Architectural anatomy of the quadriceps and the relationship with muscle strength: An observational study utilising real‐time ultrasound in healthy adults (2024)

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J Anat
v.239(4); 2021 Oct
PMC8450473

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J Anat. 2021 Oct; 239(4): 847–855.

Published online 2021 Aug 29. doi:10.1111/joa.13497

PMCID: PMC8450473

PMID: 34458993

Doa El‐Ansary,^1,^2,⁷ Charlotte J. Marshall,¹ Joshua Farragher,^1,³ Raquel Annoni,⁴ Ariane Schwank,⁵ James McFarlane,⁶ Adam Bryant,³ Jia Han,^1,^7,⁸ Marilyn Webster,³ Guy Zito,³ Selina Parry,³ and Adrian Pranata^1,⁷

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Associated Data

Data Availability Statement

Abstract

Quadriceps atrophy and morphological change is a known phenomenon that can impact significantly on strength and functional performance in patients with acute or chronic presentations conditions. Real‐time ultrasound (RTUS) imaging is a noninvasive valid and reliable method of quantifying quadriceps muscle anatomy and architecture. To date, there is a paucity of normative data on the architectural properties of superficial and deep components of the quadriceps muscle group to inform assessment and evaluation of intervention programs. The aims of this study were to (1) quantify the anatomical architectural properties of the quadriceps muscle group (rectus femoris, vastus intermedius, and vastus lateralis) using RTUS in healthy older adults and (2) to determine the relationship between RTUS muscle parameters and measures of quadriceps muscle strength. Thirty middle aged to older males and females (age range 55–79years; mean age=59.9±7.08years) were recruited. Quadriceps muscle thickness, cross‐sectional area, pennation angle, and echogenicity were measured using RTUS. Quadriceps strength was measured using hand‐held dynamometry. For the RTUS‐derived quadriceps morphological data, rectus femoris mean results; circumference 9.3cm; CSA 4.6cm²; thickness 1.5cm; echogenicity 100.2 pixels. Vastus intermedius mean results; thickness 1.8cm; echogenicity 99.1 pixels. Vastus lateralis thickness 1.9cm; pennation angle 17.3°; fascicle length 7.0cm. Quadriceps force was significantly correlated only with rectus femoris circumference (r=0.48, p=0.007), RF echogenicity (r=0.38, p=0.037), VI echogenicity (r=0.43, p=0.018), and VL fascicle length (r=0.43, p=0.019). Quadriceps force was best predicted by a three‐variable model (adjusted R²=0.46, p<0.001) which included rectus femoris echogenicity (B=0.43, p=0.005), vastus lateralis fascicle length (B=0.33, p=0.025) and rectus femoris circumference (B=0.31, p=0.041). Thus respectively, rectus femoris echogenicity explains 43%, vastus lateralis fascicle length explains 33% and rectus femoris circumference explains 31% of the variance of quadriceps force. The study findings suggest that RTUS measures were reliable and further research is warranted to establish whether these could be used as surrogate measures for quadriceps strength in adults to inform exercise and rehabilitation programs.

Keywords: echogenicity, muscle architecture, muscle strength, quadriceps, ultrasound

1. INTRODUCTION

The effects of injury, critical illness, age, chronic disease and bed rest on anatomy and morphology of the quadriceps muscle group and their functional implications has been investigated in the literature (Menon et al., 2012; Parry et al., 2019, 2015). In healthy individuals, the quadriceps femoris has been reported to atrophy faster than other thigh muscles (e.g., hamstring); however, the reasons for this phenomenon are not clear (Ogawa et al., 2012). Ogawa et al. (2012) found that quadriceps Cross Sectional Area (CSA) was significantly lower (16%) in older men (60–78years old) when compared to younger men (20–28years old), despite both groups being physically active and neither group participating in regular strength or resistance training for a minimum of 3years prior to the start of the study. Furthermore, changes have been observed in fascicle length and pennation angle of the vastus lateralis within this older population (Unhjem et al., 2017). However, most studies have not investigated all components of the quadriceps muscle group thoroughly and none have explored the anatomy and the architectural characteristics of the deeper vastus intermedius in healthy adults by ultrasound imaging (Menon et al., 2012; Parry et al., 2015). Given the higher proportion of slow twitch fibres within the vastus intermedius and its functional role in providing stability of the lower limbs during functional tasks (e.g., standing from a seated position), changes within this muscle may have implications related to mobility and functional performance in healthy, acutely ill and chronic disease populations (Menon et al., 2012; Parry et al., 2019, 2015; Toumi et al., 2007).

For critically ill populations within intensive care, muscle wasting has been found to occur rapidly, especially within the first 10days (Parry et al., 2015; Puthucheary et al., 2013). Parry et al. (2015) found a significant correlation between real‐time ultrasound (RTUS) parameters and strength measures obtained by volitional muscle testing, within individuals with critical illness (Parry et al., 2015). In addition, vastus intermedius demonstrated the greatest change in muscle quality and had the strongest relationship to volitional measures highlighting the importance of assessing the deep and superficial components of the quadriceps muscles (Parry et al., 2015). RTUS has emerged as a popular imaging mode to assess muscle anatomical and architectural features as it is noninvasive, utilises no radiation, portable, and provides real‐time information (Jedrzejczak & Chipchase, 2008). RTUS provides valid measures of skeletal muscle with reported concurrent validity with MRI (Kwah et al., 2013; Mendis et al., 2010; Scott et al., 2012). Additionally, RTUS has excellent reliability with respect to CSA, muscle thickness, muscle fibre pennation angle, fascicle length and echogenicity of the quadriceps muscle in healthy adults (English et al., 2012; Lima et al., 2012; Kwah et al., 2013; Sarwal et al., 2015). Although quadriceps muscle group strength has been shown to be predictive of function and quality of life (Bryanton & Bilodeau, 2017) there has been limited research investigating the anatomy of the deep and superficial quadriceps muscles individually in the normative population using RTUS (Arts et al., 2010; Maurits et al., 2003; Nijboer‐Oosterveld et al., 2011; Reimers et al., 1998).

2. METHOD

2.1. Study design

This was a cross‐sectional, pilot observational study.

2.2. Participants

Thirty healthy males and females (n_female=17) aged over 18years of age volunteered for this study. A pragmatic sample size of n=30 was chosen as this was a pilot observational study. Participants were excluded if they (i) had an underlying chronic disease (Diabetes, COPD), musculoskeletal disability or lower limb injury in the last 6months or (ii) were unable to understand verbal or written English. Participants were recruited through flyers and advertising at the School of Health Sciences, University of Melbourne over a 3‐month period. Ethics approval was obtained from the Faculty of Medicine, Dentistry and Health Sciences Human Ethics and Research Committee at the University of Melbourne (Ethics ID Number: 13400095). Informed consent was obtained from all participants. Participants competed the short version International Physical Activity Questionnaire (IPAQ) (International Physical Activity Questionnaire n.d.) at the start of the session to quantify their levels of physical activity over the week prior to testing.

2.3. Outcome measures

2.3.1. Real‐time ultrasound measures

All quadriceps muscle morphology data were acquired utilising B‐Mode RTUS device (SonoSite M‐Turbo; SonoSite Australasia Pty Ltd) with a 5–15MHz curvilinear array transducer. A water‐soluble transmission gel was applied to the transduce head to allow optimal acoustic contact and reduced impedance with minimal compression of the tissue applied. Three images were acquired anteriorly and laterally of both legs for each participant.

There was one assessor who performed all assessments who was trained over 3 one‐hour sessions in RTUS image acquisition and technical proficiency by the senior investigator who has over 16years of technical expertise in RTUS and a track record of research in ultrasound imaging. The senior investigator was present RTUS for all assessments for fidelity checking and to ensure compliance with the protocol. A pilot review of ultrasound measures for the first five participants by the assessor and senior investigator revealed excellent intrarater and interrater reliability (ICC=0.92 and ICC=0.97) respectively. Participants were assessed in a supine position on an adjustable plinth, with a 10‐cm towel roll placed underneath their knee for comfort allowing a standard testing position. Participants were instructed to remain relaxed to ensure the targeted muscles were imaged at rest. For the purpose of this study, we elected to image the rectus femoris and the vastus intermedius as examples of superficial and deep components of the quadriceps as they have a variance in predominant fibre type and functional roles. To investigate the architectural features of the vasti group (vastus medialis and lateralis) we selected the vastus lateralis to measure the specific parameters of an architecturally pennated muscle.

Anterior imaging was performed with the transducer placed perpendicular to the long axis of the anterior thigh, approximately two‐thirds of the way at a point between the anterior superior iliac spine and the superior patella border to capture the rectus femoris and vastus intermedius muscles (Figure (Figure1a).1a). On anterior imaging rectus femoris circumference, CSA, thickness, echogenicity were measured, along with vastus intermedius thickness, and echogenicity (Figure (Figure1b).1b). Lateral images were taken approximately 10cm laterally (as measured by a tape measure) from the first imaging point to capture the vastus lateralis (Figure (Figure1c).1c). All surface anatomy demarcations described were marked with a water‐soluble marker prior to testing to ensure consistency of measurement. On the lateral image, the vastus lateralis fascicle length and pennation angles were measured on both legs (Figure (Figure2).2). Measurement of fascicle (or fibre length) allows an evaluation of biomechanical properties of the muscle as an increase in length equates to an increase in sarcomeres in series that enables rapid contractions (Chleboun et al., 2007). Within this study, measures of fascicle length were obtained by tracing over three different fascicles that extended from the aponeurosis of the muscle to the border of the vastus lateralis muscle. Vastus lateralis pennation angle were obtained by measuring the angles in degrees between three different fascicles and their associated deep aponeurosis (Parry et al., 2015). As such, all measurements were performed three times with the average of the scores used for statistical analyses. A novel technical aspect of this study was the ability to obtain lateral images of the vastus lateralis using an extended field of view on the RTUS machine. This allowed a wider image capture of the vastus lateralis that facilitated measures for pennation angle and fascicle length.

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FIGURE 1

(a) Ultrasound (linear probe) placement for imaging of the quadriceps muscle anteriorly (RF and VI); (b) ultrasound images of the anterior thigh depicting RF CSA and RF and VI thickness; (c) ultrasound (linear probe) placement for imaging of the quadriceps laterally for imaging of the VL

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FIGURE 2

Ultrasound image of the VL depicting measures of pennation angle and fascicle length

2.3.2. Quadriceps muscle strength

A hand‐held dynamometer (Commander Powertrack II; JTech Medical Industries) was utilised for quadriceps strength assessment. The hand‐held dynamometer is a cost‐effective strength assessment tool that has been demonstrated to possess high validity with isokinetic dynamometer and high intrarater reliability (ICC 0.94 [95% CI: 0.86–0.97]) (Knols et al., 2009; Thorborg et al., 2013). For the purposes of this study, the assessor received two training sessions in the use of hand‐held dynamometer and was familiar with this apparatus as they used it in clinical practice. Using the hand‐held dynamometer, participants were supine with the assessed knee positioned as per ultrasound imaging assessment. The hand‐held dynamometer was positioned perpendicular to the tibia 15cm above the lateral malleolus on the anterior aspect of the tibia. Participants were then instructed to extend the knee against the assessor's force to generate maximum isometric force over 5s. The procedure was repeated three times for each leg with a 60‐s rest interval between trials, with the first serving as a practice trial. Standardised strength testing instructions and encouragement was provided to the participants. The mean of the 3strength measures was used for analysis.

2.4. Data analysis

All thickness parameters were measured in centimetres (cm), CSA in cm², pennation angles in degrees and echogenicity was numeric reporting. All measures were undertaken at the widest point of the muscle. All RTUS measures were analysed at the time of assessment on the proprietary software of the machine using the calliper markers. Echogenicity was determined using computer‐assisted quantitative greyscale analysis software (ImageJ; NIH). A standard square measuring 2×2cm was superimposed on each the images of the muscle mass of rectus femoris and vastus intermedius muscles to determine the region of interest (Sarwal et al., 2015) (Figure 3a,b). If the area did not facilitate a 2×2cm box then a similar sized square was selected to enable measures. Mean and standard deviation (SD) echogenicity of the derived region of interest was calculated and expressed as a value between 0 (black) and 255 (white) (Sarwal et al., 2015). Vastus intermedius fascicle length and pennation angles were calculated as reported above. Quadriceps strength was expressed as torque (Nm). Measurement obtained from the hand‐held dynamometer was multiplied by the lever arm– measured from the medial head of the tibia to 15cm above the medial malleolus, and the multiplier of 9.81.

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FIGURE 3

(a) Ultrasound image of the anterior thigh (RF and VI). (b) Resultant echogenicity and histogram for RF

2.5. Statistical analysis

Descriptive statistics were presented as mean and SD. Linearity and strength of bivariate relationships between the independent variables (i.e., RTUS variables) and dependent variable (i.e., quadriceps muscle force) were analysed using the Pearson product‐moment correlation coefficient and scatter graphs. The results of the bivariate correlations are presented in correlation matrices (Figure (Figure4).4). RTUS variables that exhibited a significant correlation with the quadriceps force were included within a stepwise multivariate linear regression model for the left and right side. All analyses were conducted with α=0.05 using SPSS Version 21.0 (IBM, Inc.).

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FIGURE 4

Relationships between quadriceps strength and rectus femoris echogenicity (a), quadriceps strength and rectus femoris circumference (b), quadriceps strength and vastus intermedius echogenicity (c) and quadriceps strength and vastus lateralis fascicle length (d)

3. RESULTS

Participant descriptive statistics are summarised in Table Table1.1. The mean (SD) of participants’ quadriceps force were 44.7 (12.4) Nm and 43.4 (13.1) Nm on the right and left leg respectively. A total of 360 images were analysed. There was no missing data. RTUS‐derived quadriceps muscle morphological data are summarized in Table Table22.

TABLE 1

Participant descriptive statistics

Variables (units)	Mean (SD)
Gender (n_male/n_female)	13/17
Age (years)	59.9 (7.1)
Height (cm)	170.3 (9.3)
Weight (kg)	76.1 (9.9)
BMI (kg/m²)	26.3 (3.1)
IPAQ (×10³MET minutes/week)	3.0 (2.9) (moderate)

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Abbreviations: BMI, body mass index; IPAQ, International Physical Activity Questionnaire; MET, metabolic equivalent; SD, standard deviation.

TABLE 2

RTUS‐derived quadriceps muscle morphological data

Variables (units)	Mean (SD)	Minimum value	Maximum value	Range
RF circumference (cm)	9.3 (2.1)	5.7	13.5	7.8
RF cross‐sectional area (cm²)	4.6 (2.8)	1.0	12.6	11.7
RF thickness (cm)	1.5 (1.6)	0.4	9.5	9.1
RF echogenicity (pixels)	100.2 (38.1)	30.8	194.7	163.9
VI thickness (cm)	1.8 (2.1)	0.7	10.2	9.5
VI echogenicity (pixels)	99.1 (39.5)	38.4	182.9	144.5
VL thickness (cm)	1.9 (0.5)	1.1	4.0	2.9
VL pennation angle (degrees)	17.3 (4.9)	1.5	27.7	26.2
VL fascicle length (cm)	7.0 (3.8)	4.1	25.7	21.6

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Abbreviations: RF, rectus femoris; VI, vastus intermedius; VL, vastus lateralis.

The bivariate correlation between the quadriceps force and their respective thigh morphological variables are summarized in Table Table3.3. Quadriceps force was significantly correlated only with rectus femoris circumference (r=0.48, p=0.007), RF echogenicity (r=0.38, p=0.037), VI echogenicity (r=0.43, p=0.018), and VL fascicle length (r=0.43, p=0.019). Thigh circumference, rectus femoris CSA, rectus femoris thickness, vastus intermedius thickness, vastus lateralis thickness, vastus lateralis pennation angle were not significantly correlated with quadriceps strength.

TABLE 3

Summary of the correlation between the right and left quadriceps forces and their respective thigh morphological variables

	Thigh circumference	RF circumference	RF cross‐sectional area	RF thickness	RF echogenicity	VI thickness	VI echogenicity	VL thickness	VL pennation angle	VL fascicle length
Quadriceps force (Nm)	−0.16	0.48^**	0.18	0.085	0.38^*	0.031	0.43^*	−0.086	−0.25	0.43^*

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Abbreviations: RF, rectus femoris; VI, vastus intermedius; VL, vastus lateralis.

^*p<0.05.

^**p<0.01.

The multivariate regression analysis results between the quadriceps force and their respective RTUS predictor variables are summarized in Table Table4.4. Quadriceps force was best predicted by a three‐variable model (adjusted R²=0.46, p<0.001) which included rectus femoris echogenicity (B=0.43, p=0.005), vastus lateralis fascicle length (B=0.33, p=0.025) and rectus femoris circumference (B=0.31, p=0.041). Thus respectively, rectus femoris echogenicity explains 43%, vastus lateralis fascicle length explains 33% and rectus femoris circumference explains 31% of the variance of quadriceps force.

TABLE 4

Summary of the multivariate regression analysis results between quadriceps force and their respective RTUS predictor variables

		Standardized B	95% CI for B	p values	Model adjusted R²	F	Model p value
Predictors of quadriceps force	RF echogenicity	0.43	[0.05, 0.23]	0.005	0.46	9.38	<0.001
	VL fascicle length	0.33	[0.15, 2.02]	0.025
	RF circumference	0.31	[0.08, 3.56]	0.041

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Abbreviations: RF, rectus femoris; VI, vastus intermedius; VL, vastus lateralis.

Through comparisons of RTUS images obtained during this study, differences in muscle quality were observed. For instance, participant 12 who was relatively sedentary had poorly defined borders of the vastus intermedius, vastus medialis and vastus lateralis; a reduced overall muscle mass with increased echogenicity, and a flat “disc‐like” RF (Figure (Figure5a).5a). In contrast, participant 14 was an active rower who completed moderate intensity training one hour a day three times a week (Figure (Figure5b).5b). As such a qualitative review of the RTUS image of the anterior thigh indicated well defined and thick vastus medialis and vastus lateralis that had reduced echogenicity (Figure (Figure5b).5b). These findings highlight the clinical implications of utilising RTUS imaging as a point of care assessment tool to facilitate decision‐making and individualised rehabilitation programs. With respect to anatomical variation, 70% of the female participants in this study also demonstrated a rectus femoris that was anterolateral to the vastus intermedius (Figure (Figure5c),5c), which may be due to the wider Q‐angle in females.

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FIGURE 5

(a) Ultrasound image of the anterior thigh in a sedentary female; (b) ultrasound image of an active female; (c) ultrasound of the anterior thigh in female depicting the anterolateral “beret‐like” relationship of the RF to the VI

4. DISCUSSION

This study aimed to explore quadriceps muscle architecture and morphology in healthy adults via ultrasound imaging. In addition, we investigated the relationship between quadriceps muscle strength and quadriceps muscle architecture. Our results indicate that increased quadriceps strength was associated with increased in rectus femoris echogenicity, vastus lateralis fascicle length and rectus femoris circumference. With respect to the architecture and morphology vastus intermedius and rectus femoris thickness reported in this cohort of healthy adults is comparable to previously reported RTUS measures in 184 healthy men by Watanabe et al. (2013). These findings suggest that RTUS measures may be a useful surrogate for quadriceps strength in healthy adults. These findings rejected our hypothesis that several positive moderate associations exist between RTUS‐derived quadriceps morphological data and quadriceps strength.

In this study, we identified that quadriceps force is associated with rectus femoris circumference, rectus femoris echogenicity, vastus intermedius echogenicity and vastus lateralis fascicle length. Moreover, quadriceps strength variance is explained largely by rectus femoris echogenicity in this study. Rectus femoris muscle echogenicity is positively correlated with quadriceps muscle strength, contradicting previous studies that found the converse (Cadore et al., 2012; f*ckumoto et al., 2012; Strasser et al., 2013). Higher muscle echogenicity has been postulated as an indication of increased intramuscular fat infiltration and muscle atrophy (Reimers et al., 1993). However, well‐defined muscle fibres may display higher echogenicity (white) due to an increase in connective tissue (e.g., perimysium, epimysium) definition (Figure 5a,b). In addition, we postulate that in individuals with increased forced output capacity have associated increases in muscle fibre and overall muscle connective tissue contrast and definition.

In contrast to Strasser et al. (2013) and Raj Selva et al. (2017), we did not find a significant relationship between rectus femoris thickness and quadriceps strength. The discrepancies from the other studies may stem from the differences in quadriceps strength measure methodology including the position of testing. Studies in the literature (Raj Selva et al., 2017; Strasser et al., 2013; Watanabe et al., 2013) utilised laboratory dynamometers in a seated position to measure isometric knee extension strength at 60–90° knee flexion. By contrast, our protocol measured isometric knee extension in supine using a hand‐hand dynamometer. Moreover, it is widely accepted that maximum isometric quadriceps torque generation is observed around 50–70° knee flexion (Haffajee et al., 1972). Thus, our findings suggest that RTUS rectus femoris thickness data may not be appropriate to extrapolate end‐range knee extension strength derived from hand‐held dynamometer assessments in a healthy population. The qualitative assessment of the RTUS images of the quadriceps and its component parts may provide further insights into individual anatomical variation; and the functional implications of muscle architecture and their relationship to injury and activity levels.

As this is a pilot study with a pragmatic sample size, the results should be interpreted with caution. As the tester is required to match participant's isometric strength, weaker assessors may encounter difficulties in assessing stronger participants. However, we minimised hand‐held dynamometer‐related limitations by having a standardised assessment position, instructions and encouragement for participants. As this was pilot study it was not sufficiently powered to control for participants’ activity level and past medical history. There was one assessor who performed all assessments, whilst this is a limitation, an experienced sonographer (DEA) with more than 15years of experience was present at all assessment sessions. A further limitation in this study is the age range (55–79years) of the participants, and the possibility that some participants may have demonstrated atrophy/sarcopenia. Future research should control for age in a larger population.

Although there is emerging evidence that RTUS‐derived measurements correlate well with functional measures (e.g., timed up and go, 6‐min walk test) in healthy adults (Raj Selva et al., 2017), future studies should investigate the relationship between quadriceps muscle echogenicity, strength and functional measures in the clinical population. This would inform the clinical assessment of patients who are acutely ill and may not be able to perform maximum strength assessment. RTUS‐derived muscle anatomical and architectural data may also guide clinicians in delivering and evaluating interventions (e.g., strength training). It is also important to study heterogenous cohorts including those with specified health impairments to identify associated patterns of architecture and morphology change reflected in the musculoskeletal system as depicted by RTUS as this may further inform diagnosis and timely intervention to drive better patient outcomes.

5. CONCLUSION

RTUS‐derived muscle architecture and morphology parameters may predict the variances of quadriceps strength in healthy adults. The study findings suggest that RTUS measures could be used to support quadriceps strength assessment in healthy adults where volitional assessment is impeded. Further research is warranted in larger healthy and clinical cohorts that consider all components of the quadriceps muscle group and their relationship to strength and functional outcome measures. This study also highlights the importance of considering quantitative data pertaining to superficial and deep quadriceps muscle components in conjunction with qualitative review of ultrasound imaging to formulate a cohesive understanding of an individual's muscle function.

CONFLICT OF INTEREST

There are no conflicts to declare.

AUTHOR CONTRIBUTIONS

DEA, SP and AB contributed to the concept and study design. DEA, AS and MW contributed to the participant recruitment and acquisition of data. AP, DEA, CM, JF and RA contributed to the data interpretation. The entire authorship team contributed to the drafting and the critiquing of the manuscript. All authors approved of the manuscript.

ACKNOWLEDGEMENTS

We would like to acknowledge Brooke Cherubin and Kimberly Roe, who were Physiotherapy students that assisted with administrative aspects of the study.

Notes

El‐Ansary, D., Marshall, C.J., Farragher, J., Annoni, R., Schwank, A., McFarlane, J., et al (2021) Architectural anatomy of the quadriceps and the relationship with muscle strength: An observational study utilising real‐time ultrasound in healthy adults. Journal of Anatomy, 239, 847–855. 10.1111/joa.13497 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

DATA AVAILABILITY STATEMENT

Data available on request from the authors.

REFERENCES

Arts, I.M.P., Pillen, S., Schelhaas, H.J., Overeem, S. & Zwarts, M.J. (2010) Normal values for quantitative muscle ultrasonography in adults. Muscle and Nerve, 41, 32–41. [PubMed] [Google Scholar]
Bryanton, M. & Bilodeau, M. (2017) The role of thigh muscular efforts in limiting sit‐to‐stand capacity in healthy young and older adults. Aging Clinical and Experimental Research, 29, 1211–1219. [PubMed] [Google Scholar]
Cadore, E.L., Izquierdo, M., Conceição, M., Radaelli, R., Pinto, R.S., Baroni, B.M. et al. (2012) Echo intensity is associated with skeletal muscle power and cardiovascular performance in elderly men. Experimental Gerontology, 47, 473–478. [PubMed] [Google Scholar]
Chleboun, G.S., Busic, A.B., Graham, K.K. & Stuckey, H.A. (2007) Fascicle length change of the human tibialis anterior and vastus lateralis during walking. Journal of Orthopaedic and Sports Physical Therapy, 37, 372–379. [PubMed] [Google Scholar]
English, C., Fisher, L. & Thoirs, K. (2012) Reliability of real‐time ultrasound for measuring skeletal muscle size in human limbs in vivo: a systematic review. Clinical Rehabilitation, 26, 934–944. [PubMed] [Google Scholar]
f*ckumoto, Y., Ikezoe, T., Yamada, Y., Tsukagoshi, R., Nakamura, M., Mori, N. et al. (2012) Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle‐aged and elderly persons. European Journal of Applied Physiology, 12, 1519–1525. [PubMed] [Google Scholar]
Haffajee, D., Moritz, U. & Svantesson, G. (1972) Isometric knee extension strength as a function of joint angle, muscle length and motor unit activity. Acta Orthopaedica Scandinavica, 43, 138–147. [PubMed] [Google Scholar]
International Physical Activity Questionnaire IPAQ(n.d). International Physical Activity Questionnaire. Available from: https://sites.google.com/site/theipaq/scoring‐protocol [Accessed 17th December 2020].
Jedrzejczak, A. & Chipchase, L.S. (2008) The availability and usage frequency of real time ultrasound by physiotherapists in South Australia: an observational study. Physiotherapy Research International, 13, 231–240. [PubMed] [Google Scholar]
Knols, R.H., Aufdemkampe, G., de Bruin, E.D., Uebelhart, D. & Aaronson, N.K. (2009) Hand‐held dynamometry in patients with haematological malignancies: measurement error in the clinical assessment of knee extension strength. BMC Musculoskeletal Disorders, 10, 31. [PMC free article] [PubMed] [Google Scholar]
Kwah, L.K., Pinto, R.Z., Diong, J. & Herbert, R. (2013) Reliability and validity of ultrasound measurements of muscle fascicle length and pennation in humans: a systematic review. Journal of Applied Physiology, 114, 761–769. [PubMed] [Google Scholar]
Lima, K.M., da Matta, T.T. & de Oliveira, L.F. (2012) Reliability of the rectus femoris muscle cross‐sectional area measurements by ultrasonography. Clinical Physiology and Functional Imaging, 32, 221–226. [PubMed] [Google Scholar]
Maurits, N.M., Bollen, A.E., Windhausen, A., De Jager, A.E.J. & Van Der Hoeven, J.H. (2003) Muscle ultrasound analysis: normal values and differentiation between myopathies and neuropathies. Ultrasound in Medicine and Biology, 29, 215–225. [PubMed] [Google Scholar]
Mendis, M.D., Wilson, S.J., Stanton, W. & Hides, J.A. (2010) Validity of real‐time ultrasound imaging to measure anterior hip muscle size: a comparison with magnetic resonance imaging. Journal of Orthopaedic and Sports Physical Therapy, 40, 577–581. [PubMed] [Google Scholar]
Menon, M.K., Houchen, L., Harrison, S., Singh, S.J., Morgan, M.D. & Steiner, M.C. (2012) Ultrasound assessment of lower limb muscle mass in response to resistance training in COPD. Respiratory Research, 13, 119. [PMC free article] [PubMed] [Google Scholar]
Nijboer‐Oosterveld, J., Van Alfen, N. & Pillen, S. (2011) New normal values for quantitative muscle ultrasound: obesity increases muscle echo intensity. Muscle and Nerve, 43, 142–143. [PubMed] [Google Scholar]
Ogawa, M., Yasuda, T. & Abe, T. (2012) Component characteristics of thigh muscle volume in young and older healthy men. Clinical Physiology and Functional Imaging, 32, 89–93. [PubMed] [Google Scholar]
Parry, S.M., Burtin, C., Denehy, L., Puthucheary, Z.A. & Bear, D. (2019) Ultrasound evaluation of quadriceps muscle dysfunction in respiratory disease. Cardiopulmonary Physical Therapy Journal, 30, 15–23. [Google Scholar]
Parry, S.M., El‐Ansary, D., Cartwright, M.S., Sarwal, A., Berney, S., Koopman, R. et al. (2015) Ultrasonography in the intensive care setting can be used to detect changes in the quality and quantity of muscle and is related to muscle strength and function. Journal of Critical Care, 30, 1151.e9‐14. [PubMed] [Google Scholar]
Puthucheary, Z.A., Rawal, J., McPhail, M., Connolly, B., Ratnayake, G., Chan, P. et al. (2013) Acute skeletal muscle wasting in critical illness. JAMA, 310, 1591–1600. [PubMed] [Google Scholar]
Raj Selva, I., Bird, S.R. & Shield, A.J. (2017) Ultrasound measurements of skeletal muscle architecture are associated with strength and functional capacity in older adults. Ultrasound in Medicine and Biology, 43, 586–594. [PubMed] [Google Scholar]
Reimers, C.D., Harder, T. & Saxe, H. (1998) Age‐related muscle atrophy does not affect all muscles and can partly be compensated by physical activity: an ultrasound study. Journal of the Neurological Sciences, 159, 60–66. [PubMed] [Google Scholar]
Reimers, K., Reimers, C.D., Wagner, S., Paetzke, I. & Pongratz, D.E. (1993) Skeletal muscle sonography: a correlative study of echogenicity and morphology. Journal of Ultrasound in Medicine, 12, 73–77. [PubMed] [Google Scholar]
Sarwal, A., Parry, S.M., Berry, M.J., Hsu, F.C., Lewis, M.T., Justus, N.W. et al. (2015) Inter‐observer reliability of quantitative muscle ultrasound analysis in the critically ill population. Journal of Ultrasound in Medicine, 34, 1191–2000. [PubMed] [Google Scholar]
Scott, J.M., Martin, D.S., Cunningham, D., Matz, T., Caine, T., Hackney, K.J. et al. (2012) Panoramic ultrasound cross‐sectional area measurements for long‐duration spaceflight. NASA Human Research Program Investigators’ Workshop.
Strasser, E.M., Draskovits, T., Praschak, M., Quittan, M. & Graf, A. (2013) Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age, 35, 2377–2388. [PMC free article] [PubMed] [Google Scholar]
Thorborg, K., Bandholm, T. & Hölmich, P. (2013) Hip‐ and knee‐strength assessments using a hand‐held dynamometer with external belt‐fixation are inter‐tester reliable. Knee Surgery, Sports Traumatology, Arthroscopy, 21, 550–555. [PubMed] [Google Scholar]
Toumi, H., Poumarat, G., Benjamin, M., Best, T., F'guyer, S. & Fairclough, J. (2007) New insights into the function of the vastus medialis with clinical implications. Medicine and Science in Sports and Exercise, 39, 1153–1159. [PubMed] [Google Scholar]
Unhjem, R., van den Hoven, L.T., Nygård, M., Hoff, J. & Wang, E. (2017) Functional performance with age: the role of long‐term strength training. Journal of Geriatric Physical Therapy, 42(3), 115–122. 10.1519/JPT.0000000000000141. [PubMed] [CrossRef] [Google Scholar]
Watanabe, Y., Yamanda, Y., f*ckumoto, T. et al. (2013) Echo intensity obtained from ultrasound images reflecting muscle strength in elderly men. Clinical Interventions in Aging, 8, 993–998. [PMC free article] [PubMed] [Google Scholar]

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