[
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]
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JACKIE L. WHITTAKER, PT, PhD, FCAMPT1,2 • CAROLYN A. EMERY, PT, PhD1,2
Sonographic Measures of the Gluteus Medius, Gluteus Minimus, and Vastus Medialis Muscles
T
he clinical use of ultrasound imaging (USI) by physiotherapists to measure muscle morphology during static and dynamic conditions falls within the scope of rehabilitative ultrasound imaging.17 Specifically, rehabilitative USI refers to the USI procedures used by physiotherapists to evaluate the morphology and behavior of muscle and its related soft tissues, to provide biofeedback about muscle behavior during restoration of function, TTSTUDY DESIGN: Intrarater, repeated-measures, within-session reliability study.
TTOBJECTIVE: To describe a standardized
method and preliminary reliability estimates for sonographic measures of resting and contracted gluteus medius (GMd), gluteus minimus (GMn), and resting vastus medialis (VM) muscles.
TTBACKGROUND: Sonography has been used to
assess the morphology of a diversity of muscles in relation to a variety of musculoskeletal dysfunctions. Although the GMd, GMn, and VM muscles are associated with dysfunctions such as patellofemoral pain and osteoarthritis, there is a paucity of information regarding protocols for sonographic measurements of these muscles.
TTMETHODS: A standardized method was devel-
contracted, and change during contraction (intraclass correlation coefficient model 3,3 [ICC3,3]) of the GMd were 0.98 (95% confidence interval [CI]: 0.97, 0.99), 0.98 (95% CI: 0.96, 0.99), and 0.84 (95% CI: 0.71, 0.92), respectively, and of the GMn were 0.98 (95% CI: 0.97, 0.99), 0.94 (95% CI: 0.88, 0.97), and 0.53 (95% CI: 0.21, 0.76), respectively. Reliability (ICC3,3) for resting VM cross-sectional area was 0.99 (95% CI: 0.99, 0.99). Standard error of measurement for GMd, GMn, and VM varied between 0.5 and 1.6 mm, 0.3 and 1.4 mm, and 0.4 cm2, respectively, and 95% minimal detectable change ranged from 0.8 to 4.5 mm for the gluteals and 0.4 to 0.5 cm2 for the VM.
TTCONCLUSION: Reliable sonographic measure-
oped and used to gather sonographic measures of resting and contracted (sidelying hip abduction task) GMd and GMn thickness and resting VM cross-sectional area during 1 measurement session in 29 female soccer players 14 to 17 years of age.
ments of the lateral hip and knee musculature at rest and during contraction are feasible. Further investigation is required to establish the generalizability and reproducibility of the protocols presented in this report. J Orthop Sports Phys Ther 2014;44(8):627-632. Epub 16 July 2014. doi:10.2519/jospt.2014.5315
ultrasound imaging measurements of resting,
reliability, ultrasonography
TTRESULTS: Intrarater reliability values for
TTKEY WORDS: gluteal muscles, quadriceps,
and to carry out research aimed at informing clinical practice.17 To date, USI has been used to investigate a variety of muscles and to address a diversity of research questions. Sonography has been shown to be a valid method (primarily in healthy adults under resting conditions) to measure the morphology of the trunk (abdominal and lumbar multifidus),2,3 as well as a range of other muscles,5,8,10,11 through comparison to magnetic resonance imaging. Further, there are numerous investigations that have assessed the reproducibility of sonographic measures of the trunk muscles.1,6,7,18 In general, these investigations report moderate to excellent reliability for repeated resting measures, and poor to good reliability for measures of morphological change during a task in both healthy and patient samples. A large number of investigations consider sonographic measures of the morphology of the trunk muscles; however, there is a paucity of information regarding other muscles that may be amenable to USI. Of particular interest, and the topic of this report, are the muscles of the lateral hip (gluteus medius [GMd] and gluteus minimus [GMn]) and knee (vastus medialis [VM]), which play an important role
Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada. 2The Alberta Children’s Hospital Research Institute for Child and Maternal Health, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada. Ethics approval was granted from the Conjoint Health Research Ethics Board at the University of Calgary, Calgary, Alberta, Canada. The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or materials discussed in the article. Address correspondence to Dr Jackie L. Whittaker, Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, 2500 University Drive NW, Calgary, Alberta, Canada T2N 1N4. E-mail: [email protected] t Copyright ©2014 Journal of Orthopaedic & Sports Physical Therapy® 1
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[
brief report
] for investigating the morphology of the GMd, GMn, and VM that is amenable to clinical research and practice, and, if adopted by other investigative teams, will facilitate the synthesis of data from future investigations. A secondary purpose was to assess the feasibility of this methodology by presenting preliminary estimates of within-session intrarater reliability.
METHODS Participants
P FIGURE 1. (A) Lateral hip muscle imaging site (gray oval). (B) GMd and GMn thickness measurements (dashed circle represents the superior lip of the acetabulum). (C) Sidelying hip abduction task. Abbreviations: GMd, gluteus medius; GMn, gluteus minimus.
articipants included 29 healthy, consenting female adolescent (aged 14 to 17 years) soccer players recruited from 2 teams (n = 36) that participated in a randomized controlled trial investigating the implementation of a neuromuscular injury-prevention program across 29 teams (n = 226) during the 2011 season. Information regarding participant recruitment and eligibility for the implementation trial is detailed elsewhere. 14 Ethics approval was granted from the Conjoint Health Research Ethics Board at the University of Calgary, Calgary, Alberta, Canada.
USI Protocol
FIGURE 2. (A) VM imaging site (gray oval). (B) VM cross-sectional area measurement. Abbreviation: VM, vastus medialis.
in the control of the hip, knee, and patellofemoral joints during gait, running, and sporting activities.16 Although there has been preliminary work published with respect to sonographic assessment of these muscles, the methods presented are difficult to replicate in clinical research due to insufficient reporting4 and the need for advanced imaging techniques and analyses. 9 If methods amenable to clinical research
could be established, they would enable the assessment and comparison of the morphology of these muscles with respect to a variety of populations (eg, healthy, sporting, and injured), dysfunctions (patellofemoral pain, osteoarthritis, etc), and interventions (eg, strengthening, balance, and injuryprevention programs). Consequently, the primary purpose of this report was to present a sonographic methodology
All sonographic images were collected by a single experienced sonographic operator (J.W.), an experienced physiotherapist with 12 years of USI experience. A USI system (MyLab 25; Esaote North America, Inc, Indianapolis, IN) with a 5.0-MHz curvilinear transducer (40-mm footprint; lateral and axial resolution of 1.0 and 0.93 mm, respectively) was used to collect bilateral anonymized resting B-mode ultrasound images of the GMd and GMn ( FIGURE 1 ) from a sidelying position, and of the VM ( FIGURE 2) from a supine position. Additionally, images of the GMd and GMn during muscular contraction were obtained during a standardized sidelying hip abduction task (20-mmHg reduction in a pressure biofeedback cuff ). Precise descriptions
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Summary of Techniques for Ultrasound Imaging of the Gluteus Medius, Gluteus Minimus, and Vastus Medialis
Journal of Orthopaedic & Sports Physical Therapy® Downloaded from www.jospt.org at University of Winnipeg Library on August 24, 2014. For personal use only. No other uses without permission. Copyright © 2014 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
TABLE 1 Muscle
Participant Position
Gluteus medius and minimus
Sidelying with the test leg up. The test-leg hip is in Place the transducer on the lateral aspect of the hip To standardize across participants, inflate the PBU so neutral flexion/extension, neutral rotation, and on the lower half of a coronal line located between that the starting position is 20° of hip adduction 20° of adduction (inclinometer confirmed). The the top of the greater trochanter and a point 25% from the horizontal. Instruct participants to gently test-leg knee is in full extension, with a PBU placed of the distance between the ASIS and PSIS. Adjust lift their leg toward the ceiling, keeping their toes under the ankle and foot. the cranial-caudal position of the transducer until pointing forward, until the reading on the PBU the superior lip of the acetabulum (dashed circle decreases by 20 mmHg. in FIGURE 1) is one third of the distance from the right border of the image.
Transducer Location
Contraction Technique
Vastus medialis
Supine with the hips of both legs in neutral flexion/ extension, rotation, abduction/adduction, and the knee in full extension.
Place the transducer in a transverse orientation just superior to the patella. Slide the transducer down until it butts up against the top of the patella, then move it medially (with care given not to adjust the cranial-caudal position and to maintain a tangential orientation to the surface of the knee) until entire CSA of the muscle is within the field of view (FIGURE 2).
NA
Abbreviations: ASIS, anterior superior iliac spine; CSA, cross-sectional area; NA, not applicable; PBU, pressure biofeedback unit (Chattanooga Stabilizer; DJO Global Inc, Vista, CA); PSIS, posterior superior iliac spine.
of participant position, imaging site, and hip abduction task are provided in TABLE 1. These procedures were chosen after review of cadaveric specimens, thorough review of previous imaging studies,4,9 and extensive pilot testing in both clinical and laboratory settings. Three images were acquired at each imaging site for both resting and contracted (GMd and GMn) conditions (ie, 3 trials). The transducer was removed and repositioned between trials, which provided the participant with a 10- to 20-second rest. To avoid an order or fatigue effect, the order in which the muscles and maneuvers were imaged was randomized. Testing of all participants occurred over a 3-day period. Images were measured offline using custom-written measurement codes in MATLAB Version 7.1 software (The MathWorks, Inc, Natick, MA). The measurement codes had 2 unique features relevant to this investigation. First, they prompted the operator to plot a reference line, which ensured that measurements could be made at the same location in the resting and contracted images. Second, the codes concealed measurements from the op-
erator by directly exporting them into an Excel (Microsoft Corporation, Redmond, WA) worksheet. This ensured blinding of the examiner throughout the measurement process. Measurements of GMd and GMn thickness (FIGURE 1) and VM (FIGURE 2) cross-sectional area were made and the mean of the 3 repetitions used for analyses. All measurements excluded the perimuscular connective tissue (thickness was defined as the distance between the inside edges of each muscle border), as this tissue has been shown to differ in thickness between case and healthy populations. 18 Information from 2 previous studies regarding the influence of transducer motion on measurements of muscle thickness, 19 as well as the pattern of transducer motion that occurs during leg-lifting maneuvers, 20 was taken into consideration during data collection. Namely, the operator made every attempt to keep the angular and inward/ outward motion of the transducer to a minimum, and paid specific attention to countering transducer motion at the point of initiation of the leg lift during the hip abduction task.
Data Analysis Statistical analyses were performed using the statistical software Stata Version 12.1 (StataCorp LP, College Station, TX). The mean and 95% confidence interval (CI) values for resting GMd and GMn thickness and VM cross-sectional area, as well as for the contracted GMd and GMn during hip abduction, were calculated. Intraclass correlation coefficients (ICCs) with 95% CIs were calculated to assess within-session intrarater reliability (model 3,3).13 To assess measurement precision, standard error of measurement (SEM) was calculated as SD × √1 – ICC.12 The 95% minimal detectable change (MDC95), which represents the minimal change in thickness that must occur to be 95% confident that a true change has occurred, was calculated as 1.96 × SEM × √2.15 To assess absolute agreement, the mean difference between measurements 1 and 3, as well as the 95% limits of agreement (mean difference between measurements ±2 SD), were calculated. Bland-Altman plots were used to look for any systematic bias, outliers, and relationships between the difference in values between images and their magnitudes.
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[
]
Descriptive Data and Within-Day Intrarater ICC, SEM, MDC, Bias, and Limits-of-Agreement Values
TABLE 2 Mean ± SD*
ICC3,3*
SEM
MDC95
Difference (Measures 1 and 3)†
Rest
20.5 ± 3.9 (19.0, 22.0)
0.98 (0.97, 0.99)
0.5
1.4
0.05 (–0.23, 0.32)
Contracted
22.6 ± 3.8 (21.1, 24.0)
0.98 (0.96, 0.99)
0.6
1.5
0.02 (–0.24, 0.29)
Change
2.1 ± 1.5 (1.5, 2.7)
0.84 (0.71, 0.92)
0.6
1.6
–0.03 (–0.34, 0.29)
Rest
20.2 ± 4.0 (18.7, 21.7)
0.96 (0.92, 0.98)
0.8
2.3
0.05 (–0.68, 0.77)
Contracted
22.5 ± 4.0 (20.9, 24.0)
0.91 (0.83, 0.95)
1.2
3.4
0.03 (–0.19, 0.25)
Change
2.1 ± 2.4 (1.1, 3.0)
0.54 (0.22, 0.77)
1.6
4.5
–0.09 (–1.02, 0.85)
Rest
12.2 ± 2.2 (11.3, 13.0)
0.98 (0.97, 0.99)
0.3
0.8
–0.03 (–0.19, 0.14)
Contracted
12.6 ± 2.1 (11.8, 13.4)
0.94 (0.88, 0.97)
0.5
1.5
–0.03 (–0.33, 0.27)
Change
0.4 ± 1.0 (0.07, 0.08)
0.53 (0.21, 0.76)
0.7
1.9
0.01 (–0.37, 0.38)
Rest
11.9 ± 2.4 (11.0, 12.8)
0.96 (0.92, 0.98)
0.5
1.4
–0.02 (–0.30, 0.27)
Contracted
12.8 ± 2.5 (11.8, 13.8)
0.83 (0.70, 0.92)
1.0
2.8
–0.05 (–0.34, 0.24)
Change
0.9 ± 2.0 (0.1, 1.6)
0.50 (0.19, 0.75)
1.4
3.9
–0.13 (–0.97, 0.70)
VM right at rest, cm2
12.7 ± 2.9 (11.6, 13.8)
0.99 (0.99, 0.99)
0.2
0.4
0.08 (–0.69, 0.86)
VM left at rest, cm2
12.5 ± 2.5 (11.6, 13.5)
0.99 (0.99, 0.99)
0.2
0.5
0.06 (–0.68, 0.81)
Muscle/State Journal of Orthopaedic & Sports Physical Therapy® Downloaded from www.jospt.org at University of Winnipeg Library on August 24, 2014. For personal use only. No other uses without permission. Copyright © 2014 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
brief report
GMd right, mm
GMd left, mm
GMn right, mm
GMn left, mm
Abbreviations: GMd, gluteus medius; GMn, gluteus minimus; ICC, intraclass correlation coefficient; MDC, minimal detectable change; SEM, standard error of measurement; VM, vastus medialis. *Values in parentheses are 95% confidence interval. † Values in parentheses are 95% limits of agreement.
RESULTS
P
articipants ranged in age from 14 to 17 years (mean ± SD age, 15.2 ± 0.79 years; 95% CI: 14.9, 15.5) and had a mean ± SD body mass index of 21.3 ± 2.2 kg/m2 (95% CI: 20.4, 22.1). Resting and contracted values (mean ± SD with 95% CI), intrarater ICC3,3 with 95% CI, SEM, and MDC95 values are summarized in TABLE 2. The mean change in thickness of the GMd during the hip abduction task was 2.1 mm, whereas the corresponding value for GMn was less than 1 mm (0.4-0.9 mm). The reliability estimates (ICC3,3) for the resting, contracted, and change during contraction of the GMd were 0.98 (95% CI: 0.97, 0.99), 0.98 (95% CI: 0.96, 0.99), and 0.84 (95% CI: 0.71, 0.92), respectively, and of the GMn were 0.98 (95% CI: 0.97, 0.99), 0.94 (95% CI: 0.88, 0.97), and 0.53 (95% CI: 0.21, 0.76), respectively. The reliability estimate for resting VM cross-sectional area was 0.99
(95% CI: 0.99, 0.99). In regard to measurement precision, SEM values for resting and contracted conditions were less than or equal to 1.6 mm for the gluteal muscles and 0.2 cm2 for the VM muscles. The SEM values for change in thickness during contraction were 0.6 mm and 1.6 mm for GMd and 0.7 mm and 1.4 mm for GMn, with the error values for GMn exceeding the observed mean change in thickness. Finally, values for MDC95 ranged from 0.8 to 4.5 mm for the gluteals and 0.4 to 0.5 cm2 for the VM. The mean absolute differences between measurements 1 and 3, as well as 95% limits of agreement, for all parameters and muscle states are summarized in TABLE 2. Difference values for the gluteal muscles ranged from an absolute value of 0.002 mm (right GMn thickness change with contraction) to –0.13 mm (left GMn thickness change with contraction), whereas differences between measurements 1 and 3 for the VM ranged between 0.06 and 0.08 cm2. Bland-Altman plots
did not reveal any significant systematic bias or relationships between the difference in measurements 1 and 3 and their magnitudes. Further, none of the mean differences were greater than the MDC95, suggesting that they did not represent a true difference.
DISCUSSION
T
his report demonstrated a feasible and potentially reliable methodology for measuring the morphology of the GMd, GMn, and VM in an athletic, adolescent female population at rest and, in the case of the hip parameters, during a dynamic task. Although only preliminary, a comparison of all sonographic measures during resting and contracted conditions showed promising within-session intrarater reliability (ICC point estimates of 0.83 or greater, with lower bounds of the 95% CI greater than or equal to 0.70). In contrast, the reliability estimates associated with measurements of absolute
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thickness change of GMd and GMn during the hip abduction task were lower and associated with wide 95% CIs (ICC point estimates of 0.50 or greater, with lower bounds of the 95% CI of 0.19 or greater). This likely reflects the fact that these measures incorporate the measurement error from both the resting and contracted measures from which they are calculated (contracted thickness – resting thickness = change in thickness), and the small absolute change in thickness seen in these muscles with the hip abduction task (less than 1 mm). In general, these findings suggest that sonographic measurements of the lateral hip and knee musculature are feasible; however, additional research is required to establish between-session and interrater reliability. Further, these data can assist future investigators with study design and, in particular, samplesize calculation.
Limitations There are several limitations to this study. First, the sample size was small and all participants were young, active girls. As such, the generalizability of the findings may be questioned. Second, as only intrarater, within-session estimates of relative and absolute reliability were calculated, further work is required to establish the reproducibility of these methods. Finally, although every attempt was made to standardize all aspects of data collection, it is important to acknowledge that the responses being measured, particularly as they relate to change in muscle thickness with contraction, are inherently unstable. However, as the goal of this investigation was to present a clinically amenable methodology, it was expected that some sources of error would not be controlled for. It is likely that the inherent instability of the parameters being measured and the clinical test employed led to this variability. Based on the size and exclusivity of the sample, and the limited conclusions regarding reliability that can be made from within-session, intrarater estimates of reproducibility, further investigation of these methods and their reproducibility is
required in larger and more diverse populations before widespread use.
CONCLUSION
T
his report presents a methodology for investigating the morphology of the GMd, GMn, and VM muscles with sonography that is amenable to the clinical setting. Having demonstrated feasibility and preliminary reliability (within-session measurements of resting and contracted conditions), these methods could be adopted by other investigative teams interested in the morphology of these muscles to facilitate future data synthesis. t ACKNOWLEDGEMENTS: This report was based
on a randomized controlled trial funded by the FIFA Medical Assessment and Research Centre and the Sport Injury Prevention Research Centre at the University of Calgary, and supported by the International Olympic Committee Research Centre Award, the Alberta Children’s Hospital Research Institute for Child and Maternal Health Professorship in Pediatric Rehabilitation (Alberta Children’s Hospital Foundation), and Alberta Team Osteoarthritis (supported by Alberta InnovatesHealth Solutions). The authors would also like to acknowledge the assistance of Maria Romiti, Tracy Blake, Catriona Peggie, and Kim LeeKnight and the participation of youth soccer players.
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4. Ikezoe T, Mori N, Nakamura M, Ichihashi N. Agerelated muscle atrophy in the lower extremities and daily physical activity in elderly women. Arch Gerontol Geriatr. 2011;53:e153-e157. http:// dx.doi.org/10.1016/j.archger.2010.08.003 5. Juul-Kristensen B, Bojsen-Møller F, Holst E, Ekdahl C. Comparison of muscle sizes and moment arms of two rotator cuff muscles measured by ultrasonography and magnetic resonance imaging. Eur J Ultrasound. 2000;11:161-173. http:// dx.doi.org/10.1016/S0929-8266(00)00084-7 6. Kiesel KB, Uhl TL, Underwood FB, Rodd DW, Nitz AJ. Measurement of lumbar multifidus muscle contraction with rehabilitative ultrasound imaging. Man Ther. 2007;12:161-166. http://dx.doi. org/10.1016/j.math.2006.06.011 7. Koppenhaver SL, Hebert JJ, Fritz JM, Parent EC, Teyhen DS, Magel JS. Reliability of rehabilitative ultrasound imaging of the transversus abdominis and lumbar multifidus muscles. Arch Phys Med Rehabil. 2009;90:87-94. http://dx.doi. org/10.1016/j.apmr.2008.06.022 8. Lee JP, Tseng WY, Shau YW, Wang CL, Wang HK, Wang SF. Measurement of segmental cervical multifidus contraction by ultrasonography in asymptomatic adults. Man Ther. 2007;12:286-294. http://dx.doi.org/10.1016/j. math.2006.07.008 9. Lin YF, Lin JJ, Cheng CK, Lin DH, Jan MH. Association between sonographic morphology of vastus medialis obliquus and patellar alignment in patients with patellofemoral pain syndrome. J Orthop Sports Phys Ther. 2008;38:196-202. http://dx.doi.org/10.2519/jospt.2008.2568 10. Mendis MD, Wilson SJ, Stanton W, Hides JA. Validity of real-time ultrasound imaging to measure anterior hip muscle size: a comparison with magnetic resonance imaging. J Orthop Sports Phys Ther. 2010;40:577-581. http://dx.doi. org/10.2519/jospt.2010.3286 11. O’Sullivan C, Meaney J, Boyle G, Gormley J, Stokes M. The validity of Rehabilitative Ultrasound Imaging for measurement of trapezius muscle thickness. Man Ther. 2009;14:572-578. http://dx.doi.org/10.1016/j.math.2008.12.005 12. Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice. 2nd ed. Upper Saddle River, NJ: Prentice Hall Health; 2000. 13. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86:420-428. 14. Steffen K, Meeuwisse WH, Romiti M, et al. Evaluation of how different implementation strategies of an injury prevention programme (FIFA 11+) impact team adherence and injury risk in Canadian female youth football players: a cluster-randomised trial. Br J Sports Med. 2013;47:480-487. http://dx.doi.org/10.1136/bjsports-2012-091887 15. Terwee CB, Bot SD, de Boer MR, et al. Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol. 2007;60:34-42. http://dx.doi. org/10.1016/j.jclinepi.2006.03.012 16. Wall-Scheffler CM, Chumanov E, Steudel-
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[ Numbers K, Heiderscheit B. Electromyography activity across gait and incline: the impact of muscular activity on human morphology. Am J Phys Anthropol. 2010;143:601-611. http://dx.doi. org/10.1002/ajpa.21356 17. W hittaker JL, Teyhen DS, Elliott JM, et al. Rehabilitative ultrasound imaging: understanding the technology and its applications. J Orthop Sports Phys Ther. 2007;37:434-449. http://dx.doi. org/10.2519/jospt.2007.2350 18. W hittaker JL, Warner MB, Stokes M. Comparison
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of the sonographic features of the abdominal wall muscles and connective tissues in individuals with and without lumbopelvic pain. J Orthop Sports Phys Ther. 2013;43:11-19. http://dx.doi. org/10.2519/jospt.2013.4450 19. Whittaker JL, Warner MB, Stokes MJ. Induced transducer orientation during ultrasound imaging: effects on abdominal muscle thickness and bladder position. Ultrasound Med Biol. 2009;35:1803-1811. http://dx.doi.org/10.1016/j. ultrasmedbio.2009.05.018
20. W hittaker JL, Warner MB, Stokes MJ. Ultrasound imaging transducer motion during clinical maneuvers: respiration, active straight leg raise test and abdominal drawing in. Ultrasound Med Biol. 2010;36:1288-1297. http://dx.doi.org/10.1016/j. ultrasmedbio.2010.04.020
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JACKIE L. WHITTAKER, PT, PhD, FCAMPT1,2 • CAROLYN A. EMERY, PT, PhD1,2
Sonographic Measures of the Gluteus Medius, Gluteus Minimus, and Vastus Medialis Muscles
T
he clinical use of ultrasound imaging (USI) by physiotherapists to measure muscle morphology during static and dynamic conditions falls within the scope of rehabilitative ultrasound imaging.17 Specifically, rehabilitative USI refers to the USI procedures used by physiotherapists to evaluate the morphology and behavior of muscle and its related soft tissues, to provide biofeedback about muscle behavior during restoration of function, TTSTUDY DESIGN: Intrarater, repeated-measures, within-session reliability study.
TTOBJECTIVE: To describe a standardized
method and preliminary reliability estimates for sonographic measures of resting and contracted gluteus medius (GMd), gluteus minimus (GMn), and resting vastus medialis (VM) muscles.
TTBACKGROUND: Sonography has been used to
assess the morphology of a diversity of muscles in relation to a variety of musculoskeletal dysfunctions. Although the GMd, GMn, and VM muscles are associated with dysfunctions such as patellofemoral pain and osteoarthritis, there is a paucity of information regarding protocols for sonographic measurements of these muscles.
TTMETHODS: A standardized method was devel-
contracted, and change during contraction (intraclass correlation coefficient model 3,3 [ICC3,3]) of the GMd were 0.98 (95% confidence interval [CI]: 0.97, 0.99), 0.98 (95% CI: 0.96, 0.99), and 0.84 (95% CI: 0.71, 0.92), respectively, and of the GMn were 0.98 (95% CI: 0.97, 0.99), 0.94 (95% CI: 0.88, 0.97), and 0.53 (95% CI: 0.21, 0.76), respectively. Reliability (ICC3,3) for resting VM cross-sectional area was 0.99 (95% CI: 0.99, 0.99). Standard error of measurement for GMd, GMn, and VM varied between 0.5 and 1.6 mm, 0.3 and 1.4 mm, and 0.4 cm2, respectively, and 95% minimal detectable change ranged from 0.8 to 4.5 mm for the gluteals and 0.4 to 0.5 cm2 for the VM.
TTCONCLUSION: Reliable sonographic measure-
oped and used to gather sonographic measures of resting and contracted (sidelying hip abduction task) GMd and GMn thickness and resting VM cross-sectional area during 1 measurement session in 29 female soccer players 14 to 17 years of age.
ments of the lateral hip and knee musculature at rest and during contraction are feasible. Further investigation is required to establish the generalizability and reproducibility of the protocols presented in this report. J Orthop Sports Phys Ther 2014;44(8):627-632. Epub 16 July 2014. doi:10.2519/jospt.2014.5315
ultrasound imaging measurements of resting,
reliability, ultrasonography
TTRESULTS: Intrarater reliability values for
TTKEY WORDS: gluteal muscles, quadriceps,
and to carry out research aimed at informing clinical practice.17 To date, USI has been used to investigate a variety of muscles and to address a diversity of research questions. Sonography has been shown to be a valid method (primarily in healthy adults under resting conditions) to measure the morphology of the trunk (abdominal and lumbar multifidus),2,3 as well as a range of other muscles,5,8,10,11 through comparison to magnetic resonance imaging. Further, there are numerous investigations that have assessed the reproducibility of sonographic measures of the trunk muscles.1,6,7,18 In general, these investigations report moderate to excellent reliability for repeated resting measures, and poor to good reliability for measures of morphological change during a task in both healthy and patient samples. A large number of investigations consider sonographic measures of the morphology of the trunk muscles; however, there is a paucity of information regarding other muscles that may be amenable to USI. Of particular interest, and the topic of this report, are the muscles of the lateral hip (gluteus medius [GMd] and gluteus minimus [GMn]) and knee (vastus medialis [VM]), which play an important role
Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada. 2The Alberta Children’s Hospital Research Institute for Child and Maternal Health, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada. Ethics approval was granted from the Conjoint Health Research Ethics Board at the University of Calgary, Calgary, Alberta, Canada. The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial interest in the subject matter or materials discussed in the article. Address correspondence to Dr Jackie L. Whittaker, Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, 2500 University Drive NW, Calgary, Alberta, Canada T2N 1N4. E-mail: [email protected] t Copyright ©2014 Journal of Orthopaedic & Sports Physical Therapy® 1
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[
brief report
] for investigating the morphology of the GMd, GMn, and VM that is amenable to clinical research and practice, and, if adopted by other investigative teams, will facilitate the synthesis of data from future investigations. A secondary purpose was to assess the feasibility of this methodology by presenting preliminary estimates of within-session intrarater reliability.
METHODS Participants
P FIGURE 1. (A) Lateral hip muscle imaging site (gray oval). (B) GMd and GMn thickness measurements (dashed circle represents the superior lip of the acetabulum). (C) Sidelying hip abduction task. Abbreviations: GMd, gluteus medius; GMn, gluteus minimus.
articipants included 29 healthy, consenting female adolescent (aged 14 to 17 years) soccer players recruited from 2 teams (n = 36) that participated in a randomized controlled trial investigating the implementation of a neuromuscular injury-prevention program across 29 teams (n = 226) during the 2011 season. Information regarding participant recruitment and eligibility for the implementation trial is detailed elsewhere. 14 Ethics approval was granted from the Conjoint Health Research Ethics Board at the University of Calgary, Calgary, Alberta, Canada.
USI Protocol
FIGURE 2. (A) VM imaging site (gray oval). (B) VM cross-sectional area measurement. Abbreviation: VM, vastus medialis.
in the control of the hip, knee, and patellofemoral joints during gait, running, and sporting activities.16 Although there has been preliminary work published with respect to sonographic assessment of these muscles, the methods presented are difficult to replicate in clinical research due to insufficient reporting4 and the need for advanced imaging techniques and analyses. 9 If methods amenable to clinical research
could be established, they would enable the assessment and comparison of the morphology of these muscles with respect to a variety of populations (eg, healthy, sporting, and injured), dysfunctions (patellofemoral pain, osteoarthritis, etc), and interventions (eg, strengthening, balance, and injuryprevention programs). Consequently, the primary purpose of this report was to present a sonographic methodology
All sonographic images were collected by a single experienced sonographic operator (J.W.), an experienced physiotherapist with 12 years of USI experience. A USI system (MyLab 25; Esaote North America, Inc, Indianapolis, IN) with a 5.0-MHz curvilinear transducer (40-mm footprint; lateral and axial resolution of 1.0 and 0.93 mm, respectively) was used to collect bilateral anonymized resting B-mode ultrasound images of the GMd and GMn ( FIGURE 1 ) from a sidelying position, and of the VM ( FIGURE 2) from a supine position. Additionally, images of the GMd and GMn during muscular contraction were obtained during a standardized sidelying hip abduction task (20-mmHg reduction in a pressure biofeedback cuff ). Precise descriptions
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Summary of Techniques for Ultrasound Imaging of the Gluteus Medius, Gluteus Minimus, and Vastus Medialis
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TABLE 1 Muscle
Participant Position
Gluteus medius and minimus
Sidelying with the test leg up. The test-leg hip is in Place the transducer on the lateral aspect of the hip To standardize across participants, inflate the PBU so neutral flexion/extension, neutral rotation, and on the lower half of a coronal line located between that the starting position is 20° of hip adduction 20° of adduction (inclinometer confirmed). The the top of the greater trochanter and a point 25% from the horizontal. Instruct participants to gently test-leg knee is in full extension, with a PBU placed of the distance between the ASIS and PSIS. Adjust lift their leg toward the ceiling, keeping their toes under the ankle and foot. the cranial-caudal position of the transducer until pointing forward, until the reading on the PBU the superior lip of the acetabulum (dashed circle decreases by 20 mmHg. in FIGURE 1) is one third of the distance from the right border of the image.
Transducer Location
Contraction Technique
Vastus medialis
Supine with the hips of both legs in neutral flexion/ extension, rotation, abduction/adduction, and the knee in full extension.
Place the transducer in a transverse orientation just superior to the patella. Slide the transducer down until it butts up against the top of the patella, then move it medially (with care given not to adjust the cranial-caudal position and to maintain a tangential orientation to the surface of the knee) until entire CSA of the muscle is within the field of view (FIGURE 2).
NA
Abbreviations: ASIS, anterior superior iliac spine; CSA, cross-sectional area; NA, not applicable; PBU, pressure biofeedback unit (Chattanooga Stabilizer; DJO Global Inc, Vista, CA); PSIS, posterior superior iliac spine.
of participant position, imaging site, and hip abduction task are provided in TABLE 1. These procedures were chosen after review of cadaveric specimens, thorough review of previous imaging studies,4,9 and extensive pilot testing in both clinical and laboratory settings. Three images were acquired at each imaging site for both resting and contracted (GMd and GMn) conditions (ie, 3 trials). The transducer was removed and repositioned between trials, which provided the participant with a 10- to 20-second rest. To avoid an order or fatigue effect, the order in which the muscles and maneuvers were imaged was randomized. Testing of all participants occurred over a 3-day period. Images were measured offline using custom-written measurement codes in MATLAB Version 7.1 software (The MathWorks, Inc, Natick, MA). The measurement codes had 2 unique features relevant to this investigation. First, they prompted the operator to plot a reference line, which ensured that measurements could be made at the same location in the resting and contracted images. Second, the codes concealed measurements from the op-
erator by directly exporting them into an Excel (Microsoft Corporation, Redmond, WA) worksheet. This ensured blinding of the examiner throughout the measurement process. Measurements of GMd and GMn thickness (FIGURE 1) and VM (FIGURE 2) cross-sectional area were made and the mean of the 3 repetitions used for analyses. All measurements excluded the perimuscular connective tissue (thickness was defined as the distance between the inside edges of each muscle border), as this tissue has been shown to differ in thickness between case and healthy populations. 18 Information from 2 previous studies regarding the influence of transducer motion on measurements of muscle thickness, 19 as well as the pattern of transducer motion that occurs during leg-lifting maneuvers, 20 was taken into consideration during data collection. Namely, the operator made every attempt to keep the angular and inward/ outward motion of the transducer to a minimum, and paid specific attention to countering transducer motion at the point of initiation of the leg lift during the hip abduction task.
Data Analysis Statistical analyses were performed using the statistical software Stata Version 12.1 (StataCorp LP, College Station, TX). The mean and 95% confidence interval (CI) values for resting GMd and GMn thickness and VM cross-sectional area, as well as for the contracted GMd and GMn during hip abduction, were calculated. Intraclass correlation coefficients (ICCs) with 95% CIs were calculated to assess within-session intrarater reliability (model 3,3).13 To assess measurement precision, standard error of measurement (SEM) was calculated as SD × √1 – ICC.12 The 95% minimal detectable change (MDC95), which represents the minimal change in thickness that must occur to be 95% confident that a true change has occurred, was calculated as 1.96 × SEM × √2.15 To assess absolute agreement, the mean difference between measurements 1 and 3, as well as the 95% limits of agreement (mean difference between measurements ±2 SD), were calculated. Bland-Altman plots were used to look for any systematic bias, outliers, and relationships between the difference in values between images and their magnitudes.
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[
]
Descriptive Data and Within-Day Intrarater ICC, SEM, MDC, Bias, and Limits-of-Agreement Values
TABLE 2 Mean ± SD*
ICC3,3*
SEM
MDC95
Difference (Measures 1 and 3)†
Rest
20.5 ± 3.9 (19.0, 22.0)
0.98 (0.97, 0.99)
0.5
1.4
0.05 (–0.23, 0.32)
Contracted
22.6 ± 3.8 (21.1, 24.0)
0.98 (0.96, 0.99)
0.6
1.5
0.02 (–0.24, 0.29)
Change
2.1 ± 1.5 (1.5, 2.7)
0.84 (0.71, 0.92)
0.6
1.6
–0.03 (–0.34, 0.29)
Rest
20.2 ± 4.0 (18.7, 21.7)
0.96 (0.92, 0.98)
0.8
2.3
0.05 (–0.68, 0.77)
Contracted
22.5 ± 4.0 (20.9, 24.0)
0.91 (0.83, 0.95)
1.2
3.4
0.03 (–0.19, 0.25)
Change
2.1 ± 2.4 (1.1, 3.0)
0.54 (0.22, 0.77)
1.6
4.5
–0.09 (–1.02, 0.85)
Rest
12.2 ± 2.2 (11.3, 13.0)
0.98 (0.97, 0.99)
0.3
0.8
–0.03 (–0.19, 0.14)
Contracted
12.6 ± 2.1 (11.8, 13.4)
0.94 (0.88, 0.97)
0.5
1.5
–0.03 (–0.33, 0.27)
Change
0.4 ± 1.0 (0.07, 0.08)
0.53 (0.21, 0.76)
0.7
1.9
0.01 (–0.37, 0.38)
Rest
11.9 ± 2.4 (11.0, 12.8)
0.96 (0.92, 0.98)
0.5
1.4
–0.02 (–0.30, 0.27)
Contracted
12.8 ± 2.5 (11.8, 13.8)
0.83 (0.70, 0.92)
1.0
2.8
–0.05 (–0.34, 0.24)
Change
0.9 ± 2.0 (0.1, 1.6)
0.50 (0.19, 0.75)
1.4
3.9
–0.13 (–0.97, 0.70)
VM right at rest, cm2
12.7 ± 2.9 (11.6, 13.8)
0.99 (0.99, 0.99)
0.2
0.4
0.08 (–0.69, 0.86)
VM left at rest, cm2
12.5 ± 2.5 (11.6, 13.5)
0.99 (0.99, 0.99)
0.2
0.5
0.06 (–0.68, 0.81)
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brief report
GMd right, mm
GMd left, mm
GMn right, mm
GMn left, mm
Abbreviations: GMd, gluteus medius; GMn, gluteus minimus; ICC, intraclass correlation coefficient; MDC, minimal detectable change; SEM, standard error of measurement; VM, vastus medialis. *Values in parentheses are 95% confidence interval. † Values in parentheses are 95% limits of agreement.
RESULTS
P
articipants ranged in age from 14 to 17 years (mean ± SD age, 15.2 ± 0.79 years; 95% CI: 14.9, 15.5) and had a mean ± SD body mass index of 21.3 ± 2.2 kg/m2 (95% CI: 20.4, 22.1). Resting and contracted values (mean ± SD with 95% CI), intrarater ICC3,3 with 95% CI, SEM, and MDC95 values are summarized in TABLE 2. The mean change in thickness of the GMd during the hip abduction task was 2.1 mm, whereas the corresponding value for GMn was less than 1 mm (0.4-0.9 mm). The reliability estimates (ICC3,3) for the resting, contracted, and change during contraction of the GMd were 0.98 (95% CI: 0.97, 0.99), 0.98 (95% CI: 0.96, 0.99), and 0.84 (95% CI: 0.71, 0.92), respectively, and of the GMn were 0.98 (95% CI: 0.97, 0.99), 0.94 (95% CI: 0.88, 0.97), and 0.53 (95% CI: 0.21, 0.76), respectively. The reliability estimate for resting VM cross-sectional area was 0.99
(95% CI: 0.99, 0.99). In regard to measurement precision, SEM values for resting and contracted conditions were less than or equal to 1.6 mm for the gluteal muscles and 0.2 cm2 for the VM muscles. The SEM values for change in thickness during contraction were 0.6 mm and 1.6 mm for GMd and 0.7 mm and 1.4 mm for GMn, with the error values for GMn exceeding the observed mean change in thickness. Finally, values for MDC95 ranged from 0.8 to 4.5 mm for the gluteals and 0.4 to 0.5 cm2 for the VM. The mean absolute differences between measurements 1 and 3, as well as 95% limits of agreement, for all parameters and muscle states are summarized in TABLE 2. Difference values for the gluteal muscles ranged from an absolute value of 0.002 mm (right GMn thickness change with contraction) to –0.13 mm (left GMn thickness change with contraction), whereas differences between measurements 1 and 3 for the VM ranged between 0.06 and 0.08 cm2. Bland-Altman plots
did not reveal any significant systematic bias or relationships between the difference in measurements 1 and 3 and their magnitudes. Further, none of the mean differences were greater than the MDC95, suggesting that they did not represent a true difference.
DISCUSSION
T
his report demonstrated a feasible and potentially reliable methodology for measuring the morphology of the GMd, GMn, and VM in an athletic, adolescent female population at rest and, in the case of the hip parameters, during a dynamic task. Although only preliminary, a comparison of all sonographic measures during resting and contracted conditions showed promising within-session intrarater reliability (ICC point estimates of 0.83 or greater, with lower bounds of the 95% CI greater than or equal to 0.70). In contrast, the reliability estimates associated with measurements of absolute
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thickness change of GMd and GMn during the hip abduction task were lower and associated with wide 95% CIs (ICC point estimates of 0.50 or greater, with lower bounds of the 95% CI of 0.19 or greater). This likely reflects the fact that these measures incorporate the measurement error from both the resting and contracted measures from which they are calculated (contracted thickness – resting thickness = change in thickness), and the small absolute change in thickness seen in these muscles with the hip abduction task (less than 1 mm). In general, these findings suggest that sonographic measurements of the lateral hip and knee musculature are feasible; however, additional research is required to establish between-session and interrater reliability. Further, these data can assist future investigators with study design and, in particular, samplesize calculation.
Limitations There are several limitations to this study. First, the sample size was small and all participants were young, active girls. As such, the generalizability of the findings may be questioned. Second, as only intrarater, within-session estimates of relative and absolute reliability were calculated, further work is required to establish the reproducibility of these methods. Finally, although every attempt was made to standardize all aspects of data collection, it is important to acknowledge that the responses being measured, particularly as they relate to change in muscle thickness with contraction, are inherently unstable. However, as the goal of this investigation was to present a clinically amenable methodology, it was expected that some sources of error would not be controlled for. It is likely that the inherent instability of the parameters being measured and the clinical test employed led to this variability. Based on the size and exclusivity of the sample, and the limited conclusions regarding reliability that can be made from within-session, intrarater estimates of reproducibility, further investigation of these methods and their reproducibility is
required in larger and more diverse populations before widespread use.
CONCLUSION
T
his report presents a methodology for investigating the morphology of the GMd, GMn, and VM muscles with sonography that is amenable to the clinical setting. Having demonstrated feasibility and preliminary reliability (within-session measurements of resting and contracted conditions), these methods could be adopted by other investigative teams interested in the morphology of these muscles to facilitate future data synthesis. t ACKNOWLEDGEMENTS: This report was based
on a randomized controlled trial funded by the FIFA Medical Assessment and Research Centre and the Sport Injury Prevention Research Centre at the University of Calgary, and supported by the International Olympic Committee Research Centre Award, the Alberta Children’s Hospital Research Institute for Child and Maternal Health Professorship in Pediatric Rehabilitation (Alberta Children’s Hospital Foundation), and Alberta Team Osteoarthritis (supported by Alberta InnovatesHealth Solutions). The authors would also like to acknowledge the assistance of Maria Romiti, Tracy Blake, Catriona Peggie, and Kim LeeKnight and the participation of youth soccer players.
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[ Numbers K, Heiderscheit B. Electromyography activity across gait and incline: the impact of muscular activity on human morphology. Am J Phys Anthropol. 2010;143:601-611. http://dx.doi. org/10.1002/ajpa.21356 17. W hittaker JL, Teyhen DS, Elliott JM, et al. Rehabilitative ultrasound imaging: understanding the technology and its applications. J Orthop Sports Phys Ther. 2007;37:434-449. http://dx.doi. org/10.2519/jospt.2007.2350 18. W hittaker JL, Warner MB, Stokes M. Comparison
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