Electrophysiological methods for estimation of the number of motor units

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Abstract

Various neurological diseases involving motor neurons or their axons lead to decrease in the number of functioning motor units (MU). Counting the number of intact MUs plays significant role in assessing the progression of the pathological process associated with motor neuron death. Quantitative estimation of MUs using routine electromyography methods is usually impossible. Therefore, electrophysiological methods for estimation of the number of MUs, currently known under the common name MUNE (motor unit number estimation), are being discovered over the past decades. The first publication on MUNE was issued in 1971. Since that time, promising, more accurate, and less time-consuming modifications have been developed, and new MU counting methods have been proposed. In recent years, we can see increasing interest in MUNE in connection with the search for new treatments for motor neuron disease, assessment of their effectiveness, and dynamic control of the disease. Today, MUNE is considered as a potential biomarker in clinical trials of new treatments for motor neuron disease. This review presents the available MUNE techniques, describes their comparative characteristics, advantages and disadvantages of each method, and discusses the experience and prospects of their application.

About the authors

Aysylu F. Murtazina

Federal Medical and Biophysical Center n.a. A.I. Burnazyan of the Federal Medical and Biological Agency of the Russian Federation

Author for correspondence.
Email: aysylumurtazina@gmail.com
Russian Federation, Moscow

Aleksandra I. Belyakova-Bodina

Federal Medical and Biophysical Center n.a. A.I. Burnazyan of the Federal Medical and Biological Agency of the Russian Federation

Email: aysylumurtazina@gmail.com
Russian Federation, Moscow

Amayak G. Brutyan

Federal Medical and Biophysical Center n.a. A.I. Burnazyan of the Federal Medical and Biological Agency of the Russian Federation

Email: aysylumurtazina@gmail.com
Russian Federation, Moscow

References

  1. Gooch C.L., Doherty T.J., Chan K.M. et. al. Motor unit number estimation: a technology and literature review. Muscle & Nerve. 2014; 50(6): 884-93. PMID: 25186553 doi: 10.1002/mus.24442.
  2. McComas A.J. Motor unit estimation: anxieties and achievements. Muscle & Nerve. 1995; 18(4):369-79. doi: 10.1002/mus.880180402. PMID: 7715621.
  3. Aoyagi Y., Strohschein F.J., Ming Chan K. Use of the collision technique to improve the accuracy of motor unit number estimation. Clinical Neurophysiology. 2000; 111(7): 1315-9. doi: 10.1016/S1388-2457(00)00318-7. PMID: 10880808
  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; 11(9): 957-8
  5. Yang J.F., Stein R.B., Jhamandas J., Gordon T. Motor unit numbers and contractile properties after spinal cord injury. Annals of Neurology. 1990; 28(4): 496–502. doi: 10.1002/ana.410280405. PMID: 2252362.
  6. Bromberg M. Motor unit estimation: reproducibility of the spike-triggered averaging technique in normal and ALS subjects. Muscle & Nerve 1993; 16(5): 466–71. doi: 10.1002/mus.880160506. PMID: 8515754.
  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; 18(12): 1412-6. doi: 10.1002/mus.880181211. PMID: 7477064.
  8. Bromberg M.B., Larson W.L. Relationships between motor-unit number estimates and isometric strength in distal muscles in ALS/MND. J Neurol Sci 1996; 139(suppl): 38–42. PMID: 8899656
  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; 20: 179–85. doi: 10.1002/(SICI)1097-4598(199702)20:2<179::AID-MUS7>3.0.CO;2-9 PMID: 9040656
  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; 21: 756–761. doi: 10.1002/(SICI)1097-4598(199806)21:6<756::AID-MUS7>3.0.CO;2-6. PMID: 9585329
  11. Wang F.C., 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; 109(1): 36-43. doi: 10.1016/S0924-980X(97)00071-4. PMID: 11003062
  12. Armon C, Brandstater ME. Motor unit number estimate-based rates of progression of ALS predict patient survival. Muscle & Nerve 1999; 22: 1571–1575. doi: 10.1002/(SICI)1097-4598(199911)22:11<1571::AID-MUS13>3.0.CO;2-0. PMID: 10514236
  13. Kuwabara S., Mizobuchi K., Ogawara K., Hattori T. Dissociated small hand muscle involvement in amyotrophic lateral sclerosis detected by motor unit number estimates. Muscle & Nerve 1999; 22: 870–873. doi: 10.1002/(SICI)1097-4598(199907)22:7<870::AID-MUS9>3.0.CO;2-O PMID: 10398204
  14. Cuturic M., Palliyath S. Motor unit number estimate (MUNE) testing in male patients with mild to moderate carpal tunnel syndrome. Electroencephalography and Clinical Neurophysiology. 2000; 40:67–72. PMID: 10746180.
  15. Hara Y., Akaboshi K., Masakado Y., Chino N. Physiologic decrease of single thenar motor units in the F-response in stroke patients. Archives of Physical Medicine and Rehabilitation. 2000; 81:418–423. doi: 10.1053/mr.2000.3872. PMID: 10768529.
  16. McComas A.J., Fawcett P.R., Campbell M.J., Sica R.E. Electrophysiological estimation of the number of motor units within a human muscle. Journal of Neurology, Neurosurgery, and Psychiatry. 1971; 34(2):121-31. doi: 10.1136/jnnp.34.2.121. PMID: 5571599.
  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; 35(6): 845-52. PMID: 4647858
  18. Brown W.F. Thenar motor unit count estimates in the carpal tunnel syndrome. J Neurol Neurosurg Psychiatry. 1973; 36(2): 194-8. PMID: 4708453
  19. Ballantyne J.P., 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 ; 37(8): 907-15. PMID: 4425377
  20. Panayiotopoulos C.P., Scarpalezos S., Papapetropoulos T. Electrophysiological estimation of motor units in Duchenne muscular dystrophy. J Neurol Sci. 1974; 23(1): 89-98. doi: 10.1016/0022-510X(74)90145-2 PMID: 4851827
  21. Sica R.E., McComas A.J., Upton A.R., Longmire D. Motor unit estimations in small muscles of the hand. J Neurol Neurosurg Psychiatry 1974; 37: 55–67. PMID: 4360400
  22. Brown W.F., 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; 39: 249–257. PMID: 180255
  23. Milner-Brown H.S., Brown W.F. New methods of estimating the number of motor units in a muscle. J Neurol Neurosurg Psychiatry. 1976; 39(3): 258-65. PMID: 932740
  24. Kadrie H.A., Yates S.K., Milner-Brown H.S., Brown WF. Multiple point electrical stimulation of ulnar and median nerves. J Neurol Neurosurg Psychiatry. 1976; 39(10): 973-85. PMID: 1003242
  25. Carleton S.A., Brown W.F. Changes in motor unit populations in motor neurone disease. J Neurol Neurosurg Psychiatry 1979; 42: 42–51. PMID: 216781
  26. Lomen-Hoerth C., Olney R.K. Comparison of multiple point and statistical motor unit number estimation. Muscle & Nerve. 2000; 23(10):1525-33. doi: 10.1002/1097-4598(200010)23:10<1525::AID-MUS8>3.0.CO;2-E. PMID: 11003787.
  27. Wang F.C., Delwaide P.J. Number and relative size of thenar motor units estimated by an adapted multiple point stimulation method. Muscle & Nerve. 1995; 18(9):969-79. doi: 10.1002/mus.880180908. PMID: 7643877.
  28. Wang F.C., Bouquiaux O., De Pasqua V., Delwaide P.J. Changes in motor unit numbers in patients with ALS: a longitudinal study using the adapted multiple point stimulation method. Amyotroph Lateral Scler Other Motor Neuron Disord. 2002; 3(1):31-8. doi: 10.1080/146608202317576516. PMID: 12061946.
  29. Albrecht E., 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. Clinical Neurophysiology. 2004; 115(3):557-63. doi: 10.1016/j.clinph.2003.11.001. PMID: 15036050.
  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; 77(3):235-41. doi: 10.1212/WNL.0b013e318225aabf. PMID: 21676915.
  31. Brown W.F., Strong M.J., Snow R. Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging. Muscle & Nerve. 1988; 11(5):423-32. doi: 10.1002/mus.880110503. PMID: 3374514.
  32. Boe S., Stashuk D., Doherty T. Motor unit number estimation by decomposition-enhanced spike-triggered averaging: control data, test–retest reliability, and contractile level effects. Muscle & Nerve. 2004; 29:693–9. doi: 10.1002/mus.20031. PMID: 15116373.
  33. Lawson V.H., Bromberg M.B., Stashuk D. Comparison of conventional and decomposition-enhanced spike triggered averaging techniques. Clinical Neurophysiology 2004; 115:564–568. doi: 10.1016/j.clinph.2003.11.006. PMID: 15036051.
  34. Daube J.R. Estimating the number of motor units in a muscle. J Clinical Neurophysiology. 1995; 12(6): 585-94. PMID: 8600173
  35. Stashuk D.W., Doherty T.J., Kassam A., Brown W.F. Motor unit number estimates based on the automated analysis of F-responses. Muscle & Nerve. 1994; 17(8):881-90. doi: 10.1002/mus.880170807. PMID: 8041395.
  36. Nandedkar S.D., Nandedkar D.S., Barkhaus P.E., Stalberg E.V. Motor unit number index (MUNIX). IEEE Trans Biomed Eng. 2004 ; 51(12): 2209-11. doi: 10.1109/TBME.2004.834281. PMID: 15605872.
  37. Nandedkar S.D., Barkhaus P.E., 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; 42(5):798-807. doi: 10.1002/mus.21824. PMID: 20976783.
  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. Clinical Neurophysiology. 2012; 123(8): 1644-9. doi: 10.1016/j.clinph.2012.01.004. PMID: 22321299.
  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. Journal of Neurology, Neurosurgery, and Psychiatry. 2015; 86(11): 1172-9. doi: 10.1136/jnnp-2015-310509. PMID: 25935892.
  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. Clinical Neurophysiology. 2016; 127(4): 1984-8. doi: 10.1016/j.clinph.2015.12.023. PMID: 26971480.
  41. Vucic S. Motor Unit Number Index (MUNIX): A novel biomarker for ALS? Clinical Neurophysiology. 2016; 127(4): 1938-9. doi: 10.1016/j.clinph.2016.01.012. PMID: 26971474.
  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; 42(5): 808-13. doi: 10.1002/mus.21765. PMID: 20976784.
  43. Nandedkar S.D., Barkhaus P.E., Stålberg E.V. Reproducibility of MUNIX in patients with amyotrophic lateral sclerosis. Muscle & Nerve. 2011; 44(6): 919-22. doi: 10.1002/mus.22204. PMID: 21953206.
  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. Clinical Neurophysiology. 2011; 122(9): 1867-72. doi: 10.1016/j.clinph.2011.02.017. PMID: 21396884.
  45. Bostock H. Estimating motor unit numbers from a CMAP scan. Muscle & Nerve. 2016; 53(6):889-96. doi: 10.1002/mus.24945. PMID: 26479267.
  46. Jacobsen A.B., Bostock H., Fuglsang-Frederiksen A. et al. Reproducibility, and sensitivity to motor unit loss in amyotrophic lateral sclerosis, of a novel MUNE method: MScanFit MUNE. Clinical Neurophysiology. 2017; pii: S1388-2457(17)30143-8. doi: 10.1016/j.clinph.2017.03.045. PMID: 28461135.
  47. Campbell M.J., McComas A.J., Petito F. Physiological changes in ageing muscles. Journal of Neurology, Neurosurgery, and Psychiatry. 1973; 36(2):174-82. PMID: 4708452.
  48. Doherty T.J., 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; 16:355–366. doi: 10.1002/mus.880160404. PMID: 8455648.
  49. Galea V. Changes in motor unit estimates with aging. J Clin Neurophysiol 1996; 13: 253–260. PMID: 8714347
  50. McNeil C.J., Doherty T.J., Stashuk D.W., Rice C.L. Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle & Nerve. 2005; 31:461–467. doi: 10.1002/mus.20276. PMID: 15685623.
  51. Wang F.C., de Pasqua V., Delwaide P.J. Age-related changes in fastest and slowest conducting axons of thenar motor units. Muscle & Nerve. 1999; 22(8):1022-9. doi: 10.1002/(SICI)1097-4598(199908)22:8<1022::AID-MUS3>3.0.CO;2-F. PMID: 10417782.
  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; 16:1213–1219. doi: 10.1002/mus.880161111. PMID: 8413373.
  53. Gooch C.L., Harati Y. Motor unit number estimation, ALS and clinical trials. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000 ;1(2): 71-82. PMID: 11467053
  54. Olney R.K., Lomen-Hoerth C. Motor unit number estimation (MUNE): how may it contribute to the diagnosis of ALS? Amyotroph Lateral Scler Other Motor Neuron Disord. 2000; 1 Suppl 2:S41-4. Review. doi: 10.1080/146608200300079473. PMID: 11464940.
  55. Gooch C.L., Shefner J.M. ALS surrogate markers. MUNE. Amyotroph Lateral Scler Other Motor Neuron Disord. 2004; 5 Suppl 1: 104-7. doi: 10.1080/17434470410019889. PMID: 15512887.
  56. de Carvalho M., Chio A., Dengler R. et al. Neurophysiological measures in amyotrophic lateral sclerosis: markers of progression in clinical trials. Amyotroph Lateral Scler Other Motor Neuron Disord. 2005; 6: 17–28. doi: 10.1080/14660820410020600. PMID: 16036422.
  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; 117:1229–1236. doi: 10.1080/14660820410020600. PMID: 17654089.
  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; 17(3): 336-9. doi: 10.4103/0972-2327.138522. PMID: 25221407.
  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; 53(6): 885-8. doi: 10.1002/mus.24958. PMID: 26509758.
  60. Benatar M., Wuu J. Presymptomatic studies in ALS: rationale, challenges, and approach. Neurology. 2012; 79: 1732–9. doi: 10.1212/WNL.0b013e31826e9b1d. PMID: 23071166.
  61. Swash M., Ingram D. Preclinical and subclinical events in motor neuron disease. J Neurol Neurosurg Psychiatry 1988;51: 165–8. PMID: 3346681
  62. Bromberg M.B., Brownell A.A. Motor unit number estimation in the assessment of performance and function in motor neuron disease. Phys Med Rehabil Clin N Am. 2008; 19(3): 509-32. doi: 10.1016/j.pmr.2008.02.006. PMID: 18625413.
  63. de Carvalho M., Turkman A., Swash M. Sensitivity of MUP parameters in detecting change in early ALS. Clinical Neurophysiology. 2014; 125: 166–9. doi: 10.1016/j.clinph.2013.06.014. PMID: 23845892.
  64. Aggarwal A., Nicholson G. Detection of preclinical motor neurone loss in SOD1 mutation carriers using motor unit number estimation. J Neurol Neurosurg Psychiatry 2002; 73: 199–201. PMID: 12122184
  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. Clinical Neurophysiology. 2017; 128(3): 495-500. doi: 10.1016/j.clinph.2016.11.026. PMID: 28043769.
  66. Neuwirth C., Nandedkar S., Stålberg E., Weber M. Motor unit number index (MUNIX): a novel neurophysiological technique to follow disease progression in amyotrophic lateral sclerosis. Muscle & Nerve. 2010; 42(3): 379-84. doi: 10.1002/mus.21707. PMID: 20589888.
  67. Zhou P., Nandedkar S.D., 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; 22(5): 992-6. doi: 10.1109/TNSRE.2014.2314391. PMID: 24710834.
  68. Escorcio-Bezerra M.L., Abrahao A., de Castro I., et al. MUNIX: Reproducibility and clinical correlations in Amyotrophic Lateral Sclerosis. Clinical Neurophysiology. 2016; 127(9): 2979-84. doi: 10.1016/j.clinph.2016.06.011. PMID: 27458836.
  69. Fukada K., Matsui T., Furuta M., et al. The Motor Unit Number Index of Subclinical Abnormality in Amyotrophic Lateral Sclerosis. J Clinical Neurophysiology. 2016; 33(6): 564-568. doi: 10.1097/WNP.0000000000000296. PMID: 27295331.
  70. Gawel M., Kuzma-Kozakiewicz M. Does the MUNIX Method Reflect Clinical Dysfunction in Amyotrophic Lateral Sclerosis: A Practical Experience. Medicine (Baltimore). 2016; 95(19): e3647. doi: 10.1097/MD.0000000000003647. PMID: 27175687.
  71. Neuwirth C., Burkhardt C., Weber M. Motor unit number index in the nasalis muscle in healthy subjects and patients with amyotrophic lateral sclerosis. Muscle & Nerve. 2016; 54(4): 733-7. doi: 10.1002/mus.25100. PMID: 26970219.
  72. Bromberg M.B., Swoboda K.J. Motor unit number estimation in infants and children with spinal muscular atrophy. Muscle & Nerve. 2002; 25(3): 445-7. doi: 10.1002/mus.10050. PMID: 11870724.
  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. Annals of Neurology. 2005; 57(5): 704-12. doi: 10.1002/ana.20473.? PMID: 15852397.
  74. Galea V., Fehlings D., Kirsch S., McComas A. Depletion and sizes of motor units by spinal muscular atrophy. Muscle & Nerve 2001; 24: 1168–72. doi: 10.1002/mus.1128. PMID: 11494269.
  75. Rhodes L.E., Freeman B.K., Auh S., et al. Clinical features of spinal and bulbar muscular atrophy. Brain. 2009; 132(12):3242-3251. doi: 10.1093/brain/awp258. PMID: 19846582.
  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; 40: 809–814. doi: 10.1002/mus.21399. PMID: 19670325.
  77. Lawson V.H., Gordon Smith A., Bromberg M.B. Assessment of axonal loss in Charcot-Marie-Tooth neuropathies. Exp Neurol. 2003; 184(2): 753-7. doi: 10.1016/S0014-4886(03)00293-0. PMID: 14769367.
  78. Paramanathan S., Tankisi H., Andersen H., Fuglsang-Frederiksen A. Axonal loss in patients with inflammatory demyelinating polyneuropathy as determined by motor unit number estimation and MUNIX. Clinical Neurophysiology. 2016; 127(1): 898-904. doi: 10.1016/j.clinph.2015.05.004. PMID: 26049677.
  79. Otto M., Markvardsen L., Tankisi H., Jakobsen J., Fuglsang-Frederiksen A. The electrophysiological response to immunoglobulin therapy in chronic inflammatory demyelinating polyneuropathy. Acta Neurol Scand. 2017; 135(6): 656-662. doi: 10.1111/ane.12663. PMID: 27546708.
  80. Kuwabara S., Ogawara K., Mizobuchi K. et al. Mechanisms of early and late recovery in acute motor axonal neuropathy. Muscle & Nerve. 2001; 24: 288–291. doi: 10.1002/1097-4598(200102)24:2<288::AID-MUS150>3.0.CO;2-H. PMID: 11180213.
  81. Bromberg M.B., Swoboda K.J., Lawson V.H. Counting motor units in chronic motor neuropathies. Exp Neurol. 2003; 184 Suppl 1: S53-7. PMID: 14597327.
  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; 28: 161–7. doi: 10.1002/mus.10419. PMID: 12872319.
  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; 71: 1254–1260. doi: 10.1212/01.wnl.0000327643.05073.eb. PMID: 18852440.
  84. Allen M.D., Choi I.H., Kimpinski K., Doherty TJ, Rice CL. Motor unit loss and weakness in association with diabetic neuropathy in humans. Muscle & Nerve. 2013; 48(2): 298-300. doi: 10.1002/mus.23792. PMID: 23629918.
  85. Koc F., Yerdelen D., Sarica Y., Sertdemir Y. Motor unit number estimation in cases with Carpal Tunnel Syndrome. Int J Neurosci 2006; 116: 1263–1270. doi: 10.1080/00207450500516479. PMID: 17000528.
  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; 35(6): 816-25. doi: 10.5535/arm.2011.35.6.816. PMID: 22506210.
  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; 35: 344–348. doi: 10.1002/mus.20698. PMID: 17143879.
  88. Trojaborg W., Kaufmann P., 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 Neuromusc Dis 2002; 3: 139–42. doi: 10.1097/00131402-200206000-00001. PMID: 19078670.
  89. Arasaki K., Igarashi O., Ichikawa Y., et al. Reduction in the motor unit number estimate (MUNE) after cerebral infarction. Journal of the Neurological Sciences. 2006; 250: 27–32. doi: 10.1016/j.jns.2006.06.024. PMID: 16904126.
  90. Daube J.R. Motor unit number estimates: A Holy Grail? Clinical Neurophysiology. 2007; 118(12): 2542-3. doi: 10.1016/j.clinph.2007.08.007. PMID: 17910936.
  91. Swash M. MUNIX in the clinic in ALS: MUNE comes of age. Clinical Neurophysiology. 2017; 128(3): 482-483. doi: 10.1016/j.clinph.2016.12.021. PMID: 28130059.

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