Abstract
Muscle contracture development is a major complication for individuals with cerebral palsy (CP) and has lifelong implications. In order to recognize contracture development early and to follow up on preventive interventions aimed at muscle health development, non-invasive, and easy to use methods are needed. The aim of the present study was to assess whether multi-frequency Bioimpedance (mfBIA) can be used to detect differences between skeletal muscle of individuals with CP and healthy controls. The mfBIA technique was applied to the medial gastrocnemius muscle of n = 24 adults with CP and n = 20 healthy controls of both genders. The phase angle (PA) and the centre frequency (fc) were significantly lower in individuals with CP when compared to controls; PA: − 25% for women and − 31.8% for men (P < 0.0001); fc: − 5.6% for women and − 5.2% for men (P < 0.009). The reactance (Xc) and the extracellular resistance (Re) of skeletal muscle from individuals with CP were significantly higher when compared to controls; Xc: + 9.9% for women and + 28.9% for men (P < 0.0001); Re: + 39.7% for women and + 91.2% for men (P < 0.0001). The present study shows that several mfBIA parameters differ significantly between individuals with CP and healthy controls. Furthermore, these changes correlated significantly with the severity of CP, as assessed using the GMFCS scale. The present data indicate that mfBIA shows promise in terms of being a useful diagnostic tool, capable of characterizing muscle health and its development in individuals with cerebral palsy.
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References
Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G (2011) Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy. Dev Med Child Neurol 53(6):543–548. https://doi.org/10.1111/j.1469-8749.2011.03913.x
Bartels EM, Sorensen ER, Harrison AP (2015) Multi-frequency bioimpedance in human muscle assessment. Physiol Rep. https://doi.org/10.14814/phy2.12354
Bartels EM, Andersen EL, Olsen JK, Kristensen LE, Bliddal H, Danneskiold-Samsoe B, Harrison AP (2019) Muscle assessment using multi-frequency bioimpedance in a healthy Danish population aged 20–69 years: a powerful non-invasive tool in sports and in the clinic. Physiol Rep 7(11):e14109. https://doi.org/10.14814/phy2.14109
Bartels EM, Korbo L, Harrison AP (2020) Novel insights into cerebral palsy. J Muscle Res Cell Motil. https://doi.org/10.1007/s10974-020-09577-4
Bonaldo P, Sandri M (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Models Mech 6(1):25–39
Booth CM, Cortina-Borja MJ, Theologis TN (2001) Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol 43(5):314–320
Buratti P, Covatti C, Centenaro LA, Brancalhao RMC, Torrejais MM (2019) Morphofunctional characteristics of skeletal muscle in rats with cerebral palsy. Int J Exp Pathol 100(1):49–59
Colver A, Fairhurst C, Pharoah PO (2014) Cerebral palsy. Lancet 383(9924):1240–1249. https://doi.org/10.1016/s0140-6736(13)61835-8
Gillett JG, Lichtwark GA, Boyd RN, Barber LA (2018) Functional capacity in adults with cerebral palsy: lower limb muscle strength matters. Arch Phys Med Rehabil 99(5):900–906 e901. https://doi.org/10.1016/j.apmr.2018.01.020
Graham HK, Rosenbaum P, Paneth N, Dan B, Lin JP, Damiano DL, Becher JG, Gaebler-Spira D, Colver A, Reddihough DS, Crompton KE, Lieber RL (2016) Cerebral palsy. Nat Rev Dis Primers 2:15082. https://doi.org/10.1038/nrdp.2015.82
Gulati S, Sondhi V (2017) Cerebral palsy: an overview. Indian J Pediatr. https://doi.org/10.1007/s12098-017-2475-1
Gupta D, Lis CG, Dahlk SL, King J, Vashi PG, Grutsch JF, Lammersfeld CA (2008) The relationship between bioelectrical impedance phase angle and subjective global assessment in advanced colorectal cancer. Nutr J 7:19. https://doi.org/10.1186/1475-2891-7-19
Harrison AP, Elbrond VS, Riis-Olesen K, Bartels EM (2015) Multi-frequency bioimpedance in equine muscle assessment. Physiol Meas 36(3):453–464. https://doi.org/10.1088/0967-3334/36/3/453
Ivorra A (2003) Bioimpedance monitoring for physicians: an overview. Centre National de Microelectronica, Barcelona. Diploma thesis published: 02 January 2014 Hospital Clínic de Barcelona https://pdfs.semanticscholar.org/6ac2/e64a57d7facf739c326982d63d48ae58af31.pdf
Jaffrin MY (2009) Body composition determination by bioimpedance: an update. Curr Opin Clin Nutr Metab Care 12(5):482–486. https://doi.org/10.1097/MCO.0b013e32832da22c
Jahnsen R, Villien L, Egeland T, Stanghelle JK, Holm I (2004) Locomotion skills in adults with cerebral palsy. Clin Rehabil 18(3):309–316
Kalvoy H, Martinsen OG, Grimnes S (2008) Determination of tissue type surrounding a needle tip by electrical bioimpedance. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference 2008:2285–2286. https://doi.org/10.1109/iembs.2008.4649653
Li L, Landin D, Grodesky J, Myers J (2002) The function of gastrocnemius as a knee flexor at selected knee and ankle angles. J Electromyogr Kinesiol 12(5):385–390. https://doi.org/10.1016/s1050-6411(02)00049-4
Makki D, Duodu J, Nixon M (2014) Prevalence and pattern of upper limb involvement in cerebral palsy. J Child Orthop 8(3):215–219. https://doi.org/10.1007/s11832-014-0593-0
Matthie JR (2008) Bioimpedance measurements of human body composition: critical analysis and outlook. Expert Rev Med Dev 5(2):239–261. https://doi.org/10.1586/17434440.5.2.239
Nescolarde L, Yanguas J, Medina D, Rodas G, Rosell-Ferrer J (2011) Assessment and follow-up of muscle injuries in athletes by bioimpedance: preliminary results. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference 2011:1137–1140. https://doi.org/10.1109/iembs.2011.6090266
Nescolarde L, Yanguas J, Lukaski H, Alomar X, Rosell-Ferrer J, Rodas G (2013) Localized bioimpedance to assess muscle injury. Physiol Meas 34(2):237–245. https://doi.org/10.1088/0967-3334/34/2/237
Nescolarde L, Yanguas J, Lukaski H, Rodas G, Rosell-Ferrer J (2014) Localized BIA identifies structural and pathophysiological changes in soft tissue after post-traumatic injuries in soccer players. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference 2014:3743–3746. https://doi.org/10.1109/embc.2014.6944437
Nescolarde L, Yanguas J, Lukaski H, Alomar X, Rosell-Ferrer J, Rodas G (2015) Effects of muscle injury severity on localized bioimpedance measurements. Physiol Meas 36(1):27–42. https://doi.org/10.1088/0967-3334/36/1/27
Otsuka S, Yakura T, Ohmichi M, Naito M, Nakano T, Kawakami Y (2018) Site specificity of mechanical and structural properties of human fascia lata and their gender differences: a cadaveric study. J Biomech 77:69–75
Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B (1997) Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 39(4):214–223
Palisano RJ, Cameron D, Rosenbaum PL, Walter SD, Russell D (2006) Stability of the gross motor function classification system. Dev Med Child Neurol 48(6):424–428. https://doi.org/10.1017/s0012162206000934
Pingel J, Bartels EM, Nielsen JB (2016) New perspectives on the development of muscle contractures following central motor lesions. J Physiol. https://doi.org/10.1113/jp272767
Pingel J, Suhr F (2017) Are mechanically sensitive regulators involved in the function and (patho)physiology of cerebral palsy-related contractures? J Muscle Res Cell Motil 38:317–330. https://doi.org/10.1007/s10974-017-9489-1
Pingel J, Andersen IT, Broholm R, Harder A, Bartels EM, Bulow J et al (2019) An acoustic myography functional assessment of cerebral palsy subjects compared to healthy controls during physical exercise. J Muscle Res Cell Motil 40(1):53–58
Robinson KG, Mendonca JL, Militar JL, Theroux MC, Dabney KW, Shah SA et al (2013) Disruption of basal lamina components in neuromotor synapses of children with spastic quadriplegic cerebral palsy. PLoS ONE 8(8):e70288
Sanchez B, Iyer SR, Li J, Kapur K, Xu S, Rutkove SB, Lovering RM (2017) Non-invasive assessment of muscle injury in healthy and dystrophic animals with electrical impedance myography. Muscle Nerve 56(6):E85–E94. https://doi.org/10.1002/mus.25559
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(Pt 10):2625–2639. https://doi.org/10.1113/jphysiol.2010.203364
Stahn A, Strobel G, Terblanche E (2008) VO(2max) prediction from multi-frequency bioelectrical impedance analysis. Physiol Meas 29(2):193–203. https://doi.org/10.1088/0967-3334/29/2/003
von Walden F, Jalaleddini K, Evertsson B, Friberg J, Valero-Cuevas FJ, Ponten E (2017) Forearm flexor muscles in children with cerebral palsy are weak, thin and stiff. Front Comput Neurosci 11:30. https://doi.org/10.3389/fncom.2017.00030
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. https://doi.org/10.1111/dmcn.12124
Willerslev-Olsen M, Choe Lund M, Lorentzen J, Barber L, Kofoed-Hansen M, Nielsen JB (2018) Impaired muscle growth precedes development of increased stiffness of the triceps surae musculotendinous unit in children with cerebral palsy. Dev Med Child Neurol. https://doi.org/10.1111/dmcn.13729
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The authors are very much in the debt of the participants, and we would like to thank them for the time they spent contributing to this study.
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This project was very kindly funded by the Elsass Foundation together with grants from the RBU research foundation, the Promobilia foundation and the Norrbacka-Eugenia foundation.
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The method applied was non-invasive, and the study followed the guidelines set by the Helsinki Declaration 2013 (https://www.wma.net/en/30publications/10policies/b3/). All participants, gave informed written consent prior to joining the two studies involved, which were approved by the Capital Region of Denmark’s Ethics Committee (H-15017787) and (H-15011541).
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Pingel, J., Harrison, A., Von Walden, F. et al. Multi-frequency bioimpedance: a non-invasive tool for muscle-health assessment of adults with cerebral palsy. J Muscle Res Cell Motil 41, 211–219 (2020). https://doi.org/10.1007/s10974-020-09579-2
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DOI: https://doi.org/10.1007/s10974-020-09579-2