Inter-Day Reliability and Changes of Surface Electromyography on Two Postural Muscles Throughout 12 Weeks of Hippotherapy on Patients with Cerebral Palsy: A Pilot Study

Hélène Viruega, Inès Gaillard, Laura Briatte, Manuel Gaviria, Hélène Viruega, Inès Gaillard, Laura Briatte, Manuel Gaviria

Abstract

Cerebral palsy (CP) is an umbrella term covering a group of permanent developmental disorders of movement and posture characterized by highly variable clinical features. The aim of this study was to assess the short-term and mid-term effects of neurorehabilitation via hippotherapy on the contractile properties of two key postural muscles during functional sitting in such patients. Thirty-minute hippotherapy sessions were conducted biweekly for 12 weeks in 18 patients (18.1 ± 5.7 years old). Surface electromyography (EMG) was implemented bilaterally in rectus abdominis and adductor magnus. We quantitatively analyzed the amplitude of EMG signals in the time domain and its spectral characteristics in the frequency domain. EMGs were recorded at the beginning and end of each session on day one and at week six and week twelve. Statistical analysis revealed a substantial inter-day reliability of the EMG signals for both muscles, validating the methodological approach. To a lesser extent, while beyond the scope of the current study, quantitative changes suggested a more selective recruitment/contractile properties' shift of the examined muscles. Exploring postural control during functional activities would contribute to understanding the relationship between structural impairment, activity performance and patient capabilities, allowing the design of neurorehabilitation programs aimed at improving postural and functional skills according to each individual's needs. The present study provides basic quantitative data supporting the body of scientific evidence making hippotherapy an approach of choice for CP neurorehabilitation.

Keywords: EMG; cerebral palsy; hippotherapy; neurorehabilitation; postural balance; postural muscles.

Conflict of interest statement

All authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Scatter dot plot of the mean values of the AM mRMS at the beginning and the end of each session (Ini/End) regardless of treatment time. Tukey multiple-comparison test: * (p < 0.05).
Figure 2
Figure 2
Scatter dot plot of the mean mRMS values of the RA muscle during the first three minutes of the session (Ini) in relation to the treatment time (T0: first session; 6 w: week 6; 12 w: week 12). Tukey multiple-comparison test: * (p < 0.05).
Figure 3
Figure 3
Scatter dot plot around the mean mRMS value of the AM muscle at the first 3 min of the session (Ini) in relation to the treatment time (T0: first session, 6 w: week 6, 12 w: week 12). Tukey multiple-comparison test: * (p < 0.05).
Figure 4
Figure 4
On the left, scatter dot plot of the mean values of RA MNF at the beginning and end of each session (Ini/End) regardless of the treatment time; on the right, scatter dot plot around the mean value of the RA MDF at the beginning and the end of each session (Ini/End) regardless of the treatment time. (T0: first session; 6w: week 6; 12w: week 12). Tukey multiple-comparison test: * (p < 0.05).
Figure 5
Figure 5
Scatter dot plot of the mean values of MNF (left graph) and MDF (right graph) of the AM muscle with respect to time of treatment (T0: first session; 6w: week 6; 12w: week 12). Data were compared at the end of the session (End). A gradually decrease trend, which was statistically confirmed, emerged at the end of the session in relation to the evolution of the treatment. *: p < 0.05 in the Tukey multiple-comparison test.

References

    1. Colver A., Fairhurst C., Pharoah P.O. Cerebral palsy. Lancet. 2014;383:1240–1249. doi: 10.1016/S0140-6736(13)61835-8.
    1. Aruin A.S. The effect of changes in the body configuration on anticipatory postural adjustments. Motor Control. 2003;7:264–277. doi: 10.1123/mcj.7.3.264.
    1. Weerdesteyn V., Laing A.C., Robinovitch S.N. Automated postural responses are modified in a functional manner by instruction. Exp. Brain Res. 2008;186:571–580. doi: 10.1007/s00221-007-1260-1.
    1. Van der Heide J.C., Hadders-Algra M. Postural muscle dyscoordination in children with cerebral palsy. Neural Plast. 2005;12:197–203. doi: 10.1155/NP.2005.197.
    1. Pavão S.L., dos Santos A.N., Woollacott M.H., Rocha N.A. Assessment of postural control in children with cerebral palsy: A review. Res. Dev. Disabil. 2013;34:1367–1375. doi: 10.1016/j.ridd.2013.01.034.
    1. Woollacott M.H., Burtner P., Jensen J., Jasiewicz J., Roncesvalles N., Sveistrup H. Development of postural responses during standing in healthy children and children with spastic diplegia. Neurosci. Biobehav. Rev. 1998;22:583–589. doi: 10.1016/S0149-7634(97)00048-1.
    1. Marshall P.W., Murphy B.A. Core stability exercises on and off a Swiss ball. Arch. Phys. Med. Rehabil. 2005;86:242–249. doi: 10.1016/j.apmr.2004.05.004.
    1. van Criekinge T., Saeys W., Vereeck L., De Hertogh W., Truijen S. Are unstable support surfaces superior to stable support surfaces during trunk rehabilitation after stroke? A systematic review. Disabil. Rehabil. 2017;40:1981–1988. doi: 10.1080/09638288.2017.1323030.
    1. Uchiyama H., Ohtani N., Ohta M. Three-dimensional analysis of horse and human gaits in therapeutic riding. Appl. Anim. Behav. Sci. 2011;135:271–276. doi: 10.1016/j.applanim.2011.10.024.
    1. Viruega H., Gaillard I., Carr J., Greenwood B., Gaviria M. Short- and Mid-Term Improvement of Postural Balance after a Neurorehabilitation Program via Hippotherapy in Patients with Sensorimotor Impairment after Cerebral Palsy: A Preliminary Kinetic Approach. Brain Sci. 2019;9:261. doi: 10.3390/brainsci9100261.
    1. Masani K., Sin V.W., Vette A.H., Thrasher T.A., Kawashima N., Morris A., Preuss R., Popovic M.R. Postural reactions of the trunk muscles to multi-directional perturbations in sitting. Clin. Biomech. 2009;24:176–182. doi: 10.1016/j.clinbiomech.2008.12.001.
    1. Bobet J., Masani K., Popovic M.R., Vette A.H. Kinematics-based prediction of trunk muscle activity in response to multi-directional perturbations during sitting. Med. Eng. Phys. 2018;58:56–63. doi: 10.1016/j.medengphy.2018.05.004.
    1. Hadders-Algra M., Brogren E., Forssberg H. Development of postural control-differences between ventral and dorsal muscles? Neurosci. Biobehav. Rev. 1998;22:501–506. doi: 10.1016/S0149-7634(97)00036-5.
    1. Jeno S.H., Schindler G.S. StatPearls [Internet] StatPearls Publishing; Treasure Island, FL, USA: 2019. Anatomy, Bony Pelvis and Lower Limb, Thigh Adductor Magnus Muscles.
    1. Angsupaisal M., Dijkstra L.J., la Bastide-van Gemert S., van Hoorn J.F., Burger K., Maathuis C.G.B., Hadders-Algra M. Effects of forward tilted seating and foot-support on postural adjustments in children with spastic cerebral palsy: An EMG-study. Eur. J. Paediatr. Neurol. 2019;23:723–732. doi: 10.1016/j.ejpn.2019.07.001.
    1. Claus A.P., Hides J.A., Moseley G.L., Hodges P.W. Different ways to balance the spine in sitting: Muscle activity in specific postures differs between individuals with and without a history of back pain in sitting. Clin. Biomech. 2018;52:25–32. doi: 10.1016/j.clinbiomech.2018.01.003.
    1. Watanabe K., Katayama K., Ishida K., Akima H. Electromyographic analysis of hip adductor muscles during incremental fatiguing pedaling exercise. Eur. J. Appl. Physiol. 2009;106:815–825. doi: 10.1007/s00421-009-1086-6.
    1. McGibbon N.H., Benda W., Duncan B.R., Silkwood-Sherer D. Immediate and long-term effects of hippotherapy on symmetry of adductor muscle activity and functional ability in children with spastic cerebral palsy. Arch. Phys. Med. Rehabil. 2009;90:966–974. doi: 10.1016/j.apmr.2009.01.011.
    1. Shurtleff T.L., Standeven J.W., Engsberg J.R. Changes in dynamic trunk/head stability and functional reach after hippotherapy. Arch. Phys. Med. Rehabil. 2009;90:1185–1195. doi: 10.1016/j.apmr.2009.01.026.
    1. Silkwood-Sherer D.J., Killian C.B., Long T.M., Martin K.S. Hippotherapy an intervention to habilitate balance deficits in children with movement disorders: A clinical trial. Phys. Ther. 2012;92:707–717. doi: 10.2522/ptj.20110081.
    1. Silva e Borges M.B., Werneck M.J., da Silva M.L., Gandolfi L., Pratesi R. Therapeutic effects of a horse riding simulator in children with cerebral palsy. Arq. Neuro-psiquiatr. 2011;69:799–804. doi: 10.1590/S0004-282X2011000600014.
    1. Pitron V., Alsmith A., de Vignemont F. How do the body schema and the body image interact? Conscious. Cogn. 2018;65:352–358. doi: 10.1016/j.concog.2018.08.007.
    1. Hermens H.J., Freriks B., Disselhorst-Klug C., Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J. Electromyogr. Kinesiol. 2000;10:361–374. doi: 10.1016/S1050-6411(00)00027-4.
    1. Huebner A., Faenger B., Schenk P., Scholle H.C., Anders C. Alteration of Surface EMG amplitude levels of five major trunk muscles by defined electrode location displacement. J. Electromyogr. Kinesiol. 2015;25:214–223. doi: 10.1016/j.jelekin.2014.11.008.
    1. Adjenti S.K., Louw G., Jelsma J., Unger M. An electromyographic study of abdominal muscle activity in children with spastic cerebral palsy. S. Afr. J. Physiother. 2017;73:341. doi: 10.4102/sajp.v73i1.341.
    1. Pantall A., Durham S., Ewins D. Surface electromyographic activity of five residual limb muscles recorded during isometric contraction in transfemoral amputees with osseointegrated prostheses. Clin. Biomech. 2011;26:760–765. doi: 10.1016/j.clinbiomech.2011.03.008.
    1. Lovell G.A., Blanch P.D., Barnes C.J. EMG of the hip adductor muscles in six clinical examination tests. Phys. Ther. Sport. 2012;13:134–140. doi: 10.1016/j.ptsp.2011.08.004.
    1. Hewson D.J., Hogrel J.Y., Langeron Y., Duchêne J. Evolution in impedance at the electrode-skin interface of two types of surface EMG electrodes during long-term recordings. J. Electromyogr. Kinesiol. 2003;13:273–279. doi: 10.1016/S1050-6411(02)00097-4.
    1. Arendt-Nielsen L., Mills K.R., Forster A. Changes in muscle fiber conduction velocity, mean power frequency, and mean EMG voltage during prolonged submaximal contractions. Muscle Nerve Off. J. Am. Assoc. Electrodiagn. Med. 1989;12:493–497. doi: 10.1002/mus.880120610.
    1. Hermens H.J., van Bruggen T.A.M., Baten C.T.M., Rutten W.L.C., Boom H.B.K. The median frequency of the surface EMG power spectrum in relation to motor unit firing and action potential properties. J. Electromyogr. Kinesiol. 1992;2:15–25. doi: 10.1016/1050-6411(92)90004-3.
    1. Basmajian J.V., De Luca C.J. Muscles Alive. Their Functions Revealed by Electromyography. 5th ed. Williams & Wilkins; Baltimore, MD, USA: 1985. pp. 65–100.
    1. Larivière C., Gagnon D., Gravel D., Bertrand Arsenault A. The assessment of back muscle capacity using intermittent static contractions. Part I—Validity and reliability of electromyographic indices of fatigue. J. Electromyogr. Kinesiol. 2008;18:1006–1019. doi: 10.1016/j.jelekin.2007.03.012.
    1. Farina D., Holobar A., Merletti R., Enoka R.M. Decoding the neural drive to muscles from the surface electromyogram. Clin. Neurophysiol. 2010;121:1616–1623. doi: 10.1016/j.clinph.2009.10.040.
    1. Eken M.M., Dallmeijer A.J., Houdijk H., Doorenbosch C.A. Muscle fatigue during repetitive voluntary contractions: A comparison between children with cerebral palsy, typically developing children and young healthy adults. Gait Posture. 2013;38:962–967. doi: 10.1016/j.gaitpost.2013.05.004.
    1. Bar-On L., Aertbeliën E., Molenaers G., Desloovere K. Muscle Activation Patterns When Passively Stretching Spastic Lower Limb Muscles of Children with Cerebral Palsy. PLoS ONE. 2014;9:e91759. doi: 10.1371/journal.pone.0091759.
    1. Li X., Shin H., Zhou P., Niu X., Liu J., Rymer W.Z. Power spectral analysis of surface electromyography (EMG) at matched contraction levels of the first dorsal interosseous muscle in stroke survivors. Clin. Neurophysiol. 2014;125:988–994. doi: 10.1016/j.clinph.2013.09.044.
    1. Brueckner D., Kiss R., Muehlbauer T. Associations Between Practice-Related Changes in Motor Performance and Muscle Activity in Healthy Individuals: A Systematic Review. Sports Med. Open. 2018;4:9. doi: 10.1186/s40798-018-0123-6.
    1. Watanabe K., Kouzaki M., Ogawa M., Akima H., Moritani T. Relationships between muscle strength and multi-channel surface EMG parameters in eighty-eight elderly. Eur. Rev. Aging Phys. Act. 2018;15:3. doi: 10.1186/s11556-018-0192-z.
    1. Renshaw D., Bice M.R., Cassidy C., Eldridge J.A., Powell D.W. A Comparison of Three Computer-based Methods Used to Determine EMG Signal Amplitude. Int. J. Exerc. Sci. 2010;3:43–48.
    1. Feltham M.G., Ledebt A., Deconinck F.J., Savelsbergh G.J. Assessment of neuromuscular activation of the upper limbs in children with spastic hemiparetic cerebral palsy during a dynamical task. J. Electromyogr. Kinesiol. 2010;20:448–456. doi: 10.1016/j.jelekin.2009.07.001.
    1. Halaki M., Ginn K. Normalization of EMG Signals: To Normalize or Not to Normalize and What to Normalize to? In: Naik G.R., editor. Computational Intelligence in Electromyography Analysis—A Perspective on Current Applications and Future Challenges. IntechOpen Limited; London, UK: 2012. pp. 175–194.
    1. Shrout P.E., Fleiss J.L. Intraclass correlations: Uses in assessing rater reliability. Psychol. Bull. 1979;86:420–428. doi: 10.1037/0033-2909.86.2.420.
    1. Landis J.R., Koch G.G. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–174. doi: 10.2307/2529310.
    1. Benda W., McGibbon N.H., Grant K.L. Improvements in muscle symmetry in children with cerebral palsy after equine-assisted therapy (hippotherapy) J. Altern. Complement. Med. 2003;9:817–825. doi: 10.1089/107555303771952163.
    1. Lee D.R., Lee N.G., Cha H.J., Yun Sung O., You S.J., Oh J.H., Bang H.S. The effect of robo-horseback riding therapy on spinal alignment and associated muscle size in MRI for a child with neuromuscular scoliosis: An experimenter-blind study. NeuroRehabilitation. 2011;29:23–27. doi: 10.3233/NRE-2011-0673.
    1. Angsupaisal M., Visser B., Alkema A., Meinsma-van der Tuin M., Maathuis C.G., Reinders-Messelink H., Hadders-Algra M. Therapist-Designed Adaptive Riding in Children with Cerebral Palsy: Results of a Feasibility Study. Phys. Ther. 2015;95:1151–1162. doi: 10.2522/ptj.20140146.
    1. Noh H.J., Kim C.M., Park J.W. A study on muscle activity based on the ankle posture for effective exercise with indoor horse riding machine. J. Phys. Ther. Sci. 2019;31:170–174. doi: 10.1589/jpts.31.170.
    1. Brandt M., Andersen L.L., Samani A., Jakobsen M.D., Madeleine P. Inter-day reliability of surface electromyography recordings of the lumbar part of erector spinae longissimus and trapezius descendens during box lifting. BMC Musculoskelet. Disord. 2017;18:519. doi: 10.1186/s12891-017-1872-y.
    1. Enoka R.M., Duchateau J. Muscle fatigue: What, why and how it influences muscle function. J. Physiol. 2008;586:11–23. doi: 10.1113/jphysiol.2007.139477.
    1. Gandevia S.C. Spinal and supraspinal factors in human muscle fatigue. Physiol. Rev. 2001;81:1725–1789. doi: 10.1152/physrev.2001.81.4.1725.
    1. Coffey V.G., Hawley J.A. The molecular bases of training adaptation. Sports Med. 2007;37:737–763. doi: 10.2165/00007256-200737090-00001.
    1. Kim J.A., Roy R.R., Zhong H., Alaynick W.A., Embler E., Jang C., Gomez G., Sonoda T., Evans R.M., Edgerton V.R. PPARδ preserves a high resistance to fatigue in the mouse medial gastrocnemius after spinal cord transection. Muscle Nerve. 2016;53:287–296. doi: 10.1002/mus.24723.
    1. Larsson L., Moss R.L. Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J. Physiol. 1993;472:595–614. doi: 10.1113/jphysiol.1993.sp019964.
    1. Qaisar R., Renaud G., Hedstrom Y., Pollanen E., Ronkainen P., Kaprio J., Alen M., Sipila S., Artemenko K., Bergquist J., et al. Hormone replacement therapy improves contractile function and myonuclear organization of single muscle fibres from postmenopausal monozygotic female twin pairs. J. Physiol. 2013;591:2333–2344. doi: 10.1113/jphysiol.2012.250092.
    1. Ferraro E., Giammarioli A.M., Chiandotto S., Spoletini I., Rosano G. Exercise-induced skeletal muscle remodeling and metabolic adaptation: Redox signaling and role of autophagy. Antioxid. Redox Signal. 2014;21:154–176. doi: 10.1089/ars.2013.5773.
    1. Castro M.J., Apple D.F., Jr., Hillegass E.A., Dudley G.A. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur. J. Appl. Physiol. Occup. Physiol. 1999;80:373–378. doi: 10.1007/s004210050606.
    1. Metaxas T.I., Mandroukas A., Vamvakoudis E., Kotoglou K., Ekblom B., Mandroukas K. Muscle fiber characteristics, satellite cells and soccer performance in young athletes. J. Sports Sci. Med. 2014;13:493–501.
    1. Ahmetov I.I., Vinogradova O.L., Williams A.G. Gene polymorphisms and fiber-type composition of human skeletal muscle. Int. J. Sport Nutr. Exerc. Metab. 2012;22:292–303. doi: 10.1123/ijsnem.22.4.292.
    1. Henriksson J., Salmons S., Chi M.Y., Hintz C.S., Lowry O.H. Chronic stimulation of mammalian muscle: Changes in metabolite concentrations in in- dividual fibers. Am. J. Physiol. 1988;255:C543–C551. doi: 10.1152/ajpcell.1988.255.4.C543.
    1. Hood D.A. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl. Physiol. Nutr. Metab. 2009;34:465–472. doi: 10.1139/H09-045.
    1. Ljubicic V., Joseph A.M., Saleem A., Uguccioni G., Collu-Marchese M., Lai R.Y., Nguyen L.M., Hood D.A. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: Effects of exercise and aging. Biochim. Biophys. Acta. 2010;1800:223–234. doi: 10.1016/j.bbagen.2009.07.031.
    1. Qaisar R., Bhaskaran S., Van Remmen H. Muscle fiber type diversification during exercise and regeneration. Free Radic. Biol. Med. 2016;98:56–67. doi: 10.1016/j.freeradbiomed.2016.03.025.
    1. Wust R.C., Gibbings S.L., Degens H. Fiber capillary supply related to fiber size and oxidative capacity in human and rat skeletal muscle. Adv. Exp. Med. Biol. 2009;645:75–80.
    1. Gouspillou G., Sgarioto N., Norris B., Barbat-Artigas S., Aubertin-Leheudre M., Morais J.A., Burelle Y., Taivassalo T., Hepple R.T. The relationship between muscle fiber type-specific PGC-1alpha content and mitochondrial content varies between rodent models and humans. PLoS ONE. 2014;9:e103044. doi: 10.1371/journal.pone.0103044.
    1. Russell A.P., Feilchenfeldt J., Schreiber S., Praz M., Crettenand A., Gobelet C., Meier C.A., Bell D.R., Kralli A., Giacobino J.P., et al. Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes. 2003;52:2874–2881. doi: 10.2337/diabetes.52.12.2874.
    1. Trompetto C., Marinelli L., Mori L., Pelosin E., Currà A., Molfetta L., Abbruzzese G. Pathophysiology of spasticity: Implications for neurorehabilitation. BioMed Res. Int. 2014;2014:354906. doi: 10.1155/2014/354906.
    1. Lucena-Antón D., Rosety-Rodríguez I., Moral-Munoz J.A. Effects of a hippotherapy intervention on muscle spasticity in children with cerebral palsy: A randomized controlled trial. Complement. Ther. Clin. Pract. 2018;31:188–192. doi: 10.1016/j.ctcp.2018.02.013.
    1. Hadders-Algra M. Early human motor development: From variation to the ability to vary and adapt. Neurosci. Biobehav. Rev. 2018;90:411–427. doi: 10.1016/j.neubiorev.2018.05.009.

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