Distinctive Steady-State Heart Rate and Blood Pressure Responses to Passive Robotic Leg Exercise and Functional Electrical Stimulation during Head-Up Tilt

Amirehsan Sarabadani Tafreshi, Robert Riener, Verena Klamroth-Marganska, Amirehsan Sarabadani Tafreshi, Robert Riener, Verena Klamroth-Marganska

Abstract

Introduction: Tilt tables enable early mobilization of patients by providing verticalization. But there is a high risk of orthostatic hypotension provoked by verticalization, especially after neurological diseases such as spinal cord injury. Robot-assisted tilt tables might be an alternative as they add passive robotic leg exercise (PE) that can be enhanced with functional electrical stimulation (FES) to the verticalization, thus reducing the risk of orthostatic hypotension. We hypothesized that the influence of PE on the cardiovascular system during verticalization (i.e., head-up tilt) depends on the verticalization angle, and FES strengthens the PE influence. To test our hypotheses, we investigated the PE effects on the cardiovascular parameters heart rate (HR), and systolic and diastolic blood pressures (sBP, dBP) at different angles of verticalization in a healthy population. Methods: Ten healthy subjects on a robot-assisted tilt table underwent four different study protocols while HR, sBP, and dBP were measured: (1) head-up tilt to 60° and 71° without PE; (2) PE at 20°, 40°, and 60° of head-up tilt; (3) PE while constant FES intensity was applied to the leg muscles, at 20°, 40°, and 60° of head-up tilt; (4) PE with variation of the applied FES intensity at 0°, 20°, 40°, and 60° of head-up tilt. Linear mixed models were used to model changes in HR, sBP, and dBP responses. Results: The models show that: (1) head-up tilt alone resulted in statistically significant increases in HR and dBP, but no change in sBP. (2) PE during head-up tilt resulted in statistically significant changes in HR, sBP, and dBP, but not at each angle and not always in the same direction (i.e., increase or decrease of cardiovascular parameters). Neither adding (3) FES at constant intensity to PE nor (4) variation of FES intensity during PE had any statistically significant effects on the cardiovascular parameters. Conclusion: The effect of PE on the cardiovascular system during head-up tilt is strongly dependent on the verticalization angle. Therefore, we conclude that orthostatic hypotension cannot be prevented by PE alone, but that the preventive effect depends on the verticalization angle of the robot-assisted tilt table. FES (independent of intensity) is not an important contributing factor to the PE effect.

Keywords: cardiovascular system; functional electrical stimulation (FES); linear mixed models; orthostatic hypotension; parametric bootstrap; rehabilitation robotics; robotic tilt table.

Figures

Figure 1
Figure 1
Erigo tilt table: verticalization is provided by changing the inclination angle of the tilt table α. Passive Robotic leg exercise is provided through a leg drive with an adjustable speed fstep. The table is further enhanced with electrical stimulation module which enables providing electrical stimulation to the leg muscles with adjustable parameters (here current IFES) during robotic leg exercise. Picture is copyrighted by Hocoma AG, Switzerland, and is adapted with permission.
Figure 2
Figure 2
(A) Study protocol 1: head-up tilt to 60° and 71° (two experiments). (B) Study protocols 2 and 3: PE at 48 steps/min (solid) without or with application of the minimum FES amplitude (dashed). The protocols were conducted at α = {20°, 40°, 60°}. The figure shows the experiment performed at each specific tilt angle. (C) Study protocol 4: during PE at 48 steps/min (solid) with FES, the FES amplitude (dashed) was changed to a higher level, i.e., 0.8IMAX. The protocol was conducted at α = {0°, 20°, 40°, 60°}. The figure shows the experiment performed at each specific tilt angle. The highlighted areas T1 and T2 show the data range used for the analysis.
Figure 3
Figure 3
Statistical models for ΔHR, ΔsBP, and ΔdBP responses (changes with respect to supine position) to head-up tilt alone (A–C). The steady-state values for each subject are connected with a line. The highlighted areas show 95% CI. The signs *, **, and *** mark significant findings with p ≤ 0.05, 0.01, and 0.001, respectively. n.s. marks non-significant differences.
Figure 4
Figure 4
Statistical models for ΔHR, ΔsBP, and ΔdBP responses to PE (independent of FES) during head-up tilt (A–C). Steady-state values correspond to the average response of two conditions, i.e., PE without and with FES application, and for each subject they are connected with lines. The highlighted areas show 95% CI. The signs * and *** mark significant findings with p ≤ 0.05 and 0.001, respectively. n.s. marks non-significant differences.

References

    1. Adami A., Pizzinelli P., Bringard A., Capelli C., Malacarne M., Lucini D., et al. . (2013). Cardiovascular re-adjustments and baroreflex response during clinical reambulation procedure at the end of 35-day bed rest in humans. Appl. Physiol. Nutr. Metab. 38, 673–680. 10.1139/apnm-2012-0396
    1. Bates D., Mächler M., Bolker B., Walker S. (2014). Fitting linear mixed-effects models using lme4. arXiv:1406.5823.
    1. Bourdin G., Barbier J., Burlem J.-F., Durante G., Passant S., Vincent B., et al. . (2010). The feasibility of early physical activity in intensive care unit patients: a prospective observational one-center study. Respir. Care 55, 400–407.
    1. Brower R. G. (2009). Consequences of bed rest. Crit. Care Med. 37, S422–S428. 10.1097/CCM.0b013e3181b6e30a
    1. Burtin C., Clerckx B., Robbeets C., Ferdinande P., Langer D., Troosters T., et al. . (2009). Early exercise in critically ill patients enhances short-term functional recovery*. Crit. Care Med. 37, 2499–2505. 10.1097/CCM.0b013e3181a38937
    1. Chi L., Masani K., Miyatani M., Thrasher T. A., Johnston K. W., Mardimae A., et al. . (2008). Cardiovascular response to functional electrical stimulation and dynamic tilt table therapy to improve orthostatic tolerance. J. Electromyogr. Kinesiol. 18, 900–907. 10.1016/j.jelekin.2008.08.007
    1. Colombo G., Schreier R., Mayr A., Plewa H., Rupp R. (2005). Novel tilt table with integrated robotic stepping mechanism: design principles and clinical application, in 9th International Conference on Rehabilitation Robotics, 2005, ICORR 2005 (Chicago, IL: IEEE; ), 227–230.
    1. Cox D. R., Hinkley D. V. (1979). Theoretical Statistics. CRC Press.
    1. Craven C. T. D., Gollee H., Coupaud S., Allan D. B. (2013). Investigation of robotic-assisted tilt-table therapy for early-stage spinal cord injury rehabilitation. J. Rehabil. Res. Dev. 50, 367–378. 10.1682/JRRD.2012.02.0027
    1. Czell D., Schreier R., Rupp R., Eberhard S., Colombo G., Dietz V. (2004). Influence of passive leg movements on blood circulation on the tilt table in healthy adults. J. Neuroeng. Rehabil. 1:4. 10.1186/1743-0003-1-4
    1. Dittmer D., Teasell R. (1993). Complications of immobilization and bed rest. part 1: musculoskeletal and cardiovascular complications. Can. Fam. Phys. 39:1428.
    1. Feldstein C., Weder A. B. (2012). Orthostatic hypotension: a common, serious and underrecognized problem in hospitalized patients. J. Am. Soc. Hypertens. 6, 27–39. 10.1016/j.jash.2011.08.008
    1. Frazzitta G., Valsecchi R., Zivi I., Sebastianelli L., Bonini S., Zarucchi A., et al. . (2015). Safety and feasibility of a very early verticalization in patients with severe traumatic brain injury. J. Head Trauma Rehabil. 30, 290–292. 10.1097/HTR.0000000000000135
    1. Freeman R., Wieling W., Axelrod F. B., Benditt D. G., Benarroch E., Biaggioni I., et al. . (2011). Consensus statement on the definition of orthostatic hypotension, neurally mediated syncope and the postural tachycardia syndrome. Clin. Auton. Res. 21, 69–72. 10.1007/s10286-011-0119-5
    1. Giggins O. M., Persson U. M., Caulfield B. (2013). Biofeedback in rehabilitation. J. Neuroeng. Rehabil. 10:60. 10.1186/1743-0003-10-60
    1. Hainsworth R., Al-Shamma Y. (1988). Cardiovascular responses to upright tilting in healthy subjects. Clin. Sci. 74, 17–22.
    1. Halekoh U., Højsgaard S. (2014). A kenward-roger approximation and parametric bootstrap methods for tests in linear mixed models–the R package pbkrtest. J. Stat. Softw. 59, 1–30. 10.18637/jss.v059.i09
    1. Illman A., Stiller K., Williams M. (2000). The prevalence of orthostatic hypotension during physiotherapy treatment in patients with an acute spinal cord injury. Spinal Cord 38, 741–747. 10.1038/sj.sc.3101089
    1. Kuznetsov A. N., Rybalko N. V., Daminov V. D., Luft A. R. (2013). Early poststroke rehabilitation using a robotic tilt-table stepper and functional electrical stimulation. Stroke Res. Treat. 2013:946056. 10.1155/2013/946056
    1. Laubacher M., Perret C., Hunt K. J. (2015). Work-rate-guided exercise testing in patients with incomplete spinal cord injury using a robotics-assisted tilt-table. Disabil. Rehabil. Assist. Technol. 10, 433–438. 10.3109/17483107.2014.908246
    1. Lim E., Chan G. S., Dokos S., Ng S. C., Latif L. A., Vandenberghe S., et al. . (2013). A cardiovascular mathematical model of graded head-up tilt. PLoS ONE 8:e77357. 10.1371/journal.pone.0077357
    1. Luther M. S., Krewer C., Müller F., Koenig E. (2008). Comparison of orthostatic reactions of patients still unconscious within the first three months of brain injury on a tilt table with and without integrated stepping. A prospective, randomized crossover pilot trial. Clin. Rehabil. 22, 1034–1041. 10.1177/0269215508092821
    1. Morris P. E. (2007). Moving our critically ill patients: mobility barriers and benefits. Crit. Care Clin. 23, 1–20. 10.1016/j.ccc.2006.11.003
    1. R Core Team (2015). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
    1. Riener R., Fuhr T. (1998). Patient-driven control of fes-supported standing up: a simulation study. IEEE Trans. Rehabil. Eng. 6, 113–124.
    1. Saengsuwan J., Huber C., Schreiber J., Schuster-Amft C., Nef T., Hunt K. J. (2015a). Feasibility of cardiopulmonary exercise testing and training using a robotics-assisted tilt table in dependent-ambulatory stroke patients. J. Neuroeng. Rehabil. 12:88. 10.1186/s12984-015-0078-5
    1. Saengsuwan J., Nef T., Laubacher M., Hunt K. J. (2015b). Comparison of peak cardiopulmonary performance parameters on a robotics-assisted tilt table, a cycle and a treadmill. PLoS ONE 10:e0122767. 10.1371/journal.pone.0122767
    1. Sarabadani Tafreshi A., Klamroth-Marganska V., Nussbaumer S., Riener R. (2015). Real-time closed-loop control of human heart rate and blood pressure. IEEE Trans. Biomed. Eng. 62, 1434–1442. 10.1109/TBME.2015.2391234
    1. Schwartz C. E., Stewart J. M. (2012). The arterial baroreflex resets with orthostasis. Front. Physiol. 3:461. 10.3389/fphys.2012.00461
    1. Taveggia G., Ragusa I., Trani V., Cuva D., Angeretti C., Fontanella M., et al. . (2015). Robotic tilt table reduces the occurrence of orthostatic hypotension over time in vegetative states. Int. J. Rehabil. Res. 38, 162–166. 10.1097/MRR.0000000000000104
    1. Toska K., Walløe L. (2002). Dynamic time course of hemodynamic responses after passive head-up tilt and tilt back to supine position. J. Appl. Physiol. 92, 1671–1676. 10.1152/japplphysiol.00465.2000
    1. Wieser M., Gisler S., Sarabadani A., Ruest R. M., Buetler L., Vallery H., et al. . (2014). Cardiovascular control and stabilization via inclination and mobilization during bed rest. Med. Biol. Eng. Comput. 52, 53–64. 10.1007/s11517-013-1119-5
    1. Wieser M. J. (2011). A Multi-Modal Approach to Improve the Rehabilitation Therapy of Bed Rest Patients. Ph.D. thesis, Diss., Eidgenössische Technische Hochschule ETH Zürich, Nr. 20032, 2011.
    1. Yoshida T., Masani K., Sayenko D. G., Miyatani K., Fisher J. A., Popovic M. R. (2013). Cardiovascular response of individuals with spinal cord injury to dynamic functional electrical stimulation under orthostatic stress. IEEE Trans. Neural Syst. Rehabil. Eng. 21, 37–46. 10.1109/TNSRE.2012.2211894

Source: PubMed

3
S'abonner