Spectral EMG Changes in Cervical Dystonia Patients and the Influence of Botulinum Toxin Treatment
Abstract
:1. Introduction
2. Results
2.1. Study Population
2.2. Maximal Force and Torque during Maximal Voluntary Muscle Contractions (MVC) Tasks
2.3. Task Performance
2.4. Raw EMG Inspection
2.5. EMG Spectral Analysis: Pooled Autospectra
2.6. EMG Spectral Analysis: 8–14 Hz Area Under the Curve (AUC’s) in SPL Muscles
2.7. EMG Spectral Analysis: 8–14 Hz AUC’s in SCM and SESP Muscles
2.8. Effect of BoNT Treatment on the 8–14 Hz AUC’s
2.9. Effect of Age, Gender and Tremor
2.10. CDF10 Analysis
2.11. Effect of BoNT
2.12. Effect of Age, Gender and Tremor
2.13. Diagnostic Potential to Discriminate Dystonia Patients from Healthy Controls
2.13.1. 8–14 Hz AUC’s
2.13.2. CDF10’s
3. Discussion
3.1. 8–14 Hz Autospectral Peaks in Healthy Controls
3.2. Absence of 8–14 Hz Autospectral Peaks in Dystonia Patients
3.3. CDF10 Analysis
3.4. Effect of BoNT
3.5. Task Performance
3.6. Limitations
3.7. Future Perspectives and Potential Clinical Applications
4. Conclusions
5. Materials and Methods
5.1. Study Population
5.2. Clinical Examination
5.3. Apparatus
5.4. EMG Recordings
5.5. Isometric Contraction Experiments
5.6. Selection of Tasks and Muscles for Spectral Analysis
5.7. EMG Visual Inspection
5.8. EMG Pre-Processing
5.9. EMG Spectral Analysis
5.10. Potential of 8–14 Hz AUC’s and CDF10 to Discriminate Dystonia Patients from Healthy Controls
5.11. Statistical Analysis
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Albanese, A.; Bhatia, K.; Bressman, S.B.; Delong, M.R.; Fahn, S.; Fung, V.S.C.; Hallett, M.; Jankovic, J.; Jinnah, H.A.; Klein, C. Phenomenology and classification of dystonia: A consensus update. Mov. Disord. 2013, 28, 863–873. [Google Scholar] [CrossRef] [PubMed]
- Snaith, A.; Wade, D. Dystonia. BMJ Clin. Evid. 2008, pii: 1211. [Google Scholar]
- Pirazzini, M.; Rossetto, O.; Eleopra, R.; Montecucco, C. Botulinum Neurotoxins: Biology, Pharmacology, and Toxicology. Pharmacol. Rev. 2017, 69, 200–235. [Google Scholar] [CrossRef] [PubMed]
- Cordivari, C.; Misra, V.P.; Vincent, A.; Catania, S.; Bhatia, K.P.; Lees, A.J. Secondary nonresponsiveness to botulinum toxin A in cervical dystonia: The role of electromyogram-guided injections, botulinum toxin A antibody assay, and the extensor digitorum brevis test. Mov. Disord. 2006, 21, 1737–1741. [Google Scholar] [CrossRef] [PubMed]
- Jankovic, J. Treatment of cervical dystonia with botulinum toxin. Mov. Disord. 2004, 19 (Suppl. 8), S109–S115. [Google Scholar] [CrossRef] [PubMed]
- Nijmeijer, S.W.R.; Koelman, J.H.T.M.; Kamphuis, D.J.; Tijssen, M.A.J. Muscle selection for treatment of cervical dystonia with botulinum toxin—A systematic review. Parkinsonism Relat. Disord. 2012, 18, 731–736. [Google Scholar] [CrossRef] [PubMed]
- Nijmeijer, S.W.R.; de Bruijn, E.; Forbes, P.A.; Kamphuis, D.J.; Happee, R.; Koelman, J.H.T.M. EMG coherence and spectral analysis in cervical dystonia: Discriminative tools to identify dystonic muscles? J. Neurol. Sci. 2014, 347, 167–173. [Google Scholar] [CrossRef] [PubMed]
- De Bruijn, E.; Nijmeijer, S.W.R.; Forbes, P.A.; Koelman, J.H.T.M.; van der Helm, F.C.T.; Tijssen, M.A.J.; Happee, R. Improved identification of dystonic cervical muscles via abnormal muscle activity during isometric contractions. J. Neurol. Sci. 2015, 354, 10–16. [Google Scholar] [CrossRef] [PubMed]
- De Bruijn, E.; Nijmeijer, S.W.R.; Forbes, P.A.; Koelman, J.H.T.M.; van der Helm, F.C.T.; Tijssen, M.A.J.; Happee, R. Dystonic neck muscles show a shift in autospectral power during isometric contractions. Clin. Neurophysiol. 2017, 128, 1937–1945. [Google Scholar]
- Dressler, D.; Rothwell, J.C. Electromyographic quantification of the paralysing effect of botulinum toxin in the sternocleidomastoid muscle. Eur. Neurol. 2000, 43, 13–16. [Google Scholar] [CrossRef] [PubMed]
- Lange, F.; van Weerden, T.W.; van der Hoeven, J.H. Age-related botulinum toxin effects on muscle fiber conduction velocity in non-injected muscles. Clin. Neurophysiol. 2007, 118, 2398–2403. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.; McCall, W.D.; Kim, Y.K.; Chung, J.W. Effect of botulinum toxin on pressure pain threshold and EMG power spectrum of masseter muscle during sustained fatiguing contraction. Am. J. Phys. Med. Rehabil. 2010, 89, 736–743. [Google Scholar] [CrossRef] [PubMed]
- Chapman, M.A.; Barron, R.; Tanis, D.C.; Gill, C.E.; Charles, D. Comparison of botulinum neurotoxin preparations for the treatment of cervical dystonia. Clin. Ther. 2007, 29, 1325–1337. [Google Scholar] [CrossRef] [PubMed]
- Tijssen, M.A.J.; Marsden, J.F.; Brown, P. Frequency analysis of EMG activity in patients with idiopathic torticollis. Brain 2000, 123 Pt 4, 677–686. [Google Scholar] [CrossRef] [PubMed]
- Blouin, J.-S.; Siegmund, G.P.; Garpenter, M.G.; Inglis, T. Neural control of superficial and deep neck muscles in humans. J. Neurophysiol. 2007, 98, 920–928. [Google Scholar] [CrossRef] [PubMed]
- Grosse, P.; Brown, P. Acoustic startle evokes bilaterally synchronous oscillatory EMG activity in the healthy human. J. Neurophysiol. 2003, 90, 1654–1661. [Google Scholar] [CrossRef] [PubMed]
- Kilner, J.M.; Baker, S.N.; Salenius, S.; Hari, R.; Lemin, R.N. Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles. J. Physiol. 1999, 516 Pt 2, 559–570. [Google Scholar] [CrossRef] [PubMed]
- Grosse, P.; Edwads, M.; Tissen, M.A.J.; Schrag, A.; Lees, A.J.; Bhatia, K.P.; Brown, P. Patterns of EMG-EMG coherence in limb dystonia. Mov. Disord. 2004, 19, 758–769. [Google Scholar] [CrossRef] [PubMed]
- Tijssen, M.A.J.; Munchau, A.; Marsden, J.F.; Lees, A.; Bhatia, K.P.; Brown, P. Descending control of muscles in patients with cervical dystonia. Mov. Disord. 2002, 17, 493–500. [Google Scholar] [CrossRef] [PubMed]
- Roberts, T.J.; Gabaldon, A.M. Interpreting muscle function from EMG: Lessons learned from direct measurements of muscle force. Integr. Comp. Biol. 2008, 48, 312–320. [Google Scholar] [CrossRef] [PubMed]
- Artug, N.T.; Goker, I.; Bolat, B.; Osman, O.; Orhan, E.K.; Baslo, M.B. The effect of recording site on extracted features of motor unit action potential. Comput. Methods Programs Biomed. 2016, 129, 172–185. [Google Scholar] [CrossRef] [PubMed]
- Consky, E.S. Clinical assessments of patients with cervical dystonia. In Therapy with Botulinum Toxin; Jancovic, J., Hallett, M., Eds.; Marcel Dekker, Inc.: New York, NY, USA, 1994; pp. 211–237. [Google Scholar]
Pat. nr. | Sex 1 | Age | Dystonic Posturing | Tremor 5 | TWSTR | Duration Symptoms (years) | BoNT Dosage (MU) and Type 6 | ||
---|---|---|---|---|---|---|---|---|---|
Rotation 2,3 | Lateroflexion 2,3 | Antecollis/Retrocollis 3,4 | |||||||
01 | F | 51 | L3 | L2 | NP | 0 | 57.5 | 4 | 320 (D) |
02 | F | 72 | L1 | R1 | A1 | 1 | 36.75 | 36 | 190 (D) |
03 | M | 67 | L2 | R1 | NP | 2 | 21 | 14 | 810 (D) |
04 | F | 74 | R2 | R1 | NP | 1 | 14 | 4 | 240 (D) |
05 | F | 65 | R3 | R1 | NP | 0 | 37.5 | 4 | 220 (D) |
06 | M | 53 | L2 | R1 | NP | 1 | 20 | 20 | 410 (D) |
07 | F | 61 | R1 | R1 | NP | 1 | 23.5 | 13 | 150 (B) |
08 | M | 64 | L2 | L1 | NP | 0 | 26 | >40 | 540 (D) |
09 | F | 46 | R1 | R1 | NP | 1 | 35 | 4 | 240 (D) |
10 | F | 66 | L2 | R1 | A2 | 1 | 27 | 20 | 350 (D) |
11 | M | 73 | L2 | R1 | NP | 1 | 29 | 3 | 640 (D) |
12 | M | 64 | R3 | R1 | A2 | 2 | 28 | 21 | 350 (D) |
21 | M | 57 | L1 | L1 | A1 | 1 | 33 | 2 | N.A. |
22 | F | 44 | L1 | R1 | R1 | 1 | 16 | 20 | N.A. |
23 | F | 63 | L3 | R3 | R3 | 2 | 48 | 16 | N.A. |
24 | F | 56 | L1 | L1 | NP | 1 | 28 | 5 | N.A. |
Studied Subjects | Mean Maximal Horizontal (Rearward) Force (N) | Mean Maximal Left Rotational Torque (Nm) | Mean Maximal Right Rotational Torque (Nm) |
---|---|---|---|
Healthy controls | 129.18 N (SD: 62.43) | 6.25 Nm (SD: 3.40) | 6.59 Nm (SD: 3.7) |
BoNT-treated patients First measurement | 93.36 N (SD: 36.24, ns) | 4.04 Nm (SD: 2.40, ns) | 4.66 Nm (SD: 2.49, ns) |
BoNT-treated patients Second measurement | 102.63 N (SD: 34.55, ns) | 5.168 Nm (SD: 2.42, ns) | 5.03 Nm (SD: 2.65, ns) |
BoNT-naïve patients | 88.10 N (SD: 28.52, ns) | 4.92 Nn (SD: 1.77, ns) | 4.86 Nm (SD: 2.34, ns) |
8–14 Hz AUC’s | SPL Muscles in Healthy Controls | Ipsilateral (Presumed Dystonic) Splenius Capitis (SPL) Muscles | ||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median 8–14 Hz AUC | 8.151 (N = 8) | 4.81 (N = 11, p < 0.001 *) | 5.02 (N = 12, p < 0.01) | 7.07 (N = 4, ns) |
IQR | 6.63–11.29 | 3.39–5.91 | 3.84–6.99 | 5.66–9.91 |
Contralateral (Presumed Non-Dystonic) SPL Muscle | ||||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median 8–14 Hz AUC | 5.19 (N = 11, p < 0.05) | 7.07(N = 11, ns) | 9.19 (N = 4, ns) | |
IQR | 4.70–7.06 | 6.29–9.06 | 7.61–12.54 | |
SCM Muscles in Healthy Controls | Contralateral (Presumed Dystonic) SCM Muscles | |||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median 8–14 Hz AUC | 6.08 (N = 7) | 4.38 (N = 11, p < 0.05) | 4.58 (N = 9, ns) | 5.79 (N = 4, ns) |
IQR | 4.80–7.26 | 3.76–5.84 | 4.18–8.37 | 5.31–6.87 |
Ipsilateral (Presumed Non-Dystonic) SCM Muscles | ||||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median 8–14 Hz AUC | 6.65 (N = 10, ns) | 6.84 (N = 12, ns) | 5.32 (N = 4, ns) | |
IQR | 5.97–7.90 | 4.92–7.98 | 4.40–8.18 | |
SESP Muscles in All Subjects (Average between Left/Right Muscles) | ||||
Healthy Controls | BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | |
Median 8–14 Hz AUC | 6.86 (N = 8) | 5.97 (N = 11, ns) | 6.13 (N = 12, ns) | 8.97 (N = 4, ns) |
IQR | 6.50–8.31 | 4.89–7.45 | 5.11–7.34 | 6.37–10.82 |
CDF10 | SPL Muscles in Healthy Controls | Ipsilateral (Presumed Dystonic) SPL Muscles | ||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median CDF10 | 0.155 (N = 8) | 0.278 (N = 11, p < 0.01 *) | 0.280 (N = 12, p < 0.001) | 0.311 (N = 4 p < 0.01) |
IQR | 0.118–0.209 | 0.256–0.354 | 0.207–0.413 | 0.253–0.480 |
Contralateral (Presumed Non-Dystonic) SPL Muscle | ||||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median CDF10 | 0.227 (N = 11, p < 0.01) | 0.319 (N = 11, p < 0.001) | 0.285 (N = 4, p < 0.05) | |
IQR | 0.199–0.304 | 0.206–0.436 | 0.198–0.323 | |
SCM Muscles in Healthy Controls | Contralateral (Presumed Dystonic) SCM Muscles | |||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median CDF10 | 0.188 (N = 7) | 0.292 (N = 11, p < 0.001) | 0.288 (N = 9, p < 0.01) | 0.350 (N = 4, p < 0.01) |
IQR | 0.129–0.194 | 0.241–0.339 | 0.240–0.417 | 0.266–0.492 |
Ipsilateral (Presumed Non-Dystonic) SCM Muscles | ||||
BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | ||
Median CDF10 | 0.241 (N = 10, ns) | 0.296 (N = 12, p < 0.01) | 0.213 (N = 4, ns) | |
IQR | 0.171–0.294 | 0.210–0.419 | 0.182–0.338 | |
SESP Muscles in All Subjects | ||||
Healthy Controls | BoNT-Treated Patients, First Measurement | BoNT-Treated Patients, Second Measurement | BoNT-Naïve Patients | |
Median CDF10 | 0.187 (N = 8) | 0.256 (N = 11, p < 0.05) | 0.289 (N = 10, p < 0.01) | 0.264 (N = 4, ns) |
IQR | 0.142–0.215 | 0.202–0.273 | 0.226–0.341 | 0.146–0.359 |
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Nijmeijer, S.W.R.; De Bruijn, E.; Verhagen, R.; Forbes, P.A.; Kamphuis, D.J.; Happee, R.; Tijssen, M.A.J.; Koelman, J.H.T.M. Spectral EMG Changes in Cervical Dystonia Patients and the Influence of Botulinum Toxin Treatment. Toxins 2017, 9, 256. https://doi.org/10.3390/toxins9090256
Nijmeijer SWR, De Bruijn E, Verhagen R, Forbes PA, Kamphuis DJ, Happee R, Tijssen MAJ, Koelman JHTM. Spectral EMG Changes in Cervical Dystonia Patients and the Influence of Botulinum Toxin Treatment. Toxins. 2017; 9(9):256. https://doi.org/10.3390/toxins9090256
Chicago/Turabian StyleNijmeijer, S. W. R., E. De Bruijn, R. Verhagen, P. A. Forbes, D. J. Kamphuis, R. Happee, M. A. J. Tijssen, and J. H. T. M. Koelman. 2017. "Spectral EMG Changes in Cervical Dystonia Patients and the Influence of Botulinum Toxin Treatment" Toxins 9, no. 9: 256. https://doi.org/10.3390/toxins9090256
APA StyleNijmeijer, S. W. R., De Bruijn, E., Verhagen, R., Forbes, P. A., Kamphuis, D. J., Happee, R., Tijssen, M. A. J., & Koelman, J. H. T. M. (2017). Spectral EMG Changes in Cervical Dystonia Patients and the Influence of Botulinum Toxin Treatment. Toxins, 9(9), 256. https://doi.org/10.3390/toxins9090256