Using Musculoskeletal Models to Explore Strategies for Improving Performance in Electrical Stimulation-Induced Leg Cycle Ergometry

Electrical stimulation-induced leg cycle ergometry has been shown to provide a variety of therapeutic benefits for spinal cord injured (SCI) paraplegics and quadriplegics [47, 53, 90, 124, 135, 137, 154]. The stimulation, however, is generally inefficient both mechanically and metabolically. As a result, the stimulated muscles fatigue quickly and the maximum power output is small. The average untrained SCI individual, for example, cannot maintain a crank cadence above 35 rpm for much more than 2 minutes at the lowest work-load[135]. To optimize the use of existing stimulation-powered ergometers, and improve the design of future systems, it is helpful to understand how the forces generated by the electrically stimulated muscles interact with the skeletal-ergometer linkage to drive the crank. Specifically, the question addressed in this dissertation is: Can performance be improved by changing either the configuration of the patient in the ergometer, the load being driven by the stimulation, or the timing of the stimulation? Performance is assessed in terms of the strength needed to produce a given motion, as well as in terms of the metabolic energy used. To achieve this goal, models were developed to represent: 1) the segmental dynamics of the lower limbs and their interaction with the ergometer, 2) the relationship between the stimulation and the force developed in the muscles, 3) the geometry of the interface between the muscles and the skeleton, 4) the control of the stimulation by the ergometer, and 5) the heat produced by the stimulated muscles. Together, the models o f the musculoskeletal system and the ergometer define a dynamical representation of the mechanical, electrical, and energetic aspects of stimulation-induced leg cycling ergometry.

To gain confidence in the model of cycling ergometry and to assess its predictive capabilities, the model results were compared to the performance of a SCI subject pedaling the Therapeutic Technology’s ERGYS under a variety of situations, and to published average measurements of oxygen consumption under various loading conditions [64].

A method was developed to quantify the strength required to maintain a steadystate pedaling cadence and the likelihood that a given individual will be capable of pedaling. These quantities give an indication of the ease of pedaling in a variety of seat configurations and loading conditions, and with different stimulation patterns. In this way, the effect of these variations can be assessed without the knowledge of patientspecific muscular strength. Additionally, the relationship between strength and metabolic energy expended was explored. Based on these evaluations, possible strategies are suggested for either decreasing the strength required for, or increasing the cardiovascular benefits of stimulation-induced leg cycle ergometry

Year	Entry
1973	Smidt GL. Biomechanical analysis of knee flexion and extension. J Biomech. January 1973;6(1):79-92.
1981	Dostal WF, Andrews JG. A three-dimensional biomechanical model of hip musculature. J Biomech. 1981;14(11):803-812.
1989	Zajac FE. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng. 1989;17(4):359-411.
1992	Spoor CW, van Leeuwen JL. Knee muscle moment arms from MRI and from tendon travel. J Biomech. February 1992;25(2):201-206.
1990	Winters JM. Hill-based muscle models: a systems engineering perspective. In: Winters JM, Woo SL-Y, eds. Multiple Muscle Systems: Biomechanics and Movement Organization. New York, NY: Springer-Verlag; 1990:69-93.
1988	Khang G. Paraplegic Standing Controlled by Functional Neuromuscular Stimulation: Computer Model, Control System Design, and Simulation Studies [PhD thesis]. Stanford University; June 1988.
1952	Abbott BC, Aubert XM. The force exerted by active striated muscle during and after change of length. J Physiol. May 28, 1952;117(1):77-86.
1972	Haut RC, Little RW. A constitutive equation for collagen fibers. J Biomech. September 1972;5(5):423-430.
1989	Zajac FE, Gordon ME. Determining muscle's force and action in multi-articular movement. Exerc Sport Sci Rev. January 1989;17(1):187-230.
1990	Yamaguchi GT, Zajac FE. Restoring unassisted natural gait to paraplegics via functional neuromuscular stimulation: a computer simulation study. IEEE Trans Biomed Eng. September 1990;37(9):886-902.
1990	Yamaguchi GT, Sawa AGU, Moran DW, Fessler MJ, Winters JM. A survey of human musculotendon actuator parameters. In: Winters JM, Woo SL-Y, eds. Multiple Muscle Systems: Biomechanics and Movement Organization. New York, NY: Springer-Verlag; 1990:717-773.
1990	Delp SL. Surgery Simulation: A Computer Graphics System to Analyze and Design Musculoskeletal Reconstructions of the Lower Limb [PhD thesis]. Stanford University; August 1990.
1986	Brand RA, Pedersen DR, Friederich JA. The sensitivity of muscle force predictions to changes in physiologic cross-sectional area. J Biomech. 1986;19(8):589-596.
1982	Brand RA, Crowninshield RD, Wittstock CE, Pedersen DR, Clark CR, van Krieken FM. A model of lower extremity muscular anatomy. J Biomech Eng. November 1982;104(4):304-310.
1989	Yamaguchi GT, Zajac FE. A planar model of the knee joint to characterize the knee extensor mechanism. J Biomech. 1989;22(1):1-10.
1990	Delp SL, Loan JP, Hoy MG, Zajac FE, Topp EL, Rosen JM. An interactive graphics-based model of the lower extremity to study orthopaedic surgical procedures. IEEE Trans Biomed Eng. 1990;37(8):757-767.
1938	Hill AV. The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci. October 10, 1938;126(843):136-195.
1985	Winters JM, Stark L. Analysis of fundamental human movement patterns through the use of in-depth antagonistic muscle models. IEEE Trans Biomed Eng. 1985;32(10):826-839.
1990	Hoy MG, Zajac FE, Gordon ME. A musculoskeletal model of the human lower extremity: the effect of muscle, tendon, and moment arm on the moment-angle relationship of musculotendon actuators at the hip, knee, and ankle. J Biomech. 1990;23(2):157-169.
1983	Wickiewicz TL, Roy RR, Powell PL, Edgerton VR. Muscle architecture of the human lower limb. Clin Orthop Relat Res. October 1983;179:275-283.
1991	Pandy MG, Zajac FE. Optimal muscular coordination strategies for jumping. J Biomech. 1991;24(1):1-10.
1990	Friederich JA, Brand RA. Muscle fiber architecture in the human lower limb. J Biomech. 1990;23(1):91-95.
1988	Winters JM, Stark L. Estimated mechanical properties of synergistic muscles involved in movements of a variety of human joints. J Biomech. 1988;21(12):1027-1041.
1939	Katz B. The relation between force and speed in muscular contraction. J Physiol. June 1939;96(1):45-64.
1967	Fung YCB. Elasticity of soft tissues in simple elongation. Am J Physiol. December 1967;213(6):1532-1544.

Year

Entry

1973

Smidt GL. Biomechanical analysis of knee flexion and extension. J Biomech. January 1973;6(1):79-92.

1981

Dostal WF, Andrews JG. A three-dimensional biomechanical model of hip musculature. J Biomech. 1981;14(11):803-812.

1989

Zajac FE. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng. 1989;17(4):359-411.

1992

Spoor CW, van Leeuwen JL. Knee muscle moment arms from MRI and from tendon travel. J Biomech. February 1992;25(2):201-206.

1990

Winters JM. Hill-based muscle models: a systems engineering perspective. In: Winters JM, Woo SL-Y, eds. Multiple Muscle Systems: Biomechanics and Movement Organization. New York, NY: Springer-Verlag; 1990:69-93.

1988

Khang G. Paraplegic Standing Controlled by Functional Neuromuscular Stimulation: Computer Model, Control System Design, and Simulation Studies [PhD thesis]. Stanford University; June 1988.

1952

Abbott BC, Aubert XM. The force exerted by active striated muscle during and after change of length. J Physiol. May 28, 1952;117(1):77-86.

1972

Haut RC, Little RW. A constitutive equation for collagen fibers. J Biomech. September 1972;5(5):423-430.

1989

Zajac FE, Gordon ME. Determining muscle's force and action in multi-articular movement. Exerc Sport Sci Rev. January 1989;17(1):187-230.

1990

Yamaguchi GT, Zajac FE. Restoring unassisted natural gait to paraplegics via functional neuromuscular stimulation: a computer simulation study. IEEE Trans Biomed Eng. September 1990;37(9):886-902.

1990

Yamaguchi GT, Sawa AGU, Moran DW, Fessler MJ, Winters JM. A survey of human musculotendon actuator parameters. In: Winters JM, Woo SL-Y, eds. Multiple Muscle Systems: Biomechanics and Movement Organization. New York, NY: Springer-Verlag; 1990:717-773.

1990

Delp SL. Surgery Simulation: A Computer Graphics System to Analyze and Design Musculoskeletal Reconstructions of the Lower Limb [PhD thesis]. Stanford University; August 1990.

1986

Brand RA, Pedersen DR, Friederich JA. The sensitivity of muscle force predictions to changes in physiologic cross-sectional area. J Biomech. 1986;19(8):589-596.

1982

Brand RA, Crowninshield RD, Wittstock CE, Pedersen DR, Clark CR, van Krieken FM. A model of lower extremity muscular anatomy. J Biomech Eng. November 1982;104(4):304-310.

1989

Yamaguchi GT, Zajac FE. A planar model of the knee joint to characterize the knee extensor mechanism. J Biomech. 1989;22(1):1-10.

1990

Delp SL, Loan JP, Hoy MG, Zajac FE, Topp EL, Rosen JM. An interactive graphics-based model of the lower extremity to study orthopaedic surgical procedures. IEEE Trans Biomed Eng. 1990;37(8):757-767.

1938

Hill AV. The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci. October 10, 1938;126(843):136-195.

1985

Winters JM, Stark L. Analysis of fundamental human movement patterns through the use of in-depth antagonistic muscle models. IEEE Trans Biomed Eng. 1985;32(10):826-839.

1990

Hoy MG, Zajac FE, Gordon ME. A musculoskeletal model of the human lower extremity: the effect of muscle, tendon, and moment arm on the moment-angle relationship of musculotendon actuators at the hip, knee, and ankle. J Biomech. 1990;23(2):157-169.

1983

Wickiewicz TL, Roy RR, Powell PL, Edgerton VR. Muscle architecture of the human lower limb. Clin Orthop Relat Res. October 1983;179:275-283.

1991

Pandy MG, Zajac FE. Optimal muscular coordination strategies for jumping. J Biomech. 1991;24(1):1-10.

1990

Friederich JA, Brand RA. Muscle fiber architecture in the human lower limb. J Biomech. 1990;23(1):91-95.

1988

Winters JM, Stark L. Estimated mechanical properties of synergistic muscles involved in movements of a variety of human joints. J Biomech. 1988;21(12):1027-1041.

1939

Katz B. The relation between force and speed in muscular contraction. J Physiol. June 1939;96(1):45-64.

1967

Fung YCB. Elasticity of soft tissues in simple elongation. Am J Physiol. December 1967;213(6):1532-1544.

Year	Entry
2015	Saul KR, Hu X, Goehler CM, Vidt ME, Daly M, Velisar A, Murray WM. Benchmarking of dynamic simulation predictions in two software platforms using an upper limb musculoskeletal model. Comput Methods Biomech Biomed Eng. 2015;18(13):1445-1458.
2004	Buchanan TS, Lloyd DG, Manal K, Besier TF. Neuromusculoskeletal modeling: estimation of muscle forces and joint moments and movements from measurements of neural command. J Appl Biomech. November 2004;20(4):367-395.
1996	Piazza SJ, Delp SL. The influence of muscles on knee flexion during the swing phase of gait. J Biomech. June 1996;29(6):723-733.
2003	Lloyd DG, Besier TF. An EMG-driven musculoskeletal model to estimate muscle forces and knee joint moments in vivo. J Biomech. June 2003;36(6):765-776.
2013	Gerus P, Sartori M, Besier TF, Fregly BJ, Delp SL, Banks SA, Pandy MG, D'Lima DD, Lloyd DG. Subject-specific knee joint geometry improves predictions of medial tibiofemoral contact forces. J Biomech. November 15, 2013;46(16):2778-2786.
2014	Amiri P. Obesity and Its Influence on Knee Joint Contact Forces in Individuals With Moderate Knee Osteoarthritis [Master's thesis]. Halifax, NS: Dalhousie University; August 2014.
1998	Piazza SJ. Simulation-Based Design of Total Knee Replacements [PhD thesis]. Evanston, IL: Northwestern University; December 1998.
2015	Nelson CM. An Investigation of Musculoskeletal Adaptation At the Paretic Elbow After Chronic Hemiparetic Stroke Using Imaging, Biomechanical and Simulation Approaches [PhD thesis]. Evanston, IL: Northwestern University; December 2015.
2015	Wohlman SJ. Understanding the Dynamics of Thumb-Tip Force Generation Through Integration of Simulation and Experimental Methods [PhD thesis]. Evanston, IL: Northwestern University; August 2015.
2018	Binder-Markey BI. An Investigation of the Musculoskeletal Changes in the Hand After Chronic Hemiparetic Stroke and Their Impact on Hand Opening: Using Integrated Experimental and Computer Simulation Methods [PhD thesis]. Evanston, IL: Northwestern University; March 2018.
2009	Lee SSM. Musculoskeletal Architecture and Plantarflexor Muscle Function in the Human Ankle Joint [PhD thesis]. State College, PA: Pennsylvania State University; December 2009.
2012	Baxter JR. Linking Foot and Ankle Musculoskeletal Structure to Locomotor Function [PhD thesis]. State College, PA: Pennsylvania State University; December 2012.
2014	van Werkhoven H. Influence of Foot and Ankle Structure on Optimal Performance in Different Motor Tasks [PhD thesis]. State College, PA: Pennsylvania State University; August 2014.
2022	Hickox L. Mechanisms Underlying Plantarflexor Structure-Function Relationships and Implications for Locomotor Function [PhD thesis]. State College, PA: Pennsylvania State University; December 2022.
1993	Fregly BJ. The Significance of Crank Load Dynamics to Steady-State Pedaling Biomechanics: An Experimental and Computer Modeling Study [PhD thesis]. Stanford University; March 1993.
2012	Arnold EM. Computer Modeling of Human Lower Limb Muscles to Study How Muscle Fiber Lengths and Velocities Affect Muscle Force Generation During Walking and Running [PhD thesis]. Stanford University; July 2012.
2006	Gardinier JD. Evaluation of an EMG-Driven Model and Its Ability to Estimate Joint Moments At the Knee [Master's thesis]. University of Delaware; F 2006.
1999	Anderson FC III. A Dynamic Optimization Solution for a Complete Cycle of Normal Gait [PhD thesis]. University of Texas at Austin; December 1999.

Year

Entry

2015

Saul KR, Hu X, Goehler CM, Vidt ME, Daly M, Velisar A, Murray WM. Benchmarking of dynamic simulation predictions in two software platforms using an upper limb musculoskeletal model. Comput Methods Biomech Biomed Eng. 2015;18(13):1445-1458.

2004

Buchanan TS, Lloyd DG, Manal K, Besier TF. Neuromusculoskeletal modeling: estimation of muscle forces and joint moments and movements from measurements of neural command. J Appl Biomech. November 2004;20(4):367-395.

1996

Piazza SJ, Delp SL. The influence of muscles on knee flexion during the swing phase of gait. J Biomech. June 1996;29(6):723-733.

2003

Lloyd DG, Besier TF. An EMG-driven musculoskeletal model to estimate muscle forces and knee joint moments in vivo. J Biomech. June 2003;36(6):765-776.

2013

Gerus P, Sartori M, Besier TF, Fregly BJ, Delp SL, Banks SA, Pandy MG, D'Lima DD, Lloyd DG. Subject-specific knee joint geometry improves predictions of medial tibiofemoral contact forces. J Biomech. November 15, 2013;46(16):2778-2786.