European Journal of Applied Physiology

, Volume 119, Issue 9, pp 2065–2073 | Cite as

Experimental knee pain impairs joint torque and rate of force development in isometric and isokinetic muscle activation

  • David A. Rice
  • Jamie Mannion
  • Gwyn N. LewisEmail author
  • Peter J. McNair
  • Lana Fort
Original Article



To investigate the effects of acute experimental knee joint pain on maximum force generation and rate of force development (RFD) of the quadriceps muscle during isometric and dynamic muscle activations.


The right knee of 20 healthy people was injected with hypertonic saline to create an acute pain experience. Measurements of maximum knee extensor torque during isometric, concentric, and eccentric contractions were undertaken using a Biodex dynamometer. The RFD was also examined during the isometric contractions. Quadriceps muscle activity was obtained using electromyography (EMG). The outcome measures were obtained at baseline, during pain, and after knee pain had resolved.


Maximum joint torque and peak EMG were significantly reduced during pain, but there were no differences across the three types of contraction. The maximum RFD and rate of EMG rise were also reduced during pain, primarily at 50–100 ms post-contraction onset. The RFD and EMG rise were largely unaffected at later time periods following contraction onset (150–200 ms).


Acute joint pain has a similar impact on isometric and isokinetic contractions despite differences in neural control strategies. Joint pain also impairs rapid muscle activation and the RFD. These findings are important for people with musculoskeletal pain as it likely contributes to impairments in joint function in these populations.


Acute pain Knee extensors Maximum voluntary contraction Rate of force development 



Analysis of variance




Maximum voluntary contraction


Rate of force development


Author contributions

DR, PM, and JM conceived and designed the research. LF and DR collected the data. LF and GL analyzed the data. GL and LF wrote the manuscript. All the authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326. CrossRefPubMedGoogle Scholar
  2. 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 96:46–52. CrossRefPubMedGoogle Scholar
  3. Andersen LL, Holtermann A, Jorgensen MB, Sjogaard G (2008) Rapid muscle activation and force capacity in conditions of chronic musculoskeletal pain. Clin Biomech 23:1237–1242. CrossRefGoogle Scholar
  4. Andersen LL, Andersen JL, Zebis MK, Aagaard P (2010) Early and late rate of force development: differential adaptive responses to resistance training? Scand J Med Sci Sports 20:e162–169. CrossRefPubMedGoogle Scholar
  5. Angelozzi M, Madama M, Corsica C, Calvisi V, Properzi G, McCaw ST, Cacchio A (2012) Rate of force development as an adjunctive outcome measure for return-to-sport decisions after anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther 42:772–780. CrossRefPubMedGoogle Scholar
  6. Arendt-Nielsen L, Graven-Nielsen T, Svarrer H, Svensson P (1996) The influence of low back pain on muscle activity and coordination during gait: a clinical and experimental study. Pain 64:231–240. CrossRefPubMedGoogle Scholar
  7. Asaki T, Wang K, Luo Y, Arendt-Nielsen T, Graven-Nielsen T, Arendt-Nielsen L (2018) Acid-induced experimental knee pain and hyperalgesia in healthy humans. Exp Brain Res 236:587–598. CrossRefPubMedGoogle Scholar
  8. Burns E, Chipchase LS, Schabrun SM (2016) Primary sensory and motor cortex function in response to acute muscle pain: A systematic review and meta-analysis. Eur J Pain 20:1203–1213. CrossRefPubMedGoogle Scholar
  9. Chourasia AO, Buhr KA, Rabago DP, Kijowski R, Irwin CB, Sesto ME (2012) Effect of lateral epicondylosis on grip force development. J Hand Ther 25:27–36. CrossRefPubMedGoogle Scholar
  10. Ciubotariu A, Arendt-Nielsen L, Graven-Nielsen T (2007) Localized muscle pain causes prolonged recovery after fatiguing isometric contractions. Exp Brain Res 181:147–158. CrossRefPubMedGoogle Scholar
  11. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M (2007) Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 583:365–380. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Del Vecchio A, Negro F, Holobar A, Casolo A, Folland JP, Felici F, Farina D (2019) You are as fast as your motor neurons: speed of recruitment and maximal discharge of motor neurons determine the maximal rate of force development in humans. J Physiol 597(9):2445–2456. CrossRefPubMedGoogle Scholar
  13. Dvir Z, Keating JL (2003) Trunk extension effort in patients with chronic low back dysfunction. Spine 28:685–692. CrossRefPubMedGoogle Scholar
  14. Enoka RM (1996) Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol 81:2339–2346. CrossRefPubMedGoogle Scholar
  15. Ervilha UF, Arendt-Nielsen L, Duarte M, Graven-Nielsen T (2004) Effect of load level and muscle pain intensity on the motor control of elbow-flexion movements. Eur J Appl Physiol 92:168–175. CrossRefPubMedGoogle Scholar
  16. Farina D, Arendt-Nielsen L, Merletti R, Graven-Nielsen T (2004) Effect of experimental muscle pain on motor unit firing rate and conduction velocity. J Neurophysiol 91:1250–1259. CrossRefPubMedGoogle Scholar
  17. Farina D, Arendt-Nielsen L, Graven-Nielsen T (2005) Experimental muscle pain reduces initial motor unit discharge rates during sustained submaximal contractions. J Appl Physiol 98:999–1005. CrossRefPubMedGoogle Scholar
  18. Farina D, Arendt-Nielsen L, Roatta S, Graven-Nielsen T (2008) The pain-induced decrease in low-threshold motor unit discharge rate is not associated with the amount of increase in spike-triggered average torque. Clin Neurophysiol 119:43–51. CrossRefPubMedGoogle Scholar
  19. Felson DT et al (2007) Knee buckling: Prevalence, risk factors, and associated limitations in function. Ann Intern Med 147:534–540CrossRefGoogle Scholar
  20. Folland JP, Buckthorpe MW, Hannah R (2014) Human capacity for explosive force production: neural and contractile determinants. Scand J Med Sci Sports 24:894–906. CrossRefPubMedGoogle Scholar
  21. Gapeyeva H, Buht N, Peterson K, Ereline J, Haviko T, Pääsuke M (2007) Quadriceps femoris muscle voluntary isometric force production and relaxation characteristics before and 6 months after unilateral total knee arthroplasty in women. Knee Surg Sports Traumatol Arthrosc 15:202–211. CrossRefPubMedGoogle Scholar
  22. Graven-Nielsen T, Arendt-Nielsen L (2009) Impact of clinical and experimental pain on muscle strength and activity. Curr Rheumatol Rep 10:475. CrossRefGoogle Scholar
  23. Graven-Nielsen T, Lund H, Arendt-Nielsen L, Danneskiold-Samsøe B, Bliddal H (2002) Inhibition of maximal voluntary contraction force by experimental muscle pain: a centrally mediated mechanism. Muscle Nerve 26:708–712. CrossRefPubMedGoogle Scholar
  24. Henriksen M, Alkjaer T, Lund H, Simonsen EB, Graven-Nielsen T, Danneskiold-Samsoe B, Bliddal H (2007) Experimental quadriceps muscle pain impairs knee joint control during walking. J Appl Physiol 103:132–139. CrossRefPubMedGoogle Scholar
  25. Henriksen M, Alkjaer T, Simonsen EB, Bliddal H (2009) Experimental muscle pain during a forward lunge-the effects on knee joint dynamics and electromyographic activity. Br J Sports Med 43:503–507. CrossRefPubMedGoogle Scholar
  26. Henriksen M, Rosager S, Aaboe J, Graven-Nielsen T, Bliddal H (2011) Experimental knee pain reduces muscle strength. J Pain 12:460–467. CrossRefPubMedGoogle Scholar
  27. Hodges PW, Richardson CA (1996) Inefficient muscular stabilization of the lumbar spine associated with low back pain: a motor control evaluation of transversus abdominis. Spine 21:2640–2650CrossRefPubMedGoogle Scholar
  28. Hodges PW, Tucker K (2011) Moving differently in pain: a new theory to explain the adaptation to pain. Pain 152:S90–S98. CrossRefPubMedGoogle Scholar
  29. Jenkins ND et al (2014) The rate of torque development: a unique, non-invasive indicator of eccentric-induced muscle damage? Int J Sports Med 35:1190–1195. CrossRefPubMedGoogle Scholar
  30. Karayannis NV, Smeets RJEM, van den Hoorn W, Hodges PW (2013) Fear of movement is related to trunk stiffness in low back pain. PLoS ONE 8:e67779. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Klass M, Baudry S (1985) 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. CrossRefGoogle Scholar
  32. Liikavainio T, Lyytinen T, Tyrvainen E, Sipila S, Arokoski JP (2008) Physical function and properties of quadriceps femoris muscle in men with knee osteoarthritis. Arch Phys Med Rehabil 89:2185–2194CrossRefPubMedGoogle Scholar
  33. Lindstedt SL, LaStayo PC, Reich TE (2001) When active muscles lengthen: properties and consequences of eccentric contractions. News Physiol Sci 16:256–261PubMedGoogle Scholar
  34. MacIntyre DL, Reid WD, McKenzie DC (1995) Delayed muscle soreness. The inflammatory response to muscle injury and its clinical implications. Sports Med 20:24–40. CrossRefPubMedGoogle Scholar
  35. 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 468:191–198. CrossRefPubMedGoogle Scholar
  36. 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 116:1091–1116. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Marshall PW, Mannion J, Murphy BA (2010) The eccentric, concentric strength relationship of the hamstring muscles in chronic low back pain. J Electromyogr Kinesiol 20:39–45. CrossRefPubMedGoogle Scholar
  38. McHugh MP, Tyler TF, Greenberg SC, Gleim GW (2002) Differences in activation patterns between eccentric and concentric quadriceps contractions. J Sports Sci 20:83–91. CrossRefPubMedGoogle Scholar
  39. Molina R, Denadai BS (2012) Dissociated time course recovery between rate of force development and peak torque after eccentric exercise. Clin Physiol Funct Imaging 32:179–184. CrossRefPubMedGoogle Scholar
  40. Moreland JD et al (2003) Progressive resistance strengthening exercises after stroke: a single-blind randomized controlled trial. Arch Phys Med Rehabil 84:1433–1440CrossRefPubMedGoogle Scholar
  41. Nederhand MJ, Hermens HJ, Ijzerman MJ, Groothuis KG, Turk DC (2006) The effect of fear of movement on muscle activation in posttraumatic neck pain disability. Clin J Pain 22:519–525. CrossRefPubMedGoogle Scholar
  42. Osman A, Barrios FX, Gutierrez PM, Kopper BA, Merrifield T, Grittmann L (2000) The pain catastrophizing scale: further psychometric evaluation with adult samples. J Behav Med 23:351–365. CrossRefPubMedGoogle Scholar
  43. Park J, Hopkins JT (2013) Induced anterior knee pain immediately reduces involuntary and voluntary quadriceps activation. Clin J Sport Med 23:19–24. CrossRefPubMedGoogle Scholar
  44. Penailillo L, Blazevich A, Numazawa H, Nosaka K (2015) Rate of force development as a measure of muscle damage. Scand J Med Sci Sports 25:417–427. CrossRefPubMedGoogle Scholar
  45. Rice DA, Graven-Nielsen T, Lewis GN, McNair PJ, Dalbeth N (2015) The effects of experimental knee pain on lower limb corticospinal and motor cortex excitability. Arthritis Res Ther 17:204. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ruiter CJd, Kooistra RD, Paalman MI, Haan Ad (2004) Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles. J Appl Physiol 97:1693–1701. CrossRefPubMedGoogle Scholar
  47. Salomoni S, Tucker K, Hug F, McPhee M, Hodges PW (2016) Reduced maximal force during acute anterior knee pain is associated with deficits in voluntary muscle activation. PLoS ONE 11:e0161487. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Shakespeare DT, Stokes M, Sherman KP, Young A (1985) Reflex inhibition of the quadriceps after meniscectomy: lack of association with pain. Clin Physiol 5:137–144CrossRefPubMedGoogle Scholar
  49. Shirado O, Ito T, Kaneda K, Strax TE (1995) Concentric and eccentric strength of trunk muscles: influence of test postures on strength and characteristics of patients with chronic low-back pain. Arch Phys Med Rehabil 76:604–611CrossRefPubMedGoogle Scholar
  50. Slater H, Arendt-Nielsen L, Wright A, Graven-Nielsen T (2003) Experimental deep tissue pain in wrist extensors - a model of lateral epicondylalgia. Eur J Pain 7:277–288. CrossRefPubMedGoogle Scholar
  51. Sohn MK, Graven-Nielsen T, Arendt-Nielsen L, Svensson P (2000) Inhibition of motor unit firing during experimental muscle pain in humans. Muscle Nerve 23:1219–1226.;2-a CrossRefPubMedGoogle Scholar
  52. Sullivan M, Tanzer M, Stanish W, Fallaha M, Keefe FJ, Simmonds MA, Dunbar M (2009) Psychological determinants of problematic outcomes following Total Knee Arthroplasty. Pain 143:123–129. CrossRefPubMedGoogle Scholar
  53. Tillin NA, Jimenez-Reyes P, Pain MT, Folland JP (2010) Neuromuscular performance of explosive power athletes versus untrained individuals. Med Sci Sports Exerc 42:781–790. CrossRefPubMedGoogle Scholar
  54. Tillin NA, Pain MTG, Folland J (2013) Explosive force production during isometric squats correlates with athletic performance in rugby union players. J Sports Sci 31:66–76. CrossRefPubMedGoogle Scholar
  55. Tucker K, Butler J, Graven-Nielsen T, Riek S, Hodges P (2009) Motor unit recruitment strategies are altered during deep-tissue pain. J Neurosci 29:10820–10826. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Vahtrik D et al (2012) Quadriceps femoris muscle function prior and after total knee arthroplasty in women with knee osteoarthritis. Knee Surg Sports Traumatol Arthrosc 20:2017–2025. CrossRefPubMedGoogle Scholar
  57. Vila-Chã C, Hassanlouei H, Farina D, Falla D (2012) Eccentric exercise and delayed onset muscle soreness of the quadriceps induce adjustments in agonist-antagonist activity, which are dependent on the motor task. Exp Brain Res 216:385–395. CrossRefPubMedGoogle Scholar
  58. Winters JD, Christiansen CL, Stevens-Lapsley JE (2014) Preliminary investigation of rate of torque development deficits following total knee arthroplasty. Knee 21:382–386. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Health and Rehabilitation Research InstituteAuckland University of TechnologyAucklandNew Zealand
  2. 2.Waitemata Pain Service, Department of Anaesthesia and Perioperative MedicineNorth Shore HospitalAucklandNew Zealand
  3. 3.Unitec Institute of TechnologyAucklandNew Zealand

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