Validity and reliability of a simple ultrasound approach to measure medial gastrocnemius muscle length

Authors


Lee Barber, School of Physiotherapy and Exercise Science, Griffith University, Gold Coast Campus, Gold Coast, Qld 4222, Australia. T: + 61 7 5552 7062; F: + 61 7 5552 8674; E: l.barber@griffith.edu.au

Abstract

Fixed shortening of a muscle, or contracture, often develops in individuals with an upper motor neuron disorder. A clinical measure of muscle length would therefore be useful for identifying the presence of muscle contracture, tracking changes over time and evaluating the effect of interventions. This study compared a novel ultrasound-tape length method with a previously validated freehand 3D ultrasound method for measuring muscle length. The ultrasound-tape method intra-session reliability was also assessed. Resting medial gastrocnemius muscle length was measured at three ankle joint angles in 15 typically developed (TD) adults and nine adults with cerebral palsy (CP) using the two methods. The ultrasound-tape method on average overestimated the muscle length in the TD group by < 0.1% (95% CI, 6%) and underestimated in the muscle length in the CP group by 0.1% (95% CI, 6%) compared with the 3D ultrasound method. Intra-session reliability of the ultrasound-tape method was high, with intra-class correlation coefficients > 0.99. The ultrasound-tape method has sufficient accuracy to detect clinically relevant differences and changes in medial gastrocnemius muscle length and may therefore be a useful clinical tool for assessing muscle length changes associated with contracture.

Introduction

Individuals with upper motor neuron lesions, such as those associated with spastic cerebral palsy (CP), stroke, traumatic brain injury and multiple sclerosis, and spinal cord injuries often present with contracture of affected muscles and associated motor impairment (Sheean, 2002). Contracture is defined as the fixed shortening of a muscle (often referred to as the muscle belly) in relation to the length of the accompanying long bone (Bache et al. 2003). Clinicians and researchers typically use joint range of motion as an indirect measure of muscle contracture (Mcdowell et al. 2000; Fry et al. 2003). However, joint range of motion measures cannot differentiate the contributions of the multiple muscles that span the joint or the contributions of the muscle and tendon of individual muscles to the contracture. A clinical measure of individual muscle length would therefore be useful for identifying the presence of contracture, tracking muscle length changes over time and evaluating the effect of treatment interventions for spasticity and contracture such as physiotherapy, immobilisation (e.g. splinting), botulinum toxin injections or orthopaedic surgery.

Magnetic resonance imaging (MRI) is the modality of choice for direct measurement of muscle length in vivo (Mitsiopoulos et al. 1998; Oberhofer et al. 2009). However, this technique is expensive, may not be available, takes a substantial amount of time for each scan (typically > 2 min) and in some cases, patients require sedation. B-mode ultrasound (US) is commonly used to visualise muscle and tendon morphology and obtain quantitative information concerning muscle properties including muscle anatomical cross-sectional area, muscle thickness, fascicle length and fascicle angle (Campbell & Wood, 2002; Maganaris, 2003; Whittaker et al. 2007; Ohata et al. 2008). Measurement of in vivo muscle length is difficult with B-mode US as the field of view is typically insufficient to visualise the whole muscle. An alternative approach is to use freehand 3D ultrasound (3DUS), which combines B-mode US with measures of 3D probe position, and yields muscle length estimates within 1.3% of MRI (Barber et al. 2009). However, this approach requires 3D motion capture and time-consuming analysis to manually segment each B-mode US image (Weller et al. 2007).

The purpose of this study was to determine the validity and reliability of muscle length measures obtained using a novel US and tape measure (US-tape) method in a typically developed and clinical sample consisting of individuals with CP. Muscle length measures of the medial gastrocnemius (MG) obtained using the US-tape method were compared with measures obtained using 3DUS. The MG muscle was chosen for analysis because it is commonly affected by contracture in neurological conditions such as spastic CP (Malaiya et al. 2007) and stroke (Gao & Zhang, 2008) and because of its functional importance in locomotion (Liu et al. 2008; Steele et al. 2010). Reductions in MG muscle length of 8–31% in CP compared with TD, and in the paretic vs. non-paretic limbs in CP have been reported (Fry et al. 2004; Malaiya et al. 2007). Further, Fry et al. (2007) reported MG muscle length changes following orthopaedic surgery in children with CP of 5–12%. We hypothesised that the measurement error associated with our US-tape method would be small enough to detect the observed differences/changes in muscle length reported in these studies.

Materials and methods

Participants

Fifteen typically developed (TD) [five females, 10 males, mean (SD) age 19 (3) years, mass 66 (8) kg, height 173 (7) cm] and nine individuals with spastic CP [three females, six males, age 17 (2) years, mass 57 (10) kg, height 164 (7) cm], volunteered to participate in the study. The CP participants were either hemiplegic (= 7) or diplegic (= 2) and all were level I on the Gross Motor Function Classification System for Cerebral Palsy (Palisano et al. 2008) and were recruited through the Cerebral Palsy League Queensland. TD participants were healthy university staff or students. All participants provided written informed consent in accordance with institutional guidelines (CPLQ-2008/09-1023, GU Ref No.: PES/21/08/HREC).

Experimental design

Three US-tape scans and three 3DUS scans were performed on the relaxed MG muscle of the right leg of the TD participants and on the most affected leg of the CP participants at each ankle angle – 30, 60 and 100% of the total ankle range of motion (ROM) from maximum plantar flexion (0% ROM) to maximum dorsiflexion (100% ROM). The knee was maintained at 0° extension using a seat belt around the thigh. The ankle range of motion was assessed and ankle angles passively positioned using an isokinetic dynamometer (Biodex System 4, Biodex Medical Systems Inc., Shirley, NY).

Ultrasound measures

A PC-based B-mode US scanner with a 128-element beamformer and a 10.0 MHz linear transducer (HL9.0/60/128Z, Telemed Echo Blaster 128 Ext-1Z system, Vilnius, Lithuania) was used for both the US-tape and 3DUS measures. A scanning depth and width of 60 mm was used for all scans. US settings such as power, gain, and focal depth were optimised to allow ease of identification of the structures under investigation (Barber et al. 2009).

The US-tape method involved the attachment of a metal tape measure to the US transducer at one end, and positioned over the Achilles tendon insertion on the calcaneus at the other end (Fig. 1). The proximal attachment of the MG was difficult to visualise with US so the most superficial aspect of the medial condyle of the femur was used as a standard proximal landmark for the US-tape method (Fig. 1A). The tape distance from the calcaneus to the edge of the US transducer scan plane was recorded. A medial to lateral sweep of the transducer head was made over the medial femoral condyle whilst the tape was kept taut (at the same length) and the scan recorded. Post-processing of the scan was performed to identify the most superficial point of the condyle and the US depth and US distance of the condyle to the edge of the scan (Fig. 1B). The most distal point of the muscle tendon junction (MTJ) was also scanned using a medial to lateral sweep of the transducer whilst the tape was kept taut (Fig. 1C). The tape distance from the calcaneus to the edge of the US transducer scan plane was recorded. Post processing was performed and the US depth and US distance of the most distal MTJ point relative to the edge of the scan measured (Fig. 1D). MTU length and tendon length were calculated using Pythagoras’ theorem based on measures of: (i) tape distance plus US distance and (ii) US depth of the condyle/MTJ. Muscle length was calculated by subtracting tendon length from MTU length.

Figure 1.

 US-tape method for measuring MG muscle belly length. (A) MTU length was measured from the calcaneus to the superficial aspect of the medial femoral condyle, posteriorly (tape distance + US distance). (B) Identification of the most superficial aspect of the condyle and the US depth and distance of the condyle to the edge of the scan. (C) Tendon length was measured from the calcaneus to the most distal aspect of the MTJ of the MG (tape distance + US distance). (D) Identification of the most distal point of the MTJ and the US depth and distance of the MTJ to the edge of the scan. Muscle belly length was calculated from the difference between MTU length and tendon length.

Freehand 3DUS was used to generate 3D reconstructions of the MG muscle as previously described in Barber et al. (2009). The same anatomical landmarks were used for segmentation of the muscle volume as used for the US-tape method – the most superficial aspect of the medial condyle of the femur proximally to the most distal point of the MTJ distally. Measurement of the muscle length was obtained from the 3D rendering using the stradwin software measurement tools.

Statistical analysis

The level of agreement between the US-tape method and the freehand 3DUS-based measurement of MG muscle length was reported as the mean difference and corresponding limits of agreement (i.e. 95% confidence intervals) (Bland & Altman, 1986) for the TD and CP groups each ankle joint angle assessed. Intra-session reliability of muscle length measurements made using the US-tape over three trials was assessed using the intra-class correlation coefficient, ICC (3,1).

Results

Validity

Medial gastrocnemius muscle length estimates using the US-tape method and freehand 3DUS, mean difference (mm), mean percentage difference and corresponding upper and lower limits of agreement for the TD and CP groups at each ankle joint angle are presented in Table 1. Mean muscle length (SD) averaged across the three ankle joint angles was 237 (12) mm in the TD group and 201 (9) mm in the CP group. The US-tape method overestimated MG muscle length by 0.2 mm (< 0.1%) in the TD group and by 0.3 mm (0.1%) in the CP group across all ankle joint angles. The limits of agreement for the mean difference between the two methods across all joint angles was 15 mm (6%) for the TD group and 13 mm (6%) for the CP group (Figs 2 and 3). It is also evident from Figs 2 and 3 that the assumption underlying use of the limits of agreement method that the mean and standard deviation of the difference between the US-Tape and 3DUS measures of muscle length are constant over the range of the data and normally distributed do not appear to have been violated.

Table 1.   Medial gastrocnemius muscle length measured using the US-tape and freehand 3DUS methods for the typically developed (TD) and cerebral palsy (CP) groups.
GroupAnkle joint angle (% ROM)Mean ankle angle (°)Muscle length (mm)Mean difference (mm)Upper LoA (mm)Lower LoA (mm)95% CI (mm)Mean difference (%)95% CI (%)
3DUSUS-tape
  1. ROM, range of motion; LoA, limit of agreement; CI, confidence interval.

  2. Mean percentage difference is the ratio of the difference and the mean of the 3DUS and US-tape measures.

  3. Data are presented as mean (SD). Positive ankle angles indicate dorsiflexion. 100% ROM,  maximum dorsiflexion.

TD10023(4)249 (26)249 (27)−0.1 (3)6.2−6.3120.0 (1)5
60−2(3)236 (24)237 (27)−0.9 (3)6.2−8.014−0.3 (1)6
30−21(4)225 (24)225 (24)0.3 (4)8.1−8.5170.2 (2)8
CP1005(5)211 (39)211 (39)0.7 (4)7.7−6.3140.3 (1)6
60−13(2)202 (41)202 (40)0.2 (3)6.1−5.6120.1 (1)5
30−26(3)192 (35)192 (36)0.1 (4)6.2−6.413−0.1 (1)6
Figure 2.

 Scatter plots (left column) and Bland–Altman plots (right column) showing correspondence between 3DUS and US-tape measures of the MG muscle length in three ankle positions (100, 60 and 30% of range of motion) for TD individuals. The diagonal line (small dash) in the scatter plots corresponds to the line of perfect agreement. The horizontal lines on the Bland–Altman plots represent perfect agreement (small dash), the mean difference between the 3DUS and US-tape measurements (solid line) and the upper and lower limits of agreement (large dash). ML, muscle length.

Figure 3.

 Scatter plots (left column) and Bland–Altman plots (right column) showing correspondence between 3DUS and US-tape measures of the MG muscle length in three ankle positions (100, 60 and 30% of range of motion) for individuals with CP. The diagonal line (small dash) in the scatter plots corresponds to the line of perfect agreement. The horizontal lines on the Bland–Altman plots represent perfect agreement (small dash), the mean difference between the 3DUS and US-tape measurements (solid line) and the upper and lower limits of agreement (large dash). ML, muscle length.

Reliability

The ICCs for repeated intra-session US-tape measures of MG muscle length at each ankle angle for the TD and CP groups were > 0.99 (Table 2).

Table 2.   Reliability of intra-session repeated measures of MG muscle length (mm) by the US-tape method assessed using the intra-class correlation coefficient (ICC).
GroupAnkle joint angle (% ROM)MG muscle length (mm)ICC (3,1)
Trial 1Trial 2Trial 3
  1. Data are presented as mean (SD).

TD100248 (28)249 (27)247 (28)0.999
60235 (27)236 (27)234 (27)0.999
30224 (25)225 (25)223 (25)0.999
CP100211 (41)212 (41)211 (41)0.999
60203 (42)202 (42)102 (44)0.999
30192 (36)192 (36)191 (37)0.998

Discussion

This study demonstrated good agreement between freehand 3DUS and the US-tape measures of MG muscle length in the TD and CP groups across a range of ankle joint angles. Compared to our 3DUS measure, which we validated against MRI (Barber et al. 2009), the US-tape method overestimated MG muscle length by < 0.2 mm (0.1%) in the TD group and underestimated MG muscle length by (0.3 mm) 0.1% in the CP group. The overall limits of agreement were 13–15 mm (6%) for the TD and CP groups, respectively. Importantly, the relative magnitude and direction of the error was unaffected by the ankle joint angle at which the measurements were made and the ICCs for intra-session reliability were high (i.e. > 0.99).

To put our findings in a clinical perspective it is necessary to compare the accuracy of our US-tape method with the expected differences or changes in muscle length that the method may be used to detect in a given patient population. Unfortunately, at present there is a general paucity of information available on muscle length adaptation following upper motor neuron lesions, with published studies on this topic generally confined to CP (see Barrett & Lichtwark, 2010 for review). Although the present study was performed using young adults and not children, 6% limits of agreement of the US-tape method reported here are in the vicinity of the lower end of the 8–31% range of differences in MG muscle length relative to TD or the less affected limb reported by Fry et al. (2004) and Malaiya et al. (2007), as well as the lower end of the 5–12% range of muscle length changes following orthopaedic surgery in children with CP (Fry et al. 2007). We therefore believe our findings in this feasibility study demonstrate proof of concept in relation to the use of the US-tape method as a clinically useful tool for quantifying muscle contracture. We are currently unaware of any studies that have measured the natural history of muscle length changes over time in any patient group following upper motor neuron lesion, and so it is currently difficult to assess the suitability of the US-tape method for this purpose. Further, larger scale studies will be therefore required to determine the suitability of the US-tape method to assess the progression of muscle contracture over time and following conservative and pharmaceutical treatment interventions in specific patient groups with contracture for which data on the magnitude of muscle length adaptations are not currently available. It would also be of value in future to assess whether the method described here is suitable for assessing muscle length adaptations in other muscles affected by contracture (e.g. upper limb muscles).

Compared to other imaging modalities, we believe the US-tape method is a relatively simple, efficient and cost-effective technique for measuring muscle contracture in the clinical environment. The method is easy to carry out and requires minimal ultrasonographic experience to localise the anatomical landmarks, scan and record the regions of interest. We were able to make the required US recordings and perform the necessary post-processing to obtain MG muscle length estimates at each ankle joint angle within a few minutes for each participant using our US-tape method. Compared to MRI, we estimate that the required capital equipment is about 10 times less for US, and that the US-tape measurements can be performed about 10 times faster due to the minimal set-up, acquisition and post-processing time involved.

Conclusion

This study demonstrated accurate measurement of MG muscle length using the US-tape method over a large range of ankle joint angles in young adults who are typically developed or have spastic CP. The ease, speed and accuracy of the US-tape method lends itself to clinical use for measurement of MG muscle lengths in individuals presenting with contracture, such as those with stroke, multiple sclerosis or spastic CP.

Acknowledgements

This work was supported by funding from the National Health and Medical Research Council, Australia (Biomedical Postgraduate Scholarship Grant ID: 481953).

Conflict of interest disclosure

No financial or personal relationships were conducted with individuals or organizations that could inappropriately influence or bias this work.

Authors’ contributions

All authors contributed to the concept and design of the project, acquisition of data, data analysis/interpretation, drafting of the manuscript, critical revision of the manuscript and approval of the article.

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