataxia Cerebellar atrophy Sensory neuropathy Sleep disorder paroxysmal cough 

References

  1. 1.
    Klockgether T, Paulson H. Milestones in ataxia. Mov Disord. 2011;26(6):1–8.CrossRefGoogle Scholar
  2. 2.
    Klockgether T. Update on degenerative ataxias. Curr Opin Neurol. 2011;24:339–45.PubMedCrossRefGoogle Scholar
  3. 3.
    Velázquez-Pérez L, Rodríguez-Labrada R, García-Rodríguez J, Almaguer-Mederos L, Cruz-Mariño T, Laffita-Mesa JM. A comprehensive review of spinocerebellar ataxia type 2 in Cuba. Cerebellum. 2011;10:184–98.PubMedCrossRefGoogle Scholar
  4. 4.
    Matilla-Dueñas A. The ever expanding spinocerebellar ataxias. (Editorial). Cerebellum. 2012;11:821–7.PubMedCrossRefGoogle Scholar
  5. 5.
    Coutinho P, Cruz V, Tuna A, Silva E, Guimaraes J. Cerebellar ataxia with paroxistic cough. A new form of dominant ataxia. Arch Neurol. 2006;63:553–5.PubMedCrossRefGoogle Scholar
  6. 6.
    Schmitz-Hubsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006;66(11):1717–20.PubMedCrossRefGoogle Scholar
  7. 7.
    Schmitz-Hubsch T, Coudert M, Bauer P, Giunti P, Globas C, Baliko L, et al. Spinocerebellar ataxia types 1, 2, 3, and 6: disease severity and nonataxia symptoms. Neurology. 2008;71(13):982–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Visser M, Marinus J, Stiggelbout AM, Van Hilten JJ. Assessment of autonomic dysfunction in Parkinson's disease: the SCOPA-AUT. Mov Disord. 2004;11(19):1306–12.CrossRefGoogle Scholar
  9. 9.
    Dorschner MO, Barden D, Stephens K. Diagnosis of five spinocerebellar ataxia disorders by multiplex amplification and capillary electrophoresis. J Mol Diagn. 2002;4(2):108–13.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Magaña JJ, Tapia-Guerrero YS, Velázquez-Pérez L, Cerecedo-Zapata C, Maldonado-Rodríguez M, Jano-Ito J, et al. Analysis of CAG repeats in five SCA loci in Mexican population: epidemiological evidence of a SCA7 founder effect. Clin Genet. 2013. doi:10.1111/cge.12114.PubMedGoogle Scholar
  11. 11.
    Torralva T, Roca M, Gleichgerrcht E, López P, Manes F. INECO Frontal Screening (IFS): a brief, sensitive, and specific tool to assess executive functions in dementia. J Int Neuropsychol Soc. 15(5):777–786.Google Scholar
  12. 12.
    Anheim M, Tranchant C, Koenig M. The autosomal recessive cerebellar ataxias. N Engl J Med. 2012;366(7):636–46.PubMedCrossRefGoogle Scholar
  13. 13.
    Anheim M, Mariani LL, Calvas P, et al. Exonic deletions of FXN cause early-onset Friedreich's ataxia. Arch Neurol. 2012;69(7):912–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Schöls L, Amoiridis G, Przuntek H, Frank G, Epplen JT, Epplen C. Friedreich's ataxia: revision of the phenotype according to molecular genetics. Brain. 1997;120:2131–40.PubMedCrossRefGoogle Scholar
  15. 15.
    Berciano J, Infante J, García A, Polo JM, Volpini V, Combarros O. Very late-onset Friedreich's ataxia with minimal GAA1 expansion mimicking multiple system atrophy of cerebellar type. Mov Disord. 2005;20:1643–5.PubMedCrossRefGoogle Scholar
  16. 16.
    Cruz Mariño T, González Zaldívar Y, Laffita JM, Almaguer LE, Aguilera R, Almaguer D, et al. Uncommon phenotypical features in Cuban families with Friedreich ataxia. Neurosci Lett. 2010;472:85–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Mazzone SB, McGovern AE, Yang SK, Woo A, Phipps S, Ando A, et al. Sensorimotor circuitry involved in the higher brain control of coughing. Cough. 2013;9(1):7.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Rybak IA, Shevtsova NA, Paton JF, Dick TE, St-John WM, Mörschel M, et al. Modeling the ponto-medullary respiratory network. Respir Physiol Neurobiol. 2004;143(2–3):307–19.PubMedCrossRefGoogle Scholar
  19. 19.
    Simonyan K, Saad ZS, Loucks TM, Poletto CJ, Ludlow CL. Functional neuroanatomy of human voluntary cough and sniff production. Neuroimage. 2007;37:401–9.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Mazzone SB, Cole LJ, Ando A, Egan GF, Farrell MJ. Investigation of the neural control of cough and cough suppression in humans using functional brain imaging. J Neurosci. 2011;31(8):2948–58.PubMedCrossRefGoogle Scholar
  21. 21.
    Hennemann HE, Rubia FJ. Vagal representation in the cerebellum of the cat. Pflugers Arch. 1978;375(2):119–23.PubMedCrossRefGoogle Scholar
  22. 22.
    Sobusiak T, Zimny R, Matlosz Z. Primary glossopharyngeal and vagal afferent projection into the cerebellum in the dog. J Hirnforsch. 1971;13:117–34.PubMedGoogle Scholar
  23. 23.
    Zheng Z, Dietrichs E, Walberg F. Cerebellar afferent fibres from the dorsal motor vagal nucleus in the cat. Neurosci Lett. 1982;32:113–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Xu F, Frazier DT, Zhang Z, Baekey DM, Shannon R. Cerebellar modulation of cough motor pattern in cats. J Appl Physiol. 1997;83:391–7.PubMedGoogle Scholar
  25. 25.
    Sriranjini SJ, Pal PK, Krishna N, Sathyaprabha TN. Subclinical pulmonary dysfunction in spinocerebellar ataxias 1, 2 and 3. Acta Neurol Scand. 2010;122(5):323–8.PubMedGoogle Scholar
  26. 26.
    Schwarzacher SW, Rüb U, Deller T. Neuroanatomical characteristics of the human pre-Bötzinger complex and its involvement in neurodegenerative brainstem diseases. Brain. 2011;134(Pt 1):24–35.PubMedCrossRefGoogle Scholar
  27. 27.
    Jung BC, Choi SI, Du AX, Cuzzocreo JL, Ying HS, Landman BA, et al. MRI shows a region-specific pattern of atrophy in spinocerebellar ataxia type 2. Cerebellum. 2012;11(1):272–9.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Velázquez-Pérez L, Seifried C, Abele M, Wirjatijasa F, Rodríguez-Labrada R, Santos-Falcón N, et al. Saccade velocity is reduced in presymptomatic spinocerebellar ataxia type 2. Clin Neurophysiol. 2009;120(3):632–5.PubMedCrossRefGoogle Scholar
  29. 29.
    Rodríguez-Labrada R, Velázquez-Perez L, Ochoa NC, Polo LG, Valencia RH, Cruz GS, et al. Subtle rapid eye movement sleep abnormalities in presymptomatic spinocerebellar ataxia type 2 gene carriers. Mov Disord. 2011;26(2):347–50.PubMedCrossRefGoogle Scholar
  30. 30.
    Velázquez-Pérez Luis and Rodríguez Labrada R. Early manifestations of spinocerebellar ataxias type 2. Holguín: Ediciones Holguín; 2012. ISBN 978-959-221-353-1 [Book in Spanish].Google Scholar
  31. 31.
    Jacobi H, Reetz K, du Montcel ST, Bauer P, Mariotti C, Nanetti L, et al. Biological and clinical characteristics of individuals at risk for spinocerebellar ataxia types 1, 2, 3, and 6 in the longitudinal RISCA study: analysis of baseline data. Lancet Neurol. 2013;12(7):650–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Manrique RK, Noval S, Aguilar-Amat MJ, Arpa J, Rosa I, Contreras I. Ophthalmic features of spinocerebellar ataxia type 7. J Neuroophthalmol. 2009;29(3):174–9.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Luis Velázquez-Pérez
    • 1
  • Rigoberto González-Piña
    • 2
  • Roberto Rodríguez-Labrada
    • 1
  • Raul Aguilera-Rodríguez
    • 1
  • Lourdes Galicia-Polo
    • 3
  • Yaimeé Vázquez-Mojena
    • 1
  • Ana M. Cortés-Rubio
    • 4
  • Marla R. Trujillo-Bracamontes
    • 5
  • Cesar M. Cerecedo-Zapata
    • 6
  • Oscar Hernández-Hernández
    • 6
  • Bulmaro Cisneros
    • 7
  • Jonathan J. Magaña
    • 6
  1. 1.Center for the Research and Rehabilitation of the Hereditary Ataxias (CIRAH)HolguínCuba
  2. 2.Department of Brain PlasticityNational Rehabilitation Institute (INR)Mexico CityMexico
  3. 3.Clinic of Sleep Disorders, School of MedicineUNAMMexico CityMexico
  4. 4.Magnetic Resonance ServiceINRMexico CityMexico
  5. 5.Department of Audiology and OtoneurologyINRMexico CityMexico
  6. 6.Laboratory of Genomic Medicine, Department of GeneticsINRMexico CityMexico
  7. 7.Departament of Genetics and Molecular BiologyCINVESTAV-IPNMexico CityMexico

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