Abstract
There is increasing appreciation of the role of rate of torque development (RTD) in physical function of older adults (OAs). This study compared various RTD strategies and electromyography (EMG) in the knee extensors and focused on discriminating groups with potential limitations in voluntary activation (VA) and associations of different RTD indices with functional tests that may be affected by VA in OAs. Neuromuscular function was assessed in 20 younger adults (YAs, 22.0 ± 1.7 years) and 50 OAs (74.4 ± 7.0 years). Isometric ballistic and peak torque during maximal voluntary contractions (pkTMVC), doublet stimulation and surface EMG were assessed and used to calculate VA during pkTMVC and RTD and rate of EMG rise during ballistic contractions. Select mobility tests (e.g., gait speed, 5× chair rise) were also assessed in the OAs. Voluntary RTD and RTD normalized to pkTMVC, doublet torque, and peak doublet RTD were compared. Rate of EMG rise and voluntary RTD normalized to pkTMVC did not differ between OAs and YAs, nor were they associated with functional test scores. Voluntary RTD indices normalized to stimulated torque parameters were significantly associated with VA (r = 0.319–0.459), and both indices were significantly lower in OAs vs YAs (all p < 0.020). These RTD indices showed significant association with the majority of mobility tests, but there was no clear advantage among them. Thus, voluntary RTD normalized to pkTMVC was ill-suited for use in OAs, while results suggests that voluntary RTD normalized to stimulated torque parameters may be useful for identifying central mechanisms of RTD impairment in OAs.
Clinical trial registration number NCT02505529; date of registration 07/22/2015.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the authors, but restrictions apply to the availability of these data. Data are, however, available from the authors upon reasonable request.
Abbreviations
- 5xCR:
-
5 Times chair rise
- 6MW:
-
Six-minute walk
- ANOVA:
-
Analysis of variance
- drRTD:
-
Doublet rate normalized rate of torque development; vRTD/pkRTDdoublet
- dtRTD:
-
Doublet torque normalized rate of torque development; vRTD/pkTdoublet
- EMG:
-
Electromyography/electromyographic
- EMGREF :
-
Reference electromyographic signal
- FSST:
-
Four square step test
- OA:
-
Older adult
- pkRTDdoublet :
-
Peak rate of torque development during doublet
- pkTdoublet :
-
Peak torque during doublet
- pkTMVC :
-
Peak torque during maximal voluntary contraction
- RMS:
-
Root mean square
- rrEMG:
-
Rate of EMG rise
- rRTD:
-
Relative rate of torque development; vRTD/pkTMVC
- SPPB:
-
Short physical performance battery
- VA:
-
Voluntary activation
- vRTD:
-
Voluntary rate of torque development
- YA:
-
Young adult
References
Andersen LL, Aagaard P (2006) Influence of maximal muscle strength and intrinsic muscle contractile properties on contractile rate of force development. Eur J Appl Physiol 96(1):46–52. https://doi.org/10.1007/s00421-005-0070-z
Bellumori M, Jaric S, Knight CA (2011) The rate of force development scaling factor (RFD-SF): protocol, reliability, and muscle comparisons. Exp Brain Res 212(3):359–369. https://doi.org/10.1007/s00221-011-2735-7
Buckthorpe MW, Hannah R, Pain TG, Folland JP (2012) Reliability of neuromuscular measurements during explosive isometric contractions, with special reference to electromyography normalization techniques. Muscle Nerve 46(4):566–576. https://doi.org/10.1002/mus.23322
Clark BC, Taylor JL (2011) Age-related changes in motor cortical properties and voluntary activation of skeletal muscle. Curr Aging Sci 4(3):192–199
Clark BC, Cook SB, Ploutz-Snyder LL (2007) Reliability of techniques to assess human neuromuscular function in vivo. J Electromyogr Kinesiol 17(1):90–101
Clark DJ, Patten C, Reid KF, Carabello RJ, Phillips EM, Fielding RA (2011) Muscle performance and physical function are associated with voluntary rate of neuromuscular activation in older adults. J Gerontol A Biol Sci Med Sci 66(1):115–121. https://doi.org/10.1093/gerona/glq153
Clark DJ, Reid KF, Patten C, Phillips EM, Ring SA, Wu SS, Fielding RA (2014) Does quadriceps neuromuscular activation capability explain walking speed in older men and women? Exp Gerontol 55:49–53. https://doi.org/10.1016/j.exger.2014.03.019
Clark BC, Taylor JL, Hong SL, Law TD, Russ DW (2015) Weaker seniors exhibit motor cortex hypoexcitability and impairments in voluntary activation. J Gerontol A Biol Sci Med Sci 70(9):1112–1119. https://doi.org/10.1093/gerona/glv030
Clark LA, Manini TM, Wages NP, Simon JE, Russ DW, Clark BC (2021) Reduced neural excitability and activation contribute to clinically meaningful weakness in older adults. J Gerontol A Biol Sci Med Sci 76(4):692–702. https://doi.org/10.1093/gerona/glaa157
de Ruiter CJ, Kooistra RD, Paalman MI, de Haan A (2004) Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles. J Appl Physiol 97(5):1693–1701. https://doi.org/10.1152/japplphysiol.00230.2004
Farina D, Merletti R, Enoka RM (2004) The extraction of neural strategies from the surface EMG. J Appl Physiol 96(4):1486–1495. https://doi.org/10.1152/japplphysiol.01070.2003
Farina D, Merletti R, Enoka RM (2014) The extraction of neural strategies from the surface EMG: an update. J Appl Physiol 117(11):1215–1230. https://doi.org/10.1152/japplphysiol.00162.2014
Folland JP, Buckthorpe MW, Hannah R (2014) Human capacity for explosive force production: neural and contractile determinants. Scand J Med Sci Sports 24(6):894–906. https://doi.org/10.1111/sms.12131
Gerstner GR, Thompson BJ, Rosenberg JG, Sobolewski EJ, Scharville MJ, Ryan ED (2017) Neural and muscular contributions to the age-related reductions in rapid strength. Med Sci Sports Exerc 49(7):1331–1339. https://doi.org/10.1249/MSS.0000000000001231
Hinkle D, Wiersma W, Jurs S (2003) Applied statistics for the behavioral sciences, 5th edn. Houghton-Mifflin, Boston
Izquierdo M, Aguado X, Gonzalez R, Lopez JL, Hakkinen K (1999) Maximal and explosive force production capacity and balance performance in men of different ages. Eur J Appl Physiol Occup Physiol 79(3):260–267. https://doi.org/10.1007/s004210050504
Jenkins ND, Buckner SL, Cochrane KC, Bergstrom HC, Palmer TB, Johnson GO, Schmidt RJ, Housh TJ, Cramer JT (2014) Age-related differences in rates of torque development and rise in EMG are eliminated by normalization. Exp Gerontol 57:18–28. https://doi.org/10.1016/j.exger.2014.04.015
Kamo T, Asahi R, Azami M, Ogihara H, Ikeda T, Suzuki K, Nishida Y (2019) Rate of torque development and the risk of falls among community dwelling older adults in Japan. Gait Posture 72:28–33. https://doi.org/10.1016/j.gaitpost.2019.05.019
Keenan KG, Farina D, Merletti R, Enoka RM (2006) Amplitude cancellation reduces the size of motor unit potentials averaged from the surface EMG. J Appl Physiol 100(6):1928–1937. https://doi.org/10.1152/japplphysiol.01282.2005
Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19(7):861–869
Klass M, Baudry S, Duchateau J (2008) Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions. J Appl Physiol 104(3):739–746. https://doi.org/10.1152/japplphysiol.00550.2007
Kozinc Z, Smajla D, Sarabon N (2022) The rate of force development scaling factor: a review of underlying factors, assessment methods and potential for practical applications. Eur J Appl Physiol 122(4):861–873. https://doi.org/10.1007/s00421-022-04889-4
Kwon M, Senefeld JW, Hunter SK (2020) Attenuated activation of knee extensor muscles during fast contractions in older men and women. Eur J Appl Physiol 120(10):2289–2299. https://doi.org/10.1007/s00421-020-04451-0
Lenhard W, Lenhard A (2014) Hypothesis tests for comparing correlations. https://www.psychometrica.de/correlation.html. Accessed 01 Mar 2023
Lin DC, McGowan CP, Blum KP, Ting LH (2019) Yank: the time derivative of force is an important biomechanical variable in sensorimotor systems. J Exp Biol. https://doi.org/10.1242/jeb.180414
Maffiuletti NA, Bizzini M, Widler K, Munzinger U (2010) Asymmetry in quadriceps rate of force development as a functional outcome measure in TKA. Clin Orthop Relat Res 468(1):191–198. https://doi.org/10.1007/s11999-009-0978-4
Maffiuletti NA, Aagaard P, Blazevich AJ, Folland J, Tillin N, Duchateau J (2016) Rate of force development: physiological and methodological considerations. Eur J Appl Physiol 116(6):1091–1116. https://doi.org/10.1007/s00421-016-3346-6
Manini TM, Visser M, Won-Park S, Patel KV, Strotmeyer ES, Chen H, Goodpaster B, De Rekeneire N, Newman AB, Simonsick EM, Kritchevsky SB, Ryder K, Schwartz AV, Harris TB (2007) Knee extension strength cutpoints for maintaining mobility. J Am Geriatr Soc 55(3):451–457
Mau-Moeller A, Behrens M, Lindner T, Bader R, Bruhn S (2013) Age-related changes in neuromuscular function of the quadriceps muscle in physically active adults. J Electromyogr Kinesiol 23(3):640–648. https://doi.org/10.1016/j.jelekin.2013.01.009
Miller RG, Mirka A, Maxfield M (1981) Rate of tension development in isometric contractions of a human hand muscle. Exp Neurol 73(1):267–285
Moskowitz S, Russ DW, Clark LA, Wages NP, Grooms DR, Woods AJ, Suhr J, Simon JE, O’Shea A, Criss CR, Fadda P, Clark BC (2021) Is impaired dopaminergic function associated with mobility capacity in older adults? Geroscience 43(3):1383–1404. https://doi.org/10.1007/s11357-020-00303-z
Osawa Y, Studenski SA, Ferrucci L (2018) Knee extension rate of torque development and peak torque: associations with lower extremity function. J Cachexia Sarcopenia Muscle 9(3):530–539. https://doi.org/10.1002/jcsm.12285
Pijnappels M, Bobbert MF, van Dieen JH (2005) Push-off reactions in recovery after tripping discriminate young subjects, older non-fallers and older fallers. Gait Posture 21(4):388–394. https://doi.org/10.1016/j.gaitpost.2004.04.009
Radaelli R, Brusco CM, Lopez P, Rech A, Machado CLF, Grazioli R, Muller DC, Tufano JJ, Cadore EL, Pinto RS (2019) Muscle quality and functionality in older women improve similarly with muscle power training using one or three sets. Exp Gerontol 128:110745. https://doi.org/10.1016/j.exger.2019.110745
Reid KF, Fielding RA (2012) Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev 40(1):4–12. https://doi.org/10.1097/JES.0b013e31823b5f13
Russ DW, Clark BC, Krause J, Hagerman FC (2012) Development of a neuromuscular electrical stimulation protocol for sprint training. Med Sci Sports Exerc. https://doi.org/10.1249/MSS.0b013e31825423f1
Suetta C, Aagaard P, Rosted A, Jakobsen AK, Duus B, Kjaer M, Magnusson SP (2004) Training-induced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. J Appl Physiol 97(5):1954–1961. https://doi.org/10.1152/japplphysiol.01307.2003
Thompson BJ, Ryan ED, Sobolewski EJ, Conchola EC, Cramer JT (2013) Age related differences in maximal and rapid torque characteristics of the leg extensors and flexors in young, middle-aged and old men. Exp Gerontol 48(2):277–282. https://doi.org/10.1016/j.exger.2012.10.009
Thompson BJ, Ryan ED, Herda TJ, Costa PB, Herda AA, Cramer JT (2014) Age-related changes in the rate of muscle activation and rapid force characteristics. Age (dordr) 36(2):839–849. https://doi.org/10.1007/s11357-013-9605-0
Tillin NA, Jimenez-Reyes P, Pain MT, Folland JP (2010) Neuromuscular performance of explosive power athletes versus untrained individuals. Med Sci Sports Exerc 42(4):781–790. https://doi.org/10.1249/MSS.0b013e3181be9c7e
Tillin NA, Pain MT, Folland JP (2012) Short-term training for explosive strength causes neural and mechanical adaptations. Exp Physiol 97(5):630–641. https://doi.org/10.1113/expphysiol.2011.063040
Funding
This study was supported by National Institutes of Health (NIH) award R01AG044424 and R01AG067758 (to BC Clark), and American Heart Association award 19PRE34380496 (to D Tavoian).
Author information
Authors and Affiliations
Contributions
All authors have read and approved the final version of this manuscript. Additional roles are as follows: DT—contributed to the conception and design of the project, collected and analyzed data, wrote the manuscript. BCC—secured funding for the project, contributed to the conception and design of the project, collected and analyzed data and reviewed all drafts of the manuscript. LAC—collected and analyzed data and reviewed the drafts of the manuscript. NPW—collected and analyzed data and reviewed the drafts of the manuscript. DWR—contributed to the conception and design of the project, analyzed and interpreted the data, wrote the manuscript and reviewed all drafts.
Corresponding author
Ethics declarations
Conflict of interest
In the past 5-years, Brian Clark received research funding from the NIH, Regeneron Pharmaceuticals, Astellas Pharma Global Development, Inc., RTI Health Solutions, Biophytis, NMD Pharma, Myolex Inc, and the Osteopathic Heritage Foundations and consulting fees from Regeneron Pharmaceuticals, Abbott Laboratories, and the Gerson Lehrman Group. Additionally, Brian Clark is co-founder with equity, and serves as the Chief of Aging Research, of OsteoDx, Inc. In the past 5 years, Nathan Wages has received funding from the NIH (F32AG069358). In the past 5 years, David Russ received research funding from the NIH and research funding from Abbott Nutrition. All other authors declare no conflicts of interest, financial or otherwise.
Ethical approval
This study was approved by the Ohio University Institutional Review Board and was performed in accordance with the 1964 Helsinki Declaration.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Communicated by Toshio Moritani.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tavoian, D., Clark, B.C., Clark, L.A. et al. Comparison of strategies for assessment of rate of torque development in older and younger adults. Eur J Appl Physiol 124, 551–560 (2024). https://doi.org/10.1007/s00421-023-05299-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-023-05299-w