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Research Article| Volume 40, P270-282, January 2023

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Quantifying muscle strength, size, and neuromuscular activation in adolescent and young adult survivors of musculoskeletal sarcoma: Identifying correlates and responses to functional strengthening

Published:December 16, 2022DOI:https://doi.org/10.1016/j.knee.2022.11.024

      Abstract

      Background

      Medical and surgical treatment for musculoskeletal sarcoma (MSS) place survivors at risk for impairments in muscle properties including muscle strength, muscle size, and neuromuscular activation. The purpose of this study was to explore muscle properties, gross motor performance, and quality of life (QoL) and the changes in response to a 6-week functional strengthening intervention (PT-STRONG) in MSS survivors of childhood cancer (CCS).

      Methods

      Eight lower extremity MSS CCS (13–23 years old) performed baseline testing and three completed PT-STRONG. Participants completed measurements of knee extension strength using handheld dynamometry, vastus lateralis (VL) and rectus femoris (RF) muscle thickness using ultrasonography at rest, and neuromuscular activation using electromyography during strength testing and a step-up task. Participants also completed gross motor and QoL assessments.

      Results

      Compared with the non-surgical limb, MSS CCS had lower surgical limb knee extension strength, VL muscle thickness, and RF step-up muscle rate of activation (RoA). Compared with normative values, MSS CCS had decreased bilateral knee extension strength, gross motor performance, and physical QoL. Positive correlations among muscle strength, muscle thickness, and gross motor performance were identified. After PT-STRONG, MSS CCS had improvements in VL muscle thickness, VL and RF RoA duing step-up, gross motor performance, and physical QoL.

      Conclusions

      Positive association between larger muscle thickness with greater knee extension strength, and higher knee extension strength with better gross motor performance indicate that comprehensive physical therapy assessment and interventions that identify and target impairments in muscle properties to guide clinical decision making should be considered for MSS CCS into survivorship.

      Keywords

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      References

        • Heare T.
        • Hensley M.A.
        • Dell’Orfano S.
        Bone tumors: Osteosarcoma and Ewing’s sarcoma.
        Curr Opin Pediatr. 2009; 21: 365-372https://doi.org/10.1097/MOP.0b013e32832b1111
        • Siegel R.L.
        • Miller K.D.
        • Jemal A.
        Cancer statistics, 2019.
        CA Cancer J Clin. 2019; 69: 7-34https://doi.org/10.3322/caac.21551
        • Gorlick R.
        • Janeway K.
        • Lessnick S.
        • Randall R.L.
        • Marina N.
        Children’s Oncology Group’s 2013 blueprint for research: Bone tumors.
        Pediatr Blood Cancer. 2013; 60: 1009-1015https://doi.org/10.1002/pbc
        • Tsauo J.Y.
        • Li W.C.
        • Yang R.S.
        Functional outcomes after endoprosthetic knee reconstruction following resection of osteosarcoma near the knee.
        Disabil Rehabil. 2006; 28: 61-66https://doi.org/10.1080/09638280500164008
        • Beebe K.
        • Song K.J.
        • Ross E.
        • Tuy B.
        • Patterson F.
        • Benevenia J.
        Functional outcomes after limb-salvage surgery and endoprosthetic reconstruction with an expandable prosthesis: A report of 4 cases.
        Arch Phys Med Rehabil. 2009; 90: 1039-1047https://doi.org/10.1016/j.apmr.2008.12.025
        • Corr A.M.
        • Liu W.
        • Bishop M.
        • Pappo A.
        • Srivastava D.K.
        • Neel M.
        • et al.
        Feasibility and functional outcomes of children and adolescents undergoing preoperative chemotherapy prior to a limb-sparing procedure or amputation.
        Rehabil Oncol. 2017; 35: 38-45https://doi.org/10.1097/01.REO.0000000000000050
        • Fernandez-Pineda I.
        • Hudson M.M.
        • Pappo A.S.
        • Bishop M.W.
        • Klosky J.L.
        • Brinkman T.M.
        • et al.
        Long-term functional outcomes and quality of life in adult survivors of childhood extremity sarcomas: a report from the St. Jude Lifetime Cohort Study.
        J Cancer Surviv. 2017; 11: 1-12https://doi.org/10.1007/s11764-016-0556-1
        • Carty C.P.
        • Bennett M.B.
        • Dickinson I.C.
        • Steadman P.
        Electromyographic assessment of gait function following limb salvage procedures for bone sarcoma.
        J Electromyogr Kinesiol. 2010; 20: 502-507https://doi.org/10.1016/j.jelekin.2009.06.001
        • Carty C.P.
        • Dickinson I.C.
        • Watts M.C.
        • Crawford R.W.
        • Steadman P.
        Impairment and disability following limb salvage procedures for bone sarcoma.
        Knee. 2009; 16: 405-408https://doi.org/10.1016/j.knee.2009.02.006
        • Ginsberg J.P.
        • Rai S.N.
        • Carlson C.
        • Meadows A.T.
        • Hinds P.S.
        • Spearing E.M.
        • et al.
        A comparative analysis of functional outcomes in adolescents and young adults with lower-extremity bone sarcoma.
        Pediatr Blood Cancer. 2007; 49: 964-969https://doi.org/10.1002/pbc
        • Bekkering W.P.
        • van Egmond-van Dam J.C.
        • Bramer J.A.M.
        • Beishuizen A.
        • Fiocco M.
        • Dijkstra P.D.S.
        Quality of life after bone sarcoma surgery around the knee: A long-term follow-up study.
        Eur J Cancer Care (Engl). 2017; 26: 1-9https://doi.org/10.1111/ecc.12603
        • Carty C.P.
        • Bennett M.B.
        • Dickinson I.C.
        • Steadman P.
        Assessment of kinematic and kinetic patterns following limb salvage procedures for bone sarcoma.
        Gait Posture. 2009; 30: 547-551https://doi.org/10.1016/j.gaitpost.2009.08.234
        • Marchese V.G.
        • Spearing E.
        • Callaway L.
        • Rai S.N.
        • Zhang L.
        • Hinds P.S.
        • et al.
        Relationships among range of motion, functional mobility, and quality of life in children and adolescents after limb-sparing surgery for lower-extremity sarcoma.
        Pediatr Phys Ther. 2006; 18: 238-244https://doi.org/10.1097/01.pep.0000232620.42407.9f
        • Nagarajan R.
        • Kamruzzaman A.
        • Ness K.K.
        • Marchese V.G.
        • Sklar C.
        • Mertens A.
        • et al.
        Twenty years of follow-up of survivors of childhood osteosarcoma.
        Cancer. 2011; 117: 625-634https://doi.org/10.1002/cncr.25446
        • Bekkering W.P.
        • Vliet Vieland T.P.
        • Kooperman H.M.
        • Schaap G.R.
        • Schreuder H.W.B.
        • Beishuizen A.
        • et al.
        Functional ability and physical activity in children and young adults after limb-salvage or ablative surgery for lower extremity bone tumors.
        J Surg Oncol. 2011; 103: 276-282https://doi.org/10.1002/jso
        • Ness K.K.
        • Mertens A.C.
        • Hudson M.M.
        • Wall M.M.
        • Leisenring W.M.
        • Oeffinger K.C.
        • et al.
        Limitations on physical performance and daily activities among long-term survivors of childhood cancer.
        Ann Intern Med. 2005; 143: 639-648https://doi.org/10.7326/0003-4819-143-9-200511010-00007
        • Bekkering W.P.
        • Vliet Vieland T.P.
        • Kooperman H.M.
        • Schapp G.R.
        • Beishuizen A.
        • Anninga J.K.
        • et al.
        A prospective study on quality of life and functional outcome in children and adolescents after malignant bone tumor surgery.
        Pediatr Blood Cancer. 2012; 58: 978-985https://doi.org/10.1002/pbc
        • Bekkering W.P.
        • Vliet Vieland T.P.
        • Kooperman H.M.
        • Schaap G.R.
        • Schreuder H.W.B.
        • Beishuizen A.
        • et al.
        Quality of life in young patients after bone tumor surgery around the knee joint and comparison with healthy controls.
        Pediatr Blood Cancer. 2010; 54: 738-745https://doi.org/10.1002/pbc
        • Nagarajan R.
        • Clohisy D.R.
        • Neglia J.P.
        • Yasui Y.
        • Mitby P.A.
        • Sklar C.
        • et al.
        Function and quality-of-life of survivors of pelvic and lower extremity osteosarcoma and Ewing’s sarcoma: The Childhood Cancer Survivor Study.
        Br J Cancer. 2004; 91: 1858-1865https://doi.org/10.1038/sj.bjc.6602220
        • Hudson M.M.
        • Mertens A.C.
        • Yasui Y.
        • Hobbie W.
        • Chen H.
        • Gurney J.G.
        • et al.
        Health status of adult long-term survivors of childhood cancer: A report from the Childhood Cancer Survivor Study.
        J Am Med Assoc. 2003; 290: 1583-1592https://doi.org/10.1001/jama.290.12.1583
        • Marina N.
        • Hudson M.M.
        • Jones K.E.
        • Mulrooney D.A.
        • Avedian R.
        • Donaldson S.S.
        • et al.
        Changes in health status among aging survivors of pediatric upper and lower extremity sarcoma: A report from the childhood cancer survivor study.
        Arch Phys Med Rehabil. 2013; 94: 1062-1073https://doi.org/10.1016/j.apmr.2013.01.013
        • Oeffinger K.C.
        • Mertens A.C.
        • Sklar C.A.
        • Kawashima T.
        • Hudson M.M.
        • Meadows A.T.
        • et al.
        Chronic health conditions in adult survivors of childhood cancer.
        New Engl J Med. 2006; 355: 1572-1582https://doi.org/10.1056/NEJMsa060185
        • Wilson C.
        • Gawade P.
        • Ness K.
        Impairments that influence physical function among survivors of childhood cancer.
        Children. 2015; 2: 1-36https://doi.org/10.3390/children2010001
        • Gilchrist L.
        • Tanner L.
        Gait patterns in children with cancer and vincristine neuropathy.
        Pediatr Phys Ther. 2016; 28: 16-22https://doi.org/10.1097/PEP.0000000000000208
        • Mizrahi D.
        • Fardell J.E.
        • Cohn R.J.
        • Partin R.E.
        • Howell C.R.
        • Hudson M.M.
        • et al.
        The 6-minute walk test is a good predictor of cardiorespiratory fitness in childhood cancer survivors when access to comprehensive testing is limited.
        Int J Cancer. 2020; 147: 847-855https://doi.org/10.1002/ijc.32819
        • Levin A.S.
        • Arkader A.
        • Morris C.D.
        Reconstruction following tumor resections in skeletally immature patients.
        J Am Acad Orthop Surg. 2017; 25: 204-213https://doi.org/10.5435/JAAOS-D-15-00619
        • Shehadeh A.
        • el Dahleh M.
        • Salem A.
        • Sarhan Y.
        • Sultan I.
        • Henshaw R.M.
        • et al.
        Standardization of rehabilitation after limb salvage surgery for sarcomas improves patients’ outcome.
        Hematol Oncol Stem Cell Ther. 2013; 6: 105-111https://doi.org/10.1016/j.hemonc.2013.09.001
        • Gilliam L.A.A.
        • St. Clair D.K.
        Chemotherapy-induced weakness and fatigue in skeletal muscle: The role of oxidative stress.
        Antioxid Redox Signal. 2011; 15: 2543-2563https://doi.org/10.1089/ars.2011.3965
        • Van Norren K.
        • Van Helvoort A.
        • Argilés J.M.
        • Van Tuijl S.
        • Arts K.
        • Gorselink M.
        • et al.
        Direct effects of doxorubicin on skeletal muscle contribute to fatigue.
        Br J Cancer. 2009; 100: 311-314https://doi.org/10.1038/sj.bjc.6604858
        • Marchese V.
        • Rock K.
        • York T.
        • Creath R.
        • Gray V.
        Neuromuscular mechanisms that contribute to gross motor performance in survivors of childhood acute lymphoblastic leukemia.
        J Pediatr Rehabil Med. 2021; 14: 415-423https://doi.org/10.3233/PRM-200784
        • Marchese V.
        • Rock K.
        • York T.
        • Ruble K.
        • Gray V.L.
        The efficacy of targeted exercise on gross motor and neuromuscular performance in survivors of childhood leukemia: A pilot study.
        Front Pediatr. 2022; 10: 4-11https://doi.org/10.3389/fped.2022.891650
        • Davidson B.S.
        • Judd D.L.
        • Thomas A.C.
        • Mizner R.L.
        • Eckhoff D.G.
        • Stevens-Lapsley J.E.
        Muscle activation and coactivation during five-time-sit-to-stand movement in patients undergoing total knee arthroplasty.
        J Electromyogr Kinesiol. 2013; 23: 1485-1493https://doi.org/10.1016/j.jelekin.2013.06.008
        • Farahmand F.
        • Senavongse W.
        • Amis A.A.
        Quantitative study of the quadriceps muscles and trochlear groove geometry related to instability of the patellofemoral joint.
        J Orthop Res. 1998; 16: 136-143https://doi.org/10.1002/jor.1100160123
      1. Bordoni B, Varacallo M. Anatomy, Bony Pelvis and Lower Limb, Thigh Quadriceps Muscle; 2022.

        • Rock K.
        • Nelson C.
        • Addison O.
        • Marchese V.
        Assessing the reliability of handheld dynamometry and ultrasonography to measure quadriceps strength and muscle thickness in children, adolescents, and young adults.
        Phys Occup Ther Pediatr. 2021; 41: 540-554https://doi.org/10.1080/01942638.2021.1881200
        • van den Beld W.A.
        • van der Sanden G.A.C.
        • Sengers R.C.A.
        • Verbeek A.L.M.
        • Gabreëls F.J.M.
        Validity and reproducibility of hand-held dynamometry in children aged 4–11 years.
        J Rehabil Med. 2006; 38: 57-64https://doi.org/10.1080/16501970510044043
        • Moreau N.G.
        • Simpson K.N.
        • Teefey S.A.
        • Damiano D.L.
        Muscle architecture predicts maximum strength and is related to activity levels in cerebral palsy.
        Phys Ther. 2010; 90: 1619-1630https://doi.org/10.2522/ptj.20090377
      2. Nelson CM, Marchese V, Rock K, Henshaw RM, Addison O, Nelson CM. Alterations in muscle architecture: A review of the relevance to individuals after limb salvage surgery for bone sarcoma 2020;8:1–10. https://doi.org/10.3389/fped.2020.00292.

        • Shelly A.
        • Davis E.
        • Waters E.
        • Mackinnon A.
        • Reddihough D.
        • Boyd R.
        • et al.
        The relationship between quality of life and functioning for children with cerebral palsy.
        Dev Med Child Neurol. 2008; 50: 199-203https://doi.org/10.1111/j.1469-8749.2008.02031.x
        • Winter C.C.
        • Müller C.
        • Hardes J.
        • Gosheger G.
        • Boos J.
        • Rosenbaum D.
        The effect of individualized exercise interventions during treatment in pediatric patients with a malignant bone tumor.
        Support Care Cancer. 2013; 21: 1629-1636https://doi.org/10.1007/s00520-012-1707-1
        • Wyon M.A.
        • Smith A.
        • Koutedakis Y.
        A comparison of strength and stretch interventions on active and passive ranges of movement in dancers: A randomized controlled trial.
        J Strength Cond Res. 2013; 27: 3053-3059https://doi.org/10.1519/JSC.0b013e31828a4842
        • Katoh M.
        Reliability of isometric knee extension muscle strength measurements made by a hand-held dynamometer and a belt: A comparison of two types of device.
        J Phys Ther Sci. 2015; 27: 851-854https://doi.org/10.1589/jpts.27.851
        • Walsworth M.
        • Schneider R.
        • Schultz J.
        • Dahl C.
        • Allison S.
        • Underwood F.
        • et al.
        Prediction of 10 repetition maximum for short-arc quadriceps exercise from hand-held dynomometer and anthropometric measurements.
        J Orthop Sports Phys Ther. 1998; 28: 97-104
        • Eek M.N.
        • Kroksmark A.K.
        • Beckung E.
        Isometric muscle torque in children 5 to 15 years of age: Normative data.
        Arch Phys Med Rehabil. 2006; 87: 1091-1099https://doi.org/10.1016/j.apmr.2006.05.012
        • Babault N.
        • Pousson M.
        • Michaut A.
        • van Hoecke J.
        Effect of quadriceps femoris muscle length on neural activation during isometric and concentric contractions.
        J Appl Physiol. 2003; 94: 983-990https://doi.org/10.1152/japplphysiol.00717.2002
        • Lanza M.B.
        • Rock K.
        • Marchese V.
        • Addison O.
        • Gray V.L.
        Hip abductor and adductor rate of torque development and muscle activation, but not muscle size, are associated with functional performance.
        Front Physiol. 2021; 12744153https://doi.org/10.3389/fphys.2021.744153
        • Katsavelis D.
        • Threlkeld A.J.
        Quantifying thigh muscle co-activation during isometric knee extension contractions: Within- and between-session reliability.
        J Electromyogr Kinesiol. 2014; 24: 502-507https://doi.org/10.1016/j.jelekin.2014.04.004. Quantifying
        • Onishi H.
        • Yagi R.
        • Oyama M.
        • Akasaka K.
        • Ihashi K.
        • Handa Y.
        EMG-angle relationship of the hamstring muscles during maximum knee flexion.
        J Electromyogr Kinesiol. 2002; 12: 399-406https://doi.org/10.1016/S1050-6411(02)00033-0
        • Falconer K.
        • Winter D.A.
        Quantitative assessment of co-contraction at the ankle joint in walking.
        Electromyogr Clin Neurophysiol. 1985; 25: 135-149
        • Banks C.L.
        • Huang H.J.
        • Little V.L.
        • Patten C.
        Electromyography exposes heterogeneity in muscle co-contraction following stroke.
        Front Neurol. 2017; 8: 1-11https://doi.org/10.3389/fneur.2017.00699
        • Marchese V.G.
        • Rai S.N.
        • Carlson C.A.
        • Hinds P.S.
        • Spearing E.M.
        • Zhang L.
        • et al.
        Assessing functional mobility in survivors of lower-extremity sarcoma: Reliability and validity of a new assessment tool.
        Pediatr Blood Cancer. 2007; 49: 183-189https://doi.org/10.1002/pbc.20932
        • Marchese V.G.
        • Oriel K.N.
        • Fry J.A.
        • Kovacs J.L.
        • Weaver R.L.
        • Reilly M.M.
        • et al.
        Development of reference values for the functional mobility assessment.
        Pediatr Phys Ther. 2012; 24: 224-230https://doi.org/10.1097/PEP.0b013e31825c87e7
        • Nicolini-Panisson R.D.
        • Donadio M.V.F.
        Timed “Up & Go” test in children and adolescents.
        Rev Paul Pediatr. 2013; 31: 377-383https://doi.org/10.1590/s0103-05822013000300016
      3. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: Guidelines for the six-minute walk test. Am J Respir Crit Care Med 2002;166:111–7. https://doi.org/10.1164/ajrccm.166.1.at1102.

        • Zaino C.A.
        • Marchese V.G.
        • Westcott S.L.
        Timed up and down stairs test: Preliminary reliability and validity of a new measure of functional mobility.
        Pediatr Phys Ther. 2004; 16: 90-98https://doi.org/10.1097/01.PEP.0000127564.08922.6A
        • Williams E.N.
        • Carroll S.G.
        • Reddihough D.S.
        • Phillips B.A.
        • Galea M.P.
        Investigation of the timed ‘Up & Go’ test in children.
        Dev Med Child Neurol. 2005; 47: 518-524https://doi.org/10.1017/S0012162205001027
      4. Borg G. Borg’s perceived exertion and pain scales. Champaign, IL, US: Human Kinetics; 1998.

      5. Ware JE, Snow KK, Kosinski M, Gandek B. SF-36 Health Survey Manual and Interpretation Guide. Lincoln: Quality Metric Inc; 2000.

        • Beenakker E.A.C.
        • van der Hoeven J.H.
        • Fock J.M.
        • Maurits N.M.
        Reference values of maximum isometric muscle force obtained in 270 children aged 4–16 years by hand-held dynamometry.
        Neuromusc Disord. 2001; 11: 441-446https://doi.org/10.1016/S0960-8966(01)00193-6
        • Haley S.M.
        • Fragala-pinkham M.A.
        Interpreting change scores of tests and measures used in physical therapy.
        Phys Ther. 2006; 86: 735-743
        • Kao Y.-C.
        • Owosho A.A.
        • Sung Y.-S.
        • Zhang L.
        • Fujisawa Y.
        • Lee J.-C.
        • et al.
        BCOR-CCNB3 Fusion positive sarcomas: A clinicopathologic and molecular analysis of 36 cases with comparison to morphologic spectrum and clinical behavior of other round cell sarcomas.
        Am J Surg Pathol. 2018; 42: 604-615https://doi.org/10.1097/PAS.0000000000000965
        • Moreau N.G.
        • Teefey S.A.
        • Damiano D.L.
        In vivo muscle architecture and size of the rectus femoris and vastus lateralis in children and adolescents with cerebral palsy.
        Dev Med Child Neurol. 2009; 51: 800-806https://doi.org/10.1111/j.1469-8749.2009.03307.x
        • Kitsuda Y.
        • Tanimura C.
        • Inoue K.
        • Park D.
        • Osaki M.
        • Hagino H.
        Effectiveness of ultrasonographic skeletal muscle assessment in patients after total knee arthroplasty.
        Osteoporos Sarcopenia. 2019; 5: 94-101https://doi.org/10.1016/j.afos.2019.09.002
        • Gellhorn A.C.
        • Stumph J.M.
        • Zikry H.E.
        • Creelman C.A.
        • Welbel R.
        Ultrasound measures of muscle thickness may be superior to strength testing in adults with knee osteoarthritis: A cross-sectional study.
        BMC Musculoskelet Disord. 2018; 19: 1-8https://doi.org/10.1186/s12891-018-2267-4
        • Okita Y.
        • Tatematsu N.
        • Nagai K.
        • Nakayama T.
        • Nakamata T.
        • Okamoto T.
        • et al.
        The effect of walking speed on gait kinematics and kinetics after endoprosthetic knee replacement following bone tumor resection.
        Gait Posture. 2014; 40: 622-627https://doi.org/10.1016/j.gaitpost.2014.07.012
        • Arnold C.M.
        • Faulkner R.A.
        The history of falls and the association of the timed up and go test to falls and near-falls in older adults with hip osteoarthritis.
        BMC Geriatr. 2007; 7: 1-9https://doi.org/10.1186/1471-2318-7-17
        • Marchese V.G.
        • Chiarello L.A.
        • Lange B.J.
        Effects of physical therapy intervention for children with acute lymphoblastic leukemia.
        Pediatr Blood Cancer. 2004; 42: 127-133https://doi.org/10.1002/pbc.10481
        • Stössel S.
        • Neu M.A.
        • Wingerter A.
        • Bloch W.
        • Zimmer P.
        • Paret C.
        • et al.
        Benefits of exercise training for children and adolescents undergoing cancer treatment: Results from the randomized controlled MUCKI trial.
        Front Pediatr. 2020; 8: 1-10https://doi.org/10.3389/fped.2020.00243
        • Weppler C.H.
        • Magnusson S.P.
        Increasing muscle extensibility: A matter of increasing length or modifying sensation?.
        Phys Ther. 2010; 90: 438-449https://doi.org/10.2522/ptj.20090012
        • Mones H.M.
        • Hassan M.K.
        • Ahmed B.A.A.H.
        Health-related quality of life of adolescents with sickle cell disease on hydroxyurea: A case–control study.
        J Appl Hematol. 2022; 13: 13-21https://doi.org/10.4103/joah.joah_7_21