Abstract
Electrically evoked torque at rest (i.e., the torque produced from supramaximal stimul applied to a resting muscle) has been shown to be related to muscle size in healthy adults, but this relationship has not been evaluated in pathological populations where atrophy is present. This study aimed to evaluate the relationship between the electrically evoked torque at rest and vastus lateralis cross-sectional area (CSA) in individuals with anterior cruciate ligament (ACL) reconstruction. Eighteen individuals with ACL reconstruction participated. Quadriceps electrically evoked torque at rest was elicited bilaterally via sex-specific, standardized supramaximal triplet stimulations. Vastus lateralis CSA was measured at 50% of thigh length using ultrasound. Pearson’s r and partial correlations were used to evaluate associations between outcomes. Evoked torque at rest was positively associated with vastus lateralis CSA in the ACL reconstructed limb (r=0.865, partial r=0.816, P<0.01), non-reconstructed limb (r=0.628, partial r=0.575, P<0.05), and side-to-side ratios (r=0.670, partial r=0.659, P<0.01). These results indicate that electrically evoked torque at rest may indirectly assess side-to-side differences in quadriceps muscle size after ACL reconstruction.
Keywords: Twitch, Resting Torque, Cross-sectional Area, Morphology
Introduction
Quadriceps muscle weakness is a complex and persistent issue in individuals with anterior cruciate ligament (ACL) reconstruction.(Lisee, Lepley, Birchmeier, O’Hagan, & Kuenze, 2019) Considerable quadriceps atrophy ensues after ACL reconstruction (i.e., reduction in muscle size or cross-sectional area [CSA]) due to disuse and altered spinal/supraspinal excitability and is known to contribute to the chronic and persistent quadriceps weakness in ACL-reconstructed individuals. (Birchmeier et al., 2019; Kuenze, Blemker, & Hart, 2016; Norte et al., 2017; Thomas, Wojtys, Brandon, & Palmieri-Smith, 2016) Further, recent evidence has demonstrated that quadriceps atrophy plays a role in suboptimal patient-reported outcomes (e.g., scores on the International Knee Documention Committee and Knee Injury and Osteaorthritis Outcome scales) after ACL reconstruction.(Garcia, Curran, & Palmieri-Smith, 2020; Garcia, Moffit, et al., 2020) Therefore, the ability to assess changes in quadriceps muscle morphology (i.e., atrophy) after ACL injury and surgery is of benefit to clinicians and researchers focusing on ACL rehabilitation research.
Muscle size, strength, and contractile properties are considered to be indirectly assessable through measurement of the electrically evoked torque at rest (also known as the resting twitch torque). (Behrens et al., 2016; Casartelli et al., 2019; Krishnan & Theuerkauf, 2015; Maffiuletti et al., 2016) Electrically evoked torque at rest involves applying a supramaximal stimulus or stimuli to the muscle of interest or its innervating nerve and analyzing the resultant torque production. Electrically evoked torque at rest is gathered as a component of interpolated twitch testing and used to help calculate voluntary activation (e.g., percent activation = 1 – (evoked torque on the maximum voluntary isometric contraction/electrically elicted torque at rest).(Shield & Zhou, 2004) Strong positive correlations (r values > 0.60) have been observed between electrically evoked torque at rest and muscle size (e.g., where greater CSA is correlated with a larger electrically evoked torque at rest).(Behrens et al., 2016; Ryan et al., 2011) As such, electrically evoked torque may be able to be considered a metric of intrinsic muscle force-generating capacity given that it bypasses influence from the brain and spinal cord (e.g., central/neural drive).(Krishnan & Williams, 2009)
Previous work has shown that side-to-side differences in electrically evoked torque at rest is predictive of side-to-side quadriceps strength deficits in a healthy cohort.(Krishnan & Williams, 2009) Similarly, side-to-side differences in electrically evoked torque at rest has also led to the hypothesis that changes in muscle size have a larger role in chronic weakness in ACL reconstructed individuals than deficits in neural drive.(Krishnan & Williams, 2011) However, electrically evoked torque at rest could also be affected by alterations in muscle or tendon architecture (e.g., pennation angle and stiffness) and composition (e.g., fiber type) (Andersen & Aagaard, 2006a; Jenkins, Palmer, & Cramer, 2014; Ryan et al., 2011) following an injury or surgery; thus, bringing into question the validity of using electrically evoked torque at rest as a surrogate measure of muscle morphology in an injured population. Unfortunately, no study has directly investigated if the electrically evoked torque at rest in persons displaying quadriceps muscle weakness, like those who have undergone ACL reconstruction, is indeed associated with measurements of muscle size. Identifying if electrically evoked torque at rest is related to muscle size will allow for a better understanding of what changes in the electrically evoked torque may represent atrophy and allow for more accurate conclusions to be drawn.
Recent studies in persons with ACL-reconstruction have quantified quadriceps muscle size via magnetic resonance imaging or ultrasonography.(e Lima, da Matta, & de Oliveira, 2012; Garcia, Curran, et al., 2020; Garcia, Moffit, et al., 2020; Morse, Degens, & Jones, 2007; Norte et al., 2018) Yet, these imaging modalities may not be readily available to many exercise and sports science researchers, are costly, and require extensive image processing thereby limiting the feasibility for routine and widespread use in typical research settings. Other indirect measures such as thigh circumference measurements can be used, though, circumference estimates are known to be inaccurate and lack the ability to differentiate between the quadriceps and hamstring muscle group.(Barber-Westin & Noyes, 2011) Conversely, electrically evoked torque measurements are known to be extremely reliable(Blacker, Fallowfield, & Willems, 2013; Jenkins et al., 2014), and thus may serve as a cost-effective, indirect measure of peripheral muscle size for exercise science researchers who already use electrical stimulation or where imaging tools are not accessible. Further, electrical stimulation is a common method to quantify voluntary activation deficits in ACL research (Garcia, Rodriguez, Brown, Palmieri-Smith, & Krishnan, 2019; Krishnan & Theuerkauf, 2015; Lepley, Ericksen, Sohn, & Pietrosimone, 2014), and therefore, researchers in this area could benefit from knowing what electrically evoked torque at rest is, quantifying it and understanding how to interpret changes this measurement. If electrically evoked torque at rest is indeed related to muscle size in ACL-reconstructed individuals, then the measure can be used synergistically with voluntary activation measures providing concurrent assessment of both centrally-mediated, and peripheral muscle deficits like atrophy. Thus, there is a need to establish the relationship between evoked torque at rest and muscle size in those with known pathology (i.e., ACL reconstruction). Furthermore, this measurement could also be of value for exercise science researchers who wish to assess changes in muscle size due to exercise, aging, etc..
Therefore, the purpose of this study was to evaluate the relationship between ultrasound-based quadriceps muscle, specifically vastus lateralis, CSA and electrically evoked torque at rest in individuals with ACL reconstruction. We hypothesized that evoked torque at rest would be positively associated with vastus lateralis muscle size. We also hypothesized that side-to-side symmetry in evoked torque at rest would be positively associated with side-to-side symmetry in vastus lateralis CSA.
Materials and Methods
Participants
Eighteen individuals with unilateral ACL reconstruction were recruited (Age =22.3±5.7 yrs., height=1.7±0.1m, weight =29.66±11.0kg, time since surgery=1.1±0.8 yrs.) participated in a cross-sectional study (Level III evidence). Participants were included if they were at least six months post-surgery and between the ages of 16–40 years of age. Participants were excluded if they had a history of injury or surgery to the lower extremity (not including the ACL injury), history of significant anterior knee pain, diabetes, hypertension, or other cardiovascular/neurological disorders. All participants provided informed written consent/assent prior to study participation and all procedures were approved by the University Institutional Review Board.
Electrically Evoked Triplet Torque at Rest
The electrically evoked torque at rest data presented herein were part of a larger study designed to examine the effect of stimulators and stimulating parameters on quadriceps voluntary activation.(Garcia et al., 2019) Evoked torque at rest was evaluated bilaterally on an isokinetic dynamometer (Humac NORM, CSMi Solutions, Stoughton, MA) at 90º of knee flexion as we have done previously.(Garcia et al., 2019) Torque data were sampled at 1000 Hz (NI-USB-6251, National Instruments) and low-pass filtered using a digital, Butterworth filter (10Hz cutoff frequency).
Prior to delivering the stimuli to elicit the electrically evoked torque at rest, the skin over the anterior thigh was cleaned using alcohol pads. After which, two large, self-adhesive electrodes (2.75 × 5.0 inches, Dura-Stick II; Chatanooga Group, Hixon, TN) were placed over the proximal vastus lateralis and distal vastus medialis.(Krishnan & Williams, 2011) The participants were then oriented to the stimulation procedures by providing several submaximal electrical stimuli to their quadriceps muscles using a constant current electrical stimulator (Model DS7AH, Digitimer LTD, Hertfordshire, UK) that was connected to the self-adhesive stimulation electrodes. The current intensities used during testing were sex-specific (290 mA: females, 360 mA: males) based on previous research.(Krishnan & Williams, 2010) Pulse parameters used to gather the electrically evoked torque at rest were kept consistent (400 V, 200ms pulse duration, 3-pulse train).(Krishnan & Williams, 2010) Potentiated triplet-evoked torque at rest was collected immediately following a maximum voluntary isometric contraction using the above-mentioned stimulus parameters. Electrically evoked torque at rest was evaluated as the maximal torque (Nm) produced from the electrical stimuli while participants were completely relaxed. All testing was conducted on the non-reconstructed leg first.
Quadriceps Ultrasonography
Bilateral panoramic ultrasound images of the vastus lateralis were acquired using a GE-Logiq e ultrasound with a 12-MHz linear array transducer. Vastus lateralis images were obtained while participants laid supine with their knee extended and images were taken at 50% of the distance from the anterior- superior iliac spine to the lateral border of the patella. (Garcia, Moffit, et al., 2020) Ultrasound parameters were kept consistent (gain: 50db, depth: 6.0 cm(Garcia et al., 2019; Raj, Bird, & Shield, 2012)) unless the entire muscle was not captured under the preset image depth. If this occurred, depth was increased to visualize the entire muscle. For consistency, depth adjustments made on the first leg were replicated when imaging the opposite leg. The transducer was aligned transversely and minimal pressure was applied on the transducer to limit compression. Three images per leg were acquired. The same individual recorded all US images for all subjects. US images were always gathered prior to electrically evoked torque at rest and after subjects rested supine on a table for 30 minutes.
Ultrasound Data Reduction
Ultrasound data were processed using ImageJ version 1.52 (National Institutes of Health, Bethesda, MD). Vastus lateralis CSA (mm2) was calculated by tracing the muscle’s inner border (polygon function) excluding the hyperechoic fascia border (Figure 1). We also calculated subcutaneous fat thickness from the ultrasound images as adipose tissue can attenuate electrical stimuli.(Petrofsky, Laymon, Prowse, Gunda, & Batt, 2009) This was done by measuring the straight-line distance from the superficial aponeurosis to the skin-muscle interface at three locations (medial, central, lateral).(Young, Jenkins, Zhao, & McCully, 2015) (Figure 1). The average distance of these lines was used for further analysis. A single experienced researcher acquired and analyzed all ultrasound images and demonstrated excellent intra-rater reliability for the right (ICC [3, 1] =0.984, 95% CI: 0.969, 0.993) and left leg (ICC [3, 1] =0.964, 95% CI: 0.930, 0.983). Evoked torque at rest and CSA were calculated for each limb individually and side-to-side differences for evoked torque at rest and CSA were evaluated via limb symmetry indices (LSI) where the involved limb was expressed relative to the contralateral limb [(ACL reconstructed limb/ non-reconstructed limb)*100]. Differences in CSA between limbs (involved limb CSA < contralateral limb CSA) was considered to be representative of muscle atrophy.
Figure 1.

Panoramic ultrasound image of the vastus lateralis muscle. The dashed line illustrates the tracing of the vastus lateralis muscle done in the ImageJ software in order to calculate the cross-sectional area. The double arrows represent the medial, central, and lateral lines drawn to calculate subcutaneous fat thickness.
Statistical Analyses
All statistical tests were performed using SPSS version 26 (SPSS Inc. Chicago, IL, USA). Data were first inspected for normality using a Shapiro-Wilke test. Prior to primary correlational analyses, examining the relationship between electrically evoked torque at rest and VL CSA, we analyzed the association between subcutaneous fat thickness (SFT) and electrically evoked resting torque because greater amounts of adipose tissue can diminish the ability of electrical stimuli to activate a muscle, and thus, greater amount of SFT could decrease the magnitude of the electrically evoked torque at rest without a change in muscle size.(Petrofsky et al., 2009) Therefore, both Pearson’s r and partial correlations (accounting for subcutaneous fat thickness) were used when evaluating associations between evoked torque at rest and vastus lateralis CSA in the reconstructed leg, non-reconstructed leg, and LSI outcomes. The magnitude of the correlation coefficients was interpreted as very weak (r = 0.0–0.19), weak (r = 0.2–0.39), moderate (r = 0.40–0.59), strong (r = 0.60–0.79), and very strong (r = 0.8–1.0).(Martella, 2013) To confirm that atrophy was present in our subjects a paired t-test was used to make between limb comparisons for CSA. Two additional paired t-tests were used to assess between limb differences in the electrically evoked torque at rest and subcutaneous fat thickness. A significance level of α = 0.05 was used for all statistical analyses.
Results
All data were normally distributed and averages for all outcome variables are listed in Table 1. Subcutaneous fat thickness was negatively correlated with the electrically evoked torque at rest in the reconstructed (r=−0.550, P=0.018), but not in the non-reconstructed leg (r=−0.313, P=0.206). Hence, we report both partial correlations controlling for subcutaneous fat thickness and Pearson’s r when evaluating associations for primary variables.
Table 1:
Average electrically evoked torque at rest, vastus lateralis cross sectional area, and subcutaneous fat thickness.
| ACL-reconstructed mean (SD) |
Non-reconstructed mean (SD) |
Side-to-side ratio mean (SD) |
|
|---|---|---|---|
| Evoked torque at rest (Nm) | 86.59 (22.92)* | 102.17 (24.76) | 84.74 (13.27) |
| Vastus Lateralis CSA (mm2) | 2228.88 (552.84)* | 2579.47 (501.31) | 86.09 (10.20) |
| SF thickness (mm) | 8.77 (4.46)* | 7.71 (3.66) | -- |
CSA = Cross-sectional area. SF = Subcutaneous Fat.
indicates statistically significant difference between the ACL-reconstructed and non-reconstructed legs.
Scatterplots depicting the associations between outcome variables can be found in Figure 2. In the reconstructed leg, there was a very strong positive association between the electrically evoked torque at rest and vastus lateralis CSA (r = 0.865, P<0.01). This relationship was minimally affected when controlling for subcutaneous fat thickness (partial r = 0.816, P<0.01). In the non-reconstructed leg, there was a strong positive association between the electrically evoked torque at rest and vastus lateralis CSA (r = 0.628, P=0.005). This relationship was minimally affected when controlling for subcutaneous fat thickness (partial r = 0.575, P = 0.016). When evaluating the limb symmetry indices, there was a strong positive association between the electrically evoked torque at rest LSI and vastus lateralis CSA LSI (r=0.670, P<0.01). This relationship was relatively unchanged when controlling for subcutaneous fat thickness (partial r = 0.659, P<0.01).
Figure 2.

Scatterplots depicting the associations between vastus lateralis and evoked torque at rest outcome variables. CSA: Cross-sectional area.
A significantly smaller VL CSA was noted in the involved compared to the uninvolved limb (P<0.001), suggesting that muscle atrophy was present in ACL-reconstructed legs of our subjects (Table 1). Additionally, the electrically evoked torque at rest was also smaller in the ACL-reconstructed compared to the non-reconstructed leg (P<0.001) (Table 1). Lastly, subcutaneous fat thickness was greater in the ACL-reconstructed leg compared to the non-reconstructed leg. (P = 0.005).
Discussion
The purpose of this study was to comprehensively evaluate the relationship between electrically evoked torque at rest and vastus lateralis CSA obtained via ultrasonography. As hypothesized, we observed strong positive correlations between electrically evoked torque at rest and vastus lateralis CSA in both the ACL-reconstructed and non-reconstructed legs (Pearson’s r=0.865, and 0.628, respectively). Similarly, we observed strong positive correlations between electrically evoked torque at rest LSI and vastus lateralis CSA LSI (r=0.670). Together, these results suggest that electrically evoked torque at rest is an indirect measure of vastus lateralis CSA in individuals with ACL reconstruction. Therefore, declines in or lower electrically evoked torque at rest after ACL reconstruction could be suggestive of increased atrophy or decreased muscle size.
We observed strong-to-very strong positive associations between VL CSA and quadriceps electrically evoked torque at rest in the ACL-reconstructed and non-reconstructed legs. This finding agrees with previous literature showing electrically evoked torque at rest accounts for a significant proportion (R2 = 0.764) of the variance in ankle plantar flexor CSA and results showing moderate-to-strong positive correlations between quadriceps electrically evoked torque at rest measured at various knee angles and VL muscle volume (r = 0.49–0.72) in healthy adults.(Ryan et al., 2011) Given that electrically evoked torque at rest is considered a valid measure of a muscle’s ability to generate force independent of neural drive and the strong relationship between muscle size to force generation(Enoka, 1988) our finding is not unexpected. Our results are, however, the first that we are aware of demonstrating a relationship between the quadriceps electrically evoked torque at rest and VL CSA in a patient population who is experiencing muscle atrophy. These findings are significant in that they show the value of electrically evoked torque at rest in detecting quadriceps muscle atrophy in ACL reconstructed patients and likely in other post-surgical patients or populations who experience muscle wasting such as aging adults or those with knee osteoarthritis.
The magnitude of the relationship between electrically evoked torque at rest and muscle size appeared to vary between limbs in our population. The electrically evoked torque at rest in the ACL reconstructed limb demonstrated very strong positive correlations with CSA (r = 0.865), while the relationship in the non-reconstructed leg was still strong, but not as great (r = 0.628). The magnitude of the relationship for the non-reconstructed leg, however, is very similar to those found in the quadriceps muscle of healthy adults (r = 0.688).(Behrens et al., 2016) While we do not know why there is a stronger relationship between CSA and electrically evoked torque at rest in the ACL reconstructed limb in our study, we speculate that it could be a product of our experimental protocol. For example, we chose to use a pre-determined current intensity based on previous research, instead of a subject-specific current intensity, to minimize discomfort associated with the number of electrical stimuli delivered during testing.(Krishnan & Williams, 2010) It is possible that the current intensity may have been suitable to induce the maximum evoked torque at rest for an atrophied muscle (i.e., ACL reconstructed limb) but may not have been sufficient for the uninvolved limb at least in some of the subjects. As a result, the evoked torque at rest in the uninvolved limb may not have captured adequate variance in the muscle CSA data. Another explanation could be related to the order in which the testing was performed. As commonly done in the ACL studies, the non-reconstructed limb was always tested first.(Ebert et al., 2018; Schmitt, Paterno, & Hewett, 2012) Thus, participants had more time to acclimatize to the electrical stimulus in the ACL reconstructed limb than in the non-reconstructed limb, which could have minimized apprehension and co-contraction when testing the involved limb, thereby yielding a more precise estimate of the evoked torque at rest.
We also observed strong positive correlations between CSA and evoked torque at rest LSIs, which supports that side-to-side deficits in evoked torque at rest are in fact attributable to differences in peripheral muscle properties like CSA.(Krishnan & Williams, 2011) Yet, the associations between side-to-side evoked torque and CSA ratios indicate a proportion of variance unexplained. The electrically evoked torque at rest is influenced by multiple peripheral properties other than CSA, like muscle architecture (i.e., pennation angle), series-elastic component differences, or fiber-type.(Andersen & Aagaard, 2006b; Jenkins et al., 2014) One can interpret the associations observed (described by correlations coefficients above by 0.6) between side-to-side ratios as evidence that CSA is the primary contributor to peripheral muscle deficits between limbs (as measured by electrically evoked torque at rest ratios). Conversely, it can be argued that side-to-side evoked torque at rest ratios do not fully explain (because correlation coefficients are less than 1) side-to-side differences in quadriceps CSA. However, given the large positive correlation coefficients noted between CSA and evoked torque twitch at rest, we reason our results support the prior and provide support that electrically evoked torque at rest is primarily mediated by peripheral muscle properties like CSA and can be used to study these changes if imaging-based methods like ultrasound are not feasible.
While associations observed in our study were strong-to-very strong, we are cautious to generalize our findings to other knee angles. Previous research found that associations between evoked torque at rest and CSA tested at a knee angle of 45° (i.e., shorter muscle lengths) were lesser or non-significant when compared to an angle of 80° (i.e., longer muscle lengths).(Behrens et al., 2016) It is possible that these findings are related to changes in the muscle-tendon unit slack and force length relationship of muscle;(Krishnan & Theuerkauf, 2015; Lieber & Friden, 2000) however, it is also possible these findings can be also be attributed to suboptimal electrical stimulus parameters. We delivered a 3-pulse train electrical stimulus while previous authors examining the relationship between electrically evoked torque at rest and muscle size in healthy adults used single, and doublet pulses.(Behrens et al., 2016) Given that resting muscle contains slack in the musculotendinous unit, single or doublet pulses may not be ideal as the contribution of the initial pulse to torque generation is impaired as it must take up slack of the elastic/contractile elements (particularly at shorter muscle lengths).(Behrens et al., 2016) Therefore, a higher number of pulses may be critical to ensuring an optimal evoked torque response in the resting muscle and in turn may improve associations with muscle size.
SFT slightly weakened associations between evoked torque at rest measures and CSA. Adipose tissue is known to attenuate electrical stimuli, particularly square wave pulses, as the increased impedance from greater adiposity decreases the amount of current delivered to underlying muscle.(Petrofsky, 2008) Indeed, previous studies have demonstrated that greater stimulus intensity is needed to elicit similar contraction force during neuromuscular electrical stimulation (NMES) in individuals with high SFT compared to those with less SFT.(Medeiros et al., 2015) Moreover, it has been advocated that stimulus intensities should be subject-specific, as studies have noted sex-differences in optimal stimulus intensities which may be attributed to differences in SFT.(Krishnan & Williams, 2010) Therefore, future studies may benefit from identifying optimal stimulus intensity on an individual basis to ensure optimal electrically evoked torque parameters thereby limiting the impact of adipose tissue like SFT.
Subcutaneous fat thickness was negatively correlated with the electrically evoked torque at rest in the ACL reconstructed, but not in the non-reconstructed leg (despite slightly weakening the associations between electrically evoked torque at rest and muscle size in both limbs). This suggests that greater amounts of SFT in the ACL reconstructed limb resulted in a smaller electrically evoked torque at rest. We believe this relationship was seen in the ACL-reconstructed leg because there was a greater magnitude of SFT present in that limb compared with the non-reconstructed limb, and thus, there may be a threshold of SFT that results in a greater influence on the electrically evoked torque at rest measurement (e.g., once you reach a certain amount of adiposity it has a greater influence on the evoked torque measure).
There are limitations to consider when interpreting results. Our ultrasound measures of vastus lateralis were cross-sectional images at mid-thigh, and thus, we are limited to assessments of only anatomical CSA. Physiological CSA is better representative of muscle force generating capacity compared to anatomical CSA as pennation angle also contributes to the muscle’s force capacity. However, it is unclear if electrically evoked torque at rest would be more strongly associated with physiological CSA than our ultrasound measures of vastus lateralis anatomical CSA. We also only reported vastus lateralis CSA as our measure of quadriceps muscle size. Given that the size of all four quadriceps muscles influences the intrinsic force generating capacity of the quadriceps, the addition of CSA for vastus intermedius, vastus medialis and rectus femoris would likely increase the association between electricaly evoked torque at rest and muscle size, however, this was not directly studied. As part of our larger study, we also obtained images of rectus femoris. While not reported here, we also explored if associations in side-to-side outcomes improved if rectus femoris and vastus lateralis CSA were summed together but associations, and interpretations, remained similar (r=0.670 vs. 0.696). Nonetheless, future consideration of the vastus intermedius and medialis seems warranted to see if they strengthen the relationships explored in this study. Previous research in healthy subjects has shown, however, that the strongest associations between electrically evoked torque at rest in vastus lateralis compared to the other quadriceps heads.(Behrens et al., 2016) Similarly, given that atrophy appears to most affect the vastii muscles of the quadriceps after ACL reconstruction (Dutaillis, Maniar, Opar, Hickey, & Timmins, 2021), it is possible that the association between the LSIs for electrically evoked torque at rest and muscle size may be strengthened if we had considered all the quadriceps muscles. Lastly, we did not quantify other muscle properties such as fiber type, pennation angle, etc. that could help better define what electrically induced torque at rest quantifies. Future studies including such factors could aid in accounting for the small explained portion of the variance not accounted for by muscle size.
Conclusions
In summary, the results of our study indicate that evoked torque at rest is able to detect differences in quadriceps, specifically vastus lateralis, muscle CSA in those with ACL reconstruction and was strongly associated with muscle CSA in both the ACL-reconstructed and non-reconstructed limb. Therefore, electrically evoked torque at rest can be at least partially attributed to muscle size and thus may be used as alternative metric of peripheral muscle CSA if imaging-based methodologies are not feasible. Given that the electrically evoked torque at rest bypasses the neural drive, it should be considered as a metric of intrinsic muscle force-generating capacity.
Acknowledgements:
This work was supported by the National Institute of Child Health and Human Development of the National Institutes of Health (Grant No. R21 HD092614
References
- Andersen LL, & Aagaard P (2006a). Influence of maximal muscle strength and intrinsic muscle contractile properties on contractile rate of force development. Eur J Appl Physiol, 96(1), 46–52. doi: 10.1007/s00421-005-0070-z [DOI] [PubMed] [Google Scholar]
- Andersen LL, & Aagaard P (2006b). Influence of maximal muscle strength and intrinsic muscle contractile properties on contractile rate of force development. European Journal of Applied Physiology, 96(1), 46–52. doi: 10.1007/s00421-005-0070-z [DOI] [PubMed] [Google Scholar]
- Barber-Westin SD, & Noyes FR (2011). Factors used to determine return to unrestricted sports activities after anterior cruciate ligament reconstruction. Arthroscopy, 27(12), 1697–1705. doi: 10.1016/j.arthro.2011.09.009 [DOI] [PubMed] [Google Scholar]
- Behrens M, Brown N, Bollinger R, Bubeck D, Mau-Moeller A, Weippert M, . . . Alt W (2016). Relationship between muscle volume and contractile properties of the human knee extensors. Appl Physiol Nutr Metab, 41(1), 110–113. doi: 10.1139/apnm-2015-0378 [DOI] [PubMed] [Google Scholar]
- Birchmeier T, Lisee C, Kane K, Brazier B, Triplett A, & Kuenze C (2019). Quadriceps Muscle Size Following ACL Injury and Reconstruction: A Systematic Review. J Orthop Res doi: 10.1002/jor.24489 [DOI] [PubMed]
- Blacker SD, Fallowfield JL, & Willems ME (2013). Intra- and interday reliability of voluntary and electrically stimulated isometric contractions of the quadriceps femoris. J Electromyogr Kinesiol, 23(4), 886–891. doi: 10.1016/j.jelekin.2013.02.007 [DOI] [PubMed] [Google Scholar]
- Casartelli NC, Item-Glatthorn JF, Friesenbichler B, Bizzini M, Salzmann GM, & Maffiuletti NA (2019). Quadriceps Neuromuscular Impairments after Arthroscopic Knee Surgery: Comparison between Procedures. J Clin Med, 8(11). doi: 10.3390/jcm8111881 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dutaillis B, Maniar N, Opar DA, Hickey JT, & Timmins RG (2021). Lower Limb Muscle Size after Anterior Cruciate Ligament Injury: A Systematic Review and Meta-Analysis. Sports Med, 51(6), 1209–1226. doi: 10.1007/s40279-020-01419-0 [DOI] [PubMed] [Google Scholar]
- e Lima KM, da Matta TT, & de Oliveira LF (2012). Reliability of the rectus femoris muscle cross-sectional area measurements by ultrasonography. Clin Physiol Funct Imaging, 32(3), 221–226. doi: 10.1111/j.1475-097X.2011.01115.x [DOI] [PubMed] [Google Scholar]
- Ebert JR, Edwards P, Yi L, Joss B, Ackland T, Carey-Smith R, . . . Hewitt B (2018). Strength and functional symmetry is associated with post-operative rehabilitation in patients following anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc, 26(8), 2353–2361. doi: 10.1007/s00167-017-4712-6 [DOI] [PubMed] [Google Scholar]
- Enoka RM (1988). Muscle strength and its development. New perspectives. Sports Med, 6(3), 146–168. doi: 10.2165/00007256-198806030-00003 [DOI] [PubMed] [Google Scholar]
- Garcia SA, Curran MT, & Palmieri-Smith RM (2020). Longitudinal Assessment of Quadriceps Muscle Morphology Before and After Anterior Cruciate Ligament Reconstruction and Its Associations With Patient-Reported Outcomes. Sports Health, 12(3), 271–278. doi: 10.1177/1941738119898210 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia SA, Moffit TJ, Vakula MN, Holmes SC, Montgomery MM, & Pamukoff DN (2020). Quadriceps Muscle Size, Quality, and Strength and Self-Reported Function in Individuals With Anterior Cruciate Ligament Reconstruction. J Athl Train, 55(3), 246–254. doi: 10.4085/1062-6050-38-19 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia SA, Rodriguez KM, Brown SR, Palmieri-Smith RM, & Krishnan C (2019). Estimates of voluntary activation in individuals with anterior cruciate ligament reconstruction: Effects of type of stimulator, number of stimuli, and quantification technique. J Sport Health Sci doi: 10.1016/j.jshs.2019.12.001 [DOI] [PMC free article] [PubMed]
- Jenkins ND, Palmer TB, & Cramer JT (2014). Comparing the reliability of voluntary and evoked muscle actions. Clin Physiol Funct Imaging, 34(6), 434–441. doi: 10.1111/cpf.12113 [DOI] [PubMed] [Google Scholar]
- Krishnan C, & Theuerkauf P (2015). Effect of knee angle on quadriceps strength and activation after anterior cruciate ligament reconstruction. J Appl Physiol (1985), 119(3), 223–231. doi: 10.1152/japplphysiol.01044.2014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krishnan C, & Williams GN (2009). Evoked tetanic torque and activation level explain strength differences by side. Eur J Appl Physiol, 106(5), 769–774. doi: 10.1007/s00421-009-1057-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krishnan C, & Williams GN (2010). Quantification method affects estimates of voluntary quadriceps activation. Muscle Nerve, 41(6), 868–874. doi: 10.1002/mus.21613 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krishnan C, & Williams GN (2011). Factors explaining chronic knee extensor strength deficits after ACL reconstruction. J Orthop Res, 29(5), 633–640. doi: 10.1002/jor.21316 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuenze CM, Blemker SS, & Hart JM (2016). Quadriceps function relates to muscle size following ACL reconstruction. J Orthop Res, 34(9), 1656–1662. doi: 10.1002/jor.23166 [DOI] [PubMed] [Google Scholar]
- Lepley AS, Ericksen HM, Sohn DH, & Pietrosimone BG (2014). Contributions of neural excitability and voluntary activation to quadriceps muscle strength following anterior cruciate ligament reconstruction. Knee, 21(3), 736–742. doi: 10.1016/j.knee.2014.02.008 [DOI] [PubMed] [Google Scholar]
- Lieber RL, & Friden J (2000). Functional and clinical significance of skeletal muscle architecture. Muscle Nerve, 23(11), 1647–1666. doi: [DOI] [PubMed] [Google Scholar]
- Lisee C, Lepley AS, Birchmeier T, O’Hagan K, & Kuenze C (2019). Quadriceps Strength and Volitional Activation After Anterior Cruciate Ligament Reconstruction: A Systematic Review and Meta-analysis. Sports Health, 11(2), 163–179. doi: 10.1177/1941738118822739 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maffiuletti NA, Barbero M, Cescon C, Clijsen R, Beretta-Piccoli M, Schneebeli A, . . . Togninalli D (2016). Validity of the twitch interpolation technique for the assessment of quadriceps neuromuscular asymmetries. J Electromyogr Kinesiol, 28, 31–36. doi: 10.1016/j.jelekin.2016.03.002 [DOI] [PubMed] [Google Scholar]
- Martella RC (2013). Understanding and interpreting educational research New York: Guilford Press. [Google Scholar]
- Medeiros FV, Vieira A, Carregaro RL, Bottaro M, Maffiuletti NA, & Durigan JL (2015). Skinfold thickness affects the isometric knee extension torque evoked by Neuromuscular Electrical Stimulation. Braz J Phys Ther, 19(6), 466–472. doi: 10.1590/bjpt-rbf.2014.0114 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morse CI, Degens H, & Jones DA (2007). The validity of estimating quadriceps volume from single MRI cross-sections in young men. Eur J Appl Physiol, 100(3), 267–274. doi: 10.1007/s00421-007-0429-4 [DOI] [PubMed] [Google Scholar]
- Norte GE, Knaus KR, Kuenze C, Handsfield GG, Meyer CH, Blemker SS, & Hart JM (2017). MRI-Based Assessment of Lower Extremity Muscle Volumes in Patients Before and After ACL Reconstruction. J Sport Rehabil, 1–40. doi: 10.1123/jsr.2016-0141 [DOI] [PubMed]
- Norte GE, Knaus KR, Kuenze C, Handsfield GG, Meyer CH, Blemker SS, & Hart JM (2018). MRI-Based Assessment of Lower-Extremity Muscle Volumes in Patients Before and After ACL Reconstruction. J Sport Rehabil, 27(3), 201–212. doi: 10.1123/jsr.2016-0141 [DOI] [PubMed] [Google Scholar]
- Petrofsky J (2008). The effect of the subcutaneous fat on the transfer of current through skin and into muscle. Med Eng Phys, 30(9), 1168–1176. doi: 10.1016/j.medengphy.2008.02.009 [DOI] [PubMed] [Google Scholar]
- Petrofsky J, Laymon M, Prowse M, Gunda S, & Batt J (2009). The transfer of current through skin and muscle during electrical stimulation with sine, square, Russian and interferential waveforms. J Med Eng Technol, 33(2), 170–181. doi: 10.1080/03091900802054580 [DOI] [PubMed] [Google Scholar]
- Raj IS, Bird SR, & Shield AJ (2012). Reliability of ultrasonographic measurement of the architecture of the vastus lateralis and gastrocnemius medialis muscles in older adults. Clin Physiol Funct Imaging, 32(1), 65–70. doi: 10.1111/j.1475-097X.2011.01056.x [DOI] [PubMed] [Google Scholar]
- Ryan ED, Thompson BJ, Herda TJ, Sobolewski EJ, Costa PB, Walter AA, & Cramer JT (2011). The relationship between passive stiffness and evoked twitch properties: the influence of muscle CSA normalization. Physiological Measurement, 32(6), 677–686. doi: 10.1088/0967-3334/32/6/005 [DOI] [PubMed] [Google Scholar]
- Schmitt LC, Paterno MV, & Hewett TE (2012). The impact of quadriceps femoris strength asymmetry on functional performance at return to sport following anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther, 42(9), 750–759. doi: 10.2519/jospt.2012.4194 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shield A, & Zhou S (2004). Assessing voluntary muscle activation with the twitch interpolation technique. Sports Med, 34(4), 253–267. doi: 10.2165/00007256-200434040-00005 [DOI] [PubMed] [Google Scholar]
- Thomas AC, Wojtys EM, Brandon C, & Palmieri-Smith RM (2016). Muscle atrophy contributes to quadriceps weakness after anterior cruciate ligament reconstruction. J Sci Med Sport, 19(1), 7–11. doi: 10.1016/j.jsams.2014.12.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young HJ, Jenkins NT, Zhao Q, & McCully KK (2015). Measurement of intramuscular fat by muscle echo intensity. Muscle Nerve, 52(6), 963–971. doi: 10.1002/mus.24656 [DOI] [PMC free article] [PubMed] [Google Scholar]
