The Effect of Quadriceps Muscle Length on Maximum Neuromuscular Electrical Stimulation Evoked Contraction, Muscle Architecture, and Tendon-Aponeurosis Stiffness

Jonathan Galvão Tenório Cavalcante, Rita de Cassia Marqueti, Jeam Marcel Geremia, Ivo Vieira de Sousa Neto, Bruno Manfredini Baroni, Karin Gravare Silbernagel, Martim Bottaro, Nicolas Babault, João Luiz Quagliotti Durigan, Jonathan Galvão Tenório Cavalcante, Rita de Cassia Marqueti, Jeam Marcel Geremia, Ivo Vieira de Sousa Neto, Bruno Manfredini Baroni, Karin Gravare Silbernagel, Martim Bottaro, Nicolas Babault, João Luiz Quagliotti Durigan

Abstract

Muscle-tendon unit length plays a crucial role in quadriceps femoris muscle (QF) physiological adaptation, but the influence of hip and knee angles during QF neuromuscular electrical stimulation (NMES) is poorly investigated. We investigated the effect of muscle length on maximum electrically induced contraction (MEIC) and current efficiency. We secondarily assessed the architecture of all QF constituents and their tendon-aponeurosis complex (TAC) displacement to calculate a stiffness index. This study was a randomized, repeated measure, blinded design with a sample of twenty healthy men aged 24.0 ± 4.6. The MEIC was assessed in four different positions: supine with knee flexion of 60° (SUP60); seated with knee flexion of 60° (SIT60); supine with knee flexion of 20° (SUP20), and seated with knee flexion of 20° (SIT20). The current efficiency (MEIC/maximum tolerated current amplitude) was calculated. Ultrasonography of the QF was performed at rest and during NMES to measure pennation angle (θ p ) and fascicle length (L f ), and the TAC stiffness index. MEIC and current efficiency were greater for SUP60 and SIT60 compared to SUP20 and SIT20. The vastus lateralis and medialis showed lower θ p and higher L f at SUP60 and SIT60, while for the rectus femoris, in SUP60 there were lower θ p and higher L f than in all positions. The vastus intermedius had a similar pattern to the other vastii, except for lack of difference in θ p between SIT60 compared to SUP20 and SIT20. The TAC stiffness index was greater for SUP60. We concluded that NMES generate greater torque and current efficiency at 60° of knee flexion, compared to 20°. For these knee angles, lengthening the QF at the hip did not promote significant change. Each QF constituent demonstrated muscle physiology patterns according to hip and/or knee angles, even though a greater L f and lower θ p were predominant in SUP60 and SIT60. QF TAC index stiffened in more elongated positions, which probably contributed to enhanced force transmission and slightly higher torque in SUP60. Our findings may help exercise physiologist better understand the impact of hip and knee angles on designing more rational NMES stimulation strategies.

Clinical trial registration: www.ClinicalTrials.gov, identifier NCT03822221.

Keywords: exercise physiology; moment-angle relationship; muscle architecture; neuromuscular electrical stimulation; tendon-aponeurosis complex.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Cavalcante, Marqueti, Geremia, Sousa Neto, Baroni, Silbernagel, Bottaro, Babault and Durigan.

Figures

FIGURE 1
FIGURE 1
Experimental design: Participants took part in five sessions each at least 7 days apart: A familiarization and four experimental sessions to test four different combinations of hip and knee joint angles randomly during quadriceps femoris (QF) NMES. In the familiarization session, participants underwent anthropometric measurements, QF ultrasound imaging (US) during passive knee movement, MVC practice, and MEIC. In each experimental session, eight MEIC were required. The primary outcomes were the MEIC (absolute and normalized by the MVC) and the current efficiency (MEIC/current amplitude). The secondary outcome was the muscle architecture at rest and during NMES (pennation angle and fascicle length) of all QF constituents and the QF tendon-aponeurosis complex stiffness index. NMES, neuromuscular electrical stimulation; SUP60, supine with 60° of knee flexion; SIT60, seated with 60 of knee flexion; SUP20, supine with 20° of knee flexion; SIT20, seated with 20° of knee flexion, where supine was 0° of hip extension, seated was 85° of hip flexion, and full knee extension; RF, rectus femoris; VL, vastus lateralis; VM, vastus medialis; VI, vastus intermedius; MVC, maximum voluntary contraction; MEIC, maximum electrically induced contraction.
FIGURE 2
FIGURE 2
Measuring the tendon-aponeurosis complex displacement: To obtain the tendon-aponeurosis complex displacement during neuromuscular electrical stimulation of each quadriceps muscle constituent, two approaches could be used: (1) We followed a fascicle’ deep insertion from rest (A) to maximal evoked contraction plateau (B) along its visible path. (2) When a fascicle’ deep insertion could not be entirely followed from rest (C) to the maximal evoked contraction plateau (D), a linear extrapolation was performed (C).
FIGURE 3
FIGURE 3
Flowchart of the randomized single-blind study.
FIGURE 4
FIGURE 4
Muscle architecture changes of the quadriceps femoris constituents in different muscle lengths according to hip and knee angles at rest and during NMES: Pennation angle (left y axis) and fascicle length (right y axis) of all constituents of the quadriceps femoris individually and grouped at rest, during NMES (continuous lines), and main effect of position (dotted lines). Data are presented as mean and 95% CI. (A,B)Rectus femoris- (C,D)Vastus lateralis- (E,F)Vastus medialis-(G,H)Vastus intermedius. Legend: NMES, neuromuscular electrical stimulation; SUP60, supine with 60° of knee flexion; SIT60, seated with 60° of knee flexion; SUP20, supine with 20° of knee flexion; SIT20, seated with 20° of knee flexion, where supine was 0° of hip extension, seated was 85° of hip flexion, and full knee extension. Statistically significant differences: adifferent from SUP60; bdifferent from SIT60. *Indicate significant difference (p ≤ 0.05) between rest and MEIC when there was a position by time effect. The significance threshold was set at α < 0.05.
FIGURE 5
FIGURE 5
The tendon-aponeurosis complex stiffness index of the quadriceps femoris in different muscle lengths according to hip and knee angles during neuromuscular electrical stimulation. Abbreviations: SUP60, lying with 60° of knee flexion; SIT60, seated with 60° of knee flexion; SUP20, lying with 20° of knee flexion; SIT20, seated with 20° of knee flexion. Statistically significant differences: aP < 0.05 vs. SUP60; bP < 0.05 vs. SIT60. cP < 0.05 vs. SUP20. Data are presented as mean and 95% CI.

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