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Insights into muscle metabolic energetics: Modelling muscle-tendon mechanics and metabolicrates during walking across speeds
KTH, School of Engineering Sciences (SCI), Engineering Mechanics.ORCID iD: 0000-0002-1561-4000
Vrije Universiteit Amsterdam.ORCID iD: 0000-0002-9120-7925
KU Leuven.ORCID iD: 0000-0002-4255-8673
KTH, School of Engineering Sciences (SCI), Centres, BioMEx. KTH, School of Engineering Sciences (SCI), Engineering Mechanics, Vehicle Engineering and Solid Mechanics.ORCID iD: 0000-0001-5417-5939
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The metabolic energy rate of individual muscles is impossible to measure without invasive procedures. Priorstudies have produced models to predict metabolic rates based on experimental observations of isolated musclecontraction from various species. Such models can provide reliable predictions of metabolic rates in humans ifmuscle properties and control are accurately modelled. This study aimed to examine how muscle-tendon modelcalibration and metabolic energy models influenced estimation of muscle-tendon states and time-seriesmetabolic rates, to evaluate the agreement with empirical data, and to provide predictions of the metabolic rateof muscle groups and gait phases across walking speeds. Three-dimensional musculoskeletal simulations withprescribed kinematics and dynamics were performed. An optimal control formulation was used to computemuscle-tendon states with four levels of individualization, ranging from a scaled generic model and musclecontrols based on minimal activations, to calibration of passive muscle forces, personalization of Achilles andquadriceps tendon stiffnesses, to finally informing muscle controls with electromyography. We computedmetabolic rates based on existing models. Simulations with calibrated passive forces and personalized tendonstiffness most accurately estimate muscle excitations and fiber lengths. Interestingly, the inclusion ofelectromyography did not improve our estimates. The whole-body average metabolic cost was better estimatedusing Bhargava et al. 2004 and Umberger 2010 models. We estimated metabolic rate peaks near early stance,pre-swing, and initial swing at all walking speeds. Plantarflexors accounted for the highest cost among musclegroups at the preferred speed and was similar to the cost of hip adductors and abductors combined. Also, theswing phase accounted for slightly more than one-quarter of the total cost in a gait cycle, and its relative costdecreased with walking speed. Our prediction might inform the design of assistive devices and rehabilitationtreatment. The code and experimental data are available online.

Keywords [en]
Oxygen consumption, cost of transportation, neuromechanics, biomechanics, bipedal locomotion, EMG, musculoskeletal simulation, optimal motor control
National Category
Medical and Health Sciences
Research subject
Applied Medical Technology; Applied and Computational Mathematics
Identifiers
URN: urn:nbn:se:kth:diva-342773OAI: oai:DiVA.org:kth-342773DiVA, id: diva2:1833091
Funder
Promobilia foundation, 8200Swedish Research Council, 2018-00750
Note

QC 20240202

Available from: 2024-01-31 Created: 2024-01-31 Last updated: 2024-02-02Bibliographically approved
In thesis
1. Walking efficiently with smart springs
Open this publication in new window or tab >>Walking efficiently with smart springs
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Numerous assistive exoskeletons have been developed in recent years to assist walking in individuals with and without motor disorders. A standard metric to measure the efficacy of assistance is the change in the metabolic energy cost between unassisted and assisted conditions. Various experimental methods, such as human-in-the-loop optimization, have been developed to find the optimal exoskeleton control to minimize metabolic energy. Such an approach is powerful yet time- and resource-intensive. In this regard, computational methods might complement state-of-the-art experimental approaches. Developing accurate models of the musculoskeletal system and neuromuscular commands could accelerate the development of exoskeletons and improve our understanding of human-exoskeleton interaction. The aims of the thesis were to model and simulate muscle-tendon mechanics and energetics of walking across speeds in unassisted conditions and with the support of ideal exoskeleton assistance with two modes of assistance: motor-based and spring-based actuators. 

The first three studies examined multiple musculoskeletal models, calibration methods of the muscle-tendon architecture, performance criteria for solving the muscle redundancy, and metabolic energy models to accurately estimate muscle excitations, fiber lengths, and metabolic energy cost compared to available experimental data. The musculoskeletal model proposed by Rajagopal et al. with calibrated muscle passive fiber-length curves and personalized Achilles and patellar tendon stiffness provided good agreement with muscle excitations and fiber lengths obtained from electromyographic signal and ultrasound imaging, respectively. Also, among multiple metabolic energy models in the literature, the model proposed by Bhargava et al. best estimated the average metabolic rates of the whole body compared to experimental measurements computed from spiroergometry. With the best estimations of muscle-tendon mechanics and energetics, the relative cost of the stance phase was predicted to increase significantly with walking speeds, and the metabolic cost of ankle plantarflexors was the highest among muscle groups and increased with walking speeds. The fourth study examined the optimal assistance to reduce muscle activations using motor-based and spring-based assistance of ankle plantarflexor, knee extensor, hip flexor, and hip abductor muscle groups. The largest reduction of muscle activation compared to unassisted conditions was obtained with hip flexor assistance with both actuation systems at high walking speeds. The reduction of metabolic rates compared to unassisted conditions was greater with walking speed with motor-based ankle plantarflexor assistance. In contrast, assisting this muscle group with spring-based actuation resulted in lower metabolic cost compared to unassisted conditions as walking speed increased. Interestingly, the decrease in muscle activations did not necessarily imply a reduction of metabolic energy cost compared to unassisted conditions, for instance with spring-based hip flexor and abductor assistance at some walking speeds. Metabolic energy rates during specific periods of the gait cycle were larger than in unassisted conditions due to increased muscle positive work, which is associated with high metabolic cost. 

The computational methods in the thesis might inspire future studies in the field. The software to calibrate muscle-tendon parameters, such as tendon compliance based on electromyography and muscle passive force-length curves based on ultrasound imaging, and to simulate exoskeleton assistance, are available in public repositories and can be adapted to integrate more experimental observations and simulate other motions than walking. Future studies will validate the predicted muscle-tendon mechanics with exoskeleton assistance.

Abstract [sv]

Flera exoskelett har utvecklats under de senaste åren för att hjälpa personer med och utan motoriska funktionsnedsättningar att gå. Ett standardmått för att utvärdera prestation hos ett exoskelett är förändringen i metabola energikostnad mellan oassisterad och assisterad gång. Flera experimentella metoder, t.ex. human-in-the-loop-optimering, har utvecklats för att identifiera den optimala exoskelettassistansen som minimerar den metabola energin. Sådan metoder är mycket kraftfulla men är också mycket tids- och resurskrävande. I detta avseende kan beräkningsmetoder komplettera de experimentella metoderna. Noggranna modeller av rörelsesystemet och dess motoriska kontroll kan påskynda exoskelettutvecklingen och ge viktig information om samspeket mellan en människa och ett exoskelett. Syftet med avhandlingen är att modellera och simulera muskelmekanik och energiförbrukning vid gång i olika hastigheter, både utan assistans och med ett exoskelett med idealisk assistans från motorer och från fjädrar. 

I de tre första studierna undersökte vi flera modellvariationer för att identifiera den kombination vars resultat bäst matchade experimentella fynd.  Specifikt undersökte vi: flera biomekaniska modeller, olika metoder för att kalibrera muskelarkitekturen, flera kriterier för att lösa det underbestämda muskelkraftsystemet, och flera ekvationer som uppskattar metabolisk energi. Vi jämförde våra resultat med uppmätta eller tillgängliga experimentella data, såsom muskelaktivering, muskelfiberlängd och metabolisk energikostnad. Den biomekaniska modellen av Rajagopal et al. med justeringar för passiva muskelkrafter och häl- och patellarsenstelhet uppskattade muskelaktiveringar och muskelfiberlängder som överensstämde med experiment eller befintlig data.  Bland metabolisk energimodeller, resultaten från modellen av Bhargava et al. stämde bäst med experimentella mätningar från spiroergometri. Med den modellkombinationen som bäst uppskattade muskeldynamiken kunde vi mäta att den relativa metabola kostnad för stödfasen ökar med gånghastighet, där vadmusklerna stod för den största energiförbrukningen. I den fjärde studien uppskattade vi optimal assistans vid varje nedre extremitetsled som minimerar muskelaktiveringar, både från simulerade motorer och fjädrar. De största minskningarna av muskelaktivering uppnåddes med höftböjarassistans från antigen en motor eller en fjäder vid höga gånghastigheter. Vadmuskelassistans med motorer minskade metabola kostnader mer när gånghastigheten ökade. Däremot minskade inte metabola kostnader med vadmuskelassistans från fjädrar när gånghastigheten ökade. Det är intressant att påpeka att exoskelett som minskade muskelaktiveringar inte alltid minskade den metabola kostnaden, t.ex. med höftböjare och höftabduktorassistans från fjädrar. I vissa gångfaser var metabola energin till och med högre med assistans än utan, eftersom muskelarbete var högre vid dessa ögonblick.

De beräkningsmetoder som presenterades i avhandlingen kan inspirera och påskynda framtida studier inom området. Källkoden för kalibrering och justering av muskelparametrar samt senor och muskelpassiva egenskaper är fritt tillgänglig online i ett datarepository, liksom källkoden för simulering av exoskelettassistans. Framtida studier med exoskelettprototyper syftar till att validera simuleringarna.

Place, publisher, year, edition, pages
Stockholm: Kungliga Tekniska högskolan, 2024. p. xii, 58
Series
TRITA-SCI-FOU ; 2023:67
Keywords
Musculoskeletal modeling and simulation, muscle-tendon biomechanics, muscle parameter calibration, metabolic energy models, gait analysis, exoskeleton assistance, biomechanics, Biomekanisk modellering och simulering, rörelseorganen, biomekanik, muskel, muskelmodell och muskelarkitektur, metabolisk energi och kostnad, gång, gånganalys, exoskelett, hjälpmedel, gångpatologi
National Category
Engineering and Technology
Research subject
Engineering Mechanics
Identifiers
urn:nbn:se:kth:diva-342790 (URN)978-91-8040-823-3 (ISBN)
Public defence
2024-02-23, https://kth-se.zoom.us/j/66088467200, Kollegiesalen, Brinellvägen 6, Stockholm, 09:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council, 2018-00750Promobilia foundation, 18200
Available from: 2024-02-01 Created: 2024-01-31 Last updated: 2024-02-20Bibliographically approved

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Luis, IsraelGutierrez-Farewik, Elena

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