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      Resistance Training Combined With Stretching Increases Tendon Stiffness and Is More Effective Than Stretching Alone in Children With Cerebral Palsy: A Randomized Controlled Trial

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          Abstract

          Aim: Stretching is often used to increase/maintain muscle length and improve joint range of motion (ROM) in children with cerebral palsy (CP). However, outcomes at the muscle (remodeling) and resulting function appear to be highly variable and often unsatisfactory. During passive joint rotation, the Achilles tendon lengthens more than the in-series medial gastrocnemius muscle in children with CP, which might explain the limited effectiveness of stretching interventions. We aimed to ascertain whether increasing tendon stiffness, by performing resistance training, improves the effectiveness of passive stretching, indicated by an increase in medial gastrocnemius fascicle length.

          Methods: Sixteen children with CP (Age median [IQR]: 9.6 [8.6, 10.5]) completed the study. Children were randomly assigned to a combined intervention of stretching and strengthening of the calf muscles ( n = 9) or a control (stretching-only) group ( n = 7). Medial gastrocnemius fascicle length at a resting ankle angle, lengthening during passive joint rotations, and tendon stiffness were assessed by combining dynamometry and ultrasound imaging. The study was registered on clinicaltrials.gov (NCT02766491).

          Results: Resting fascicle length and tendon stiffness increased more in the intervention group compared to the control group (median [95% CI] increase fascicle length: 2.2 [1.3, 4.3] mm; stiffness: 13.6 [9.9, 17.7] N/mm) Maximum dorsiflexion angle increased equally in both groups.

          Conclusion: This study provides proof of principle that a combined resistance and stretching intervention can increase tendon stiffness and muscle fascicle length in children with CP. This demonstrates that remodeling of muscle structure is possible with non-invasive interventions in spastic CP.

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          Most cited references54

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          A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture.

          1. In human pennate muscle, changes in anatomical cross-sectional area (CSA) or volume caused by training or inactivity may not necessarily reflect the change in physiological CSA, and thereby in maximal contractile force, since a simultaneous change in muscle fibre pennation angle could also occur. 2. Eleven male subjects undertook 14 weeks of heavy-resistance strength training of the lower limb muscles. Before and after training anatomical CSA and volume of the human quadriceps femoris muscle were assessed by use of magnetic resonance imaging (MRI), muscle fibre pennation angle (theta(p)) was measured in the vastus lateralis (VL) by use of ultrasonography, and muscle fibre CSA (CSA(fibre)) was obtained by needle biopsy sampling in VL. 3. Anatomical muscle CSA and volume increased with training from 77.5 +/- 3.0 to 85.0 +/- 2.7 cm(2) and 1676 +/- 63 to 1841 +/- 57 cm(3), respectively (+/- S.E.M.). Furthermore, VL pennation angle increased from 8.0 +/- 0.4 to 10.7 +/- 0.6 deg and CSA(fibre) increased from 3754 +/- 271 to 4238 +/- 202 microm (2). Isometric quadriceps strength increased from 282.6 +/- 11.7 to 327.0 +/- 12.4 N m. 4. A positive relationship was observed between theta(p) and quadriceps volume prior to training (r = 0.622). Multifactor regression analysis revealed a stronger relationship when theta(p) and CSA(fibre) were combined (R = 0.728). Post-training increases in CSA(fibre) were related to the increase in quadriceps volume (r = 0.749). 5. Myosin heavy chain (MHC) isoform distribution (type I and II) remained unaltered with training. 6. VL muscle fibre pennation angle was observed to increase in response to resistance training. This allowed single muscle fibre CSA and maximal contractile strength to increase more (+16 %) than anatomical muscle CSA and volume (+10 %). 7. Collectively, the present data suggest that the morphology, architecture and contractile capacity of human pennate muscle are interrelated, in vivo. This interaction seems to include the specific adaptation responses evoked by intensive resistance training.
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            Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length.

            Cerebral palsy (CP) results from an upper motoneuron (UMN)lesion in the developing brain. Secondary to the UMNl esion,which causes spasticity, is a pathological response by muscle - namely, contracture. However, the elements within muscle that increase passive mechanical stiffness, and therefore result in contracture, are unknown. Using hamstring muscle biopsies from pediatric patients with CP (n =33) and control (n =19) patients we investigated passive mechanical properties at the protein, cellular, tissue and architectural levels to identify the elements responsible for contracture. Titin isoform, the major load-bearing protein within muscle cells, was unaltered in CP. Correspondingly, the passive mechanics of individual muscle fibres were not altered. However, CP muscle bundles, which include fibres in their constituent ECM, were stiffer than control bundles. This corresponded to an increase in collagen content of CP muscles measured by hydroxyproline assay and observed using immunohistochemistry. In vivo sarcomere length of CP muscle measured during surgery was significantly longer than that predicted for control muscle. The combination of increased tissue stiffness and increased sarcomere length interact to increase stiffness greatly of the contracture tissue in vivo. These findings provide evidence that contracture formation is not the result of stiffening at the cellular level, but stiffening of the ECM with increased collagen and an increase of in vivo sarcomere length leading to higher passive stresses.
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              Effect of strength training on human patella tendon mechanical properties of older individuals.

              This study investigated the effect of strength training on the mechanical properties of the human patella tendon of older individuals. Subjects were assigned to training (n = 9; age 74.3 +/- 3.5 years, body mass 69.7 +/- 14.8 kg and height 163.4 +/- 9.1 cm, mean +/- S.D.) and control (n = 9; age 67.1 +/- 2 years, body mass 73.5 +/- 14.9 kg and height 168.3 +/- 11.5 cm) groups. Strength training (two series of 10 repetitions at 80 % of five-repetition maximum) was performed three times per week for 14 weeks using leg extension and leg press exercises. Measurements of tendon elongation during a ramp isometric knee extension were performed before and after training and control periods in vivo using ultrasonography. Training caused a decreased tendon elongation and strain at all levels of force and stress (P 0.05). This study shows for the first time that strength training in old age increases the stiffness and Young's modulus of human tendons. This may reduce the risk of tendon injury in old age and has implications for contractile force production and the rapid execution of motor tasks.
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                Author and article information

                Contributors
                Journal
                Front Pediatr
                Front Pediatr
                Front. Pediatr.
                Frontiers in Pediatrics
                Frontiers Media S.A.
                2296-2360
                13 August 2019
                2019
                : 7
                : 333
                Affiliations
                [1] 1INSIGNEO Institute for in silico Medicine, University of Sheffield , Sheffield, United Kingdom
                [2] 2Alder Hey Children's NHS Foundation Trust , Liverpool, United Kingdom
                [3] 3Department of Rehabilitation Medicine, Amsterdam Movement Sciences, Vrije Universiteit Amsterdam , Amsterdam, Netherlands
                [4] 4Department of Rehabilitation Sciences, Katholieke Universiteit Leuven , Leuven, Belgium
                [5] 5Research Institute for Sport and Exercise Science, Liverpool John Moores University , Liverpool, United Kingdom
                Author notes

                Edited by: Ulf Kessler, Universitätsklinik für Kinderchirurgie, Kinderklinik, Universitätsspital Bern, Switzerland

                Reviewed by: Christopher I. Morse, Manchester Metropolitan University, United Kingdom; Joanna Diong, University of Sydney, Australia; Huub Maas, Vrije Universiteit Amsterdam, Netherlands

                *Correspondence: Barbara M. Kalkman b.kalkman@ 123456sheffield.ac.uk

                This article was submitted to Pediatric Orthopedics, a section of the journal Frontiers in Pediatrics

                Article
                10.3389/fped.2019.00333
                6700382
                b1898e59-21b2-48c3-85f4-c83596b2920c
                Copyright © 2019 Kalkman, Holmes, Bar-On, Maganaris, Barton, Bass, Wright, Walton and O'Brien.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 March 2019
                : 24 July 2019
                Page count
                Figures: 3, Tables: 4, Equations: 0, References: 55, Pages: 10, Words: 7926
                Funding
                Funded by: Engineering and Physical Sciences Research Council 10.13039/501100000266
                Award ID: EP/K03877X/1
                Funded by: Nederlandse Organisatie voor Wetenschappelijk Onderzoek 10.13039/501100003246
                Award ID: 016.186.144
                Funded by: Fonds Wetenschappelijk Onderzoek 10.13039/501100003130
                Award ID: 12R4215N
                Categories
                Pediatrics
                Clinical Trial

                stretching,cerebral palsy,fascicle,ultrasound,tendon,stiffness
                stretching, cerebral palsy, fascicle, ultrasound, tendon, stiffness

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