Gait analysis of a patient with severe motor impairment post- intensive care due to COVID-19: 1 year follow up and physical therapy

Análise da marcha de paciente com comprometimento motor grave após terapia intensiva por COVID-19: acompanhamento de 1 ano e fisioterapia

Abstract

Introduction

Viral infections, such as infection by SARS-CoV-2, can affect gait biomechanics, but this effect can be overlapped by consequences of critical illness and time in intensive care unit.

Objective

To report biomechanical alterations during the clinical evolution of a post-COVID-19 patient who presented severe motor impairment after intensive care.

Methods

Data was collected from the patient’s chart at José Silveira Foundation and previous medical reports from the hospitalization period. The patient was wheelchair bound, with physiotherapy twice a week, and by the end of 1-year follow-up was able to walk independently. Three-dimensional gait analysis with kinetics and electromyography were conducted at three time points.

Results

All spatiotemporal gait parameters, kinematic, kinetic and electromyographic data was importantly altered when compared to the normal range of values. With physiotherapy, gait quality indicators showed important improvements and all muscles presented a significant increase in the magnitude of the electromyographic signal (at least a two-fold increase). Trunk kinematic alterations decreased significantly during this period. Kinetic and kinematic changes perceived in the hips, knees and ankles showed approximation to the expected pattern, however still without normalizing, and patient's muscle coordination improved over time.

Conclusion

This report has great clinical importance, as it describes, using an instrumented gait laboratory, the evolution of a patient with severe motor impairment post intensive care due to COVID-19, a condition in lack of description in the literature, which will help health professionals in the planning of rehabilitation strategies.

Critical illness patient; COVID-19; Gait biomechanics; Polyneuropathy

Resumo

Introdução

Infecções virais, como a infecção por SARS-CoV-2, podem afetar a biomecânica da marcha, mas esse efeito pode ser sobreposto por consequências de doença crítica e tempo em unidade de terapia intensiva.

Objetivo

Relatar as alterações biomecânicas durante a evolução clínica de um paciente pós-COVID-19 que apresentou comprometimento motor severo após terapia intensiva.

Métodos

Os dados foram coletados a partir do prontuário do paciente na Fundação José Silveira e dos relatórios médicos anteriores referentes ao período de inter-nação. O paciente estava em cadeira de rodas, com fisioterapia duas vezes por semana, e ao final de 1 ano de acompanhamento era capaz de deambular de forma independente. A análise tridimensional da marcha com cinética e eletromiografia foi realizada em três momentos.

Resultados

Todos os parâmetros espaço-temporais da marcha, dados cinemáticos, cinéticos e eletromiográficos estavam significativamente alterados quando comparados com a faixa normal de valores. Com a fisioterapia, os indicadores de qualidade da marcha apresentaram melhorias importantes e todos os músculos apresentaram um aumento significativo na magnitude do sinal eletromiográfico (aumento de pelo menos duas vezes). As alterações cinemáticas do tronco diminuíram significativamente neste período. As alterações cinéticas e cinemáticas percebidas nos quadris, joelhos e tornozelos mostraram aproximação do padrão esperado, porém ainda sem normalização, e a coordenação muscular do paciente melhorou com o passar do tempo.

Conclusão

Este relato é de grande importância clínica, pois descreve, por meio de um laboratório de marcha instrumentado, a evolução de um paciente com comprometimento motor severo após terapia intensiva por COVID-19, quadro pouco descrito na literatura, o que ajudará profissionais de saúde no planejamento de estratégias de reabilitação.

Paciente crítico; COVID-19; Biomecânica da marcha; Polineuropatia

Introduction

Patients with moderate forms of COVID-19 usually have a full recovery, but patients who presented severe or critical form of the disease may present multiple impairments.¹ The clinical presentation after COVID-19 may be due to viral infection² or to the consequences of post-intensive care syndrome (PICS), which can result in impairment of physical and cognitive function.³ PICS consequences are observed for up to six months post-discharge, emphasizing the importance of rehabilitation for these patients.⁴

Important gait impairments previously reported are Guillain-Barré syndrome,² axonal polyneuropathy,⁵ bilateral intentional tremor and increased base support,⁶ and coordination and strength loss.⁷ Description of gait biomechanics in patients with polyneuropathies⁸-¹² and patients with PICS¹³ are scarce. However, to the best of our knowledge, there are no reports on changes in gait kinematics, kinetics, and electromyography in patients with severe motor impairment and peripheral polyneuropathy after intensive care by COVID-19. Such description is fundamental to better understand pathologies effects in movement strategies.¹⁴ Thus, the aim of this study was to report gait biomechanics of a patient who presented severe motor impairment and peripheral polyneuropathy due to COVID-19 and PICS.

Methods

This study followed all ethical instructions by National Health Council and was approved by local Ethics Com-mittee (53183221.0.0000.5543). Data was collected from patient’s chart at Bahian Institute of Rehabilitation of the José Silveira Foundation (IBR-FJS) and from reports of hospitalization period.

Case description

A 53-yo male patient with a medical history of hyper-tension, type 2 diabetes, myalgia and polyarthralgia presented with a fever lasting two days (April 27th, 2020). Despite normal vital signs, the patient experienced glycemic decompensation (HGT 375 mg/DI) and tested positive for dengue (IgG and IgM antibodies), along with mild thrombocytopenia (Hb 16.1 and plaq 103000). The patient returned with severe myalgia, high blood glucose levels (HGT 310mg/DI), dry cough and severe sweating (May 1st). RT-PCR test was positive for SARS-CoV-2, leading to the patient's admission to the intensive care unit due to acute respiratory failure and oxygen desaturation (May 4th). Nasal oxygen catheter was administered, followed by intubation, and 15 days later a tracheostomy was performed. The patient also started hemodialysis (May 7th) due to renal dysfunction.

Additionally, the patient experienced a tonic-clonic seizure, which was successfully treated with Diazepam, and Hidantal was prescribed. A skull magnetic reso-nance imaging revealed the presence of a bilateral mastoiditis jugulotympanic glomus tumor. The patient remained hospitalized for a duration of 95 days, during which he received 30-minute physiotherapy sessions consistently throughout his hospital stay, including the period spent in the intensive care unit. Following his discharge on August 6th, the patient initiated home-based physiotherapy, 30-minute sessions twice a week, starting August 11th.

On November 25th the patient was evaluated at IBR-FJS, still relying on a wheelchair and with no respira-tory complaints. He presented significant muscular atrophy and initiated clinical physical therapy for lower limbs strengthening, functional independence and gait retraining with a walker. Outdoors he used a wheelchair until December. In January he started to use a walker full time. Polyneuropathy was diagnosed (February 11th, 2021) and in February he performed the first gait analysis (A1). In March he began using crutches at home and walker on outdoor walks. In April he started using crutches outdoor and a cane at home.

On April 13th, an ankle foot orthosis was prescribed due to footdrop of the right foot. On July 27th, he began using a cane outdoors and independent gait at home. In August the second gait analysis (A2) was performed. On August 26th, he progressed to a fully independent gait. He maintained rehabilitation until the last gait analysis (A3), in October 2021. Events are summarized in Figure 1.

Figure 1
Timeline of events occurred from disease onset until end of follow-up period.

Data acquisition

Kinematic (8 SMART-DX 400 infrared cameras), Kinetic (4 P-6000 force platforms), and EMG (8 channels FreeEMG 1000) gait data was collected from three-dimensional gait reports (BTS Bioengineering Milano, Italy) from February (A1), August (A2) and October (A3) using 22 markers Helen-Hayes protocol.¹⁵,¹⁶ Surface electromyography of tibialis anterior, gastrocnemius medialis, rectus femoris and semitendinosus muscles were acquired according to SENIAM project recommen-dations (Surface ElectroMyoGraphy for Non-Invasive Assessment of Muscles). Selected data from the three-dimensional gait reports were: the patient's joints angles, joints internal moments, muscle power and electromyographic data during the three evaluations; and the following spatiotemporal gait parameters (SGP): stride, stance and swing times; stance, swing, single support, double support phases; stride length, step length, mean velocity, cadence, step width, propulsion, Gait Profile Score (GPS),¹⁷ Gait Deviation Index (GDI)¹⁸ and Timed Up and Go (TUG) test time.

Results

All SGP were below expected in A1. After physio-therapy, gait speed, cadence, swing phase and single support increased, while stance phase and double support phase decreased, showing improvements. Against expectations, step length decreased and step width increased. Both GPS and GDI improved (Table 1). In A1 the patient presented high trunk flexion and anterior pelvic tilt (Figure 2). A normalized trunk kinematics and reduced pelvic tilt was seen in A2 (Figure 2). From A1 to A3, decreased flexion angle of the hips can be observed (Figure 2) with persistent extensor moment during mid-stance (Figure 3). In A3, there was an incipient hip flexor moment and power (Figures 3 and 4, respectively). Persistent knee flexion during stance and delayed peak flexion during swing phase (Figure 2) associated with persistent knee extensor moment was noted in all assessments (Figure 3). Despite the incresead knee flexion angle, rectus femoris showed a better pattern in A2 and A3 compared to A1 (Figure 5). Simultaneously, hamstrings were coactivated during initial contact and load response (Figure 5).

Table 1
Results of the spatiotemporal gait parameters, scores and gait indexes of the patient during the three evaluations

Spatiotemporal Gait Parameters	Assessment 1		Assessment 2		Assessment 3		Normal values*
	RL	LL	RL	LL	RL	LL
Stride time (s)	3.62 ± 0.15	3.40 ± 0.47	1.76 ± 0.07	1.74 ± 0.08	1.41 ± 0.07	1.42 ± 0.06	1.10 ± 0.09
Stance time (s)	2.81 ± 0.17	1.28 ± 0.09	1.28 ± 0.09	1.24 ± 0.10	0.95 ± 0.05	0.95 ± 0.07	0.65 ± 0.07
Swing time (s)	0.81 ± 0.02	0.47 ± 0.04	0.47 ± 0.04	0.50 ± 0.08	0.46 ±0.05	0.47 ± 0.05	0.44 ± 0.05
Stance phase (%)	77.66 ± 1.40	72.52 ± 2.55	72.52 ± 2.55	71.06 ± 4.26	67.59 ± 2.43	66.63 ± 3.27	59.98 ± 1.97
Swing Phase (%)	22.34 ± 1.40	26.75 ± 2.72	26.75 ± 2.72	28.87 ± 4.63	32.41 ± 2.43	33.39 ± 3.27	40.03 ± 3.56
Single support phase (%)	23.48 ± 1.71	28.49 ± 4.66	28.49 ± 4.66	27.14 ± 2.84	33.79 ± 3.99	32.13 ± 2.95	38.87 ± 2.57
Double support phase (%)	28.90 ± 2.73	22.49 ± 1.63	22.49 ± 1.63	21.97 ± 3.61	18.26 ± 0.74	15.74 ± 2.16	10.27 ± 3.09
Stride length (m)	0.56 ± 0.04	0.45 ± 0.06	0.45 ± 0.06	0.44 ± 0.04	0.65 ± 0.06	0.66 ± 0.05	1.36 ± 0.11
Stride length (%height)	34.76 ± 2.37	28.20 ± 3.57	28.20 ± 3.57	27.03 ± 2.70	40.47 ± 3.55	40.87 ± 3.01	80.00 ± 0.10
Step length (m)	0.25 ± 0.02	0.22 ± 0.04	0.22 ± 0.04	0.23 ± 0.02	0.34 ± 0.03	0.32 ± 0.07	0.62 ± 0.05
Mean velocity (m/s)	0.20 ± 0.00		0.30 ± 0.00		0.50 ± 0.00		1.20 ± 0.20
Mean velocity (%height/s)	9.50 ± 0.73		16.00 ± 2.50		28.80 ± 2.70		80.00 ± 5.00
Cadence (steps/min)	34.65 ± 3.24		68.70 ± 3.99		85.00 ± 4.05		114.00 ± 4.20
Step width (m)	0.17 ± 0.01		0.24 ± 0.01		0.19 ± 0.01		0.08 ± 0.05
Propulsion	0.60	0.70	1.00	1.50	2.80	3.40	-
Gait profile score	15.80 ± 0.20	14.60 ± 0.20	13.50 ± 0.60	10.80 ± 0.30	12.20 ± 0.30	10.40 ± 0.40	< 7
Gait deviation index	70.36 ± 0.48	72.72 ± 0.56	76.63 ± 1.51	85.58 ± 1.41	81.37 ± 1.35	86.66 ± 1.29	> 100
TUG (s)	63.71		23.37		15.66		< 15s

• Note: RL = right limb; LL = left limb; TUG = Timed Up and Go test; m = meters; s = seconds. Results presented in average ± standard deviation.
• *Normality values are offered by the manufacturer of the acquisition system (BTS Bioengineering, Milan Italy).

Figure 2
Joints kinematics results during the three assessments. The red line represents the left lower limb, and the green line represents the right lower limb, while the gray-filled area represents the normal gait pattern described by the system.

Figure 3
Results of kinetics of the hips (A), knees (B) and ankles (C) during the three assessments. The first row shows the results of kinematics (same as figure 2, for better visualization) and the second row shows joint internal moment. The red line represents the left lower limb, and the green line represents the right lower limb, while the gray-filled area represents the normal gait pattern described by the system.

Figure 4
Results of kinetics of the hips (A), knees (B) and ankles (C) during the three assessments. The first row shows the results of kinematics (same as Figure 2, for better visualization) and the second row shows joint muscle power. The red line represents the left lower limb, and the green line represents the right lower limb, while the gray-filled area represents the normal gait pattern described by the system.

Figure 5
Surface electromyography of the tibialis anterior, gastrocnemius medialis, rectus femoris and semitendinosus muscles during the three assessments of the right lower limb (A) and the left lower limb (B). The blue line represents mean EMG activation while the blue-filled area represents the standard deviation.

All assessments showed inadequate ankle pre-positioning, increased dorsiflexion, delayed plantar flexion (Figure 2) and low production of plantar flexor moment (Figure 3). However, we observed a great gain in muscle power and EMG (Figures 4 and 5, respectively).

Discussion

SARS-CoV-2 patients may present peripheral nervous system impairments such as polyneuropathy.⁵ It is possible that the viral infection itself can affect funda-mental aspects of gait biomechanics, but this effect can be overlapped by PICS¹³,¹⁹ and by hyperglycemia comorbidities.⁸,¹⁰ It is known that hyperglycemia is asso-ciated with a poor prognosis and severe COVID-19 even without diabetes diagnosis prior to admission.²⁰,²¹ We do not have a gait analysis prior to patient’s admission, however, as reported by the patient and family, he was functional and active before COVID-19. Therefore, it can be inferred that the disease, hospitalization, and their associated complications were responsible for the severe motor impairments observed.

Three assessments were conducted post-discharge, including spatiotemporal, electromyographic, kinetic, and kinematic evaluations of gait. It is worth noting that the most significant improvements in electromyographic, kinetic, and kinematic variables were already observed at A2 and remained consistent at A3. However, various spatiotemporal variables such as stance time, stance phase, single support phase, stride length, velocity, cadence, and TUG continued to show progress from A1 to A2 and from A2 to A3, even without notable changes in the kinetic, kinematic, and electromyographic graphs.

In A1, stance phase, double support phase, gait speed, cadence, step length, variables commonly associated with gait stability and functional capacity were far below normal.²²-²⁵ Individuals with diabetic neuropathy may present alterations in gait speed, cadence, and step length.¹⁰,²⁶ Changes in the stance phase and double support phase may be attributed to central nervous system impairments caused by COVID-19.¹⁰,²⁷ Step length and gait speed are associated with lower limb weakness, while time variables may indicate balance impairments due to neuropathology.²⁸ During A3, de-spite the improvement compared to A2, a reduction in velocity was still observed, indicating the need for further intervention (physiotherapy or exercises) in this variable as it is highly related to the patient's life expectancy.²⁹ Additionally, step width, cadence, and stance time still deviated from normal values in A3, suggesting the persistence of deficits in balance control and residual motor control impairments even after the rehabilitation period.³⁰,³¹

Patients discharged from intensive care unit may present a "cautious" gait pattern due to decreased joint range of motion and power deficits related to limb weak-ness and stiffness.¹³ Physiotherapy program increased speed, stance time and cadence⁹ attributable to improve-ment of joint range of motion,³² as well as lower limbs strength gains¹³ in the early weeks of intervention.³³-³⁵ Furthermore, the progression of TUG test results over assessments indicates functional gains, similar to what is observed in cases of peripheral neuropathy.¹¹

Patients´ hip gait kinematics is similar to patients with other neuropathy, showing a reduced range of motion and increased hip flexion.³⁶,³⁷ Similar hip moments can be found in diabetic patients.³⁷,³⁸These similarities in gait alterations can be due to similar neuromotor issues between pathologies. In A2 and A3, the slight increase in hip flexor moment may have occurred by psoas and iliac muscles action.³⁹,⁴⁰

The decreased knee range of motion may be asso-ciated with stiffening of the joint in order to maintain postural balance.¹⁰ In A2 and A3, rectus femoris EMG demonstrated a clear peak during stance, possibly caused by increase in gait speed, once the quadriceps has the function of deceleration during stance phase. ⁴¹

Contrary to expected, hamstrings presented recruit-ment during initial contact and loading response in A2 and A3.³⁹,⁴¹,⁴² Four mechanisms may explain the increased hamstring activity: coactivation caused by increased knee flexion; hip and knee flexion acceleration deficits during stance to swing transition, caused by the plantar flexion weakness; the need to generate an exaggerated knee flexion during the swing phase; the performance as synergists in attempt to extend the hips.³⁹,⁴²,⁴³ By Ockham's razor, the first mechanism is the most likely.

Recruitment deficits of distal musculature such as tibialis anterior and gastrocnemius medialis can cause changes in proximal joints kinematics.⁴²,⁴⁴ This may partly explain certain kinematic changes in A1 and A2, such as decreased knee flexion peak during the transition from stance to swing, and increased knee and hip flexion during the stance phase.⁴¹-⁴³ In addition, the triceps surae contributes to the upright posture,³⁹,⁴⁰ extending all three joints and providing a large contribution to body weight support,⁴¹ which may have also contributed to important trunk and hip flexion at A1. These are similar alterations found in patients with diabetic polyneuropathy who adopt a gait pattern with propulsion generated predominantly by the hips.¹⁰

During A1 and A2, the recruitment of tibialis anterior was affected, as it failed to provide clearance of the foot during the swing phase.³⁹,⁴⁰ This recruitment deficit justifies the foot drop during A1, A2 and A3, a recurrent condition in patients with neurological lesions,⁴⁵,⁴⁶ which reinforces the hypothesis of COVID-19 and PICS impact on patients important neurological aspects.

The patient presented slightly flexed hip and knees throughout evaluations, similar to crouch knee gait,⁴¹,⁴³ which can be explained by the persistent insufficiency of the plantar flexor mechanism,⁴⁰,⁴¹,⁴³,⁴⁷ usually related to muscle weakness, motor control deficits and lack of proprioceptive feedback.⁴⁸

This study has limitations, once we had limited information on patient’s previous gait condition, drug treatments and diagnoses. Nonetheless, this report has great clinical importance as it describes complete clinical gait analysis evolution of a patient with PICS due to COVID-19.

Conclusion

We observed important improvements in gait kinematics, kinetics, and electromyography of a patient with severe motor impairment post-COVID-19, after 12 months of follow-up, and the results are similar to other neurological diseases already known.

Acknowledgments

The authors acknowledge support from José Silveira Foundation (Brazil) and the National Program to Support Health Care for Persons with Disabilities (Pronas/PCD) (Brazil).

References

• ¹
  Carda S, Invernizzi M, Bavikatte G, Bensmaïl D, Bianchi F, Deltombe T, et al. COVID-19 pandemic. What should Physical and Rehabilitation Medicine specialists do? A clinician's perspective. Eur J Phys Rehabil Med. 2020;56(4):515-24. https://doi.org/10.23736/s1973-9087.20.06317-0
  » https://doi.org/10.23736/s1973-9087.20.06317-0
• ²
  Orrù G, Conversano C, Malloggi E, Francesconi F, Ciacchini R, Gemignani A. Neurological complications of covid-19 and possible neuroinvasion pathways: A systematic review. Int J Environ Res Public Health. 2020;17(18):6688. https://doi.org/10.3390/ijerph17186688
  » https://doi.org/10.3390/ijerph17186688
• ³
  Kosilek RP, Schmidt K, Baumeister SE, Gensichen J. Frequency and risk factors of post-intensive care syndrome components in a multicenter randomized controlled trial of German sepsis survivors. J Crit Care. 2021;65:268-73. https://doi.org/10.1016/j.jcrc.2021.07.006
  » https://doi.org/10.1016/j.jcrc.2021.07.006
• ⁴
  Sidiras G, Patsaki I, Karatzanos E, Dakoutrou M, Kouvarakos A, Mitsiou G, et al. Long term follow-up of quality of life and functional ability in patients with ICU acquired Weakness – A post hoc analysis. J Crit Care. 2019;53:223-30. https://doi.org/10.1016/j.jcrc.2019.06.022
  » https://doi.org/10.1016/j.jcrc.2019.06.022
• ⁵
  Tramonti C, Vatteroni E, Iacopini F, Carli V, Iardella M. Axonal polineuropathy associated with Sars-CoV 2 infection: A case report. Eur J Transl Myol. 2021;31(3):9900. https://doi.org/10.4081/ejtm.2021.9900
  » https://doi.org/10.4081/ejtm.2021.9900
• ⁶
  Klein S, Davis F, Berman A, Koti S, D'Angelo J, Kwon N. A case report of Coronavirus Disease 2019 presenting with tremors and gait disturbance. Clin Pract Cases Emerg Med. 2020;4(3): 324-6. https://doi.org/10.5811/cpcem.2020.5.48023
  » https://doi.org/10.5811/cpcem.2020.5.48023
• ⁷
  Abdelnour L, Abdalla ME, Babiker S. COVID-19 infection presenting as motor peripheral neuropathy. J Formos Med Assoc. 2020;119(6):1119-20. https://doi.org/10.1016/j.jfma.2020.04.024
  » https://doi.org/10.1016/j.jfma.2020.04.024
• ⁸
  Shin KJ, Kang JW, Sung KH, Park SH, Kim SE, Park KM, et al. Quantitative gait and postural analyses in patients with diabetic polyneuropathy. J Diabetes Complic. 2021;35(4):107857. https://doi.org/10.1016/j.jdiacomp.2021.107857
  » https://doi.org/10.1016/j.jdiacomp.2021.107857
• ⁹
  Vo ML, Chin RL, Miranda C, Latov N. Changes in spatiotem-poral gait parameters following intravenous immunoglobulin treatment for chronic inflammatory demyelinating polyneu-ropathy. Muscle Nerve. 2017;56(4):732-6. https://doi.org/10.1002/mus.25553
  » https://doi.org/10.1002/mus.25553
• ¹⁰
  Sawacha Z, Gabriella G, Cristoferi G, Guiotto A, Avogaro A, Cobelli C. Diabetic gait and posture abnormalities: A biomechanical investigation through three dimensional gait analysis. Clin Biomech (Bristol, Avon). 2009;24(9):722-8. https://doi.org/10.1016/j.clinbiomech.2009.07.007
  » https://doi.org/10.1016/j.clinbiomech.2009.07.007
• ¹¹
  Caronni A, Picardi M, Pintavalle G, Aristidou E, Redaelli V, Antoniotti P, et al. Responsiveness to rehabilitation of balance and gait impairment in elderly with peripheral neuropathy. J Biomech. 2019;94:31-8. https://doi.org/10.1016/j.jbiomech.2019.07.007
  » https://doi.org/10.1016/j.jbiomech.2019.07.007
• ¹²
  Bozovic I, Peric M, Azanjac AA, Palibrk A, Bulatovic I, Aleksic D, et al. Prospective analysis of disability and quality of life in patients with chronic inflammatory demyelinating polyradiculoneuropathy. Qual Life Res. 2021;30(9):2573-9. https://doi.org/10.1007/s11136-021-02838-w
  » https://doi.org/10.1007/s11136-021-02838-w
• ¹³
  Kiriella JB, Araujo T, Vergara M, Lopez-Hernandez L, Cameron JI, Herridge M, et al. Quantitative evaluation of muscle function, gait, and postural control in people experiencing critical illness after discharge from the intensive care unit. Phys Ther. 2018;98(1):8-15. https://doi.org/10.1093/ptj/pzx102
  » https://doi.org/10.1093/ptj/pzx102
• ¹⁴
  Patikas D, Wolf SI, Schuster W, Armbrust P, Dreher T, Döderlein L. Electromyographic patterns in children with cerebral palsy: do they change after surgery? Gait Posture. 2007;26(3):362-71. https://doi.org/10.1016/j.gaitpost.2006.10.012
  » https://doi.org/10.1016/j.gaitpost.2006.10.012
• ¹⁵
  Hamner SR, Seth A, Delp SL. Muscle contributions to propulsion and support during running. J Biomech. 2010; 43(14):2709-16. https://doi.org/10.1016/j.jbiomech.2010.06.025
  » https://doi.org/10.1016/j.jbiomech.2010.06.025
• ¹⁶
  Kadaba MP, Ramakrishnan HK, Wootten ME. Measurement of lower extremity kinematics during level walking. J Orthop Res. 1990;8(3):383-92. https://doi.org/10.1002/jor.1100080310
  » https://doi.org/10.1002/jor.1100080310
• ¹⁷
  Baker R, McGinley JL, Schwartz MH, Beynon S, Rozumalski A, Graham HK, et al. The gait profile score and movement analysis profile. Gait Posture. 2009;30(3):265-9. https://doi.org/10.1016/j.gaitpost.2009.05.020
  » https://doi.org/10.1016/j.gaitpost.2009.05.020
• ¹⁸
  Schwartz MH, Rozumalski A. The Gait Deviation Index: a new comprehensive index of gait pathology. Gait Posture. 2008;28(3):351-7. https://doi.org/10.1016/j.gaitpost.2008.05.001
  » https://doi.org/10.1016/j.gaitpost.2008.05.001
• ¹⁹
  Morelli N, Parry SM, Steele A, Lusby M, Montgomery-Yates AA, Morris PE, et al. Patients surviving critical COVID-19 have Impairments in dual-task performance related to post-intensive care syndrome. J Intensive Care Med. 2022;37(7):890-8. https://doi.org/10.1177/08850666221075568
  » https://doi.org/10.1177/08850666221075568
• ²⁰
  Ushigome E, Hamaguchi M, Sudo K, Kitagawa N, Kondo Y, Imai D, et al. Impact of untreated diabetes and COVID-19-related diabetes on severe COVID-19. Heliyon. 2022;8(1):e08801. https://doi.org/10.1016/j.heliyon.2022.e08801
  » https://doi.org/10.1016/j.heliyon.2022.e08801
• ²¹
  Grasselli G, Zangrillo A, Zanella A, Antonelli M, Cabrini L, Castelli A, et al. Baseline characteristics and outcomes of 1591 patients infected with SARS-CoV-2 admitted to ICUs of the Lombardy Region, Italy. JAMA. 2020;323(16):1574-81. https://doi.org/10.1001/jama.2020.5394
  » https://doi.org/10.1001/jama.2020.5394
• ²²
  Dingwell JB, Marin LC. Kinematic variability and local dynamic stability of upper body motions when walking at different speeds. J Biomech. 2006;39(3):444-52. https://doi.org/10.1016/j.jbiomech.2004.12.014
  » https://doi.org/10.1016/j.jbiomech.2004.12.014
• ²³
  Peebles AT, Reinholdt A, Bruetsch AP, Lynch SG, Huisinga JM. Dynamic margin of stability during gait is altered in persons with multiple sclerosis. J Biomech. 2016;49(16):3949-55. https://doi.org/10.1016/j.jbiomech.2016.11.009
  » https://doi.org/10.1016/j.jbiomech.2016.11.009
• ²⁴
  Madehkhaksar F, Klenk J, Sczuka K, Gordt K, Melzer I, Schwenk M. The effects of unexpected mechanical perturbations during treadmill walking on spatiotemporal gait parameters, and the dynamic stability measures by which to quantify postural response. PLoS One. 2018;13(4):e0195902. https://doi.org/10.1371/journal.pone.0195902
  » https://doi.org/10.1371/journal.pone.0195902
• ²⁵
  van Vugt Y, Stinear J, Davies TC, Zhang Y. Postural stability during gait for adults with hereditary spastic paraparesis. J Biomech. 2019;88:12-7. https://doi.org/10.1016/j.jbiomech.2019.03.001
  » https://doi.org/10.1016/j.jbiomech.2019.03.001
• ²⁶
  Menz HB, Lord SR, St George R, Fitzpatrick RC. Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. Arch Phys Med Rehabil. 2004;85(2):245-52. https://doi.org/10.1016/j.apmr.2003.06.015
  » https://doi.org/10.1016/j.apmr.2003.06.015
• ²⁷
  Chuang DT, Aydemir S, Magda P, Thomas C, Zarnegar R. Neurological manifestations as primary presentation of COVID-19 in hospitalized patients. Acta Neurol Scand. 2021; 143(5):569-74. https://doi.org/10.1111/ane.13399
  » https://doi.org/10.1111/ane.13399
• ²⁸
  Bozovic I, Peric S, Basta I, Rakocevic-Stojanovic V, Lavrnic D, Stevic Z, et al. Prospective analysis of gait characteristics in chronic inflammatory demyelinating polyradiculoneuropathy. J Clin Neurosci. 2020;80:6-10. https://doi.org/10.1016/j.jocn.2020.08.009
  » https://doi.org/10.1016/j.jocn.2020.08.009
• ²⁹
  Studenski S, Perera S, Patel K, Rosano C, Faulkner K, Inzitari M, et al. Gait speed and survival in older adults. JAMA. 2011;305(1):50-8. https://doi.org/10.1001/jama.2010.1923
  » https://doi.org/10.1001/jama.2010.1923
• ³⁰
  Costa TM, Simieli L, Bersotti FM, Mochizuki L, Barbieri FA, Coelho DB. Gait and posture are correlated domains in Parkinson's disease. Neurosci Lett. 2022;775:136537. https://doi.org/10.1016/j.neulet.2022.136537
  » https://doi.org/10.1016/j.neulet.2022.136537
• ³¹
  Zhou H, Nguyen H, Enriquez A, Morsy L, Curtis M, Piser T, et al. Assessment of gait and balance impairment in people with spinocerebellar ataxia using wearable sensors. Neurol Sci. 2022;43(4):2589-99. https://doi.org/10.1007/s10072-021-05657-6
  » https://doi.org/10.1007/s10072-021-05657-6
• ³²
  Caravaggi P, Giacomozzi C, Lullini G, Marchesini G, Baccolini L, Ortolani M, et al. The effect of neuropathy and diabetes type on multisegment foot kinematics: A cohort study on 70 participants with diabetes. Appl Sci (Switzerland). 2021;11(19):8848. https://doi.org/10.3390/app11198848
  » https://doi.org/10.3390/app11198848
• ³³
  Volpe D, Spolaor F, Sawacha Z, Guiotto A, Pavan D, Bakdounes L, et al. Muscular activation changes in lower limbs after underwater gait training in Parkinson’s disease: A surface emg pilot study. Gait Posture. 2020;80:185-91. https://doi.org/10.1016/j.gaitpost.2020.03.017
  » https://doi.org/10.1016/j.gaitpost.2020.03.017
• ³⁴
  Colborne GR, Olney SJ, Griffin MP. Feedback of ankle joint angle and soleus electromyography in the rehabilitation of hemiplegic gait. Arch Phys Med Rehabil. 1993;74(10):1100-6. https://doi.org/10.1016/0003-9993(93)90069-m
  » https://doi.org/10.1016/0003-9993(93)90069-m
• ³⁵
  Teasell RW, Bhogal SK, Foley NC, Speechley MR. Gait re-training post stroke. Top Stroke Rehabil. 2003;10(2):34-65. https://doi.org/10.1310/udxe-mjff-53v2-eap0
  » https://doi.org/10.1310/udxe-mjff-53v2-eap0
• ³⁶
  Hazari A, Maiya AG, Shivashankara KN, Agouris I, Monteiro A, Jadhav R, et al. Kinetics and kinematics of diabetic foot in type 2 diabetes mellitus with and without peripheral neuropathy: a systematic review and meta-analysis. Springerplus. 2016; 5(1):1819. https://doi.org/10.1186/s40064-016-3405-9
  » https://doi.org/10.1186/s40064-016-3405-9
• ³⁷
  Fernando M, Crowther R, Lazzarini P, Sangla K, Cunningham M, Buttner P, et al. Biomechanical characteristics of peripheral diabetic neuropathy: A systematic review and meta-analysis of findings from the gait cycle, muscle activity and dynamic barefoot plantar pressure. Clin Biomech (Bristol, Avon). 2013; 28(8):831-45. https://doi.org/10.1016/j.clinbiomech.2013.08.004
  » https://doi.org/10.1016/j.clinbiomech.2013.08.004
• ³⁸
  Sacco ICN, Picon AP, Macedo DO, Butugan MK, Watari R, Sartor CD. Alterations in the lower limb joint moments precede the peripheral neuropathy diagnosis in diabetes patients. Diabetes Technol Ther. 2015;17(6):405-12. https://doi.org/10.1089/dia.2014.0284
  » https://doi.org/10.1089/dia.2014.0284
• ³⁹
  Perry J, Burnfield JM. Gait analysis: normal and pathological function. 2 ed. Thorofare, NJ: Slack Inc.; 2010. 551 p.
• ⁴⁰
  Brunner R, Romkes J. Abnormal EMG muscle activity during gait in patients without neurological disorders. Gait Posture. 2008;27(3):399-407. https://doi.org/10.1016/j.gaitpost.2007.05.009
  » https://doi.org/10.1016/j.gaitpost.2007.05.009
• ⁴¹
  Steele KM, Seth A, Hicks JL, Schwartz MS, Delp SL. Muscle contributions to support and progression during single-limb stance in crouch gait. J Biomech. 2010;43(11):2099-105. https://doi.org/10.1016/j.jbiomech.2010.04.003
  » https://doi.org/10.1016/j.jbiomech.2010.04.003
• ⁴²
  Knarr BA, Reisman DS, Binder-Macleod SA, Higginson JS. Understanding compensatory strategies for muscle weakness during gait by simulating activation deficits seen post-stroke. Gait Posture. 2013;38(2):270-5. https://doi.org/10.1016/j.gaitpost.2012.11.027
  » https://doi.org/10.1016/j.gaitpost.2012.11.027
• ⁴³
  Arnold AS, Anderson FC, Pandy MG, Delp SL. Muscular contributions to hip and knee extension during the single limb stance phase of normal gait: a framework for investigating the causes of crouch gait. J Biomech. 2005;38(11):2181-9. https://doi.org/10.1016/j.jbiomech.2004.09.036
  » https://doi.org/10.1016/j.jbiomech.2004.09.036
• ⁴⁴
  Błażkiewicz M, Wit A. Compensatory strategy for ankle dorsiflexion muscle weakness during gait in patients with drop-foot. Gait Posture. 2019;68:88-94. https://doi.org/10.1016/j.gaitpost.2018.11.011
  » https://doi.org/10.1016/j.gaitpost.2018.11.011
• ⁴⁵
  Slowik JS, McNitt-Gray JL, Requejo PS, Mulroy SJ, Neptune RR. Compensatory strategies during manual wheelchair propul-sion in response to weakness in individual muscle groups: A simulation study. Clin Biomech (Bristol, Avon). 2016;33:34-41. https://doi.org/10.1016/j.clinbiomech.2016.02.003
  » https://doi.org/10.1016/j.clinbiomech.2016.02.003
• ⁴⁶
  Błażkiewicz M, Wiszomirska I, Kaczmarczyk K, Brzuszkiewicz-Kuźmicka G, Wit A. Mechanisms of compensation in the gait of patients with drop foot. Clin Biomech (Bristol, Avon). 2017;42:14-9. https://doi.org/10.1016/j.clinbiomech.2016.12.014
  » https://doi.org/10.1016/j.clinbiomech.2016.12.014
• ⁴⁷
  Sutherland DH, Cooper L, Daniel D. The role of the ankle plantar flexors in normal walking. J Bone Joint Surg Am. 1980; 62(3):354-63. https://journals.lww.com/jbjsjournal/citation/1980/62030/the_role_of_the_ankle_plantar_flexors_in_normal.5.aspx
  » https://journals.lww.com/jbjsjournal/citation/1980/62030/the_role_of_the_ankle_plantar_flexors_in_normal.5.aspx
• ⁴⁸
  Melai T, Schaper NC, Ijzerman TH, Willems PJB, de Lange TLH, Meijer K, et al. Strength training affects lower extremity gait kinematics, not kinetics, in people with diabetic polyneuropathy. J Appl Biomech. 2014;30(2):221-30. https://doi.org/10.1123/jab.2013-0186
  » https://doi.org/10.1123/jab.2013-0186

Publication Dates

• Publication in this collection
  25 Sept 2023
• Date of issue
  2023

History

• Received
  8 May 2023
• Reviewed
  14 July 2023
• Accepted
  23 Aug 2023