Variability of hip muscle volume determined by computed tomography

IRBM 30 (2009) 14–19

Original article

Variability of hip muscle volume determined by computed tomography Variabilité des volumes musculaires de la hanche déterminés à partir de tomodensitométrie E. Jolivet a,∗,b , E. Daguet b , V. Bousson b , C. Bergot b , W. Skalli a , J.D. Laredo b,c a CNRS, LBM, arts et métiers Paristech, 151, boulevard de l’Hôpital, 75013 Paris, France CNRS UMR 7052, laboratoire de radiologie expérimentale, service de radiologie de l’hôpital Lariboisière Assistance publique–Hôpitaux de Paris, faculté Lariboisière–Saint-Louis de l’université Paris-VII, Paris, France c Department of radiology, university of Pennsylvania Health System, Philadelphia, États-Unis b

Received 14 October 2008; accepted 6 January 2009 Available online 14 February 2009

Abstract Muscle volume is an essential parameter in clinical evaluation and in biomechanical model development. Nevertheless, the difficulty in volumic muscle reconstruction from medical images is the noise they contain that limits the efficiency of image processing to automatically segment muscle. This study was conducted to explore hip muscle volume from CT-scan acquisition and to analyze the variability of muscle volume for a population of 98 subjects with age ranged from 21 to 94 years. To obtain three-dimensional muscle reconstruction, a method based on a deformation of a parametric specific object generated from a reduced number of muscle contours was used. A reproducibility study was conducted for muscle volume estimation. Coefficient of variation was found less than 8.9% and intraclass correlation coefficients were greater than 0.88. Results showed no significant difference between left and right muscles for this population. After adjustment to age and body mass index, hip muscle volumes were significantly different between men and women. This muscle volume reconstruction method allowed quantifying muscle volume distribution within a large population. © 2009 Elsevier Masson SAS. All rights reserved. Résumé Le volume du muscle est un paramètre essentiel dans l’évaluation clinique et pour le développement de modèles biomécaniques. Cependant, la reconstruction volumique des muscles à partir des modalités d’imagerie médicale s’avère difficile par la présence de bruit limitant l’efficacité des méthodes basées sur le traitement d’images. Pour obtenir la reconstruction volumique des muscles, une méthode basée sur la déformation d’un objet paramétré prépersonnalisé construit à partir d’un nombre réduit de contours musculaires a été développée. Cette étude a pour but d’explorer les muscles de la hanche en utilisant l’imagerie scanner et d’analyser la variabilité de leur volume au sein d’une population de 98 sujets âgés de 21 à 94 ans. Une étude de reproductibilité a été menée. Le coefficient de variation de l’estimation des volumes musculaires est inférieur à 8,9 % et les coefficients de corrélation intraclasse sont supérieurs à 0,88. Les résultats montrent qu’il n’existe pas de différence significative entre les muscles droits et gauches pour cette population. Après ajustement à l’âge et à l’indice de masse corporelle, les volumes des muscles de la hanche sont significativement différents entre les hommes et les femmes. Cette étude à large échelle, rendue possible grâce à l’utilisation d’une méthode rapide et efficace, a permis d’analyser la distribution des volumes musculaires pour une population importante. © 2009 Elsevier Masson SAS. Tous droits réservés. Keywords: Muscle volume; Computed tomography; Imaging; Hip Mots clés : Volume musculaire ; Tomodensitométrie ; Imagerie ; Hanche

1. Introduction ∗

Corresponding author. E-mail address: [email protected] (E. Jolivet).

1959-0318/$ – see front matter © 2009 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.irbm.2009.01.003

A good knowledge of the musculoskeletal biomechanics, geometric and physical muscle characteristics are essential to

E. Jolivet et al. / IRBM 30 (2009) 14–19

clinical evaluation [1] and for development of biomechanical models. In biomechanical models, muscle force is often relied on its cross-sectional area (CSA) and length [2,3]. Such data have been registered from cadaver to represent an average adult [2,4,5]. However, such generic data may not be adapted to the wide variability of human muscular system. Moreover, muscle CSA measurements can not represent the entire muscle volume variability [6]. In addition, assessing individual muscle volume and geometry in vivo from medical imaging is a technical challenge. Authors usually manually had to outline muscle contours on many magnetic resonance (MR) or CT-scan axial images in order to obtain a three-dimensional reconstruction of the muscle [7–10]. Other methods to estimate muscle volume from sparse muscle CSA measurement on medical images include using truncated cone formula approximation [11,12], cavalieri principle [13,14] and regression equation [6,15]. Only one study focused on hip muscle volume estimation from systematic manual contouring on MRI images in three subjects [7]. More recently, muscle three-dimensional reconstruction has been obtained thanks to deformation of a parametric specific object (DPSO) generated from muscle contouring on a small number of axial images enabling quantitative analysis of muscle volume in a large number of subjects [16]. The aim of the present study is to evaluate first the reproducibility of the DPSO reconstruction method of muscle volume estimation and secondly, to perform a volumic analysis of hip muscles using CT-scan acquisitions. 2. Material & Method Ninety-eight subjects were included in the study. The population consisted of 57 men and 41 women with a mean age of 54.3 years (range 21–94 years). Subject’s characteristics are presented in Table 1. The protocol was approved by the ethical committee of our institution and all subjects gave their informed written consent before participation in the examination to the protocol. The exclusion criteria were pregnancy, psychological incapacity to answer the health questionnary, self-reported myopathy and hip surgery history. 2.1. Computed Tomography Axial CT-scan at the abdomen and pelvic levels were obtained with a Mx 8000 CT-scanner unit (Marconi, Medical Systems, Cleveland, OH). Patients were imaged in the supine position with the arms above abdomen. CT-scan acquisition covered from the iliac crest to lowest pole of the iliac bone. Scans were perTable 1 Study population: age, sex, height and body mass index (BMI).

Age (years) Weight (kg) Height (cm) BMI (kg/m−2 )

Mean (SD)

Minimum

Maximum

54.1 (16) 72.9 (14.5) 170 (8) 32.36 (12.18)

21 43.0 149 11.56

94 118.0 198 78.22

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formed with a 512 × 512 matrix and a 460 mm field of view. Pixel resolution was of 0.90 × 0.90 mm2 . A quality review was performed on each subject’s images to ensure that all images were present, that the proper scan acquisition technique was used, and that images were appropriate to the analysis. A calibration phantom (European Forearm Phantom® ) was placed below the flank during the CT-scan examination in order to ensure the stability and reproductiblity of the CT-scan acquisition. The density measured in water-equivalent epoxy resine presented a mean value equal to 1.59 Hounsfield Unit (HU) with a standard deviation of 3.53 HU. 2.2. Volume reconstruction The Gluteus maximus, gluteus medius, gluteus minimus, sartorius and tensor fascia lata muscles were studied. The DPSO method was used to obtain three-dimensional muscle reconstruction from contours on a small number CT-scan images [16]. The method consists in the generation of approximate parametric ellipses using basic dimensions of muscle contours on a small number of images. A regular volumic surface is built by an interpolation of the ellipses, and the surface of the approximate object obtained are deformed to fit the exact muscle contours on the selected images providing a three-dimensional muscle subject-specific geometry. Since the DPSO method does not require muscle contours on all images, a first step consisted in the selection of slices of analysis where muscles had to be outlined. Thus, for each side, the first image containing iliac crest (ETS ) and the last image including the inferior extremity of ischial tuberosity (ETI ) were identified. Then, four slices were defined to evaluate left muscles (slice name: ETL,i with i ranged from 1 to 4) and four slices for right muscles (slice name: ETR,i with i ranged from 1 to 4). These images were distributed using distance ratios with regard to ETS – ETI distance. They were equal to 0.38, 0.58 0.80 and 1, respectively for ETL,1 , ETL,2 , ETL,3 and ETL,4 for the left side (Fig. 1). Same ratios were used to identify ETR,i (i ranged from 1 to 4) slices for the right side. After slice selection, muscles were manually outlined on these slices. Table 2 shows on which slice each muscle was seen. Each evaluated muscle was contoured. A self adjustment prevented interpenetration of contours (Fig. 2). Finally, muscle volume geometry were generated using DPSO method and muscle volume were computed (Vm,DPSO ).

Table 2 Presence of each individual muscle on the four images of analysis ETS,i with S corresponding to the left side (L) or right (R) and i ranged from 1 to 4. Muscle

ETS,1

ETS,2

ETS,3

ETS,4

Gluteus Maximus Gluteus Medius Gluteus Minimus Tensor fascia latae Sartorius

P P P

P P P P P

P

P

P P

P P

P: muscle present in the slice of analysis.

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E. Jolivet et al. / IRBM 30 (2009) 14–19

Fig. 1. Selection of CT-scan slices analyzed.

To estimate the quality of muscle volume estimation, reference muscle volume reconstruction (Vm,Ref ) were obtained for 10 subjects as follows. To obtain a reference volume of hip muscles for these subjects, each muscle was manually outlined in each slice of the CT-scans acquisition between ETI and ETS slices and muscle reference geometry were generated using all these contours to computed Vm,Ref . The mean volume difference Vm,Ref –Vm,DPSO for the 10 subjects was then calculated for each muscle. This mean volume difference was finally expressed in percentage of Vm,Ref .

The data analysis consisted in slice selection of ETS and ETI and manual segmentation of muscle on slices of analysis. The intra-observer reproducibility and inter-observer reproducibility on and muscular volume (Vm,DPSO ) were assessed with intraclass correlation coefficient (ICC) on the software SPSS 13.0 (SPSS Inc., Chicago, Illinois). Shrout et al., defined the intraclass correlations coefficients for intra-observer ICC1,1 and for inter-observer ICC3,1 as follows (Shrout et al., [17]): ICC1,1 =

(BMS − WMS) (BMS + (K − 1) ∗ WMS)

(1)

ICC3,1 =

(BMS − EMS) (BMS + (K − 1) ∗ EMS)

(2)

2.3. Reproducibility of muscular volume evaluation Three observers made the data analysis on 30 subjects, and one observer repeated the measurement with a gap of 1 month.

Fig. 2. (a): manual muscle contour contouring; (b): and muscle outline after geometric adjustment with muscle outline already present on the slices.

E. Jolivet et al. / IRBM 30 (2009) 14–19

BMS represents the variability between subjects, WMS the variability within subjects and EMS the residual error. These values are extracted from a one-way Anova for ICC1,1 and from a two-way Anova for ICC3,1 . K is the number of observers or observations dependent on the case. An intraclass correlation coefficient superior to 0.75 indicate an acceptable correlation between occasions or between observations respectively. The method error and coefficient of variation of muscle volume determination (Vm,DPSO ) were evaluated using the definition of Gluer et al., and considering all the four observations [18].

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Table 3 Mean reference muscle volume (Vm,Ref ) of each individual muscle in the 10 subjects and mean difference (in %) between muscle volume (Vm,DPSO ) and reference muscle volume (Vm,Ref ). Muscle

Reference muscle volume (Vm,Ref ) (cm3 )

Reconstruction volume error (%)

Gluteus maximus Gluteus medius Gluteus minimus Tensor fascia latae Sartorius

648.1 306.8 81.8 55.5 30.3 Mean value

2.5 10.3 7.6 6.3 7.7 6.9

2.4. Statistical analysis First, mean volume, standard deviation, the minimum, the maximum and percentile ranking were determined for each muscle included in this study from 98 subjects. The coefficient of variation (standard deviation divided by mean volume) of each muscle among population was calculated. Then, difference in left and right muscles was assessed with a paired Wilcoxon signed rank test. Potential difference in muscle volume between males and females was tested with an analysis of covariance considering age and body mass index as covariates. The critical level of significance in the present study was set at p < 0.01. 3. Results Mean time necessary to obtain muscle volume with the DPSO method (Vm,DPSO ) was 25 minutes, comparing to 2 hours when all slices were used to generate muscle volume (Vm,Ref ). Mean volume difference between Vm,DPSO and Vm,Ref computed from muscle volume obtained with DPSO method and muscle volume computed with manual segmentation in all images, was equal to 6.9%. Minimal volume difference was observed for Gluteus maximus muscle (2.5%) and the maximum difference was 10.3% for Gluteus medius (Table 3).

Concerning reproducibility study, intraclass correlation coefficients for intra-observer reproducibility (ICC1,1 ) and interobserver (ICC3,1 ) were greater than 0.88 (Table 4). Minimum were observed for Gluteus medius muscle (ICC1,1 equal to 0.88 and ICC3,1 0.91). The method error ranged from 2524 (Sartorius muscle) to 23,966 mm3 (Gluteus medius muscle) leading to coefficient of variation equal to 2.4% for Gluteus maximus muscle, 8.9% for Gluteus medius muscle, 7.4% for Gluteus minimus muscle, 6.6% for tensor fascia latae muscle and 7.8% for Sartorius muscle (Table 4). Gluteus maximus muscle has the largest mean volume (512,342 mm3 ) and Sartorius muscle the lowest one (24,541 mm3 ) (Table 5). The gluteus maximus muscle represented 35.1 % on average of total muscle volume. The sartorius and tensor fascia lata muscles showed the largest volume variation. Among this population, coefficients of variation were 27.3%, 23.9%, 23.8%, 32.5% and 32.3% for the gluteus maximus, gluteus medius, gluteus minimus, tensor fascia lata and sartorius muscles respectively. No significant difference was observed between left and right muscles with a paired Wilcoxon signed rank test. The mean muscle volume (and standard deviation) for men and women are presented in Fig. 3. After verification of the nor-

Table 4 Intraclass coefficient of correlation for intra-observer (ICC1,1 ) and inter-observer (ICC3,1 ) reproductibility for volume measurement (Vm,DPSO ), method error precision (expressed in mm3 ) and coefficient of variation. Muscle

Intra-observer ICC1,1

Inter-observer ICC3,1

Precision (mm3 )

Coefficient of variation (%)

Gluteus Maximus Gluteus Medius Gluteus Minimus Tensor Fascia Lata Sartorius

0.99 0.88 0.94 0.99 0.96

0.99 0.91 0.93 0.96 0.95

13 927 23 966 7069 3706 2524

2.4 8.9 7.4 6.6 7.8

Table 5 Descriptive statistics of hip muscle volumes (Vm,DPSO ): mean standard deviation, minimum, maximum and percentiles, (in mm3 ). Muscle

Gluteus maximus Gluteus medius Gluteus minimus Tensor fascia latae Sartorius

Mean

512,342 96,701 47,531 43,920 245,411

Standard deviation

139,490 23,131 11,319 14,296 7,919

Minimum

198,144 52,273 26,384 15,177 9,891

Percentiles

Maximum

25th

50th

75th

407,278 79,884 38,727 35,293 18,485

528,432 96,174 46,296 44,552 24,106

614,580 116,098 57,054 53,451 29,565

852,482 148,981 75,927 81,496 46,919

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E. Jolivet et al. / IRBM 30 (2009) 14–19

Fig. 3. Mean volume (mm3 ) and standard deviation of pelvic muscles for men and women.

mal distribution hypothesis for muscle volume variable with a Kolmogorov-Smirnov test, a significant difference was observed after adjustment to age and body mass index (Fig. 3). 4. Discussion Hip muscle volumes have been measured in a population of 98 asymptomatic subjects. To obtain three-dimensional muscle reconstruction, a DSPO method which allows generating muscle volume from a reduced number of manual contours was used. Thus, population analyzed in the study was compared to existing studies on muscle volume reconstruction from systematic manual contours on many CT-scan or MRI images [7,10,12,19]. The validation of DPSO method was realized by comparison with muscle volume obtained with manual contouring on all images. Thus, the volume error was evaluated and was less than 6.9% with a drastically reduction of time of analysis (divided by five). Considering muscle volume estimation from medical images, another difficulty was the determination of distal and proximal muscle endings between muscle tissue and tendons. For that, we have chosen to delimit the volume of interest of each muscle using anatomical bone characteristics and distance ratio. This method is less subjective and volumes of interest were comparable for each of the subject. Nevertheless, we did not determine the volume of the entire muscle volume. Our goal was to analyze the variability of muscle volume, so we considered that it was important to ensure that measured volume was reproducible. The reproducibility study, including slice selection and manual muscle segmentation, were conducted on 30 subjects. Results show a good agreement of measurement for intra-

observer and inter-observer analysis (ICC > 0.88). The less reproducible muscle was Gluteus medius muscle with a coefficient of variation equal to 8.9%. This result could be explained by the presence of fat accumulation between Gluteus medius and Gluteus minimus muscle making muscle delineation difficult. Another limitation concerns the choice of muscles analyzed in this study. To apply the DPSO method, it was necessary to observe muscle on several images. In this way and considering the axial orientation of CT-scan image reconstruction used here, muscle orientation had to be close to the normal to image orientation. Despite these limitations, this study shows the efficiency of the DPSO muscle volume reconstruction method to analyze muscle variability for a population with age ranged from 21 to 94 years old. Thus, men presented largest muscle volume than women after adjustment to age and body mass index, and no significant difference was observed between left and right muscles. We expect that these data could help to design further study focusing on muscle volume estimation. Conflict of Interest None. References [1] Inan M, Alkan A, Harma A, Ertem K. Evaluation of the gluteus medius muscle after a pelvic support osteotomy to treat congenital dislocation of the hip. J Bone Joint Surg Am 2005;87:2246–52.

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