Residual Force Enhancement in Humans: A Systematic Review

in Journal of Applied Biomechanics

Click name to view affiliation

Neil Chapman Southern Cross University

Search for other papers by Neil Chapman in
Current site
Google Scholar
PubMed Close
*
,
John Whitting Southern Cross University

Search for other papers by John Whitting in
Current site
Google Scholar
PubMed Close
*
,
Suzanne Broadbent University of the Sunshine Coast

Search for other papers by Suzanne Broadbent in
Current site
Google Scholar
PubMed Close
*
,
Zachary Crowley-McHattan Southern Cross University

Search for other papers by Zachary Crowley-McHattan in
Current site
Google Scholar
PubMed Close
*
, and
Rudi Meir Southern Cross University

Search for other papers by Rudi Meir in
Current site
Google Scholar
PubMed Close
*
DOI:
https://doi.org/10.1123/jab.2017-0234
Keywords:
muscle physiology; voluntary contraction; activation reduction; Downs and Black checklist
In Print:
Volume 34: Issue 3
Page Range:
240–248
Restricted access

A systematic literature search was conducted to review the evidence of residual force enhancement (RFE) in vivo human muscle. The search, adhered to the PRISMA statement, of CINAHL, EBSCO, Embase, MEDLINE, and Scopus (inception—July 2017) was conducted. Full-text English articles that assessed at least 1 measure of RFE in vivo voluntarily contracted human skeletal muscle were selected. The methodologies of included articles were assessed against the Downs and Black checklist. Twenty-four studies were included (N = 424). Pooled Downs and Black scores ranked “fair” (x¯=17 [2.26]). RFE was observed in all muscles tested. Joint range of motion varied from 15° to 60°. Contraction intensities ranged from 10% to >95% maximum. Although transient force enhancement during the stretch phase may change with angular velocity, RFE in the subsequent isometric phase is independent of velocity. The magnitude of RFE was influenced by smaller stretch amplitudes and greatest at joint angles indicative of longer muscle lengths. Contraction and activation intensity influenced RFE, particularly during the initial isometric contraction phase of a poststretch isometric contraction. RFE resulted in increased torque production, reduced muscular activation, and enhanced torque production when the neuromuscular system is weakened seen in an aged population.

Chapman, Whitting, Crowley-McHattan, and Meir are with Southern Cross University, Lismore, NSW, Australia. Broadbent is with the University of the Sunshine Coast, Sippy Downs, QLD, Australia.

Chapman (neil.chapman@scu.edu.au) is corresponding author.
  • Collapse
  • Expand

Journal of Applied Biomechanics

Cover Journal of Applied Biomechanics
  • 1.

    Abbott BC, Aubert XM. The force exerted by active striated muscle during and after change of length. J Physiol. 1952;117(1):77–86. PubMed

  • 2.

    Fenn WO. The relation between the work performed and the energy liberated in muscular contraction. J Physiol. 1924;58(6):373–395. doi:10.1113/jphysiol.1924.sp002141

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Fenn WO, Marsh BS. Muscular force at different speeds of shortening. J Physiol. 1935;85(3):277–297. PubMed doi:10.1113/jphysiol.1935.sp003318

  • 4.

    Hill AV. The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci. 1938;126(843):136–195. doi:10.1098/rspb.1938.0050

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Hill AV. First and Last Experiments in Muscle Mechanics. Cambridge, MA: University Press; 1970.

  • 6.

    Huxley AF. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318.

  • 7.

    Katz B. The relation between force and speed in muscular contraction. J Physiol. 1939;96(1):45–64. PubMed doi:10.1113/jphysiol.1939.sp003756

  • 8.

    Edman KA, Elzinga G, Noble MI. Residual force enhancement after stretch of contracting frog single muscle fibers. J Gen Physiol. 1982;80(5):769–784. doi:10.1085/jgp.80.5.769

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Rassier DE. The mechanisms of the residual force enhancement after stretch of skeletal muscle: non-uniformity in half-sarcomeres and stiffness of titin. Proc R Soc Lond B Biol Sci. 2012;279:2705–2713. doi:10.1098/rspb.2012.0467

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Hahn D, Seiberl W, Schmidt S, Schweizer K, Schwirtz A. Evidence of residual force enhancement for multi-joint leg extension. J Biomech. 2010;43(8):1503–1508. PubMed doi:10.1016/j.jbiomech.2010.01.041

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Peterson DR, Rassier DE, Herzog W. Force enhancement in single skeletal muscle fibres on the ascending limb of the force–length relationship. J Exp Biol. 2004;207(pt 16):2787–2791. PubMed doi:10.1242/jeb.01095

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Rassier DE, Herzog W, Wakeling J, Syme DA. Stretch-induced, steady-state force enhancement in single skeletal muscle fibers exceeds the isometric force at optimum fiber length. J Biomech. 2003;36(9):1309–1316. PubMed doi:10.1016/S0021-9290(03)00155-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Herzog W, Leonard TR. The history dependence of force production in mammalian skeletal muscle following stretch-shortening and shortening-stretch cycles. J Biomech. 2000;33(5):531–542. PubMed doi:10.1016/S0021-9290(99)00221-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Schachar R, Herzog W, Leonard TR. The effects of muscle stretching and shortening on isometric forces on the descending limb of the force–length relationship. J Biomech. 2004;37(6):917–926. PubMed doi:10.1016/j.jbiomech.2003.10.006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Campbell SG, Campbell KS. Mechanisms of residual force enhancement in skeletal muscle: insights from experiments and mathematical models. Biophys Rev. 2011;3(4):199–207. PubMed doi:10.1007/s12551-011-0059-2

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Cook CS, McDonagh MJ. Force responses to controlled stretches of electrically stimulated human muscle-tendon complex. Exp Physiol. 1995;80(3):477–490. PubMed doi:10.1113/expphysiol.1995.sp003862

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Lee HD, Herzog W. Force enhancement following muscle stretch of electrically stimulated and voluntarily activated human adductor pollicis. J Physiol. 2002;545(pt 1):321–330. PubMed doi:10.1113/jphysiol.2002.018010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Pinniger GJ, Cresswell AG. Residual force enhancement after lengthening is present during submaximal plantar flexion and dorsiflexion actions in humans. J Appl Physiol. 2007;102(1):18–25. PubMed doi:10.1152/japplphysiol.00565.2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Ruiter CJ, Didden WJ, Jones DA, Haan AD. The force–velocity relationship of human adductor pollicis muscle during stretch and the effects of fatigue. J Physiol. 2000;526(pt 3):671–681. doi:10.1111/j.1469-7793.2000.00671.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Oskouei AE, Herzog W. Observations on force enhancement in submaximal voluntary contractions of human adductor pollicis muscle. J Appl Physiol. 2005;98(6):2087–2095. PubMed doi:10.1152/japplphysiol.01217.2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Tilp M, Steib S, Herzog W. Force–time history effects in voluntary contractions of human tibialis anterior. Eur J Appl Physiol. 2009;106(2):159–166. PubMed doi:10.1007/s00421-009-1006-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Seiberl W, Hahn D, Herzog W, Schwirtz A. Feedback controlled force enhancement and activation reduction of voluntarily activated quadriceps femoris during sub-maximal muscle action. J Electromyogr Kinesiol. 2012;22(1):117–123. PubMed doi:10.1016/j.jelekin.2011.10.010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Seiberl W, Power GA, Hahn D. Residual force enhancement in humans: current evidence and unresolved issues. J Electromyogr Kinesiol. 2015;25(4):571–580. PubMed doi:10.1016/j.jelekin.2015.04.011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Hahn D, Seiberl W, Schwirtz A. Force enhancement during and following muscle stretch of maximal voluntarily activated human quadriceps femoris. Eur J Appl Physiol. 2007;100(6):701–709. PubMed doi:10.1007/s00421-007-0462-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Oskouei AE, Herzog W. Force enhancement at different levels of voluntary contraction in human adductor pollicis. Eur J Appl Physiol. 2006;97(3):280–287. doi:10.1007/s00421-006-0167-z

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Seiberl W, Hahn D, Kreuzpointner F, Schwirtz A, Gastmann U. Force enhancement of quadriceps femoris in vivo and its dependence on stretch-induced muscle architectural changes. J Appl Biomech. 2010;26(3):256–264. PubMed doi:10.1123/jab.26.3.256

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Seiberl W, Paternoster F, Achatz F, Schwirtz A, Hahn D. On the relevance of residual force enhancement for everyday human movement. J Biomech. 2013;46(12):1996–2001. PubMed doi:10.1016/j.jbiomech.2013.06.014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Herzog W, Leonard TR, Joumaa V, Mehta A. Mysteries of muscle contraction. J Appl Biomech. 2008;24(1):1–13. PubMed doi:10.1123/jab.24.1.1

  • 29.

    Bigland B, Lippold OCJ. The relation between force, velocity and integrated electrical activity in human muscles. J Physiol. 1954;123(1):214–224. PubMed doi:10.1113/jphysiol.1954.sp005044

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Paternoster F, Hahn D, Stöcker F, Schwirtz A, Seiberl W. Oxygen consumption of gastrocnemius medialis muscle during submaximal voluntary isometric contractions with and without preceding stretch. Sci Rep. 2017;7(1):4674. PubMed doi:10.1038/s41598-017-04068-y

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Kushmerick M, Davies R. The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscles. Proc R Soc Lond B Biol Sci. 1969;174(1036):315–347. PubMed doi:10.1098/rspb.1969.0096

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Julian FJ, Morgan DL. The effect on tension of non-uniform distribution of length changes applied to frog muscle fibres. J Physiol. 1979;293(1):379–392. doi:10.1113/jphysiol.1979.sp012895

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Komi PV. Stretch-shortening cycle: a powerful model to study normal and fatigued muscle. J Biomech. 2000;33(10):1197–1206. PubMed doi:10.1016/S0021-9290(00)00064-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Paternoster FK, Seiberl W, Hahn D, Schwirtz A. Residual force enhancement during multi-joint leg extensions at joint-angle configurations close to natural human motion. J Biomech. 2016;49(5):773–779. PubMed doi:10.1016/j.jbiomech.2016.02.015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:2535. PubMed doi:10.1136/bmj.b2535

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Commun Health. 1998;52(6):377–384. doi:10.1136/jech.52.6.377

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Power GA, Herzog W, Rice CL. Decay of force transients following active stretch is slower in older than young men: support for a structural mechanism contributing to residual force enhancement in old age. J Biomech. 2014;47(13):3423–3427. PubMed doi:10.1016/j.jbiomech.2014.08.026

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Power GA, Makrakos DP, Rice CL, Vandervoort AA. Enhanced force production in old age is not a far stretch: an investigation of residual force enhancement and muscle architecture. Physiol Rep. 2013;1(1):e00004. PubMed doi:10.1002/phy2.4

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Power GA, Makrakos DP, Stevens DE, Rice CL, Vandervoort AA. Velocity dependence of eccentric strength in young and old men: the need for speed! Appl Physiol Nutr Metab. 2015;40(7):703–710. PubMed doi:10.1139/apnm-2014-0543

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Power GA, Rice CL, Vandervoort AA. Residual force enhancement following eccentric induced muscle damage. J Biomech. 2012;45(10):1835–1841. PubMed doi:10.1016/j.jbiomech.2012.04.006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Power GA, Rice CL, Vandervoort AA. Increased residual force enhancement in older adults is associated with a maintenance of eccentric strength. PLoS ONE. 2012;7(10):e48044. PubMed doi:10.1371/journal.pone.0048044

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Altenburg TM, de Ruiter CJ, Verdijk PW, van Mechelen W, de Haan A. Vastus lateralis surface and single motor unit EMG following submaximal shortening and lengthening contractions. Appl Physiol Nutr Metab. 2008;33(6):1086–1095. PubMed doi:10.1139/H08-092

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Oskouei AE, Herzog W. The dependence of force enhancement on activation in human adductor pollicis. Eur J Appl Physiol. 2006;98(1):22–29. PubMed doi:10.1007/s00421-006-0170-4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Shim J, Garner B. Residual force enhancement during voluntary contractions of knee extensors and flexors at short and long muscle lengths. J Biomech. 2012;45(6):913–918. PubMed doi:10.1016/j.jbiomech.2012.01.026

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Tilp M, Steib S, Schappacher-Tilp G, Herzog W. Changes in fascicle lengths and pennation angles do not contribute to residual force enhancement/depression in voluntary contractions. J Appl Biomech. 2011;27(1):64–73. PubMed doi:10.1123/jab.27.1.64

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Seiberl W, Hahn D, Paternoster F. Reduced activation in isometric muscle action after lengthening contractions is not accompanied by reduced performance fatigability. Sci Rep. 2016;6:39052. PubMed doi:10.1038/srep39052

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Jones AA, Power GA, Herzog W. History dependence of the electromyogram: implications for isometric steady-state EMG parameters following a lengthening or shortening contraction. J Electromyogr Kinesiol. 2016;27:30–38. PubMed doi:10.1016/j.jelekin.2016.01.008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Siebert T, Kurch D, Blickhan R, Stutzig N. Does weightlifting increase residual force enhancement? J Biomech. 2016;49(10):2047–2052. PubMed doi:10.1016/j.jbiomech.2016.05.017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Altenburg TM, de Ruiter CJ, Verdijk PW, van Mechelen W, de Haan A. Vastus lateralis surface and single motor unit electromyography during shortening, lengthening and isometric contractions corrected for mode-dependent differences in force-generating capacity. Acta Physiol. 2009;196(3):315–328.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 50.

    Leonard TR, Herzog W. Regulation of muscle force in the absence of actin-myosin-based cross-bridge interaction. Am J Physiol Cell Physiol. 2010;299(1):C14–20. PubMed doi:10.1152/ajpcell.00049.2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Webber S, Kriellaars D. Neuromuscular factors contributing to in vivo eccentric moment generation. J Appl Physiol. 1997;83(1):40–45. PubMed doi:10.1152/jappl.1997.83.1.40

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Edman KA. Residual force enhancement after stretch in striated muscle. A consequence of increased myofilament overlap? J Physiol. 2012;590(6):1339–1345. PubMed doi:10.1113/jphysiol.2011.222729

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Fukutani A, Joumaa V, Herzog W. Influence of residual force enhancement and elongation of attached cross-bridges on stretch-shortening cycle in skinned muscle fibers. Physiol Rep. 2017;5(22):e13477. PubMed doi:10.14814/phy2.13477

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Fukutani A, Misaki J, Isaka T. Effect of preactivation on torque enhancement by the stretch-shortening cycle in knee extensors. PLoS ONE. 2016;11(7):e0159058. PubMed doi:10.1371/journal.pone.0159058

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 3155 824 13
Full Text Views 83 20 2
PDF Downloads 61 16 4