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Egyptian Rheumatology and Rehabilitation
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Sensory changes in pediatric patients with spinal muscular atrophy: an electrophysiologic study

Egyptian Rheumatology and Rehabilitation volume 43, pages 1–6 (2016)Cite this article

Abstract

Context

Spinal muscular atrophy (SMA) is well known to be a pure motor neuron disease. However, it was reported that sensory neuron degeneration can also occur in pediatric SMA.

Aim of the work

The aim of the present study was to assess peripheral and central sensory abnormalities in pediatric SMA patients.

Materials and methods

The present study included 29 type I and 11 type II SMA patients diagnosed on the basis of clinical history and typical electromyographic patterns, and 25 age-matched and sex-matched healthy pediatric participants, who comprised the control group. Sensory and motor conduction studies were carried out for both groups. Sensory conduction studies of sural and median nerves assessed peak latency, sensory nerve action potential (SNAP) amplitude, and sensory nerve conduction velocity. Mixed posterior tibial somatosensory evoked potential latency and amplitude were also assessed for both groups.

Results

SMA I patients had lower sural and median SNAP amplitudes, as well as lower peroneal and femoral compound muscle action potential amplitudes, slower tibial motor conduction velocity (MCV), and prolonged femoral and peroneal distal latency compared with the control group. SMA II patients had lower sural SNAP amplitude, slower sural sensory nerve conduction velocity, lower tibial somatosensory evoked potential amplitude, and lower tibial peroneal and femoral compound muscle action potential amplitudes, as well as slower tibial motor conduction velocity and prolonged peroneal distal latency, compared with the control group.

Conclusion

Sensory neuron and/or axonal affection have been demonstrated in the studied series of pediatric SMA patients suggesting that the pathological changes in SMA may also involve the sensory system.

References

  1. Yonekawa T, Komaki H, Saito Y, Sugai K, Sasaki M. Peripheral nerve abnormalities in pediatric patients with spinal muscular atrophy. Brain Dev 2013; 35:165–171.

    Article  Google Scholar 

  2. Farrar MA, Vucic S, Johnston HM, du Sart D, Kiernan MC. Pathophysiological insights derived by natural history and motor function of spinal muscular atrophy. J Pediatr 2013; 162:155-159.

    Article  Google Scholar 

  3. Burghes AH, Beattie CE. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci 2009; 10:597–609.

    Article  CAS  Google Scholar 

  4. Markowitz JA, Singh P, Darras BT. Spinal muscular atrophy: a clinical and research update. Pediatr Neurol 2012; 46:1–12.

    Article  Google Scholar 

  5. Zerres K, Davies KE. 59th ENMC International Workshop: Spinal muscular atrophies: recent progress and revised diagnostic criteria 17e19 April 1998, Soestduinen, The Netherlands. Neuromuscul Disord 1999; 9:272–278.

    Article  CAS  Google Scholar 

  6. Dubowitz V. Chaos in the classification of SMA: a possible resolution. Neuromuscul Disord 1995; 5:3–5.

    Article  CAS  Google Scholar 

  7. Mentis GZ, Blivis D, Liu W, Drobac E, Crowder ME, Kong L, et al. Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 2011; 69:453–467.

    Article  CAS  Google Scholar 

  8. Chien YY, Nonaka I. Peripheral nerve involvement in Werdnig–Hoffmann disease. Brain Dev 1989; 11:221–229.

    Article  CAS  Google Scholar 

  9. Rudnik-Schöneborn S, Goebel HH, Schlote W, Molaian S, Omran H, Ketelsen U, et al. Classical infantile spinal muscular atrophy with SMN deficiency causes sensory neuronopathy. Neurology 2003; 60:983–987.

    Article  Google Scholar 

  10. Carpenter S, Karpati G, Rothman S, Watters G, Andermann F. Pathological involvement of primary sensory neurons in Werdnig– Hoffmann disease. Acta Neuropathol 1978; 42:91–97.

    Article  CAS  Google Scholar 

  11. Marshall A, Duchen LW. Sensory system involvement in infantile spinal muscular atrophy. J Neurol Sci 1975; 26:349–359.

    Article  CAS  Google Scholar 

  12. Schwartz MS, Moosa A. Sensory nerve conduction in spinal muscular atrophies. Dev Med Child Neurol 1977; 19:50–53.

    Article  CAS  Google Scholar 

  13. Ryniewicz B. Motor and sensory conduction velocity in spinal muscular atrophy. Follow-up study. Electromyogr Clin Neurophysiol 1977; 17:385–391.

    CAS  PubMed  Google Scholar 

  14. Cheliout-Heraut F, Barois A, Urtizberea A, Viollet L, Estournet Mathiaud B. Evoked potentials in spinal muscular atrophy. J Child Neurol 2003; 18:383-390.

    Article  Google Scholar 

  15. Munsat TL. Workshop report: International SMA Collaboration. Neuromuscul Disord 1991; 1:81.

    Article  Google Scholar 

  16. Ling KK, Lin MY, Zingg B, Feng Z, Ko CP. Synaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy. PLoS One 2010; 5:e15457.

    Google Scholar 

  17. Raff MC, Whitmore AV, Finn JT. Axonal self-destruction and neurodegeneration. Science 2002; 296:868–871.

    Article  CAS  Google Scholar 

  18. Wishart TM, Parson SH, Gillingwater TH. Synaptic vulnerability in neurodegenerative disease. J Neuropathol Exp Neurol 2006; 65:733–739.

    Article  CAS  Google Scholar 

  19. Schütz B. Imbalanced excitatory to inhibitory synaptic input precedes motor neuron degeneration in an animal model of amyotrophic lateral sclerosis. Neurobiol Dis 2005; 20:131–140.

    Article  Google Scholar 

  20. Jiang M, Schuster JE, Fu R, Siddique T, Heckman CJ. Progressive changes in synaptic inputs to motoneurons in adult sacral spinal cord of a mouse model of amyotrophic lateral sclerosis. J Neurosci 2009; 29:15031–15038.

    Article  CAS  Google Scholar 

  21. Ikemoto A, Nakamura S, Akiguchi I, Hirano A. Differential expression between synaptic vesicle proteins and presynaptic plasma membrane proteins in the anterior horn of amyotrophic lateral sclerosis. Acta Neuropathol 2002; 103:179–187.

    Article  CAS  Google Scholar 

  22. Nagao M, Misawa H, Kato S, Hirai S. Loss of cholinergic synapses on the spinal motor neurons of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1998; 57:329–333.

    Article  CAS  Google Scholar 

  23. Zang DW, Lopes EC, Cheema SS. Loss of synaptophysin-positive boutons on lumbar motor neurons innervating the medial gastrocnemius muscle of the SOD1G93A G1H transgenic mouse model of ALS. J Neurosci Res 2005; 79:694–699.

    Article  CAS  Google Scholar 

  24. Ikemoto A, Hirano A, Matsumoto S, Akiguchi I, Kimura J. Synaptophysin expression in the anterior horn of Werdnig–Hoffmann disease. J Neurol Sci 1996; 136:94–100.

    Article  CAS  Google Scholar 

  25. Yamanouchi Y, Yamanouchi H, Becker LE. Synaptic alterations of anterior horn cells in Werdnig–Hoffmann disease. Pediatr Neurol 1996; 15:32–35.

    Article  CAS  Google Scholar 

  26. Gogliotti RG, Quinlan KA, Barlow CB, Heier CR, Heckman CJ, DiDonato CJ. Motor neuron rescue in spinal muscular atrophy mice demonstrates that sensory-motor defects are a consequence, not a cause, of motor neuron dysfunction, J Neurosci. 2012; 32:3818–3829.

    Article  CAS  Google Scholar 

  27. Moosa A, Dubowitz V. Motor nerve conduction velocity in spinal muscular atrophy of childhood. Arch Dis Child 1976; 51:974–977.

    Article  CAS  Google Scholar 

  28. Kimura J. Basics in nerve conduction study: evoked potentials and electromyography: principles and practice (in Japanese). Tokyo: Igakushoin; 1990.

    Google Scholar 

  29. Gilliatt RW, Hopf HC, Rudge P, Baraiser M. Axonal velocities of motor units in the hand and foot muscles of the baboon. J Neurol Sci 1976; 29:249–258.

    Article  CAS  Google Scholar 

  30. Miyanomae Y, Takeuchi Y, Nishimura A, Kawase S, Hirai K, Ochi M, et al. Motor nerve conduction studies on children with spinal muscular atrophy. Acta Paediatr Jpn 1996; 38:576–579.

    Article  CAS  Google Scholar 

  31. Kumagai T, Hashizume Y. Morphological and morphometric studies on the spinal cord lesion in Werdnig–Hoffmann disease. Brain Dev 1982; 4:87–96.

    Article  CAS  Google Scholar 

  32. Murayama S, Bouldin TW, Suzuki K. Immunocytochemical and ultrastructural studies of Werdnig–Hoffmann disease. Acta Neuropathol 1991; 81:408–417.

    Article  CAS  Google Scholar 

  33. Osawa M, Shishikura K. Werdnig–Hoffmann disease and variants. In: de Jong JMBV, editor. Handbook of clinical neurology. Amsterdam: Elsevier; 1991. 15:51–80.

    Google Scholar 

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Authors and Affiliations

  1. Physical Medicine, Rheumatology and Rehabilitation Department, Faculty of Medicine, Alexandria University, Alexandria, Egypt

    Hussien E. Sultan & Wafaa S. El-Emary MD

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  1. Hussien E. Sultan
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  2. Wafaa S. El-Emary MD
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Correspondence to Wafaa S. El-Emary MD.

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Sultan, H.E., El-Emary, W.S. Sensory changes in pediatric patients with spinal muscular atrophy: an electrophysiologic study. Egypt Rheumatol Rehabil 43, 1–6 (2016). https://doi.org/10.4103/1110-161X.177419

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