Updated Perspectives on the Role of Biomechanics in COPD: Considerations for the Clinician

Figures & data

Figure 1 Simplified depiction of COPD pathophysiology that leads to biomechanical alterations. Mitochondrial loss/dysfunction, increased circulating inflammatory cells, muscle atrophy, and alterations at the neuromuscular junction contribute to decreased muscle force, rate of force generation, and physical activity, as well as increased muscle fatigue and weakness. These factors, along with many others, contribute to altered biomechanics, decreased exercise capacity, increased physical inactivity, and exercise intolerance. Created with BioRender.com.

Table 1 Definitions of Biomechanical Terms

Term	Definition	Implication
Fascicle length	“distance between the intersection of the fascicle with the superficial and deeper aponeurosis”^Citation172	Length is a function of the number of in series sarcomeres; considered by some as the single most important architectural parameter of a muscle affecting its function
Fascicle velocity	Time derivative of fascicle length	Increased fascicle shortening velocity is associated with an increased rate of force development
Muscle contractility	Ability to contract	Paralysis is the inability to contract muscle tissue
Muscle elasticity	Ability to recoil after being stretched	Allows the muscle to return to its normal shape
Muscle extensibility	Ability of the muscle to be stretched	A lack of extensibility would be spasticity
Muscle irritability (also known as excitability)	Ability to respond to a stimulus	Rippling muscle disease is a condition in which muscles are unusually hyperexcitable
Muscle stiffness	Change in force divided by the corresponding change in length or resistance of muscle to length change	Limits excessive joint motion or translation after a perturbation
Muscle tension	Force generated by a contracting muscle	Amount of tension (force) a muscle can produce is dependent upon the number of cross-bridges formed between actin and myosin
Pennation angle	Muscle fiber architecture; the angle between fiber orientation and the longitudinal axis of the bone	The greater a pennation angle provides a mechanical advantage, the more force can be generated in the muscle
Shear wave elastography	Produces “an acoustic radiofrequency force impulse, which generates transversely-oriented shear waves that propagate through the surrounding tissue and provide biomechanical information about tissue quality”^Citation173	Quantifies mechanical and elastic properties of skeletal muscle tissue
Stretch-shortening cycle	Active stretching of a muscle before active contraction. Sometimes referred to as “pre-stretch” or “countermovement”	Storage of elastic energy. Resulting force, work, and power are enhanced with an active pre-stretch

Figure 2 Typical biomechanical methods. (A and B) Motion capture represented by cameras systems in the background (solid red circle) record where markers are in space (dotted red circle) and provide information about where the person is in space (kinematics). (C) Force platforms provide information about forces (kinetics). (D) Dynamometers provide information regarding muscle strength and power.

Table 2 Studies of Balance in PwCOPD That Used Biomechanical Measures of Postural Sway

Study	Subjects	Conditions	Dependent Variables	Results
Silva Almeida, et al^Citation43	14 PR PwCOPD 9 controls	EO, EC, ECF, EO with respiratory overload	COP area COP displacement COP variability COP velocity	Increased COP area and displacement, variability in ML, velocity in AP compared to controls
Butcher, et al^Citation15	30 PwCOPD 21 controls	SOT	Sway magnitude Peak sway displacement	Increased COP sway magnitude and displacement during test 3, EO and platform tilted anteriorly and posteriorly compared to controls
Costa Boffino, et al^Citation174	30 PwCOPD 30 OA controls 30 YA controls	Modified SOT	COP amplitude COP variability COP velocity	Increased COP amplitude, variability, and velocity compared to OA and YA controls
de Castro, et al^Citation54	33 PwCOPD 33 controls	EO, EC, EOF, OLS	COP area COP velocity EMG	Increased COP area and velocity of AP and ML during OLS, with higher activation of scalenes compared to controls
de Castro, et al^Citation16	47 PwCOPD 25 controls	OLS	COP area COP velocity	Increased COP area compared to controls
de Castro, et al^Citation175	31 PwCOPD completed 3 mo. land or water exercise program	EO, EC, EO feet together, OLS	COP area	No differences
Eymir, et al^Citation42	24 PwCOPD 24 controls	Biodex balance system	Stability index	Worse postural stability overall and in both AP and ML directions compared to controls.
Gloeckl, et al^Citation48	48 PR PwCOPD with whole-body vibration training or conventional balance training	EC, OLS, Semi-tandem stance with EC	Absolute path length	Whole-body vibration group had a greater change in absolute path length in semi-tandem stance and OLS compared to conventional balance group
Janssens, et al^Citation46	20 PwCOPD 20 controls	ECF w/ and w/o muscle vibration	COP RMS	Increased sway in AP compared to controls Increased reliance on ankle proprioceptive signals, lower reliance on back muscle signals compared to controls
Jirange, et al^Citation11	42 PwCOPD 45 controls	EO, EC, EOF, ECF	COP velocity COP velocity moment	During EO, velocity in AP was faster and velocity moment was increased in COPD During EC, velocity in AP and ML was faster in COPD compared to controls No results given for foam condition
Molouki, et al^Citation47	15 PwCOPD 14 controls	EO, EC, EO & EC with counting task	COP variability COP velocity COP variability of velocity Lyapunov exponent	PwCOPD had greater COPD variability of sway and velocity, and Lyapunov exponents compared to controls across all conditions
Oliveira, et al^Citation36	26 PwCOPD & exacerbation 26 stable PwCOPD 25 controls	EO, EC, EOF, EO feet together	COP path length COP amplitude	Those experiencing exacerbations performed worse than controls for most variables in all conditions Only during EOF did stable COPD perform worse than controls
Park, et al^Citation44	34 PwCOPD 22 controls	EO	COP velocity COP displacement COP area	Increased AP velocity compared to controls
Porto, et al^Citation52	93 PwCOPD 39 controls	Tetrax (8 conditions)	COP sway	No difference
Roig, et al^Citation30	20 PwCOPD 20 controls	SOT	Equilibrium score (amount of sway)	During conditions when only vestibular systems were useful for postural control were there differences between PwCOPD and controls
Smith, et al^Citation45	12 PwCOPD 12 controls	EO, EC, EOF, EO short base	COP max amplitude COP RMS	PwCOPD had greater RMS in ML during all conditions and greater max amplitude in ML when standing on foam
Smith, et al^Citation53	15 PwCOPD 15 controls	EO with perturbation (rapid shoulder flexion/extension) before and after arm ergometry exercise	COP displacement COP velocity	PwCOPD took longer to return to baseline after perturbation and did not always return to baseline in AP direction Exercise had no effect
Van Hove, et al^Citation49	21 PwCOPD 21 controls	EO, EC, EO & EC with cognitive tasks (serial 3 subtraction, category fluency)	COP displacement COP area COP range COP variability COP velocity	PwCOPD had worse balance than controls Addition of cognitive tasks mainly affected speed related measures

Abbreviations: EO, eyes open; EC, eyes closed; F, Foam; OLS, one-legged stance; COP, center of pressure; ML, mediolateral; AP, anteroposterior; PR, pulmonary rehabilitation; SOT, sensory organization test; OA, older adults; YA, young adults; RMS, root mean square.

Table 3 Studies of Balance in PwCOPD Using Non-Biomechanical Tests

Study	Subjects	Conditions	Findings
Beauchamp, et al^Citation24	23 PwCOPD fallers 16 PwCOPD non-fallers	BBS ABC scale TUG	Poorer performance on the BBS, less confidence as reported on the ABC, and longer time to complete TUG in fallers compared to non-fallers
Chauvin, et al^Citation176	34 PwCOPD fallers 38 PwCOPD non-fallers	BESTest	Balance subcomponent that could identify fallers from non-fallers was stability limits/verticality
Jácome, et al^Citation40	49 mild PwCOPD 63 moderate PwCOPD 48 severe PwCOPD	TUG	Those with severe to very severe disease took significantly longer to complete the TUG compared to moderate and mild disease Compared to reference values, those aged 70+ took longer to complete the TUG
Janssens, et al^Citation56	18 PwCOPD 18 controls	EC Sit-to-Stand-to-Sit	Required 46% more time to complete five sit-to-stand-to-sit due to longer stand and stand-to-sit phases
Voica, et al^Citation35	13 Emphysematous PwCOPD 14 Bronchitic COPD 17 controls	ABC BBS TUG SLS	All COPD had worse balance compared to controls Bronchitic PwCOPD had less confidence (lower ABC), shorter single leg stance times, took longer to complete the TUG compared to emphysemateous PwCOPD
Tudorache, et al^Citation9	22 stable PwCOPD 19 PwCOPD & exacerbation 20 controls	FES BBS TUG SLS	All COPD had worse balance compared to controls Balance was worse for those experiencing exacerbation compared to those with stable COPD for all measures

Abbreviations: BBS, Berg Balance Scale; ABC, Activity-specific balance confidence scale; TUG, Timed Up and Go; SLS, Single limb stance time; FES, Falls efficacy scale.

Table 4 Studies of Gait in PwCOPD

Study	Subjects	Conditions	Dependent Variables	Results
Annegarn, et al^Citation75	79 PwCOPD 24 controls	6MWT	Cadence (strides/min) Inter-stride trunk acceleration variability (autocorrelation)	PwCOPD had a slower cadence and increased variability for medio-lateral acceleration of the trunk compared to controls
Butcher, et al^Citation15	30 PwCOPD (15 w/oxygen, 15 w/o) 21 controls	10-meter walk	Fast gait speed from middle 6-meters	PwCOPD and using oxygen have a slower fast gait speed compared to those not using oxygen and controls
Fallahtafti, et al^Citation73	17 PwCOPD 23 controls	6-minutes of walking on treadmill at 3 speeds	Gait stability Cost of transport	PwCOPD walk with wider stability margins in the ML direction and have less metabolic power than controls
Heraud, et al^Citation83	25 PR PwCOPD 20 controls	15 min of walking with and without a cognitive task (serial 3 subtraction)	Gait speed Stride time variability	Both groups walked slower during the cognitive task Stride time variability did not differ during walking only; however, was greater during the cognitive task in PwCOPD No effect of PR on dual task performance
Iwakura, et al^Citation65	34 male PwCOPD 16 male controls	10-meter walk	Gait speed Step length Cadence Walk ratio Step time variability Acceleration magnitude	PwCOPD had slower gait speed and cadence, shorter step lengths, and greater step time variability compared to controls PwCOPD had a decreased acceleration magnitude compared to controls
Jirange, et al^Citation11	42 PwCOPD 45 controls	Win-Track gait analyzer	Step duration Gait cycle duration Swing duration Step length Gait cycle duration	Swing duration was longer in PwCOPD compared to controls
Karpman, et al^Citation177	130 PwCOPD	8-meter walk	4-meter usual gait speed 4-meter fast gait speed Physical activity 6MWT	Gait speed is independently associated with 6MWT distance but not physical activity
Lahousse, et al^Citation63	196 PwCOPD 898 controls	GAITRite mat under normal walk, turn, and tandem walk	Global gait Rhythm Pace Variability	PwCOPD and disease severity were associated with taking slower steps (rhythm)
Liu, et al^Citation12	80 PwCOPD 38 controls	6MWT on treadmill (GRAIL)	Mean and variability of spatiotemporal measures	PwCOPD had longer duration of strides and decreased stride and step lengths Stride length variability was greater in PwCOPD
Liu, et al^Citation67	44 PR PwCOPD	6MWT on treadmill (GRAIL)	Variability of spatiotemporal measures Gait fluctuation	PR patients were divided into good and poor responders to PR Good responders had longer stride length and shorter stride times Fluctuations in gait did not change
Liu, et al^Citation81	22 PwCOPD 22 controls	3 minutes of treadmill walking at 3 speeds	Variability and fluctuations of joint angles and range of motion	Controls had more organized fluctuations of hip and knee joint Controls adapted to speed changes compared to PwCOPD
McCamley, et al^Citation70	16 PwCOPD 25 patients with peripheral artery disease 25 controls	Overground walking at self-selected speed	Kinematic and kinetic gait variables	No significant difference was found between controls and PwCOPD Patients with peripheral artery disease did have differences compared to PwCOPD and controls
McCrum, et al^Citation74	12 PR PwCOPD 12 controls	Treadmill walking with forward perturbations	Gait stability	No apparent change in gait stability following a forward perturbation
Morlino, et al^Citation13	40 PwCOPD 28 controls	GAITRite mat	Mean spatiotemporal Variability of step length, duration, and width	Slower cadence and speed, and shorter step length in PwCOPD Variability of step length was greater in PwCOPD
Nantsupawat, et al^Citation25	14 PwCOPD	6- to 10-meter walk	Spatiotemporal variables	Compared to published norms, PwCOPD had shorter steps, slower cadence, slower walking speed, and spent more time in double support
Sanseverino, et al^Citation82	11 PwCOPD 11 controls	Cardiopulmonary exercise test across 6 speeds	Walking speed Stride frequency variability	PwCOPD had a slower self-selected walking speed. Only at −40% and +20% of self-selected speed did gait variability differ between groups; however, this difference was gone when compared at isovelocity
Saraiva, et al^Citation79	36 PwCOPD 19 controls	6MWT	Minimum, mean, and maximum gait speed	Mean and max speeds were slower in PwCOPD
Terui, et al^Citation55	16 PwCOPD 26 controls	10-minute walk	Trunk acceleration symmetry	PwCOPD demonstrate greater asymmetry of trunk acceleration when walking
Yentes, et al^Citation68	7 PwCOPD	Overground walking at self-selected speed before and after exercise intervention	Kinematic and kinetic gait variables	Step width decreased following a 6-week exercise intervention
Yentes, et al^Citation72	17 PwCOPD 21 controls	Overground walking at self-selected speed before and after an acute exercise bout	Kinematic and kinetic gait variables	Ankle kinetics are altered in PwCOPD PwCOPD walk with a wider step width
Yentes, et al^Citation71	20 PwCOPD 20 controls	3 minutes of treadmill walking at 3 speeds	Step length, time, width variability and fluctuations (sample entropy)	PwCOPD have longer step times and greater variability of step time PwCOPD have a narrower step width and greater variability that is exacerbated with increased gait speed
Yentes, et al^Citation146	17 PwCOPD 23 controls	6 minutes of treadmill walking at 3 speeds	Locomotor respiratory coupling	PwCOPD have a more rigid coupling that is associated with increased energy expenditure

Abbreviations: 6MWT, six minute walk test; AP, anteroposterior; ML, mediolateral; PR, pulmonary rehabilitation.

Table 5 Studies of Muscle Mechanics in PwCOPD

Study	Subjects	Conditions	Dependent Variables	Findings
Casabona, et al^Citation178	10 PwCOPD 10 controls	Flexion/extension of the knee	EMG amplitude, mean and median frequencies	PwCOPD have less amplitude of activity in extension but not flexion movements compared to controls Frequencies were higher in PwCOPD compared to controls Frequency was correlated with disease severity
Navarro-Cruz, et al^Citation89	26 PwCOPD 10 physically active controls	Leg press exercise	4-meter gait speed Vastus lateralis muscle thickness, pennation angle, fascicle length Force-velocity relationship	PwCOPD had a slower gait speed The stretch-shortening cycle-induced potentiation was higher in PwCOPD The stretch-shortening cycle-induced potentiation was associated with slower gait speed, less muscle thickness, and smaller pennation angles
Sariabous, et al^Citation117	13 PwCOPD 7 controls	Quiet breathing an incremental ventilatory effort protocol	Inspiratory mouth pressure Respiratory muscle MMG Efficiency of inspiratory muscle activation	Increases in COPD severity was associated with increases in muscle activation Efficiency of muscle activation was lower in PwCOPD and decreased with severity
Valle, et al^Citation86	11 PwCOPD 11 controls	Passive leg oscillations (pendulum test)	EMG Viscosity and stiffness coefficients	PwCOPD had less EMG activation PwCOPD had lower viscosity and stiffness values compared to controls

Abbreviations: EMG, electromyography; MMG, mechanomyography.

Table 6 Studies of Breathing Mechanics in PwCOPD

Study	Subjects	Conditions	Dependent Variables	Findings
Barros de Sá, et al^Citation179	28 PwCOPD (14 Tx group; 14 controls)	Single session of rib cage muscles stretching in treatment group	Compartmental volumes using OEP EMG	Tx group increased pulmonary and abdominal rib cage tidal volume Decreased activity in sternocleidomastoid and upper trap
Bhatt, et al^Citation180	297 PwCOPD (3 groups based on rankings of spirometry compared to CT emphysema)	Inspiratory and expiratory CT images	Jacobian determinant Strain information Anisotropic deformation index	All three dependent variables were associated with FEV1 Variability of Jacobian and strain may be markers of biomechanical lung heterogeneity
Bianchi, et al^Citation110	30 PwCOPD	Supervised pursed-lip breathing	Compartmental volumes and displacement using OEP	Two different pursed-lip breathing patterns identified: euvolumics and hyperinflators
Binazzi, et al^Citation181	15 PwCOPD	Quiet breathing, reading aloud, singing, and high-effort whispering	Chest wall motion using OEP	Phonation imposes breathing more with the abdomen in men Females used more costal breathing compared to men
Bodduluri, et al^Citation182	490 PwCOPD	Inspiratory and expiratory CT images	St. George Respiratory Questionnaire 6MWD BODE index Wall area percentage Jacobian determinant	Jacobian determinant was associated with the St. George Respiratory Questionnaire, 6MWD, and BODE index
Capeletti, et al^Citation183	25 PwCOPD	Pre/post adapted Glittre-Activities of Daily Living test	Compartmental volumes using OEP	Reduction in upper thoracic contribution with no change in lower thoracic contribution post test Increase in abdominal compartment contribution post test
Chynkiamis, et al^Citation184	14 PwCOPD	Intermittent cycle ergometer exercise bouts with portable noninvasive ventilation or pursed-lip breathing during recovery	Compartmental volumes using OEP	Two groups of dynamic hyperinflation responders: 7 subjects responded to portable noninvasive ventilation (responders) and 7 responded to pursed-lip breathing (non-responders) Responders reduced end-expiratory dynamic hyperinflation primarily by reducing abdominal compartment volume
Gagliardi, et al^Citation185	14 PwCOPD	24-session exercise program	Compartmental volumes using OEP	No change in compartmental volumes
Kruapanich, et al^Citation186	21 PwCOPD 21 controls	Pre/post unsupported arm elevations (resting, shoulder flexion, scaption, and abduction)	Compartmental volumes using OEP Thoracoabdominal asynchrony	PwCOPD had significantly less volume in the chest wall and rib cage compared to controls Volume of the pulmonary rib cage in PwCOPD was significantly less during the three shoulder elevations compared to controls Thoracoabdominal asynchrony was affected in PwCOPD during scaption and abduction
Lee, et al^Citation187	30 PwCOPD	Pre/post inspiratory muscle training at 30% and 50% of maximal inspiratory pressure	EMG	Activation of the sternocleidomastoid and diaphragm increased during 30% and 50% training compared to quiet breathing Compared to the diaphragm, the sternocleidomastoid was activated to a greater extent
Mendes, et al^Citation188	17 PwCOPD	Pre/post quiet, diaphragmatic, and diaphragmatic + pursed-lip breathing	Compartmental volumes using OEP Thoracoabdominal asynchrony	Abdominal contribution was less than 50% for all three breathing conditions During diaphragmatic + pursed-lip breathing, the percent contribution of the pulmonary rib cage increased compared to quiet breathing Thoracoabdominal asynchrony was increased during diaphragmatic and diaphragmatic + pursed-lip breathing compared to quiet breathing
Priori, et al^Citation189	23 severe PwCOPD 12 controls	Quiet breathing in seated and supine positions	Thoracoabdominal asynchrony using OEP Diaphragm zone of apposition	In both seated and supine, controls had no thoracoabdominal asynchrony PwCOPD was similar to controls during seated During supine, asynchrony between pulmonary rib cage and abdominal compartments emerged in PwCOPD PwCOPD had greater diaphragmatic displacement when seated compared to controls with no difference in supine
Romagnoli, et al^Citation190	13 PwCOPD	No exercise, incremental and constant load unsupported arm exercise	Compartmental volumes using OEP Thoracoabdominal asynchrony	Chest wall dynamic hyperinflation was not found during constant unsupported arm exercise Thoracoabdominal asynchrony was not associated with dyspnea Arm symptoms stopped exercise, not dyspnea
Willeput, et al^Citation154	11 PwCOPD	Spontaneous breathing, low-frequency breathing, lower level breathing (prolonging expiration), high level breathing (emphasizing inspiratory effort), abdominodiaphragmatic breathing (inspiration with diaphragm alone and expiration with contraction of abdominal muscles); thoracic breathing (inspiration using thoracic accessory muscles, passive expiration)	Rib cage and abdominal motion	In most subjects, abdominodiaphragmatic breathing induced paradoxical movements compared to spontaneous breathing
Yan, et al^Citation21	19 PwCOPD	Three full inflations, three maximal sniff maneuvers, and return to spontaneous breathing	Respiratory flow Oesophageal and gastric pressures Motion of rib cage and abdomen Diaphragm electrical activity	PwCOPD divided into passive expiration group (n=9) and active expiration group (n=10) Most variables not different between groups The active group derecruited the diaphragm and recruited inspiratory rib cage muscles compared to the passive group

Abbreviations: Tx, Treatment; OEP, optoelectronic plethysmography; EMG, electromyography.

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