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Human Physiology

, Volume 44, Issue 8, pp 827–837 | Cite as

Electrophysiological Techniques for Motor Unit Number Estimation

  • A. F. MurtazinaEmail author
  • A. I. Belyakova-Bodina
  • A. G. Brutyan
Article

Abstract

Various neurological diseases involving motor neurons damage lead to a decrease in the number of functioning motor units (MUs). Accurate estimation of the number of intact MUs plays significant role in evaluating motor neuron death. Quantitative analysis of MUs by methods of routine electromyography is usually not possible. Therefore, electrophysiological techniques for MU number estimation (so-called motor unit number estimation, MUNE), have been rapidly developing over the past decades. The first article on MUNE was published in 1971. Promising, accurate, and less time-consuming modifications have been developed since, and new methods for counting MU have been proposed. In recent years, one can see increasing interest in MUNE explained by the ongoing research on new possibilities of motor neuron disease treatment, and evaluation of their effectiveness, dynamic control of the disease. Today, MUNE is considered to be a potential biomarker in many clinical trials involving patients with motor neuron disease. This review provides in sights on available MUNE techniques, describes their comparative characteristics, advantages and disadvantages of each method and their application perspectives.

Keywords:

motor units electromyography MUNE motor neuron disease 

REFERENCES

  1. 1.
    Gooch, C.L., Doherty, T.J., Chan, K.M., et al., Motor unit number estimation: a technology and literature review, Muscle Nerve, 2014, vol. 50, no. 6, pp. 884–893. PMID 25186553. doi 10.1002/mus.24442CrossRefGoogle Scholar
  2. 2.
    McComas, A.J., Motor unit estimation: anxieties and achievements, Muscle Nerve, 1995, vol. 18, no. 4, pp. 369–379. PMID 7715621. doi 10.1002/mus. 880180402CrossRefGoogle Scholar
  3. 3.
    Aoyagi, Y., Strohschein, F.J., and Ming Chan, K., Use of the collision technique to improve the accuracy of motor unit number estimation, Clin. Neurophysiol., 2000, vol. 111, no. 7, pp. 1315–1319. PMID 10880808. doi 10.1016/S1388-2457(00)00318-7CrossRefGoogle Scholar
  4. 4.
    Daube, J.R., Statistical estimates of number of motor units in thenar and foot muscles in patients with amyotrophic lateral sclerosis or the residue of poliomyelitis, Muscle Nerve, 1988, vol. 11, no. 9, pp. 957–958.CrossRefGoogle Scholar
  5. 5.
    Yang, J.F., Stein, R.B., Jhamandas, J., and Gordon, T., Motor unit numbers and contractile properties after spinal cord injury, Ann. Neurol., 1990, vol. 28, no. 4, pp. 496–502. PMID 2252362. doi 10.1002/ ana.410280405CrossRefGoogle Scholar
  6. 6.
    Bromberg, M., Motor unit estimation: reproducibility of the spike-triggered averaging technique in normal and ALS subjects, Muscle Nerve, 1993, vol. 16, no. 5, pp. 466–471. PMID 8515754. doi 10.1002/ mus.880160506CrossRefGoogle Scholar
  7. 7.
    Felice, K.J., Thenar motor unit number estimates using the multiple point stimulation technique: reproducibility studies in ALS patients and normal subjects, Muscle Nerve, 1995, vol. 18, no. 12, pp. 1412–1416. PMID 7477064. doi 10.1002/mus.880181211CrossRefGoogle Scholar
  8. 8.
    Bromberg, M.B. and Larson, W.L., Relationships between motor-unit number estimates and isometric strength in distal muscles in ALS/MND, J. Neurol. Sci., 1996, vol. 139, suppl., pp. 38–42. PMID 8899656CrossRefGoogle Scholar
  9. 9.
    Felice, K., A longitudinal study comparing thenar motor unit numbe estimates to other quantitative tests in patients with amyotrophic lateral sclerosis, Muscle Nerve, 1997, vol. 20, pp. 179–185. PMID 9040656. doi 10.1002/(SICI)1097-4598(199702)20:2< 179::AID-MUS7>3.0.CO;2-9Google Scholar
  10. 10.
    Felice, K.J., Nerve conduction velocities of single thenar motor axons based on the automated analysis of F waves in amyotrophic lateral sclerosis, Muscle Nerve, 1998, vol. 21, pp. 756–761. PMID 9585329. doi 10.1002/(SICI)1097-4598(199806)21:6<756::AID-MUS7>3.0.CO;2-6CrossRefGoogle Scholar
  11. 11.
    Wang, F.C. and Delwaide, P.J., Number and relative size of thenar motor units in ALS patients: application of the adapted multiple point stimulation method, Electroencephalogr. Clin. Neurophysiol., 1998, vol. 109, no. 1, pp. 36–43. PMID 11003062. doi 10.1016/ S0924-980X(97)00071-4CrossRefGoogle Scholar
  12. 12.
    Armon, C. and Brandstater, M.E., Motor unit number estimate-based rates of progression of ALS predict patient survival, Muscle Nerve, 1999, vol. 22, pp. 1571–1575. PMID 10514236. doi 10.1002/(SICI)1097-4598(199911)22:11<1571:AID-MUS13>3.0.CO;2-0CrossRefGoogle Scholar
  13. 13.
    Kuwabara, S., Mizobuchi, K., Ogawara, K., and Hattori, T., Dissociated small hand muscle involvement in amyotrophic lateral sclerosis detected by motor unit number estimates, Muscle Nerve, 1999, vol. 22, pp. 870–873. PMID 10398204. doi 10.1002/ SICI)1097-4598(199907)22:7<870::AID-MUS9>3.0. CO;2-OCrossRefGoogle Scholar
  14. 14.
    Cuturic, M. and Palliyath, S., Motor unit number estimate (MUNE) testing in male patients with mild to moderate carpal tunnel syndrome, Electroencephalogr. Clin. Neurophysiol., 2000, vol. 40, pp. 67–72. PMID 10746180Google Scholar
  15. 15.
    Hara, Y., Akaboshi, K., Masakado, Y., and Chino, N., Physiologic decrease of single thenar motor units in the F-response in stroke patients, Arch. Phys. Med. Rehabil., 2000, vol. 81, pp. 418–423. PMID 10768529. doi 10.1053/mr.2000.3872CrossRefGoogle Scholar
  16. 16.
    McComas, A.J., Fawcett, P.R., Campbell, M.J., and Sica, R.E., Electrophysiological estimation of the number of motor units within a human muscle, J. Neurol., Neurosurg. Psychiatry, 1971, vol. 34, no. 2, pp. 121–131. PMID 5571599. doi 10.1136/ jnnp.34.2.121CrossRefGoogle Scholar
  17. 17.
    Brown, W.F., A method for estimating the number of motor units in thenar muscles and the changes in motor unit count with aging, J. Neurol., Neurosurg. Psychiatry, 1972, vol. 35, no. 6, pp. 845–852. PMID 4647858CrossRefGoogle Scholar
  18. 18.
    Brown, W.F., Thenar motor unit count estimates in the carpal tunnel syndrome, J. Neurol., Neurosurg. Psychiatry, 1973, vol. 36, no. 2, pp. 194–198. PMID 4708453CrossRefGoogle Scholar
  19. 19.
    Ballantyne, J.P. and Hansen, S., A new method for the estimation of the number of motor units in a muscle. I. Control subjects and patients with myasthenia gravis, J. Neurol., Neurosurg. Psychiatry, 1974, vol. 37, no. 8, pp. 907–915. PMID 4425377CrossRefGoogle Scholar
  20. 20.
    Panayiotopoulos, C.P., Scarpalezos, S., and Papapetropoulos, T., Electrophysiological estimation of motor units in Duchenne muscular dystrophy, J. Neurol. Sci., 1974, vol. 23, no. 1, pp. 89–98. PMID 4851827. doi 10.1016/0022-510X(74)90145-2CrossRefGoogle Scholar
  21. 21.
    Sica, R.E., McComas, A.J., Upton, A.R., and Longmire, D., Motor unit estimations in small muscles of the hand, J. Neurol., Neurosurg. Psychiatry, 1974, vol. 37, pp. 55–67. PMID 4360400CrossRefGoogle Scholar
  22. 22.
    Brown, W.F. and Milner-Brown, H.S., Some electrical properties of motor units and their effects on the methods of estimating motor unit numbers, J. Neurol., Neurosurg. Psychiatry, 1976, vol. 39, pp. 249–257. PMID 180255CrossRefGoogle Scholar
  23. 23.
    Milner-Brown, H.S. and Brown, W.F. New methods of estimating the number of motor units in a muscle, J. Neurol., Neurosurg. Psychiatry, 1976, vol. 39, no. 3, pp. 258–265. PMID 932740CrossRefGoogle Scholar
  24. 24.
    Kadrie, H.A., Yates, S.K., Milner-Brown, H.S., and Brown, W.F., Multiple point electrical stimulation of ulnar and median nerves, J. Neurol., Neurosurg. Psychiatry, 1976, vol. 39, no. 10, pp. 973–985. PMID 1003242CrossRefGoogle Scholar
  25. 25.
    Carleton, S.A. and Brown, W.F., Changes in motor unit populations in motor neuron disease, J. Neurol., Neurosurg. Psychiatry, 1979, vol. 42, pp. 42–51. PMID 216781CrossRefGoogle Scholar
  26. 26.
    Lomen-Hoerth, C. and Olney, R.K., Comparison of multiple point and statistical motor unit number estimation, Muscle Nerve, 2000, vol. 23, no. 10, pp. 1525–1533. PMID 11003787. doi 10.1002/1097-4598(200010)23:10<1525::AID-MUS8>3.0.CO;2-ECrossRefGoogle Scholar
  27. 27.
    Wang, F.C. and Delwaide, P.J., Number and relative size of thenar motor units estimated by an adapted multiple point stimulation method, Muscle Nerve, 1995, vol. 18, no. 9, pp. 969–979. PMID 7643877. doi 10.1002/mus.880180908CrossRefGoogle Scholar
  28. 28.
    Wang, F.C., Bouquiaux, O., De Pasqua, V., and Delwaide, P.J., Changes in motor unit numbers in patients with ALS: a longitudinal study using the adapted multiple point stimulation method, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2002, vol. 3, no. 1, pp. 31–8. PMID 12061946. doi 10.1080/ 146608202317576516CrossRefGoogle Scholar
  29. 29.
    Albrecht, E. and Kuntzer, T., Number of Edb motor units estimated using an adapted multiple point stimulation method: normal values and longitudinal studies in ALS and peripheral neuropathies, Clin. Neurophysiol., 2004, vol. 115, no. 3, pp. 557–563. PMID 15036050. doi 10.1016/j.clinph.2003.11.001CrossRefGoogle Scholar
  30. 30.
    Shefner, J.M., Watson, M.L., Simionescu, L., et al., Multipoint incremental motor unit number estimation as an outcome measure in ALS, Neurology, 2011, vol. 77, no. 3, pp. 235–241. PMID 21676915. doi 10.1212/WNL.0b013e318225aabfCrossRefGoogle Scholar
  31. 31.
    Brown, W.F., Strong, M.J., and Snow, R., Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging, Muscle Nerve, 1988, vol. 11, no. 5, pp. 423–432. PMID 3374514. doi 10.1002/mus.880110503CrossRefGoogle Scholar
  32. 32.
    Boe, S., Stashuk, D., and Doherty, T., Motor unit number estimation by decomposition-enhanced spike-triggered averaging: control data, test–retest reliability, and contractile level effects, Muscle Nerve, 2004, vol. 29, pp. 693–699. PMID 15116373. doi 10.1002/ mus.20031CrossRefGoogle Scholar
  33. 33.
    Lawson, V.H., Bromberg, M.B., and Stashuk, D., Comparison of conventional and decomposition-enhanced spike triggered averaging techniques, Clin. Neurophysiol., 2004, vol. 115, pp. 564–568. PMID 15036051. doi 10.1016/j.clinph.2003.11.006CrossRefGoogle Scholar
  34. 34.
    Daube, J.R., Estimating the number of motor units in a muscle, J. Clin. Neurophysiol., 1995, vol. 12, no. 6, pp. 585–594. PMID 8600173CrossRefGoogle Scholar
  35. 35.
    Stashuk, D.W., Doherty, T.J., Kassam, A., and Brown, W.F., Motor unit number estimates based on the automated analysis of F-responses, Muscle Nerve, 1994, vol. 17, no. 8, pp. 881–890. PMID 8041395. doi 10.1002/mus.880170807CrossRefGoogle Scholar
  36. 36.
    Nandedkar, S.D., Nandedkar, D.S., Barkhaus, P.E., and Stålberg, E.V., Motor unit number index (MUNIX), IEEE Trans. Biomed. Eng., 2004, vol. 51, no. 12, pp. 2209–2211. PMID 15605872. doi 10.1109/TBME.2004.834281CrossRefGoogle Scholar
  37. 37.
    Nandedkar, S.D., Barkhaus, P.E., and Stålberg, E.V., Motor unit number index (MUNIX): principle, method, and findings in healthy subjects and in patients with motor neuron disease, Muscle Nerve, 2010, vol. 42, no. 5, pp. 798–807. PMID 20976783. doi 10.1002/ mus.21824CrossRefGoogle Scholar
  38. 38.
    Boekestein, W.A., Schelhaas, H.J., van Putten, M.J., et al., Motor unit number index (MUNIX) versus motor unit number estimation (MUNE): a direct comparison in a longitudinal study of ALS patients, Clin. Neurophysiol., 2012, vol. 123, no. 8, pp. 1644–1649. PMID 22321299. doi 10.1016/j.clinph.2012.01.004CrossRefGoogle Scholar
  39. 39.
    Neuwirth, C., Barkhaus, P.E., Burkhardt, C., et al., Tracking motor neuron loss in a set of six muscles in amyotrophic lateral sclerosis using the Motor Unit Number Index (MUNIX): a 15-month longitudinal multicentre trial, J. Neurol., Neurosurg. Psychiatry, 2015, vol. 86, no. 11, pp. 1172–1179. PMID 25935892. doi 10.1136/jnnp-2015-310509CrossRefGoogle Scholar
  40. 40.
    Fathi, D., Mohammadi, B., Dengler, R., et al., Lower motor neuron involvement in ALS assessed by motor unit number index (MUNIX): long-term changes and reproducibility, Clin. Neurophysiol., 2016, vol. 127, no. 4, pp. 1984–1988. PMID 26971480. doi 10.1016/ j.clinph.2015.12.023CrossRefGoogle Scholar
  41. 41.
    Vucic, S., Motor Unit Number Index (MUNIX): A novel biomarker for ALS? Clin. Neurophysiol., 2016, vol. 127, no. 4, pp. 1938–1939. PMID 26971474. doi 10.1016/j.clinph.2016.01.012CrossRefGoogle Scholar
  42. 42.
    Ahn, S.W., Kim, S.H., Kim, J.E., et al., Reproducibility of the motor unit number index (MUNIX) in normal controls and amyotrophic lateral sclerosis patients, Muscle Nerve, 2010, vol. 42, no. 5, pp. 808–813. PMID 20976784. doi 10.1002/mus.21765CrossRefGoogle Scholar
  43. 43.
    Nandedkar, S.D., Barkhaus, P.E., and Stålberg, E.V., Reproducibility of MUNIX in patients with amyotrophic lateral sclerosis, Muscle Nerve, 2011, vol. 44, no. 6, pp. 919–922. PMID 21953206. doi 10.1002/ mus.22204CrossRefGoogle Scholar
  44. 44.
    Neuwirth, C., Nandedkar, S., Stålberg, E., et al., Motor Unit Number Index (MUNIX): a novel neurophysiological marker for neuromuscular disorders; test-retest reliability in healthy volunteers, Clin. Neurophysiol., 2011, vol. 122, no. 9, pp. 1867–1872. PMID 21396884. doi 10.1016/j.clinph.2011.02.017CrossRefGoogle Scholar
  45. 45.
    Bostock, H., Estimating motor unit numbers from a CMAP scan, Muscle Nerve, 2016, vol. 53, no. 6, pp. 889–896. PMID 26479267. doi 10.1002/mus.24945CrossRefGoogle Scholar
  46. 46.
    Jacobsen, A.B., Bostock, H., Fuglsang-Frederik-sen, A., et al., Reproducibility, and sensitivity to motor unit loss in amyotrophic lateral sclerosis, of a novel MUNE method: MScanFit MUNE, Clin. Neurophysiol., 2017, vol. 128, no. 7, pp. 1380–1388. PMID 28461135. doi 10.1016/j.clinph.2017.03.045CrossRefGoogle Scholar
  47. 47.
    Campbell, M.J., McComas, A.J., and Petito, F., Physiological changes in ageing muscles, J. Neurol., Neurosurg. Psychiatry, 1973, vol. 36, no. 2, pp. 174–182. PMID 4708452CrossRefGoogle Scholar
  48. 48.
    Doherty, T.J. and Brown, W.F., The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults, Muscle Nerve, 1993, vol. 16, pp. 355–366. PMID 8455648. doi 10.1002/mus.880160404CrossRefGoogle Scholar
  49. 49.
    Galea, V., Changes in motor unit estimates with aging, J. Clin. Neurophysiol., 1996, vol. 13, pp. 253–260. PMID 8714347CrossRefGoogle Scholar
  50. 50.
    McNeil, C.J., Doherty, T.J., Stashuk, D.W., and Rice, C.L., Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men, Muscle Nerve, 2005, vol. 31, pp. 461–467. PMID 15685623. doi 10.1002/mus.20276CrossRefGoogle Scholar
  51. 51.
    Wang, F.C., de Pasqua, V., and Delwaide, P.J., Age-related changes in fastest and slowest conducting axons of thenar motor units, Muscle Nerve, 1999, vol. 22, no. 8, pp. 1022–1029. PMID 10417782. doi 10.1002/(SICI)1097-4598(199908)22:8<1022:AID-MUS3>3.0.CO;2-FCrossRefGoogle Scholar
  52. 52.
    Bromberg, M.B., Forshew, D.A., Nau, K.L., et al., Motor unit number estimation, isometric strength, and electromyographic measures in amyotrophic lateral sclerosis, Muscle Nerve, 1993, vol. 16, pp. 1213–1219. PMID 8413373. doi 10.1002/mus.880161111CrossRefGoogle Scholar
  53. 53.
    Gooch, C.L. and Harati, Y., Motor unit number estimation, ALS and clinical trials, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2000, vol. 1, no. 2, pp. 71–82. PMID 11467053CrossRefGoogle Scholar
  54. 54.
    Olney, R.K. and Lomen-Hoerth, C., Motor unit number estimation (MUNE): how may it contribute to the diagnosis of ALS? Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2000, vol. 1, suppl. 2, pp. S41–S44. PMID 11464940. doi 10.1080/146608200300079473CrossRefGoogle Scholar
  55. 55.
    Gooch, C.L. and Shefner, J.M., ALS surrogate markers. MUNE, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2004, vol. 5, suppl. 1, pp. 104–107. PMID 15512887. doi 10.1080/17434470410019889CrossRefGoogle Scholar
  56. 56.
    de Carvalho, M., Chio, A., Dengler, R., et al., Neurophysiological measures in amyotrophic lateral sclerosis: markers of progression in clinical trials, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2005, vol. 6, pp. 17–28. PMID 16036422. doi 10.1080/ 14660820410020600CrossRefGoogle Scholar
  57. 57.
    Sartucci, F., Maritato, P., Moscato, G., et al., Motor unit number estimation (MUNE) as a quantitative measure of disease progression and motor unit reorganization in amyotrophic lateral sclerosis, Int. J. Neurosci., 2007, vol. 117, pp. 1229–1236. PMID 17654089. doi 10.1080/14660820410020600CrossRefGoogle Scholar
  58. 58.
    Jagtap, S.A., Kuruvilla, A., Govind, P., et al., Multipoint incremental motor unit number estimation versus amyotrophic lateral sclerosis functional rating scale and the medical research council sum score as an outcome measure in amyotrophic lateral sclerosis, Ann. Indian Acad. Neurol., 2014, vol. 17, no. 3, pp. 336–339. PMID 25221407. doi 10.4103/0972-2327.138522CrossRefGoogle Scholar
  59. 59.
    Kim, D.G., Hong, Y.H., Shin, J.Y., et al., Split-hand phenomenon in amyotrophic lateral sclerosis: A motor unit number index study, Muscle Nerve, 2016, vol. 53, no. 6, pp. 885–888. PMID 26509758. doi 10.1002/mus.24958CrossRefGoogle Scholar
  60. 60.
    Benatar, M. and Wuu, J., Presymptomatic studies in ALS: rationale, challenges, and approach, Neurology, 2012, vol. 79, pp. 1732–1739. PMID 23071166. doi 10.1212/WNL.0b013e31826e9b1dCrossRefGoogle Scholar
  61. 61.
    Swash, M. and Ingram, D., Preclinical and subclinical events in motor neuron disease, J. Neurol., Neurosurg. Psychiatry, 1988, vol. 51, pp. 165–168. PMID 3346681CrossRefGoogle Scholar
  62. 62.
    Bromberg, M.B. and Brownell, A.A., Motor unit number estimation in the assessment of performance and function in motor neuron disease, Phys. Med. Rehabil. Clin. North Am., 2008, vol. 19, no. 3, pp. 509–532. PMID 18625413. doi 10.1016/j.pmr.2008.02.006CrossRefGoogle Scholar
  63. 63.
    de Carvalho, M., Turkman, A., and Swash, M., Sensitivity of MUP parameters in detecting change in early ALS, Clin. Neurophysiol., 2014, vol. 125, pp. 166–169. PMID 23845892. doi 10.1016/j.clinph.2013.06.014CrossRefGoogle Scholar
  64. 64.
    Aggarwal, A. and Nicholson, G., Detection of preclinical motor neuron loss in SOD1 mutation carriers using motor unit number estimation, J. Neurol., Neurosurg. Psychiatry, 2002, vol. 73, pp. 199–201. PMID 12122184CrossRefGoogle Scholar
  65. 65.
    Neuwirth, C., Barkhaus, P.E., Burkhardt, C., et al., Motor Unit Number Index (MUNIX) detects motor neuron loss in pre-symptomatic muscles in amyotrophic lateral sclerosis, Clin. Neurophysiol., 2017, vol. 128, no. 3, pp. 495–500. PMID 28043769. doi 10.1016/j.clinph.2016.11.026CrossRefGoogle Scholar
  66. 66.
    Neuwirth, C., Nandedkar, S., Stålberg, E., and Weber, M., Motor unit number index (MUNIX): a novel neurophysiological technique to follow disease progression in amyotrophic lateral sclerosis, Muscle Nerve, 2010, vol. 42, no. 3, pp. 379–384. PMID 20589888. doi 10.1002/mus.21707CrossRefGoogle Scholar
  67. 67.
    Zhou, P., Nandedkar, S.D., and Barkhaus, P.E., Voluntary contraction direction dependence of motor unit number index in patients with amyotrophic lateral sclerosis, IEEE Trans. Neural. Syst. Rehabil. Eng., 2014, vol. 22, no. 5, pp. 992–996. PMID 24710834. doi 10.1109/TNSRE.2014.2314391CrossRefGoogle Scholar
  68. 68.
    Escorcio-Bezerra, M.L., Abrahao, A., de Castro, I., et al., MUNIX: reproducibility and clinical correlations in amyotrophic lateral sclerosis, Clin. Neurophysiol., 2016, vol. 127, no. 9, pp. 2979–2984. PMID 27458836. doi 10.1016/j.clinph.2016.06.011CrossRefGoogle Scholar
  69. 69.
    Fukada, K., Matsui, T., Furuta, M., et al., The motor unit number index of subclinical abnormality in amyotrophic lateral sclerosis, J. Clin. Neurophysiol., 2016, vol. 33, no. 6, pp. 564–568. PMID 27295331. doi 10.1097/WNP.0000000000000296CrossRefGoogle Scholar
  70. 70.
    Gawel, M. and Kuzma-Kozakiewicz, M., Does the MUNIX method reflect clinical dysfunction in amyotrophic lateral sclerosis: a practical experience, Medicine (Baltimore), 2016, vol. 95, no. 19, p. e3647. PMID 27175687. doi 10.1097/MD.0000000000003647CrossRefGoogle Scholar
  71. 71.
    Neuwirth, C., Burkhardt, C., and Weber, M., Motor unit number index in the nasalis muscle in healthy subjects and patients with amyotrophic lateral sclerosis, Muscle Nerve, 2016, vol. 54, no. 4, pp. 733–737. PMID 26970219. doi 10.1002/mus.25100CrossRefGoogle Scholar
  72. 72.
    Bromberg, M.B. and Swoboda, K.J., Motor unit number estimation in infants and children with spinal muscular atrophy, Muscle Nerve, 2002, vol. 25, no. 3, pp. 445–447. PMID 11870724. doi 10.1002/mus.10050CrossRefGoogle Scholar
  73. 73.
    Swoboda, K.J., Prior, T.W., Scott, C.B., et al., Natural history of denervation in SMA: relation to age, SMN2 copy number, and function, Ann. Neurol., 2005, vol. 57, no. 5, pp. 704–712. PMID 15852397. doi 10.1002/ ana.20473?CrossRefGoogle Scholar
  74. 74.
    Galea, V., Fehlings, D., Kirsch, S., and McComas, A., Depletion and sizes of motor units by spinal muscular atrophy, Muscle Nerve, 2001, vol. 24, pp. 1168–1172. PMID 11494269. doi 10.1002/mus.1128CrossRefGoogle Scholar
  75. 75.
    Rhodes, L.E., Freeman, B.K., Auh, S., et al., Clinical features of spinal and bulbar muscular atrophy, Brain, 2009, vol. 132, no. 12, pp. 3242–3251. PMID 19846582. doi 10.1093/brain/awp258CrossRefGoogle Scholar
  76. 76.
    Lehky, T.J., Chen, C.J., di Prospero, N.A., et al., Standard and modified statistical MUNE evaluations in spinal-bulbar muscular atrophy, Muscle Nerve, 2009, vol. 40, pp. 809–814. PMID 19670325. doi 10.1002/mus.21399CrossRefGoogle Scholar
  77. 77.
    Lawson, V.H., Gordon Smith, A., and Bromberg, M.B., Assessment of axonal loss in Charcot-Marie-Tooth neuropathies, Exp. Neurol., 2003, vol. 184, no. 2, pp. 753–757. PMID 14769367. doi 10.1016/S0014-4886(03)00293-0CrossRefGoogle Scholar
  78. 78.
    Paramanathan, S., Tankisi, H., Andersen, H., and Fuglsang-Frederiksen, A., Axonal loss in patients with inflammatory demyelinating polyneuropathy as determined by motor unit number estimation and MUNIX, Clin. Neurophysiol., 2016, vol. 127, no. 1, pp. 898–904. PMID 26049677. doi 10.1016/j.clinph.2015.05.004CrossRefGoogle Scholar
  79. 79.
    Otto, M., Markvardsen, L., Tankisi, H., et al., The electrophysiological response to immunoglobulin therapy in chronic inflammatory demyelinating polyneuropathy, Acta Neurol. Scand., 2017, vol. 135, no. 6, pp. 656–662. PMID 27546708. doi 10.1111/ane.12663CrossRefGoogle Scholar
  80. 80.
    Kuwabara, S., Ogawara, K., Mizobuchi, K., et al., Mechanisms of early and late recovery in acute motor axonal neuropathy, Muscle Nerve, 2001, vol. 24, pp. 288–291. PMID 11180213. doi 10.1002/1097-4598(200102)24:2<288::AID-MUS150>3.0.CO;2-HCrossRefGoogle Scholar
  81. 81.
    Bromberg, M.B., Swoboda, K.J., and Lawson, V.H., Counting motor units in chronic motor neuropathies, Exp. Neurol., 2003, vol. 184, suppl. 1, pp. S53–S57. PMID 14597327CrossRefGoogle Scholar
  82. 82.
    Lewis, R., Li, J., Fuerst, D., et al., Motor unit number estimate of distal and proximal muscles in Charcot–Marie–Tooth disease, Muscle Nerve, 2003, vol. 28, pp. 161–167. PMID 12872319. doi 10.1002/mus.10419CrossRefGoogle Scholar
  83. 83.
    Videler, A.J., van Dijk, J.P., Beelen, A., et al., Motor axon loss is associated with hand dysfunction in Charcot–Marie–Tooth disease 1a, Neurology, 2008, vol. 71, pp. 1254–1260. PMID 18852440. doi 10.1212/ 01.wnl.0000327643.05073.ebCrossRefGoogle Scholar
  84. 84.
    Allen, M.D., Choi, I.H., Kimpinski, K., Doherty, T.J., and Rice, C.L., Motor unit loss and weakness in association with diabetic neuropathy in humans, Muscle Nerve, 2013, vol. 48, no. 2, pp. 298–300. PMID 23629918. doi 10.1002/mus.23792CrossRefGoogle Scholar
  85. 85.
    Koç, F., Yerdelen, D., Sarica, Y., and Sertdemir, Y., Motor unit number estimation in cases with Carpal Tunnel Syndrome, Int. J. Neurosci., 2006, vol. 116, pp. 1263–1270. PMID 17000528. doi 10.1080/ 00207450500516479CrossRefGoogle Scholar
  86. 86.
    Sohn, M.K., Jee, S.J., Hwang, S.L., et al., Motor unit number estimation and motor unit action potential analysis in carpal tunnel syndrome, Ann. Rehabil. Med., 2011, vol. 35, no. 6, pp. 816–825. PMID 22506210. doi 10.5535/arm.2011.35.6.816CrossRefGoogle Scholar
  87. 87.
    Bayrak, I.K., Bayrak, A.O., Tilki, H.E., et al., Ultrasonography in carpal tunnel syndrome: comparison with electrophysiological stage and motor unit number estimate, Muscle Nerve, 2007, vol. 35, pp. 344–348. PMID 17143879. doi 10.1002/mus.20698CrossRefGoogle Scholar
  88. 88.
    Trojaborg, W., Kaufmann, P., and Gooch, C., Motor unit estimate number in the anterior tibial muscle: normative data versus findings in critically ill patients in intensive care units, J. Clin. Neuromuscular Dis., 2002, vol. 3, pp. 139–142. PMID 19078670. doi 10.1097/ 00131402-200206000-00001CrossRefGoogle Scholar
  89. 89.
    Arasaki, K., Igarashi, O., Ichikawa, Y., et al., Reduction in the motor unit number estimate (MUNE) after cerebral infarction, J. Neurol. Sci., 2006, vol. 250, pp. 27–32. PMID 16904126. doi 10.1016/j.jns. 2006.06.024CrossRefGoogle Scholar
  90. 90.
    Daube, J.R., Motor unit number estimates: A Holy Grail? Clin. Neurophysiol., 2007, vol. 118, no. 12, pp. 2542–2543. PMID 17910936. doi 10.1016/ j.clinph.2007.08.007CrossRefGoogle Scholar
  91. 91.
    Swash, M., MUNIX in the clinic in ALS: MUNE comes of age, Clin. Neurophysiol., 2017, vol. 128, no. 3, pp. 482–483. PMID 28130059. doi 10.1016/ j.clinph.2016.12.021CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • A. F. Murtazina
    • 1
    Email author
  • A. I. Belyakova-Bodina
    • 2
  • A. G. Brutyan
    • 2
  1. 1.Federal Medical and Biophysical Center n.a. A.I. Burnazyan of the Federal Medical and Biological Agency of the Russian FederationMoscowRussia
  2. 2.Research Center of NeurologyMoscowRussia

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