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Ultrasound imaging is a valid method of measuring the cross-sectional area of the quadratus femoris muscle.

Classical ballet dancers are required to move their hip joints through extreme ranges of motion while maintaining external rotation, or "turnout." This unique action requires great technical skill, strength, flexibility, stability, and coordination in order to execute the manoeuvre effectively and safely. Quadratus femoris (QF), piriformis, obturator internus, obturator externus, and superior and inferior gemelli are the deep external rotator muscles of the hip joint (Fig). (1) With the exception of piriformis, these short external rotators have a near-horizontal line of force that can produce an external rotational torque and provide compression, thus promoting stability in the hip joint. (2-4) Studies have demonstrated that QF has the most effective external rotator moment arm throughout 0[degrees] to 90[degrees] of hip flexion. (2,3) QF also assists hip adduction and extension. (2-4) Although unproven at this time, it is possible that QF could apply an inferomedial force to the femoral head in the extreme ranges of hip flexion or abduction, such as grand battement a la seconde, thus providing dynamic stability to the joint. Therefore, this muscle may be of particular importance to the classical ballet dancer for achieving optimal execution of hip motion while minimizing the risk of injury.

There is growing recognition of QF muscle pathologies, such as muscle tear, oedema, and fatty infiltration. (5-19) Although there is limited understanding of the function of this muscle, (2-4) atrophy and deterioration in quality of QF has been associated with chronic hip pain, (8,10,13) aging, (5) and prolonged unloading, as during bed rest. (20) Therapeutic exercises that specifically target QF could prevent injury or ongoing dysfunction of the hip joint and promote injury resolution. As QF is small, deep, and has several agonists, conventional strength testing is too global to measure QF function accurately. A specific method of measuring QF muscle size could allow for objective measurements of atrophy and evaluation of the effectiveness of muscle strengthening exercises.

Computed tomography (CT) and magnetic resonance imaging (MRI) provide high resolution images for objective measurement of muscle size (21) and have been used to measure the size of QF. (5,10,20) CT delivers relatively large doses of ionizing radiation; therefore, MRI is the "gold standard" for measuring muscle size, as it provides excellent osseous and soft-tissue detail without the negative effects of radiation. (22-24) Unfortunately, MRI is expensive, contraindicated in people with pacemakers and metal implants, and not a tool that can be readily used in a clinical setting. Ultrasound imaging (USI) is non-ionizing, affordable, portable, and an accessible alternative for measurements of muscle morphology, although it is operator dependent. (22,25,26) This modality can perform serial measures of muscle size in a clinical or research setting, (27,28) and systematic reviews have concluded that it is a valid and reliable tool for accurately measuring skeletal muscle size in healthy individuals. (29-31) USI measurements of the size of anterior hip muscles (32-34) and the adductor group (35) have been found to be valid and reliable. To our knowledge, the use of USI to measure the size of QF has not been reported in the literature.

[FIGURE 2 OPMITTED]

The primary aim of this study was to establish the criterion validity of USI against the "gold standard," MRI, for measuring QF muscle cross-sectional area (CSA), and the secondary aim was to investigate the intra-rater reliability of USI.

Methods

Eleven current or retired professional ballet dancers (six women, five men; mean age: 30.27 [+ or -] 12.15 years) volunteered for USI of their QF muscle within 1 week of an MRI scan. All participants were employed in a national professional ballet company as dancers or ballet staff. They were all enrolled in a larger MRI study investigating hip joint pathology in dancers. All were actively teaching or participating in ballet classes and rehearsals. Each participant's height, weight, BMI, age, and current and past history of hip pain were recorded (Table 1). They provided written informed consent, and ethics approval was granted by the Monash University Human Research Ethics Committee.

Volunteers were excluded if there were any contraindications to MRI or USI, such as pacemaker, metal implant, possible pregnancy, or claustrophobia. Other exclusion criteria were a history of Perthes disease, slipped capital femoral epiphysis, hip trauma or serious injury, hip surgery, hip tumor, hip fracture, known inflammatory joint disease, systemic, metabolic, or neurological disorders, and pain that could preclude lying comfortably in the required position for the MRI or USI.

Figure 3 Formula for calculating the
volume of quadratus femoris (Ai, area of
the muscle in the ith slice; Di-1,i, distance
between the ith and (i - 1)th slices; N,
number of slices).

Volume = [N.summation over (i=2)] [(Ai) + (Ai - 1)/2] x Di - 1, i


MRI Protocol

Participants were scanned while supine, with padding used to maintain neutral spine and hip alignment. All studies were performed with a 3Tesla Siemens Trio scanner (Siemens, Erlangen, Germany) using an 8-channel phased array body coil. Left and right hips were imaged separately. The following sequence was used for QF CSA measurement: true axial proton density weighted (PD) fast pin-echo (fs) sequences (repetition time = 3590 ms, echo time = 30 ms, slice thickness = 4 mm/slice gap = 1.5 mm, field of view = 200 mm, resolution = 288 x 384, number of averages = 1). Transverse images of the whole QF were acquired from the greatest circumference of the head of femur to the inferior edge of the lesser QF trochanter. Measurement of left and right QF muscle CSA was performed on electronic imaging software, InteleViewer (Intelerad, Montreal, Canada), by manually tracing around the muscle borders of the four most cephalad slices that were inferior to obturator internus and inferior gemellus. These four slices were found to have the most distinct muscle borders and were clear despite variations in anatomy and size of the participants. The most proximal MRI slice was used for comparison with the USI image (Fig. 2).

Partial volume was calculated by interpolating the four QF CSAs in order to determine whether the most proximal image CSA was representative of the whole muscle. Partial volume of QF was calculated using the "Cavalieri Principle" (36) (Fig. 3).

USI Protocol

Participants were positioned prone with the hip joint in the same position as in the MRI. Adhesive tape was applied to the thigh along the shaft of the femur in standing and then aligned with the horizontal plane to ensure there was no hip flexion once positioned in prone. A portable brightness mode ultrasound system (VIAMO, Toshiba SSA 640A) fitted with either a 5-MHz or 4-MHz curvilinear transducer was used to image QF of each participant. (37) The transducer was placed along a transverse line drawn 6 cm inferior to the superior edge of the greater trochanter (Fig. 4).

The transducer placement was adjusted until the most proximal image of QF with distinct borders was located inferior to obturator internus and inferior gemellus. The medium-sized curvilinear probe was required to ensure that bony landmarks, ischial tuberosity and the posterior border of the greater trochanter of the femur, were well defined in the image. Care was taken to align the plane of images taken with USI as closely as possible to the axial plane of the MRI images. Three still images were captured with the participant at rest on both left and right sides. Six participants repeated the ultrasound procedure on both left and right hips after a mean of 6 days (SD [+ or -] 6.72) for intra-rater reliability testing.

A musculoskeletal radiologist with 22 years of MRI experience oversaw the MRI procedure. The chief investigator, a physiotherapist with 8 years of experience in the use of USI, performed all the USI procedures and MRI and USI measurements. The stored ultrasound images were coded differently from the stored MRI images to ensure that the assessor was blinded to the identity and results of all imaging measurements. The CSA of QF was calculated by manually tracing inside the fascial border of the QF (Fig. 5). The mean CSA of three images at rest was used for analysis. (30)

Statistical Analysis

All statistical analyses were performed using the SPSS, Version 21 (SPSS Inc., Chicago, IL, USA). The mean CSA and SD of QF measured with USI and MRI were recorded. There was no significant difference in the USI CSA between left and right sides (t = 0.77, p = 0.45), so the data were pooled and Pearson's correlation coefficient and the Student's paired t-test were used to examine the correlation and difference between the CSA of QF with USI and MRI. To evaluate the absolute agreement and consistency of measures from both modes of imaging, ICCs of reliability and two-sided 95% CIs were calculated using a two-way mix for absolute agreement and consistency. A Bland-Altman plot (38) was used to demonstrate the mean difference of the USI and MRI estimates of CSA, whereby lower values represent greater agreement between imaging modalities. Pearson's correlation coefficient was used to determine the relationship between the most proximal MRI image and a partial volume. ICC (2-way mixed, absolute agreement) was used to calculate the intra-rater reliability of using USI to measure the CSA of QF. The standard error of measurement (SEM) and the minimal detectable change at a 95% CI (MDC95), which is the measurement of change necessary to exceed the measurement error of two repeated measures, (39) was calculated using the formulas MDC95 = SEM x 1.96 x [square root of ((2.))] (SD = pooled SD of test and re-test; SEM = SD [square root of ((1-ICC))). The significance level was set at p < 0.05.

Results

Of the three participants who reported hip pain, two were experiencing current anterior pain, and three had a past history of anterior hip pain (Table 1). One participant had an absent QF on the left side on both MRI and USI, and the MRI demonstrated that the obturator externus had aberrant anatomy and had filled the QF space. The data for this hip were excluded from analysis. In two women, it was necessary to use a 4 MHz transducer to increase the depth of penetration in an effort to optimize the image.

CSA with MRI (4.8 [cm.sup.2] [+ or -] 1.54 [cm.sup.2]) was significantly greater than USI CSA (4.29 [cm.sup.2] [+ or -] 1.56 [cm.sup.2]: t = 5.82; p < 0.001). However, Pearson's correlation coefficient showed that the measurements were highly correlated (r = 0.96, p < 0.001). ICC (2-way mixed, absolute agreement) also showed high correlation, demonstrating agreement of measures (ICC = 0.90; 95% CI: 0.20 to 0.97), and ICC (2-way mixed, consistency) showed high correlation, establishing consistency of measures (ICC = 0.96; 95% CI: 0.90 to 0.98). The Bland-Altman plot (Fig. 6) indicated that the mean difference between the USI and MRI estimates of muscle CSA was 0.41 [cm.sup.2], which represents 9% of the mean CSA of QF. The limits of agreement were [+ or -] 0.51 [cm.sup.2] (1.41 to -0.59 [cm.sup.2]) for the CSA estimates.

The CSA of the most proximal image on MRI was highly correlated with the partial volume of QF (r = 0.93, p < 0.001). Intra-rater reliability of measuring QF with USI was excellent between two trials (ICC = 0.98; 95% CI: 0.96 to 0.99). The SEM was 0.14 [cm.sup.2], and the MDC95 was 0.38 [cm.sup.2], which represents 3.5 % and 9.5% of the mean QF muscle CSA, respectively. When the post hoc power was calculated, the effect size was 1.1, and the power was 0.93.

Discussion

This study demonstrated that USI can be an efficient and clinically useful tool in measuring the size of QF. The CSA measurements were highly correlated, and the intra-rater reliability of measuring QF with USI was excellent between two trials. The most proximal CSA on MRI was highly correlated with the partial volume of QF and can be used to estimate the volume of this muscle. Therefore, the use of USI to measure changes in axial plane CSA of the QF is valid and reliable.

In the present study, the CSA of QF with USI was significantly smaller than with MRI. Earlier studies have also reported that USI underestimated muscle size when compared with MRI. (26,27,40-45) Our results are comparable to those of Ahtiainen and coworkers, (27) who reported a mean difference of 10% between modalities for measuring the CSA of vastus lateralis. Manual tracing of QF on images is a potential source of error, and may account for the under-estimation of muscle size with USI when compared to MRI. This study traced the inner fascial border around QF. (46) The peri-muscular connective tissue (PMCT) bordering muscle appears thicker and easier to visualize with USI than with MRI. (42,47,48) As these tissues were excluded in the region of interest on the USI, it is feasible that more tissue was included in the MRI CSA, resulting in larger MRI CSA measures. (26,47,48) Previous studies have used USI to quantitatively evaluate PMCT of the abdominal wall (46) and lumbar multifidus. (49) They revealed a significant increase in the thickness of PMCT in participants with chronic lumbopelvic (46) or lower back pain (49) after adjusting for BMI. These findings highlight the importance of differentiating between muscle and PMCT when measuring muscle size. Furthermore, future investigation that measures the thickness of PMCT around QF with USI could determine if thicker PMCT is associated with hip pain or dysfunction.

Another possible explanation for the smaller CSA of QF when measured with USI is the orientation of the transducer during image capture. Previous studies have suggested that a change in transducer orientation of 20[degrees] can increase the muscle CSA by 6.5%, and the error can grow with increasing depth of the muscle. (23,50) In our study, the MRI image was captured in an axial plane in supine, while the USI was performed in prone. A strict protocol was implemented for both MRI and USI to ensure the plane was matched between modalities. It is possible, however, that the USI transducer orientation did not mimic the plane of the MRI exactly in a cephalad-caudad direction. As the MRI CSAs were larger than the USI CSAs, it may have been the MRI that did not capture images in a true axial plane.

Excessive pressure of the transducer causing reduction in the USI measures has been noted in previous research, with the effect on thickness being greater than CSA. (50) In our study, a significant amount of pressure was required, due to the depth of penetration needed to image QF with adequate resolution. The QF sits deep to gluteus maximus in a gutter between the bony attachments and is somewhat protected from superficial compression. The gluteus maximus was compressed by transducer pressure in USI and by lying during MRI. Future research could image the QF in hip flexion, as less pressure would be required due to a reduced thickness of gluteus maximus underneath the transducer. It is recommended that CSA rather than linear measurements of QF be calculated to reduce the effect of transducer pressure on reliability.

Despite the systematic difference in size between USI and MRI estimates of CSA, Pearson's correlation coefficient demonstrated that measures were highly correlated. These results are corroborated by previous studies measuring CSA of skeletal muscle, with values ranging from r = 0.78 to 0.96. (51,52) A high consistency and agreement between measures was demonstrated in the present study. However, the wide CI for absolute agreement highlights the systematic bias in the measures. Previous studies that have compared CSA measures between USI and MRI have reported ICCs ranging from 0.81 to 0.999. (27,32,53) Mendis and colleagues (32) was the only study to report CIs, and these ranged from 0.39 to 0.95 to 0.61 to 0.97 for measuring the CSA of anterior hip muscles. The wide CIs reported in the Mendis study and our study indicate variability of measures but could have been narrowed with a larger sample size.

Intra-rater reliability of measuring the size of QF with USI was excellent. The SEM of 0.14 [cm.sup.2] (3.5%) in our study was low, and the minimal detectable change (95% CI) was 0.38 [cm.sup.2] (9.5%). Consequently, changes in size would have to be greater than 9.5% of the QF muscle CSA to be sure that real change had occurred. Comparable reliability has been reported for measuring CSA of other hip muscles. (32) However, the previous studies reported higher SEM values (0.2 to 1.1 [cm.sup.2]). The lower SEM in the present study could have been due to using the mean of three measures. (30) Research testing inter-rater reliability of USI of QF is also essential.

USI measures from a single site have been used to predict muscle volume. (54) To ensure repeatability, we chose to use the most cephalad CSA of QF that could be imaged with USI. The axial image of QF on MRI that matched this ultrasound image was found to be highly correlated with the partial volume. Therefore, the use of this single CSA as a representation of QF size is valid. Further research that investigates the reliability of measuring a single CSA of QF with USI in clinical populations is warranted.

Muscle strength is related to the muscle's CSA and can change over time with either disuse or strengthening. (25,47) The CSA of QF measured with MRI has been shown to be responsive to change in size. Quadratus femoris atrophied significantly faster than the other external rotator muscles (p [less than or equal to] 0.0001 for all) and demonstrated the greatest loss of muscle volume throughout 60 days of bed rest. (20) Furthermore, as people age beyond 50, QF atrophy and fatty infiltration has been shown to increase to a greater degree compared with other hip muscles. (5) Fatty infiltration of QF has also been associated with chronic injury. (10,13) Recent studies have identified a type of ischiofemoral impingement where QF is reportedly compressed between the ischium-hamstring tendon origin and the lesser trochanter. (6-15) In an MRI study investigating ischiofemoral impingement, QF muscle volume was significantly lower, and QF muscle fatty infiltration was significantly higher in people with QF oedema and hip pain (p < 0.001). (10) Quadratus femoris appears to have a unique response to injury, aging, and unloading, and may not recover automatically following injury resolution. Therefore, further research is required to determine whether the single axial CSA on MRI and the USI CSA of QF is sensitive to small changes in size with atrophy or hypertrophy.

The main limitation of using USI to measure muscle size is that it cannot accurately measure fat or connective tissue infiltrate; therefore, the size of the muscle may be over-estimated. (22,48) As a result of these intramuscular changes, images of pathological or deconditioned muscle can be more difficult to measure accurately due to hyperechogenicity of the muscle, poorer bone edge definition, and loss of clarity of the fascial borders. (47,48,55) The participants investigated in the present study were professional or retired ballet dancers who were lean, and the echogenic fascial borders were easily identified with USI. (42,47,48) Therefore, the results of this study may not be generalized to populations with pain, pathology, or the elderly without further research.

It has been suggested that ballet is associated with hip OA due to the repetitive, extreme range of hip movement that is required to succeed at an elite level. (56) Anecdotes suggest that ballet dancers are at a high risk of developing hip joint degenerative changes, such as labral injury and ligamentum teres lesions. (57,58) Studies investigating hip OA in dancers that have been based on questionnaires and radiography have been inconclusive. (59-61) However, the findings of an MRI study have supported the theory that elite ballet dancers are at risk of degenerative hip joint pathology. (62) Hip muscle atrophy has been associated with hip OA in MRI and CT studies. (63-66) One MRI study has demonstrated significant atrophy of piriformis in participants with severe hip OA (p < 0.05). (64) However, research investigating the association of pain or intra-articular hip joint pathology with the size of QF has not been done. Ultrasound imaging could be utilized to investigate an association of QF atrophy with hip joint pain and pathology in a dance population.

Conservative methods of managing hip pain could be improved if the stabilizing muscles, such as QF, could be accurately measured and targeted with specific strengthening exercises. USI is potentially useful in performing serial measures of muscle size in a clinical or research setting. (27,28) Therefore, USI could be used in future research to investigate the outcomes of a specific therapeutic exercise program to strengthen QF.

Conclusion

This study has demonstrated that USI can be a reliable and clinically useful tool for measuring the size of QF in a non-invasive manner. Even though USI produced consistently smaller values than MRI, these differences were equivalent to 9% of QF CSA, and the values were highly correlated with excellent repeatability. Therefore, the use of USI to measure changes in the axial plane CSA of this muscle in research and clinical settings is valid. The findings of USI studies could improve our understanding of the function of QF. USI could be used to investigate an association of QF size with hip pain and injury and to assess the outcomes of specific therapeutic exercise programs.

http://dx.doi.org/10.12678/1089-313X.19.1.3

Acknowledgments

The authors sincerely thank the dancers and staff of The Australian Ballet who participated in the study. We also thank Toshiba for supplying the ultrasound system with technical support and Peter Smith and the staff of MIA East Melbourne Radiology for assistance with the MRI procedure. We thank Sophie Emery, Jamie Gaida, and Peta Stellar for assistance in manuscript preparation. Funding from ANZ Trustees is gratefully acknowledged. Professor Cook was supported by the Australian Centre for Research into Sports Injury and its Prevention, which is one of the International Research Centres for Prevention of Injury and Protection of Athlete Health supported by the International Olympic Committee (IOC).

Caption: Figure 1 Quadratus femoris originates from the external border of the ischial tuberosity, inserts into the linea quadrata and is innervated by L5 and S1 nerves (4) (P, piriformis; SG, superior gemellus; OI, obturator internus; IG, inferior gemellus; OE, obturator externus; QF, quadratus femoris). View this figure in color at http://dx.doi.org/10.12678/1089-313X.19.L3.

Caption: Figure 2 Diagram indicating the levels of the four transverse images that were used to measure QF CSA on MRI. The thick line represents the most proximal of these images on MRI and was used for comparison with the single USI image (OI, obturator internus; IG, inferior gemellus; QF, quadratus femoris). View this figure in color at http://dx.doi.org/10.12678/1089-313X.19.1.3.

Caption: Figure 4 A, USI set-up for measurement of quadratus femoris; B, Black line represents transverse line drawn 6 cm distal to superior edge of greater trochanter.

Caption: Figure 5 Axial ultrasound image of the left hip showing the borders of the quadratus femoris muscle.

Caption: Figure 6 Bland-Altman plot demonstrates the mean difference between the MRI and USI estimates of QF axial CSA (thick line) and the limits of agreement (thin lines).

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Susan J. Mayes, P.T., Paula H. Baird-Colt, A.P.M.A., and Jill L. Cook, P.T., Ph.D.

Susan J. Mayes, P.T., The Australian Ballet, Southbank, and School of Primary Health Care, Monash University, Frankston, Victoria, Australia. Paula H. Baird-Colt, A.P.M.A., The Australian Ballet, Southbank, Victoria, Australia. Jill L. Cook, P.T., Ph.D., School of Primary Health Care, Monash University, Frankston, Victoria, Australia.

Correspondence: Susan Mayes, P.T., The Australian Ballet, 2 Kavanagh Street, Southbank, Victoria 3006, Australia; suem@australianballet.com.au.

Table 1 Demographic Data of Participants

                           Male (N = 5)         Female (N = 6)

Height (m)               1.82 [+ or -] 0.09     1.64 [+ or -] 0.03
Weight (kg)              75.4 [+ or -] 6.77       51 [+ or -] 3.58
Body Mass Index (BMI)   22.75 [+ or -] 2.64    18.84 [+ or -] 1.03
Age (years)              29.4 [+ or -] 12.14      31 [+ or -] 13.27
Current Hip Pain (N)             1                     1
Past History of                  2                     1
  Hip Pain (N)


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Author:Mayes, Susan J.; Baird-Colt, Paula H.; Cook, Jill L.
Publication:Journal of Dance Medicine & Science
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Date:Jan 1, 2015
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