Abstract
Purpose
Activation of the calf (gastrocnemius and soleus) and tibialis anterior muscles play an important role in blood pressure regulation (via muscle-pump mechanism) and postural control. Parkinson’s disease is associated with calf (and tibialis anterior muscles weakness and stiffness, which contribute to postural instability and associated falls. In this work, we studied the role of the medial and lateral gastrocnemius, tibialis anterior, and soleus muscle contractions in maintaining blood pressure and postural stability in Parkinson’s patients and healthy controls during standing. In addition, we investigated whether the activation of the calf and tibialis anterior muscles is baroreflex dependent or postural-mediated.
Methods
We recorded electrocardiogram, blood pressure, center of pressure as a measure of postural sway, and muscle activity from the medial and lateral gastrocnemius, tibialis anterior, and soleus muscles from twenty-six Parkinson’s patients and eighteen sex and age-matched healthy controls during standing and with eyes open. The interaction and bidirectional causalities between the cardiovascular, musculoskeletal, and postural variables were studied using wavelet transform coherence and convergent cross-mapping techniques, respectively.
Results
Parkinson’s patients experienced a higher postural sway and demonstrated mechanical muscle-pump dysfunction of all individual leg muscles, all of which contribute to postural instability. Moreover, our results showed that coupling between the cardiovascular, musculoskeletal, and postural variables is affected by Parkinson’s disease while the contribution of the calf and tibialis anterior muscles is greater for blood pressure regulation than postural sway.
Conclusion
The outcomes of this study could assist in the development of appropriate physical exercise programs that target lower limb muscles to improve the muscle-pump function and reduce postural instability in Parkinson’s disease.
Similar content being viewed by others
References
Lanier, J. B., M. B. Mote, and E. C. Clay. Evaluation and management of orthostatic hypotension. AFP. 84(5):527–536, 2011.
Fanciulli, A., F. Leys, C. Falup-Pecurariu, R. Thijs, and G. K. Wenning. Management of orthostatic hypotension in Parkinson’s disease. J. Parkinson’s Dis. 10(s1):S57–S64, 2020. https://doi.org/10.3233/JPD-202036.
Mar, P. L., and S. R. Raj. Orthostatic hypotension for the cardiologist. Curr. Opin. Cardiol. 33(1):66–72, 2018. https://doi.org/10.1097/HCO.0000000000000467.
Allen, N. E., A. K. Schwarzel, and C. G. Canning. Recurrent falls in Parkinson’s disease: a systematic review. Parkinsons Dis. 2013:906274, 2013. https://doi.org/10.1155/2013/906274.
LeWitt, P. A., S. Kymes, and R. A. Hauser. Parkinson disease and orthostatic hypotension in the elderly: recognition and management of risk factors for falls. Aging Dis. 11(3):679–691, 2019. https://doi.org/10.14336/AD.2019.0805.
Degani, A. M., V. S. Cardoso, A. T. Magalhães, A. L. S. Assunção, E. C. de Soares, and A. Danna-Dos-Santos. Postural behavior in medicated Parkinson disease patients: a preliminary study searching for indicators to track progress. J. Cent. Nerv. Syst. Dis. 12:1179573520922645, 2020. https://doi.org/10.1177/1179573520922645.
Orawiec, R. B., S. B. Nowak, and P. Tomaszewski. Postural stability in Parkinson’s disease patients’ wives and in elderly women leading different lifestyles. Health Care Women Int. 40(10):1070–1083, 2019. https://doi.org/10.1080/07399332.2018.1531865.
Nallegowda, M., et al. Role of sensory input and muscle strength in maintenance of balance, gait, and posture in Parkinson’s disease: a pilot study. Am. J. Phys. Med. Rehabil. 83(12):898–908, 2004. https://doi.org/10.1097/01.phm.0000146505.18244.43.
Di Giulio, I., C. N. Maganaris, V. Baltzopoulos, and I. D. Loram. The proprioceptive and agonist roles of gastrocnemius, soleus and tibialis anterior muscles in maintaining human upright posture. J. Physiol. 587(Pt 10):2399–2416, 2009. https://doi.org/10.1113/jphysiol.2009.168690.
Le Mouel, C., and R. Brette. Mobility as the purpose of postural control. Front. Comput. Neurosci. 2017. https://doi.org/10.3389/fncom.2017.00067.
Yodchaisarn, W., R. Puntumetakul, A. Emasithi, R. Boucaut, and U. Chatchawan. Altered postural sway during quiet standing in women with clinical lumbar instability. J. Phys. Ther. Sci. 30(8):1099–1102, 2018. https://doi.org/10.1589/jpts.30.1099.
Winter, D. Human balance and posture control during standing and walking. Gait Posture. 3(4):193–214, 1995. https://doi.org/10.1016/0966-6362(96)82849-9.
Verma, A. K., D. Xu, A. Garg, A. P. Blaber, and K. Tavakolian. Effect of aging on muscle-pump baroreflex of individual leg muscles during standing. Front. Physiol. 10:845, 2019. https://doi.org/10.3389/fphys.2019.00845.
Verma, A. K., et al. Skeletal muscle pump drives control of cardiovascular and postural systems. Sci. Rep. 7(1):45301, 2017. https://doi.org/10.1038/srep45301.
Tian, F., T. Tarumi, H. Liu, R. Zhang, and L. Chalak. Wavelet coherence analysis of dynamic cerebral autoregulation in neonatal hypoxic–ischemic encephalopathy. NeuroImage. 11:124–132, 2016. https://doi.org/10.1016/j.nicl.2016.01.020.
de Boer, R. W., and J. M. Karemaker. Cross-wavelet time-frequency analysis reveals sympathetic contribution to baroreflex sensitivity as cause of variable phase delay between blood pressure and heart rate. Front. Neurosci. 13:694, 2019. https://doi.org/10.3389/fnins.2019.00694.
Hammami, I., L. Salhi, and S. Labidi. Voice pathologies classification and detection using EMD-DWT analysis based on higher order statistic features. IRBM. 41(3):161–171, 2020. https://doi.org/10.1016/j.irbm.2019.11.004.
Gupta, V., and M. Mittal. A comparison of ECG signal pre-processing using FrFT, FrWT and IPCA for improved analysis. IRBM. 40(3):145–156, 2019. https://doi.org/10.1016/j.irbm.2019.04.003.
Xu, D., et al. Significant role of the cardiopostural interaction in blood pressure regulation during standing. Am. J. Physiol. Heart Circ. Physiol. 313(3):H568–H577, 2017. https://doi.org/10.1152/ajpheart.00836.2016.
Garg, A., D. Xu, A. Laurin, and A. P. Blaber. Physiological interdependence of the cardiovascular and postural control systems under orthostatic stress. Am. J. Physiol. Heart Circ. Physiol. 307(2):H259-264, 2014. https://doi.org/10.1152/ajpheart.00171.2014.
Grinsted, A., J. C. Moore, and S. Jevrejeva. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Process. Geophys. 11(5/6):561–566, 2004.
Sugihara, G., et al. Detecting causality in complex ecosystems. Science. 338(6106):496–500, 2012. https://doi.org/10.1126/science.1227079.
Xu, D., M. F. Tremblay, A. K. Verma, K. Tavakolian, N. Goswami, and A. P. Blaber. Cardio-postural interactions and muscle-pump baroreflex are severely impacted by 60-day bedrest immobilization. Sci. Rep. 10(1):12042, 2020. https://doi.org/10.1038/s41598-020-68962-8.
del Ferreira-Sánchez, M. R., M. Moreno-Verdú, and R. Cano-de-la-Cuerda. Quantitative measurement of rigidity in Parkinson’s disease: a systematic review. Sensors (Basel). 20(3):880, 2020. https://doi.org/10.3390/s20030880.
Kang, G. A., J. M. Bronstein, D. L. Masterman, M. Redelings, J. A. Crum, and B. Ritz. Clinical characteristics in early Parkinson’s disease in a central California population-based study. Mov. Disord. 20(9):1133, 2005. https://doi.org/10.1002/mds.20513.
Durmus, B., O. Baysal, S. Altinayar, Z. Altay, Y. Ersoy, and C. Ozcan. Lower extremity isokinetic muscle strength in patients with Parkinson’s disease. J Clin. Neurosci. 17(7):893–896, 2010. https://doi.org/10.1016/j.jocn.2009.11.014.
Termoz, N., S. E. Halliday, D. A. Winter, J. S. Frank, A. E. Patla, and F. Prince. The control of upright stance in young, elderly and persons with Parkinson’s disease. Gait Posture. 27(3):463, 2008. https://doi.org/10.1016/j.gaitpost.2007.05.015.
Cantú, H., J. Nantel, M. Millán, C. Paquette, and J. N. Côté. Abnormal muscle activity and variability before, during, and after the occurrence of freezing in Parkinson’s disease. Front. Neurol. 2019. https://doi.org/10.3389/fneur.2019.00951.
Costa, S., et al. Biomechanical evaluation of an exoskeleton for rehabilitation of individuals with Parkinson’s disease. IRBM. 44(1):100741, 2023. https://doi.org/10.1016/j.irbm.2022.11.002.
Kamieniarz, A., et al. Detection of postural control in early Parkinson’s disease: clinical testing vs modulation of center of pressure. PLoS ONE. 16(1):e0245353, 2021. https://doi.org/10.1371/journal.pone.0245353.
Sabino-Carvalho, J. L., and L. C. Vianna. Altered cardiorespiratory regulation during exercise in patients with Parkinson’s disease: a challenging non-motor feature. SAGE Open Med. 8:2050312120921603, 2020. https://doi.org/10.1177/2050312120921603.
Pérez, T., et al. Cardiocirculatory manifestations in Parkinson’s disease patients without orthostatic hypotension. J. Hum. Hypertens. 29(10):604–609, 2015. https://doi.org/10.1038/jhh.2014.131.
Del Din, S., A. Godfrey, S. Coleman, B. Galna, S. Lord, and L. Rochester. Time-dependent changes in postural control in early Parkinson’s disease: what are we missing? Med. Biol. Eng. Comput. 54(2):401–410, 2016. https://doi.org/10.1007/s11517-015-1324-5.
Lalo, E., et al. Design of technology and technology of design. activity analysis as a resource for a personalised approach for patients with Parkinson disease. IRBM. 37(2):90–97, 2016. https://doi.org/10.1016/j.irbm.2016.02.010.
Fadil, R., et al. Effect of Parkinson’s disease on cardio-postural coupling during orthostatic challenge. Front. Physiol. 2022. https://doi.org/10.3389/fphys.2022.863877.
Andrezik, J. A., K. J. Dormer, R. D. Foreman, and R. J. Person. Fastigial nucleus projections to the brain stem in beagles: pathways for autonomic regulation. Neuroscience. 11(2):497–507, 1984. https://doi.org/10.1016/0306-4522(84)90040-x.
Rector, D. M., C. A. Richard, and R. M. Harper. Cerebellar fastigial nuclei activity during blood pressure challenges. J. Appl. Physiol. 101(2):549–555, 2006. https://doi.org/10.1152/japplphysiol.00044.2006.
Lutherer, L. O., J. L. Williams, and S. J. Everse. Neurons of the rostral fastigial nucleus are responsive to cardiovascular and respiratory challenges. J. Auton. Nerv. Syst. 27(2):101–111, 1989. https://doi.org/10.1016/0165-1838(89)90092-1.
Zhang, X.-Y., J.-J. Wang, and J.-N. Zhu. Cerebellar fastigial nucleus: from anatomic construction to physiological functions. Cerebellum Ataxias. 2016. https://doi.org/10.1186/s40673-016-0047-1.
Nasreddine, Z. S., et al. The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53(4):695–699, 2005. https://doi.org/10.1111/j.1532-5415.2005.53221.x.
Goetz, C. G., et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov. Disord. 22(1):41–47, 2007. https://doi.org/10.1002/mds.21198.
Kaufmann, H., R. Malamut, L. Norcliffe-Kaufmann, K. Rosa, and R. Freeman. The Orthostatic Hypotension Questionnaire (OHQ): validation of a novel symptom assessment scale. Clin. Auton. Res. 22(2):79–90, 2012. https://doi.org/10.1007/s10286-011-0146-2.
Visser, M., J. Marinus, A. M. Stiggelbout, and J. J. Van Hilten. Assessment of autonomic dysfunction in Parkinson’s disease: the SCOPA-AUT. Mov. Disord. 19(11):1306–1312, 2004. https://doi.org/10.1002/mds.20153.
Smets, E. M., B. Garssen, B. Bonke, and J. C. De Haes. The Multidimensional Fatigue Inventory (MFI) psychometric qualities of an instrument to assess fatigue. J. Psychosom. Res. 39(3):315–325, 1995. https://doi.org/10.1016/0022-3999(94)00125-o.
Tomlinson, C. L., R. Stowe, S. Patel, C. Rick, R. Gray, and C. E. Clarke. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov. Disord. 25(15):2649–2653, 2010. https://doi.org/10.1002/mds.23429.
Hermens, H., et al. SENIAM 8: European recommendations for surface electromyography. Roessingh Res. Dev. 8:13–54, 1999.
Xu, D., M. F. Tremblay, A. K. Verma, K. Tavakolian, N. Goswami, and A. P. Blaber. Cardio-postural interactions and muscle-pump baroreflex are severely impacted by 60-day bedrest immobilization. Sci. Rep. 10:985, 2020. https://doi.org/10.1038/s41598-020-68962-8.
Xu, D., et al. Significant role of the cardiopostural interaction in blood pressure regulation during standing. Am. J. Physiol. Heart Circ. Physiol. 313:H568, 2017. https://doi.org/10.1152/ajpheart.00836.2016.
Fadil, R., A. K. Verma, F. Sadeghian, A. P. Blaber, and K. Tavakolian. Cardio-respiratory interactions in response to lower-body negative pressure. Physiol. Meas. 44(2):025005, 2023. https://doi.org/10.1088/1361-6579/acb7c6.
Sadeghian, F., D. N. Divsalar, R. Fadil, K. Tavakolian, and A. P. Blaber. Canadian aging and inactivity study: spaceflight-inspired exercises during head-down tilt bedrest blunted reductions in muscle-pump but not cardiac baroreflex in older persons. Front. Physiol. 2022. https://doi.org/10.3389/fphys.2022.943630.
Verma, A. K., et al. Skeletal muscle pump drives control of cardiovascular and postural systems. Sci. Rep. 2017. https://doi.org/10.1038/srep45301.
Wallot, S., and D. Mønster. Calculation of average mutual information (AMI) and false-nearest neighbors (FNN) for the estimation of embedding parameters of multidimensional time series in matlab. Front. Psychol. 9:1679, 2018. https://doi.org/10.3389/fpsyg.2018.01679.
Blaber, A. P., C. K. Landrock, and P. A. Souvestre. Cardio-postural deconditioning: a model for post-flight orthostatic intolerance. Respir. Physiol. Neurobiol. 169(Suppl 1):S21-25, 2009. https://doi.org/10.1016/j.resp.2009.04.007.
Garg, A., D. Xu, and A. P. Blaber. Statistical validation of wavelet transform coherence method to assess the transfer of calf muscle activation to blood pressure during quiet standing. Biomed. Eng. Online. 12:132, 2013. https://doi.org/10.1186/1475-925X-12-132.
du Prel, J.-B., B. Röhrig, G. Hommel, and M. Blettner. Choosing statistical tests. Dtsch. Arztebl. Int. 107(19):343–348, 2010. https://doi.org/10.3238/arztebl.2010.0343.
Pinho, N., et al. The impact of the right coronary artery geometric parameters on hemodynamic performance. Cardiovasc. Eng. Technol. 10(2):257–270, 2019. https://doi.org/10.1007/s13239-019-00403-8.
R Development Core Team, A language and environment for statistical computing: reference index. Vienna: R Foundation for Statistical Computing, 2010. Accessed: Nov. 23, 2021. http://www.polsci.wvu.edu/duval/PS603/Notes/R/fullrefman.pdf
Naruse, R., C. Taki, M. Yaegashi, Y. Sakaue, N. Shiozawa, and T. Kimura. Attenuated spontaneous postural sway enhances diastolic blood pressure during quiet standing. Eur. J. Appl. Physiol. 121(1):251–264, 2021. https://doi.org/10.1007/s00421-020-04519-x.
Zhang, X.-Y., J.-J. Wang, and J.-N. Zhu. Cerebellar fastigial nucleus: from anatomic construction to physiological functions. Cerebellum Ataxias. 3(1):9, 2016. https://doi.org/10.1186/s40673-016-0047-1.
Fujita, H., T. Kodama, and S. du Lac. Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis. Elife. 9:e58613, 2020. https://doi.org/10.7554/eLife.58613.
Williams, C. L., D. Men, and E. C. Clayton. The effects of noradrenergic activation of the nucleus tractus solitarius on memory and in potentiating norepinephrine release in the amygdala. Behav. Neurosci. 114(6):1131–1144, 2000. https://doi.org/10.1037/0735-7044.114.6.1131.
Mello-Carpes, P. B., and I. Izquierdo. The Nucleus of the Solitary Tract → Nucleus Paragigantocellularis → Locus Coeruleus → CA1 region of dorsal hippocampus pathway is important for consolidation of object recognition memory. Neurobiol. Learn. Mem. 100:56–63, 2013. https://doi.org/10.1016/j.nlm.2012.12.002.
Lopes, L. T., et al. Anatomical and functional connections between the locus coeruleus and the nucleus tractus solitarius in neonatal rats. Neuroscience. 324:446–468, 2016. https://doi.org/10.1016/j.neuroscience.2016.03.036.
Somana, R., and F. Walberg. The cerebellar projection from locus coeruleus as studied with retrograde transport of horseradish peroxidase in the cat. Anat. Embryol. (Berl.). 155(1):87–94, 1978. https://doi.org/10.1007/BF00315733.
Tao, W., W. Jianjun, C. Hong, L. Hongzhao, and Y. Qixiang. Modulation of neuronal activity of cerebellar fastigial nucleus by locus coeruleus stimulation in the rat. Chin. Sci. Bull. 43(11):940–944, 1998. https://doi.org/10.1007/BF02884618.
Yu, M., and S.-M. Wang. “Neuroanatomy, Nucleus Fastigial”, in StatPearls. Treasure Island: StatPearls Publishing, 2022.
Durmus, B., O. Baysal, S. Altinayar, Z. Altay, Y. Ersoy, and C. Ozcan. Lower extremity isokinetic muscle strength in patients with Parkinson’s disease. J. Clin. Neurosci. 17(7):893–896, 2010. https://doi.org/10.1016/j.jocn.2009.11.014.
Skinner, J. W., E. A. Christou, and C. J. Hass. Lower extremity muscle strength and force variability in persons with Parkinson disease. J. Neurol. Phys. Ther. 43(1):56–62, 2019. https://doi.org/10.1097/NPT.0000000000000244.
Daubney, M. E., and E. G. Culham. Lower-extremity muscle force and balance performance in adults aged 65 years and older. Phys. Ther. 79(12):1177–1185, 1999.
Kouzaki, M., and M. Shinohara. Steadiness in plantar flexor muscles and its relation to postural sway in young and elderly adults. Muscle Nerve. 42(1):78–87, 2010. https://doi.org/10.1002/mus.21599.
McClenaghan, B. A., H. G. Williams, J. Dickerson, M. Dowda, L. Thombs, and P. Eleazer. Spectral characteristics of aging postural control. Gait Posture. 4(2):112–121, 1996. https://doi.org/10.1016/0966-6362(95)01040-8.
Rhea, C. K., A. W. Kiefer, F. J. Haran, S. M. Glass, and W. H. Warren. A new measure of the CoP trajectory in postural sway: dynamics of heading change. Med. Eng. Phys. 36(11):1473–1479, 2014. https://doi.org/10.1016/j.medengphy.2014.07.021.
Slobounov, S., M. Hallett, C. Cao, and K. Newell. Modulation of cortical activity as a result of voluntary postural sway direction: an EEG study. Neurosci. Lett. 442(3):309–313, 2008. https://doi.org/10.1016/j.neulet.2008.07.021.
Lee, Y.-J., J. N. Liang, B. Chen, and A. S. Aruin. Characteristics of medial-lateral postural control while exposed to the external perturbation in step initiation. Sci. Rep. 2019. https://doi.org/10.1038/s41598-019-53379-9.
McGraw, B., B. A. McClenaghan, H. G. Williams, J. Dickerson, and D. S. Ward. Gait and postural stability in obese and nonobese prepubertal boys. Arch. Phys. Med. Rehabil. 81(4):484–489, 2000. https://doi.org/10.1053/mr.2000.3782.
Stylianou, A. P., M. A. McVey, K. E. Lyons, R. Pahwa, and C. W. Luchies. Postural sway in patients with mild to moderate Parkinson’s disease. Int. J. Neurosci. 121(11):614–621, 2011. https://doi.org/10.3109/00207454.2011.602807.
Kato, K., T. Vogt, and K. Kanosue. Brain activity underlying muscle relaxation. Front. Physiol. 2019. https://doi.org/10.3389/fphys.2019.01457.
Grasso, M., L. Mazzini, and M. Schieppati. Muscle relaxation in Parkinson’s disease: a reaction time study. Mov. Disord. 11(4):411–420, 1996. https://doi.org/10.1002/mds.870110410.
Inkster, L. M., J. J. Eng, D. L. MacIntyre, and A. J. Stoessl. Leg muscle strength is reduced in PD and relates to the ability to rise from a chair. Mov. Disord. 18(2):157–162, 2003. https://doi.org/10.1002/mds.10299.
Masani, K., D. G. Sayenko, and A. H. Vette. What triggers the continuous muscle activity during upright standing? Gait Posture. 37(1):72–77, 2013. https://doi.org/10.1016/j.gaitpost.2012.06.006.
Carpinella, I., et al. Counteracting postural perturbations through body weight shift: a pilot study using a robotic platform in subjects with Parkinson’s disease. IEEE Trans. Neural Syst. Rehabil. Eng. 2018. https://doi.org/10.1109/TNSRE.2018.2862463.
Hagio, K., H. Obata, and K. Nakazawa. Effects of breathing movement on the reduction of postural sway during postural-cognitive dual tasking. PLoS ONE. 13(5):e0197385, 2018. https://doi.org/10.1371/journal.pone.0197385.
Howorka, K., et al. Effects of guided breathing on blood pressure and heart rate variability in hypertensive diabetic patients. Auton. Neurosci. 179(1–2):131–137, 2013. https://doi.org/10.1016/j.autneu.2013.08.065.
Nuckowska, M. K., et al. Impact of slow breathing on the blood pressure and subarachnoid space width oscillations in humans. Sci. Rep. 9(1):6232, 2019. https://doi.org/10.1038/s41598-019-42552-9.
Rodrigues, G. D., J. L. Gurgel, T. R. Gonçalves, F. Porto, and P. P. S. da Soares. Influence of breathing patterns and orthostatic stress on postural control in older adults. Geriatr. Gerontol. Int. 18(5):692–697, 2018. https://doi.org/10.1111/ggi.13231.
Acknowledgements
The authors would like to thank Mr. and Mrs. Joseph Peltier for their endowment to Sanford Parkinson’s disease laboratory. The authors appreciate the valuable help of the participants to complete this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to disclose.
Additional information
Associate Editor Jamshid Karimov oversaw the review of this article.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Fadil, R., Huether, A.X.A., Sadeghian, F. et al. The Effect of Skeletal Muscle-Pump on Blood Pressure and Postural Control in Parkinson's Disease. Cardiovasc Eng Tech 14, 755–773 (2023). https://doi.org/10.1007/s13239-023-00685-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13239-023-00685-z