EDITORIAL
Fatigue and Fatigability in Spinal Muscular Atrophy; a Proposed Taxonomy to Enhance Assessment and Treatment
This article relates to:
-
Performance fatigability in adults with spinal muscular atrophy treated long-term with nusinersen
- Benjamin Stolte MD,
- Svenja Neuhoff MD,
- Jaqueline Lipka,
- Melina Schlag,
- Otgonzul von Velsen BSc,
- Teresa Kruse DMD,
- Cornelius Deuschl MD,
- Christoph Kleinschnitz MD,
- Tim Hagenacker MD,
- Volume 70Issue 6Muscle & Nerve
- pages: 1223-1229
- First Published online: October 3, 2024
Rafael Rodriguez-Torres,
Jacqueline Montes,
Rafael Rodriguez-Torres
Department of Rehabilitation and Regenerative Medicine, Columbia University Irving Medical Center, New York, NY, USA
Department of Neurology, Columbia University Irving Medical Center, New York, NY, USA
Department of Biobehavioral Sciences, Teachers College, Columbia University, New York, New York, USA
Contribution: Conceptualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorCorresponding Author
Jacqueline Montes
Department of Rehabilitation and Regenerative Medicine, Columbia University Irving Medical Center, New York, NY, USA
Correspondence:
Jacqueline Montes ([email protected])
Contribution: Conceptualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorRafael Rodriguez-Torres,
Jacqueline Montes,
Rafael Rodriguez-Torres
Department of Rehabilitation and Regenerative Medicine, Columbia University Irving Medical Center, New York, NY, USA
Department of Neurology, Columbia University Irving Medical Center, New York, NY, USA
Department of Biobehavioral Sciences, Teachers College, Columbia University, New York, New York, USA
Contribution: Conceptualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorCorresponding Author
Jacqueline Montes
Department of Rehabilitation and Regenerative Medicine, Columbia University Irving Medical Center, New York, NY, USA
Correspondence:
Jacqueline Montes ([email protected])
Contribution: Conceptualization, Writing - original draft, Writing - review & editing
Search for more papers by this author
Conflicts of Interest
J.M. has received honoraria for non-CME events from Genentech and Scholar Rock and served as a consultant or on advisory boards for Biogen, Scholar Rock, F. Hoffman LaRoche, Argenx, and NMD Pharma. R.R.T. has received honoraria for serving as a consultant for Scholar Rock, F. Hoffman LaRoche, and UCB.
Open Research
Data Availability Statement
The authors have nothing to report.
References
- 1A. M. Ruiter, J. Verschuuren, and M. R. Tannemaat, “Fatigue in Patients With Myasthenia Gravis. A Systematic Review of the Literature,” Neuromuscular Disorders 30, no. 8 (2020): 631–639.
- 2N. Royer, M. Duboeuf, J. P. Camdessanché, and G. Y. Millet, “Prevalence of Fatigue and Its Explicative Variables Among People With Multiple Sclerosis,” NeuroRehabilitation 51, no. 3 (2022): 509–517.
- 3J. H. Friedman, R. G. Brown, C. Comella, et al., “Fatigue in Parkinson's Disease: A Review,” Movement Disorders 22, no. 3 (2007): 297–308.
- 4B. M. Kluger, L. B. Krupp, and R. M. Enoka, “Fatigue and Fatigability in Neurologic Illnesses: Proposal for a Unified Taxonomy,” Neurology 80, no. 4 (2013): 409–416.
- 5R. S. Rodriguez-Torres, D. Uher, E. L. Gay, et al., “Measuring Fatigue and Fatigability in Spinal Muscular Atrophy (SMA): Challenges and Opportunities,” Journal of Clinical Medicine 12, no. 10 (2023): 3458.
- 6B. Wirth, “Spinal Muscular Atrophy: In the Challenge Lies a Solution,” Trends in Neurosciences 44, no. 4 (2021): 306–322.
- 7E. Mercuri, R. S. Finkel, F. Muntoni, et al., “Diagnosis and Management of Spinal Muscular Atrophy: Part 1: Recommendations for Diagnosis, Rehabilitation, Orthopedic and Nutritional Care,” Neuromuscular Disorders 28, no. 2 (2018): 103–115.
- 8Y. Noto, S. Misawa, M. Mori, et al., “Prominent Fatigue in Spinal Muscular Atrophy and Spinal and Bulbar Muscular Atrophy: Evidence of Activity-Dependent Conduction Block,” Clinical Neurophysiology 124, no. 9 (2013): 1893–1898.
- 9L. Belter, R. Cruz, and J. Jarecki, “Quality of Life Data for Individuals Affected by Spinal Muscular Atrophy: A Baseline Dataset From the Cure SMA Community Update Survey,” Orphanet Journal of Rare Diseases 15, no. 1 (2020): 217, https://doi.org/10.1186/s13023-020-01498-2.
- 10L. Belter, I. Peterson, and J. Jarecki, “Evaluating Perceived Fatigue Within an Adult Spinal Muscular Atrophy Population,” Neurology and Therapy 12, no. 6 (2023): 2161–2175.
- 11M. de Lemus, M. G. Cattinari, S. I. Pascual, et al., “Identification of the Most Relevant Aspects of Spinal Muscular Atrophy (SMA) With Impact on the Quality of Life of SMA Patients and Their Caregivers: The PROfuture Project, a Qualitative Study,” Journal of Patient-Reported Outcomes 8, no. 1 (2024): 78.
- 12B. Stolte, S. Neuhoff, J. Lipka, et al., “Performance Fatigability in Adults With Spinal Muscular Atrophy Treated Long-Term With Nusinersen,” Muscle & Nerve 70 (2024): 1223–1229.
- 13S. Dunaway Young, J. Montes, S. S. Kramer, et al., “Six-Minute Walk Test Is Reliable and Valid in Spinal Muscular Atrophy,” Muscle & Nerve 54, no. 5 (2016): 836–842.
- 14J. Montes, S. Dunaway Young, E. S. Mazzone, et al., “Nusinersen Improves Walking Distance and Reduces Fatigue in Later-Onset Spinal Muscular Atrophy,” Muscle & Nerve 60, no. 4 (2019): 409–414.
- 15S. C. Gandevia, R. M. Enoka, A. J. McComas, D. G. Stuart, and C. K. Thomas, “Neurobiology of Muscle Fatigue. Advances and Issues,” Advances in Experimental Medicine and Biology 384 (1995): 515–525.
- 16M. Sanjak, R. Konopacki, R. Capasso, et al., “Dissociation Between Mechanical and Myoelectrical Manifestation of Muscle Fatigue in Amyotrophic Lateral Sclerosis,” Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders 5, no. 1 (2004): 26–32.
- 17A. M. B. van der Heul, R. P. A. van Eijk, R. I. Wadman, et al., “Mastication in Patients With Spinal Muscular Atrophy Types 2 and 3 Is Characterized by Abnormal Efficiency, Reduced Endurance, and Fatigue,” Dysphagia 37, no. 4 (2022): 715–723.
- 18J. L. Taylor, M. Amann, J. Duchateau, et al., “Neural Contributions to Muscle Fatigue: From the Brain to the Muscle and Back Again,” Medicine and Science in Sports and Exercise 48, no. 11 (2016): 2294–2306.
- 19S. Dunaway Young, J. Montes, S. S. Kramer, B. Podwika, A. K. Rao, and D. C. de Vivo, “Perceived Fatigue in Spinal Muscular Atrophy: A Pilot Study,” Journal of Neuromuscular Diseases 6, no. 1 (2019): 109–117, https://doi.org/10.3233/jnd-180342.
- 20B. Bartels, J. F. de Groot, L. E. Habets, et al., “Correlates of Fatigability in Patients With Spinal Muscular Atrophy,” Neurology 96, no. 6 (2021): e845–e852.
- 21M. Woodward and E. P. Debold, “Acidosis and Phosphate Directly Reduce Myosin's Force-Generating Capacity Through Distinct Molecular Mechanisms,” Frontiers in Physiology 9 (2018): 862.
- 22G. Z. Mentis, D. Blivis, W. Liu, et al., “Early Functional Impairment of Sensory-Motor Connectivity in a Mouse Model of Spinal Muscular Atrophy,” Neuron 69, no. 3 (2011): 453–467.
- 23S. Kariya, G. H. Park, Y. Maeno-Hikichi, et al., “Reduced SMN Protein Impairs Maturation of the Neuromuscular Junctions in Mouse Models of Spinal Muscular Atrophy,” Human Molecular Genetics 17, no. 16 (2008): 2552–2569.
- 24M. Ripolone, D. Ronchi, R. Violano, et al., “Impaired Muscle Mitochondrial Biogenesis and Myogenesis in Spinal Muscular Atrophy,” JAMA Neurology 72, no. 6 (2015): 666–675.
- 25J. F. Tornero-Aguilera, J. Jimenez-Morcillo, A. Rubio-Zarapuz, and V. J. Clemente-Suárez, “Central and Peripheral Fatigue in Physical Exercise Explained: A Narrative Review,” International Journal of Environmental Research and Public Health 19, no. 7 (2022): 3909.
- 26F. Errico, C. Marino, M. Grimaldi, et al., “Nusinersen Induces Disease-Severity-Specific Neurometabolic Effects in Spinal Muscular Atrophy,” Biomolecules 12, no. 10 (2022): 1431.
- 27C. M. Simon, N. Delestree, J. Montes, et al., “Dysfunction of Proprioceptive Sensory Synapses Is a Pathogenic Event and Therapeutic Target in Mice and Humans With Spinal Muscular Atrophy,” medRxiv (2024), https://doi.org/10.1101/2024.06.03.24308132.
10.1101/2024.06.03.24308132 Google Scholar
- 28M. Papadopoulou, C. Zompola, G. Papagiannopoulou, et al., “Neurophysiological Evaluation of Autonomic Dysfunction in Spinal Muscular Atrophy: A Case-Control Study,” Acta Neurologica Scandinavica 2024, no. 1 (2024): 6575677.
10.1155/2024/6575677 Google Scholar
- 29M. Papadopoulou, E. Bakola, A. Papapostolou, et al., “Autonomic Dysfunction in Amyotrophic Lateral Sclerosis: A Neurophysiological and Neurosonology Study,” Journal of Neuroimaging 32, no. 4 (2022): 710–719.
- 30G. Y. Millet, M. F. Bertrand, T. Lapole, L. Féasson, V. Rozand, and D. Hupin, “Measuring Objective Fatigability and Autonomic Dysfunction in Clinical Populations: How and Why?,” Frontiers in Sports and Active Living 5 (2023): 1140833.
- 31C. Binz, O. Schreiber-Katz, M. Kumpe, et al., “An Observational Cohort Study on Impact, Dimensions and Outcome of Perceived Fatigue in Adult 5q-Spinal Muscular Atrophy Patients Receiving Nusinersen Treatment,” Journal of Neurology 268, no. 3 (2021): 950–962.
- 32F. Torri, P. Lopriore, V. Montano, G. Siciliano, M. Mancuso, and G. Ricci, “Pathophysiology and Management of Fatigue in Neuromuscular Diseases,” International Journal of Molecular Sciences 24, no. 5 (2023): 5005.
- 33J. Montes, A. M. Goodwin, M. P. McDermott, et al., “Diminished Muscle Oxygen Uptake and Fatigue in Spinal Muscular Atrophy,” Annals of Clinical Translational Neurology 8 (2021): 1086–1095.
- 34A. Govoni, G. Ricci, S. Bonanno, et al., “Six-Minute Walk Test as Outcome Measure of Fatigability in Adults With Spinal Muscular Atrophy Treated With Nusinersen,” Muscle & Nerve 70, no. 4 (2024): 816–823.
- 35U. Werlauff, A. Højberg, R. Firla-Holme, B. F. Steffensen, and J. Vissing, “Fatigue in Patients With Spinal Muscular Atrophy Type II and Congenital Myopathies: Evaluation of the Fatigue Severity Scale,” Quality of Life Research: An International Journal of Quality of Life Aspects of Treatment, Care and Rehabilitation 23, no. 5 (June 2014): 1479–1488, https://doi.org/10.1007/s11136-013-0565-8.
- 36C. E. Zizzi, E. Luebbe, P. Mongiovi, et al., “The Spinal Muscular Atrophy Health Index: A Novel Outcome for Measuring How a Patient Feels and Functions,” Muscle & Nerve 63, no. 6 (June 2021): 837–844, https://doi.org/10.1002/mus.27223.
- 37J. F. Vázquez-Costa, M. Branas-Pampillón, J. Medina-Cantillo, et al., “Validation of a Set of Instruments to Assess Patient- and Caregiver-Oriented Measurements in Spinal Muscular Atrophy: Results of the SMA-TOOL Study,” Neurology and Therapy (October 2022): 89–105, https://doi.org/10.1007/s40120-022-00411-2.
- 38C. Binz, A. Osmanovic, N. H. Thomas, et al., “Validity and Reliability of the German Multidimensional Fatigue Inventory in Spinal Muscular Atrophy,” Annals of Clinical and Translational Neurology 9, no. 3 (March 2022): 351–362, https://doi.org/10.1002/acn3.51520.
Citing Literature
