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European Journal of Applied Physiology

, Volume 119, Issue 5, pp 1127–1136 | Cite as

Characterization of torque generating properties of ankle plantar flexor muscles in ambulant adults with cerebral palsy

  • Rasmus Feld FriskEmail author
  • Jakob Lorentzen
  • Lee Barber
  • Jens Bo Nielsen
Original Article
  • 70 Downloads

Abstract

Purpose

Weakness of plantar flexor muscles is related to reduced push-off and forward propulsion during gait in persons with cerebral palsy (CP). It has not been clarified to what an extent altered muscle contractile properties contribute to this muscle weakness. Here, we investigated the torque generating capacity and muscle fascicle length in the triceps surae muscle throughout ankle range of motion (ROM) in adults with CP using maximal single muscle twitches elicited by electrical nerve stimulation and ultrasonography.

Methods

Fourteen adults with CP (age 36, SD 10.6, GMFCS I–III) and 17 neurological intact (NI) adults (age 36, SD 4.5) participated. Plantar flexor torque during supramaximal stimulation of the tibial nerve was recorded in a dynamometer at 8 ankle angles throughout ROM. Medial gastrocnemius (MG) fascicle length was tracked using ultrasonography.

Results

Adults with CP showed reduced plantar flexor torque and fascicle shortening during supramaximal stimulation throughout ROM. The largest torque generation was observed at the ankle joint position where the largest shortening of MG fascicles was observed in both groups. This was at a more plantarflexed position in the CP group.

Conclusion

Reduced torque and fascicle shortening during supramaximal stimulation of the tibial nerve indicate impaired contractile properties of plantar flexor muscles in adults with CP. Maximal torque was observed at a more plantarflexed position in adults with CP indicating an altered torque-fascicle length/ankle angle relation. The findings suggest that gait rehabilitation in adults with CP may require special focus on improvement of muscle contractility.

Keywords

Cerebral palsy Torque generation Plantar flexors Contractile properties 

Abbreviations

BM

Body mass

CI

Confidence interval

CP

Cerebral palsy

EMG

Electromyography

GMFCS

Gross motor function classification scale

MG

Medial gastrocnemius muscle

MIXED

Mixed model regression analysis

MVC

Maximal voluntary (isometric) contraction

NI

Neurological intact

ROM

Range of motion

SCI

Spinal cord injury

SE

Standard error

SD

Standard deviation

TD

Typical developed

Notes

Acknowledgements

We are grateful to Michaël Bertrand and Rafael Curbelo for valuable help with the experiments and to all participants. The study was supported by the Elsass foundation, Charlottenlund, Denmark. The foundation was not involved in the conduct or decision making regarding the work presented in the paper.

Author contributions

JBN, JLO and RFF have conceived and designed research. JBN, JLO and RFF conducted the experiments. RFF and LB analyzed data. RFF did the statistics and wrote the manuscript in collaboration with JBN. All authors have read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the authors. All authors have contributed essentially to the work and have approved the final publication.

Supplementary material

421_2019_4102_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 17 KB)

References

  1. Barber L, Barrett R, Lichtwark G (2011) Passive muscle mechanical properties of the medial gastrocnemius in young adults with spastic cerebral palsy. J Biomech 44:2496–2500CrossRefGoogle Scholar
  2. Barber L, Barrett R, Lichtwark G (2012) Medial gastrocnemius muscle fascicle active torque-length and Achilles tendon properties in young adults with spastic cerebral palsy. J Biomech 45:2526–2530CrossRefGoogle Scholar
  3. Barber LA, Barrett RS, Gillett JG, Cresswell AG, Lichtwark GA (2013) Neuromechanical properties of the triceps surae in young and older adults. Exp Gerontol 48:1147–1155CrossRefGoogle Scholar
  4. Barber L, Carty C, Modenese L, Walsh J, Boyd R, Lichtwark G (2017) Medial gastrocnemius and soleus muscle-tendon unit, fascicle, and tendon interaction during walking in children with cerebral palsy. Dev Med Child Neurol 59:843–851CrossRefGoogle Scholar
  5. Barrett RS, Lichtwark GA (2010) Gross muscle morphology and structure in spastic cerebral palsy: a systematic review. Dev Med Child Neurol 52:794–804CrossRefGoogle Scholar
  6. Benard MR, Becher J, Harlaar J, Huijing PA, Jaspers R (2008) Ultrasound measurements of muscle parameters of human gastrocnemius medialis are critically determined by probe orientation. Gait Posture 28:S16–S17CrossRefGoogle Scholar
  7. Benard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT (2009) Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve 39:652–665CrossRefGoogle Scholar
  8. Cronin NJ, Carty CP, Barrett RS, Lichtwark G (2011) Automatic tracking of medial gastrocnemius fascicle length during human locomotion. J Appl Physiol (1985) 111:1491–1496CrossRefGoogle Scholar
  9. Elder GC, Kirk J, Stewart G, Cook K, Weir D, Marshall A, Leahey L (2003) Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol 45:542–550CrossRefGoogle Scholar
  10. Friden J, Lieber RL (2003) Spastic muscle cells are shorter and stiffer than normal cells. Muscle Nerve 27:157–164CrossRefGoogle Scholar
  11. Gao F, Zhang LQ (2008) Altered contractile properties of the gastrocnemius muscle poststroke. J Appl Physiol (1985) 105:1802–1808CrossRefGoogle Scholar
  12. Geertsen SS, Kirk H, Lorentzen J, Jorsal M, Johansson CB, Nielsen JB (2015) Impaired gait function in adults with cerebral palsy is associated with reduced rapid force generation and increased passive stiffness. Clin Neurophysiol 126:2320–2329CrossRefGoogle Scholar
  13. Gillett JG, Barrett RS, Lichtwark GA (2013) Reliability and accuracy of an automated tracking algorithm to measure controlled passive and active muscle fascicle length changes from ultrasound. Comput Methods Biomech Biomed Eng 16:678–687CrossRefGoogle Scholar
  14. Gillett JG, Lichtwark GA, Boyd RN, Barber LA (2018) Functional anaerobic and strength training in young adults with cerebral palsy. Med Sci Sports Exerc 50:1549–1557CrossRefGoogle Scholar
  15. Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192CrossRefGoogle Scholar
  16. Gough M, Shortland AP (2012) Could muscle deformity in children with spastic cerebral palsy be related to an impairment of muscle growth and altered adaptation?. Dev Med Child Neurol 54:495–499CrossRefGoogle Scholar
  17. Hösl M, Bohm H, Arampatzis A, Keymer A, Doderlein L (2016) Contractile behavior of the medial gastrocnemius in children with bilateral spastic cerebral palsy during forward, uphill and backward-downhill gait. Clin Biomech (Bristol Avon) 36:32–39CrossRefGoogle Scholar
  18. Hussain AW, Onambele GL, Williams AG, Morse CI (2014) Muscle size, activation, and coactivation in adults with cerebral palsy. Muscle Nerve 49:76–83CrossRefGoogle Scholar
  19. Hussain AW, Onambele GL, Williams AG, Morse CI (2017) Medial gastrocnemius specific force of adult men with spastic cerebral palsy. Muscle Nerve 56:298–306CrossRefGoogle Scholar
  20. Hutton RS, Roy RR, Edgerton VR (1988) Coexistent Hoffmann reflexes in human leg muscles are commonly due to volume conduction. Exp Neurol 100:265–273CrossRefGoogle Scholar
  21. Jahnsen R, Villien L, Egeland T, Stanghelle JK, Holm I (2004a) Locomotion skills in adults with cerebral palsy. Clin Rehabil 18:309–316CrossRefGoogle Scholar
  22. Jahnsen R, Villien L, Aamodt G, Stanghelle JK, Holm I (2004b) Musculoskeletal pain in adults with cerebral palsy compared with the general population. J Rehabil Med 36:78–84CrossRefGoogle Scholar
  23. Johnson DL, Miller F, Subramanian P, Modlesky CM (2009) Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr 154:715–720CrossRefGoogle Scholar
  24. Kalkman BM, Bar-On L, Cenni F, Maganaris CN, Bass A, Holmes G, Desloovere K, Barton GJ, O’Brien TD (2017). Achilles tendon moment arm length is smaller in children with cerebral palsy than in typically developing children. J Biomech 56:48–54CrossRefGoogle Scholar
  25. Kirk H, Geertsen SS, Lorentzen J, Krarup KB, Bandholm T, Nielsen JB (2016) Explosive resistance training increases rate of force development in ankle dorsiflexors and gait function in adults with cerebral palsy. J Strength Cond Res 30:2749–2760CrossRefGoogle Scholar
  26. Lichtwark GA, Wilson AM (2006) Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion. J Exp Biol 209:4379–4388CrossRefGoogle Scholar
  27. Lichtwark GA, Wilson AM (2008) Optimal muscle fascicle length and tendon stiffness for maximising gastrocnemius efficiency during human walking and running. J Theor Biol 252:662–673CrossRefGoogle Scholar
  28. Lieber RL, Friden J (2000) Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23:1647–1666CrossRefGoogle Scholar
  29. Lieber RL, Friden J (2002) Spasticity causes a fundamental rearrangement of muscle-joint interaction. Muscle Nerve 25:265–270CrossRefGoogle Scholar
  30. Lieber RL, Steinman S, Barash IA, Chambers H (2004) Structural and functional changes in spastic skeletal muscle. Muscle Nerve 29:615–627CrossRefGoogle Scholar
  31. Lorentzen J, Grey MJ, Crone C, Mazevet D, Biering-Sorensen F, Nielsen JB (2010) Distinguishing active from passive components of ankle plantar flexor stiffness in stroke, spinal cord injury and multiple sclerosis. Clin Neurophysiol 121:1939–1951CrossRefGoogle Scholar
  32. Lorentzen J, Kirk H, Fernandez-Lago H, Frisk R, Scharff Nielsen N, Jorsal M, Nielsen JB (2017) Treadmill training with an incline reduces ankle joint stiffness and improves active range of movement during gait in adults with cerebral palsy. Disabil Rehabil 39:987–993CrossRefGoogle Scholar
  33. Maffiuletti NA, Martin A, Babault N, Pensini M, Lucas B, Schieppati M (2001) Electrical and mechanical H(max)-to-M(max) ratio in power- and endurance-trained athletes. J Appl Physiol (1985) 90:3–9CrossRefGoogle Scholar
  34. Maganaris CN, Baltzopoulos V, Ball D, Sargeant AJ (2001) In vivo specific tension of human skeletal muscle. J Appl Physiol (1985) 90:865–872CrossRefGoogle Scholar
  35. Malaiya R, McNee AE, Fry NR, Eve LC, Gough M, Shortland AP (2007) The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. J Electromyogr Kinesiol 17:657–663CrossRefGoogle Scholar
  36. Matthiasdottir S, Hahn M, Yaraskavitch M, Herzog W (2014) Muscle and fascicle excursion in children with cerebral palsy. Clin Biomech (Bristol, Avon) 29:458–462CrossRefGoogle Scholar
  37. McDonald MF, Kevin Garrison M, Schmit BD (2005) Length-tension properties of ankle muscles in chronic human spinal cord injury. J Biomech 38:2344–2353CrossRefGoogle Scholar
  38. Meinders M, Gitter A, Czerniecki JM (1998) The role of ankle plantar flexor muscle work during walking. Scand J Rehabil Med 30:39–46CrossRefGoogle Scholar
  39. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzopoulos V, Maganaris CN (2007) Differences in gastrocnemius muscle architecture between the paretic and non-paretic legs in children with hemiplegic cerebral palsy. Clin Biomech (Bristol, Avon) 22:718–724CrossRefGoogle Scholar
  40. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzopoulos V, Maganaris CN (2008) In vivo gastrocnemius muscle fascicle length in children with and without diplegic cerebral palsy. Dev Med Child Neurol 50:44–50CrossRefGoogle Scholar
  41. Morgan P, Murphy A, Opheim A, McGinley J (2016) Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy: an observational study. Gait Posture 48:243–248CrossRefGoogle Scholar
  42. Neptune RR, Kautz SA, Zajac FE (2001) Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. J Biomech 34:1387–1398CrossRefGoogle Scholar
  43. Neyroud D, Armand S, De Coulon G, Sarah RDDS, Maffiuletti NA, Kayser B, Place N (2017) Plantar flexor muscle weakness and fatigue in spastic cerebral palsy patients. Res Dev Disabil 61:66–76CrossRefGoogle Scholar
  44. Olney SJ, MacPhail HE, Hedden DM, Boyce WF (1990) Work and power in hemiplegic cerebral palsy gait. Phys Ther 70:431–438CrossRefGoogle Scholar
  45. Parkes J, McCullough N, Madden A (2010) To what extent do children with cerebral palsy participate in everyday life situations?. Health Soc Care Community 18:304–315Google Scholar
  46. Ranatunga KW (2011) Skeletal muscle stiffness and contracture in children with spastic cerebral palsy. J Physiol 589:2665CrossRefGoogle Scholar
  47. Riad J, Modlesky CM, Gutierrez-Farewik EM, Brostrom E (2012) Are muscle volume differences related to concentric muscle work during walking in spastic hemiplegic cerebral palsy?. Clin Orthop Relat Res 470:1278–1285CrossRefGoogle Scholar
  48. Robinson KG, Mendonca JL, Militar JL, Theroux MC, Dabney KW, Shah SA, Miller F, Akins RE (2013) Disruption of basal lamina components in neuromotor synapses of children with spastic quadriplegic cerebral palsy. PLoS One 8:e70288CrossRefGoogle Scholar
  49. Roche N, Pradon D, Cosson J, Robertson J, Marchiori C, Zory R (2014) Categorization of gait patterns in adults with cerebral palsy: a clustering approach. Gait Posture 39:235–240CrossRefGoogle Scholar
  50. Ross SA, Engsberg JR (2002) Relation between spasticity and strength in individuals with spastic diplegic cerebral palsy. Dev Med Child Neurol 44:148–157CrossRefGoogle Scholar
  51. Shikako-Thomas K, Dahan-Oliel N, Shevell M, Law M, Birnbaum R, Rosenbaum P, Poulin C, Majnemer A (2012) “Play and be happy? Leisure participation and quality of life in school-aged children with cerebral palsy.” Int J Pediatr 2012:387280CrossRefGoogle Scholar
  52. Shortland AP, Harris CA, Gough M, Robinson RO (2002) Architecture of the medial gastrocnemius in children with spastic diplegia. Dev Med Child Neurol 44:158–163CrossRefGoogle Scholar
  53. Shortland AP, Fry NR, Eve LC, Gough M (2004) Changes to medial gastrocnemius architecture after surgical intervention in spastic diplegia. Dev Med Child Neurol 46:667–673CrossRefGoogle Scholar
  54. Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL (2011) Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. J Physiol 589:2625–2639CrossRefGoogle Scholar
  55. Spector SA, Simard CP, Fournier M, Sternlicht E, Edgerton VR (1982) Architectural alterations of rat hind-limb skeletal muscles immobilized at different lengths. Exp Neurol 76:94–110CrossRefGoogle Scholar
  56. Stackhouse SK, Binder-Macleod SA, Lee SC (2005) Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 31:594–601CrossRefGoogle Scholar
  57. Taylor NF, Dodd KJ, Baker RJ, Willoughby K, Thomason P, Graham HK (2013) Progressive resistance training and mobility-related function in young people with cerebral palsy: a randomized controlled trial. Dev Med Child Neurol 55:806–812CrossRefGoogle Scholar
  58. Theroux MC, Oberman KG, Lahaye J, Boyce BA, Duhadaway D, Miller F, Akins RE (2005) Dysmorphic neuromuscular junctions associated with motor ability in cerebral palsy. Muscle Nerve 32:626–632CrossRefGoogle Scholar
  59. Vieira TM, Botter A, Minetto MA, Hodson-Tole EF (2015) Spatial variation of compound muscle action potentials across human gastrocnemius medialis. J Neurophysiol 114:1617–1627CrossRefGoogle Scholar
  60. Wakahara T, Kanehisa H, Kawakami Y, Fukunaga T (2007) Fascicle behavior of medial gastrocnemius muscle in extended and flexed knee positions. J Biomech 40:2291–2298CrossRefGoogle Scholar
  61. Willerslev-Olsen M, Lorentzen J, Sinkjaer T, Nielsen JB (2013) Passive muscle properties are altered in children with cerebral palsy before the age of 3 years and are difficult to distinguish clinically from spasticity. Dev Med Child Neurol 55:617–623CrossRefGoogle Scholar
  62. Willerslev-Olsen M, Lorentzen J, Nielsen JB (2014) Gait training reduces ankle joint stiffness and facilitates heel strike in children with cerebral palsy. NeuroRehabilitation 35:643–655Google Scholar
  63. Williams PE, Goldspink G (1973) The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat 116:45–55Google Scholar
  64. Winter DA (1983) Energy generation and absorption at the ankle and knee during fast, natural, and slow cadences. Clin Orthop Relat Res: 147–154Google Scholar
  65. Wren TA, Cheatwood AP, Rethlefsen SA, Hara R, Perez FJ, Kay RM (2010) Achilles tendon length and medial gastrocnemius architecture in children with cerebral palsy and equinus gait. J Pediatr Orthop 30:479–484CrossRefGoogle Scholar
  66. Zhao H, Ren Y, Wu YN, Liu SQ, Zhang LQ (2009) Ultrasonic evaluations of Achilles tendon mechanical properties poststroke. J Appl Physiol (1985) 106:843–849CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of NeuroscienceUniversity of CopenhagenCopenhagen NDenmark
  2. 2.Professionshøjskolen AbsalonRoskildeDenmark
  3. 3.Elsass InstituteCharlottenlundDenmark
  4. 4.School of Health, Medical and Allied SciencesCentral Queensland UniversityBundabergAustralia
  5. 5.Child Health Research Centre, Faculty of MedicineThe University of QueenslandBrisbaneAustralia

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