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Erschienen in: Magnetic Resonance Materials in Physics, Biology and Medicine 2/2016

16.03.2016 | Research Article

Volume measurements of individual muscles in human quadriceps femoris using atlas-based segmentation approaches

verfasst von: Arnaud Le Troter, Alexandre Fouré, Maxime Guye, Sylviane Confort-Gouny, Jean-Pierre Mattei, Julien Gondin, Emmanuelle Salort-Campana, David Bendahan

Erschienen in: Magnetic Resonance Materials in Physics, Biology and Medicine | Ausgabe 2/2016

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Abstract

Objectives

Atlas-based segmentation is a powerful method for automatic structural segmentation of several sub-structures in many organs. However, such an approach has been very scarcely used in the context of muscle segmentation, and so far no study has assessed such a method for the automatic delineation of individual muscles of the quadriceps femoris (QF). In the present study, we have evaluated a fully automated multi-atlas method and a semi-automated single-atlas method for the segmentation and volume quantification of the four muscles of the QF and for the QF as a whole.

Subjects and methods

The study was conducted in 32 young healthy males, using high-resolution magnetic resonance images (MRI) of the thigh. The multi-atlas-based segmentation method was conducted in 25 subjects. Different non-linear registration approaches based on free-form deformable (FFD) and symmetric diffeomorphic normalization algorithms (SyN) were assessed. Optimal parameters of two fusion methods, i.e., STAPLE and STEPS, were determined on the basis of the highest Dice similarity index (DSI) considering manual segmentation (MSeg) as the ground truth. Validation and reproducibility of this pipeline were determined using another MRI dataset recorded in seven healthy male subjects on the basis of additional metrics such as the muscle volume similarity values, intraclass coefficient, and coefficient of variation. Both non-linear registration methods (FFD and SyN) were also evaluated as part of a single-atlas strategy in order to assess longitudinal muscle volume measurements. The multi- and the single-atlas approaches were compared for the segmentation and the volume quantification of the four muscles of the QF and for the QF as a whole.

Results

Considering each muscle of the QF, the DSI of the multi-atlas-based approach was high 0.87 ± 0.11 and the best results were obtained with the combination of two deformation fields resulting from the SyN registration method and the STEPS fusion algorithm. The optimal variables for FFD and SyN registration methods were four templates and a kernel standard deviation ranging between 5 and 8. The segmentation process using a single-atlas-based method was more robust with DSI values higher than 0.9. From the vantage of muscle volume measurements, the multi-atlas-based strategy provided acceptable results regarding the QF muscle as a whole but highly variable results regarding individual muscle. On the contrary, the performance of the single-atlas-based pipeline for individual muscles was highly comparable to the MSeg, thereby indicating that this method would be adequate for longitudinal tracking of muscle volume changes in healthy subjects.

Conclusion

In the present study, we demonstrated that both multi-atlas and single-atlas approaches were relevant for the segmentation of individual muscles of the QF in healthy subjects. Considering muscle volume measurements, the single-atlas method provided promising perspectives regarding longitudinal quantification of individual muscle volumes.
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Literatur
1.
Zurück zum Zitat Barnouin Y, Butler-Browne G, Voit T, Reversat D, Azzabou N, Leroux G, Behin A, McPhee JS, Carlier PG, Hogrel J-Y (2014) Manual segmentation of individual muscles of the quadriceps femoris using MRI: A reappraisal. J Magn Reson Imaging 40:239–247CrossRefPubMed Barnouin Y, Butler-Browne G, Voit T, Reversat D, Azzabou N, Leroux G, Behin A, McPhee JS, Carlier PG, Hogrel J-Y (2014) Manual segmentation of individual muscles of the quadriceps femoris using MRI: A reappraisal. J Magn Reson Imaging 40:239–247CrossRefPubMed
2.
Zurück zum Zitat Baudin PY, Azzabou N, Carlier PG, Paragios N (2012) Prior knowledge, random walks and human skeletal muscle segmentation. Med Image Comput Comput Assist Interv 15:569–576PubMed Baudin PY, Azzabou N, Carlier PG, Paragios N (2012) Prior knowledge, random walks and human skeletal muscle segmentation. Med Image Comput Comput Assist Interv 15:569–576PubMed
3.
Zurück zum Zitat Baudin P-Y, Goodman D, Kumrnar P, Azzabou N, Carlier PG, Paragios N, Kumar MP (2013) Discriminative parameter estimation for random walks segmentation. Med Image Comput Comput Assist Interv 16:219–226PubMed Baudin P-Y, Goodman D, Kumrnar P, Azzabou N, Carlier PG, Paragios N, Kumar MP (2013) Discriminative parameter estimation for random walks segmentation. Med Image Comput Comput Assist Interv 16:219–226PubMed
4.
Zurück zum Zitat Makrogiannis S, Serai S, Fishbein KW, Schreiber C, Ferrucci L, Spencer RG (2012) Automated quantification of muscle and fat in the thigh from water-, fat-, and nonsuppressed MR images. J Magn Reson Imaging 35:1152–1161CrossRefPubMedPubMedCentral Makrogiannis S, Serai S, Fishbein KW, Schreiber C, Ferrucci L, Spencer RG (2012) Automated quantification of muscle and fat in the thigh from water-, fat-, and nonsuppressed MR images. J Magn Reson Imaging 35:1152–1161CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Prescott JW, Best TM, Swanson MS, Haq F, Jackson RD, Gurcan MN (2011) Anatomically anchored template-based level set segmentation: Application to quadriceps muscles in MR images from the osteoarthritis initiative. J Digit Imaging 24:28–43CrossRefPubMedPubMedCentral Prescott JW, Best TM, Swanson MS, Haq F, Jackson RD, Gurcan MN (2011) Anatomically anchored template-based level set segmentation: Application to quadriceps muscles in MR images from the osteoarthritis initiative. J Digit Imaging 24:28–43CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Ahmad E, Yap MH, Degens H, McPhee JS (2014) Atlas-registration based image segmentation of MRI human thigh muscles in 3D space. In: Proceedings of SPIE 9037. Medical imaging 2014: image perception, observer performance, and technology assessment. doi:10.1117/12.2043606 Ahmad E, Yap MH, Degens H, McPhee JS (2014) Atlas-registration based image segmentation of MRI human thigh muscles in 3D space. In: Proceedings of SPIE 9037. Medical imaging 2014: image perception, observer performance, and technology assessment. doi:10.​1117/​12.​2043606
7.
Zurück zum Zitat Ma D, Cardoso MJ, Modat M, Powell N, Wells J, Holmes H, Wiseman F, Tybulewicz V, Fisher E, Lythgoe MF, Ourselin S (2014) Automatic structural parcellation of mouse brain MRI using multi-atlas label fusion. PLoS One 9:e86576CrossRefPubMedPubMedCentral Ma D, Cardoso MJ, Modat M, Powell N, Wells J, Holmes H, Wiseman F, Tybulewicz V, Fisher E, Lythgoe MF, Ourselin S (2014) Automatic structural parcellation of mouse brain MRI using multi-atlas label fusion. PLoS One 9:e86576CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Eugenio Iglesias J, Rory Sabuncu M, Van Leemput K (2013) A unified framework for cross-modality multi-atlas segmentation of brain MRI. Med Image Anal 17:1181–1191CrossRefPubMed Eugenio Iglesias J, Rory Sabuncu M, Van Leemput K (2013) A unified framework for cross-modality multi-atlas segmentation of brain MRI. Med Image Anal 17:1181–1191CrossRefPubMed
9.
Zurück zum Zitat Heckemann RA, Hajnal JV, Aljabar P, Rueckert D, Hammers A (2006) Automatic anatomical brain MRI segmentation combining label propagation and decision fusion. Neuroimage 33:115–126CrossRefPubMed Heckemann RA, Hajnal JV, Aljabar P, Rueckert D, Hammers A (2006) Automatic anatomical brain MRI segmentation combining label propagation and decision fusion. Neuroimage 33:115–126CrossRefPubMed
10.
Zurück zum Zitat Wu G, Wang Q, Zhang D, Nie F, Huang H, Shen D (2014) A generative probability model of joint label fusion for multi-atlas based brain segmentation. Med Image Anal 18:881–890CrossRefPubMedPubMedCentral Wu G, Wang Q, Zhang D, Nie F, Huang H, Shen D (2014) A generative probability model of joint label fusion for multi-atlas based brain segmentation. Med Image Anal 18:881–890CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Klein S, van der Heide UA, Lips IM, van Vulpen M, Staring M, Pluim JPW (2008) Automatic segmentation of the prostate in 3D MR images by atlas matching using localized mutual information. Med Phys 35:1407CrossRefPubMed Klein S, van der Heide UA, Lips IM, van Vulpen M, Staring M, Pluim JPW (2008) Automatic segmentation of the prostate in 3D MR images by atlas matching using localized mutual information. Med Phys 35:1407CrossRefPubMed
12.
Zurück zum Zitat Gubern-Mérida A, Kallenberg M, Martí R, Karssemeijer N (2012) Segmentation of the pectoral muscle in breast MRI using atlas-based approaches. Med Image Comput Comput Assist Interv 15:371–378PubMed Gubern-Mérida A, Kallenberg M, Martí R, Karssemeijer N (2012) Segmentation of the pectoral muscle in breast MRI using atlas-based approaches. Med Image Comput Comput Assist Interv 15:371–378PubMed
13.
Zurück zum Zitat Thomas MS, Newman D, Leinhard OD, Kasmai B, Greenwood R, Malcolm PN, Karlsson A, Rosander J, Borga M, Toms AP (2014) Test–retest reliability of automated whole body and compartmental muscle volume measurements on a wide bore 3T MR system. Eur Radiol 24:2279–2291CrossRefPubMed Thomas MS, Newman D, Leinhard OD, Kasmai B, Greenwood R, Malcolm PN, Karlsson A, Rosander J, Borga M, Toms AP (2014) Test–retest reliability of automated whole body and compartmental muscle volume measurements on a wide bore 3T MR system. Eur Radiol 24:2279–2291CrossRefPubMed
14.
Zurück zum Zitat Karlsson A, Rosander J, Romu T, Tallberg J, Grönqvist A, Borga M, Dahlqvist Leinhard O (2015) Automatic and quantitative assessment of regional muscle volume by multi-atlas segmentation using whole-body water-fat MRI. J Magn Reson Imaging 41:1558–1569CrossRefPubMed Karlsson A, Rosander J, Romu T, Tallberg J, Grönqvist A, Borga M, Dahlqvist Leinhard O (2015) Automatic and quantitative assessment of regional muscle volume by multi-atlas segmentation using whole-body water-fat MRI. J Magn Reson Imaging 41:1558–1569CrossRefPubMed
15.
Zurück zum Zitat Zijdenbos AP, Dawant BM, Margolin RA, Palmer AC (1994) Morphometric analysis of white matter lesions in MR images: Method and validation. IEEE Trans Med Imaging 13:716–724CrossRefPubMed Zijdenbos AP, Dawant BM, Margolin RA, Palmer AC (1994) Morphometric analysis of white matter lesions in MR images: Method and validation. IEEE Trans Med Imaging 13:716–724CrossRefPubMed
16.
Zurück zum Zitat Udupa JK, LeBlanc VR, Zhuge Y, Imielinska C, Schmidt H, Currie LM, Hirsch BE, Woodburn J (2006) A framework for evaluating image segmentation algorithms. Comput Med Imaging Graph 30:75–87CrossRefPubMed Udupa JK, LeBlanc VR, Zhuge Y, Imielinska C, Schmidt H, Currie LM, Hirsch BE, Woodburn J (2006) A framework for evaluating image segmentation algorithms. Comput Med Imaging Graph 30:75–87CrossRefPubMed
17.
Zurück zum Zitat Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790CrossRefPubMed Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790CrossRefPubMed
18.
Zurück zum Zitat Positano V, Christiansen T, Santarelli MF, Ringgaard S, Landini L, Gastaldelli A (2009) Accurate segmentation of subcutaneous and intermuscular adipose tissue from MR images of the thigh. J Magn Reson Imaging 29:677–684CrossRefPubMed Positano V, Christiansen T, Santarelli MF, Ringgaard S, Landini L, Gastaldelli A (2009) Accurate segmentation of subcutaneous and intermuscular adipose tissue from MR images of the thigh. J Magn Reson Imaging 29:677–684CrossRefPubMed
19.
Zurück zum Zitat Xu C, Prince JL (1998) Snakes, shapes, and gradient vector flow. IEEE Trans Image Process 7:359–369CrossRefPubMed Xu C, Prince JL (1998) Snakes, shapes, and gradient vector flow. IEEE Trans Image Process 7:359–369CrossRefPubMed
20.
Zurück zum Zitat Rueckert D, Sonoda LI, Hayes C, Hill DLG, Leach MO, Hawkes DJ (1999) Nonrigid registration using free-form deformations: Application to breast MR images. IEEE Trans Med Imaging 18:712–721CrossRefPubMed Rueckert D, Sonoda LI, Hayes C, Hill DLG, Leach MO, Hawkes DJ (1999) Nonrigid registration using free-form deformations: Application to breast MR images. IEEE Trans Med Imaging 18:712–721CrossRefPubMed
21.
Zurück zum Zitat Modat M, Ridgway GR, Taylor ZA, Lehmann M, Barnes J, Hawkes DJ, Fox NC, Ourselin S (2010) Fast free-form deformation using graphics processing units. Comput Methods Programs Biomed 98:278–284CrossRefPubMed Modat M, Ridgway GR, Taylor ZA, Lehmann M, Barnes J, Hawkes DJ, Fox NC, Ourselin S (2010) Fast free-form deformation using graphics processing units. Comput Methods Programs Biomed 98:278–284CrossRefPubMed
22.
Zurück zum Zitat Avants B, Epstein C, Grossman M, Gee J (2008) Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12:26–41CrossRefPubMedPubMedCentral Avants B, Epstein C, Grossman M, Gee J (2008) Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12:26–41CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Jorge Cardoso M, Leung K, Modat M, Keihaninejad S, Cash D, Barnes J, Fox NC, Ourselin S (2013) STEPS: similarity and truth estimation for propagated segmentations and its application to hippocampal segmentation and brain parcelation. Med Image Anal 17:671–684CrossRefPubMed Jorge Cardoso M, Leung K, Modat M, Keihaninejad S, Cash D, Barnes J, Fox NC, Ourselin S (2013) STEPS: similarity and truth estimation for propagated segmentations and its application to hippocampal segmentation and brain parcelation. Med Image Anal 17:671–684CrossRefPubMed
24.
Zurück zum Zitat Warfield SK, Zou KH, Wells WM (2004) Simultaneous truth and performance level estimation (STAPLE): An algorithm for the validation of image segmentation. IEEE Trans Med Imaging 23:903–921CrossRefPubMedPubMedCentral Warfield SK, Zou KH, Wells WM (2004) Simultaneous truth and performance level estimation (STAPLE): An algorithm for the validation of image segmentation. IEEE Trans Med Imaging 23:903–921CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Zou KH, Warfield SK, Bharatha A, Tempany CM, Kaus MR, Haker SJ, Wells WM, Jolesz FA, Kikinis R (2004) Statistical validation of image segmentation quality based on a spatial overlap index 1: Scientific reports. Acad Radiol 11:178–189CrossRefPubMedPubMedCentral Zou KH, Warfield SK, Bharatha A, Tempany CM, Kaus MR, Haker SJ, Wells WM, Jolesz FA, Kikinis R (2004) Statistical validation of image segmentation quality based on a spatial overlap index 1: Scientific reports. Acad Radiol 11:178–189CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Nordez A, Jolivet E, Südhoff I, Bonneau D, de Guise JA, Skalli W (2009) Comparison of methods to assess quadriceps muscle volume using magnetic resonance imaging. J Magn Reson Imaging 30:1116–1123CrossRefPubMed Nordez A, Jolivet E, Südhoff I, Bonneau D, de Guise JA, Skalli W (2009) Comparison of methods to assess quadriceps muscle volume using magnetic resonance imaging. J Magn Reson Imaging 30:1116–1123CrossRefPubMed
27.
Zurück zum Zitat Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med Auckl N Z 30:1–15CrossRef Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med Auckl N Z 30:1–15CrossRef
28.
Zurück zum Zitat Shrout PE, Fleiss JL (1979) Intraclass correlations: Uses in assessing rater reliability. Psychol Bull 86:420–428CrossRefPubMed Shrout PE, Fleiss JL (1979) Intraclass correlations: Uses in assessing rater reliability. Psychol Bull 86:420–428CrossRefPubMed
29.
Zurück zum Zitat Reeves ND, Narici MV, Maganaris CN (2004) Effect of resistance training on skeletal muscle-specific force in elderly humans. J Appl Physiol (1985) 96:885–892CrossRef Reeves ND, Narici MV, Maganaris CN (2004) Effect of resistance training on skeletal muscle-specific force in elderly humans. J Appl Physiol (1985) 96:885–892CrossRef
30.
Zurück zum Zitat Gondin J, Guette M, Ballay Y, Martin A (2005) Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 37:1291–1299CrossRefPubMed Gondin J, Guette M, Ballay Y, Martin A (2005) Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 37:1291–1299CrossRefPubMed
31.
Zurück zum Zitat Fouré A, Duhamel G, Wegrzyk J, Boudinet H, Mattei J-P, Le Troter A, Bendahan D, Gondin J (2015) Heterogeneity of muscle damage induced by electrostimulation: A multimodal MRI study. Med Sci Sports Exerc 47:166–175CrossRefPubMed Fouré A, Duhamel G, Wegrzyk J, Boudinet H, Mattei J-P, Le Troter A, Bendahan D, Gondin J (2015) Heterogeneity of muscle damage induced by electrostimulation: A multimodal MRI study. Med Sci Sports Exerc 47:166–175CrossRefPubMed
32.
Zurück zum Zitat Thom JM, Thompson MW, Ruell PA, Bryant GJ, Fonda JS, Harmer AR, Janse de Jonge XA, Hunter SK (2001) Effect of 10-day cast immobilization on sarcoplasmic reticulum calcium regulation in humans. Acta Physiol Scand 172:141–147CrossRefPubMed Thom JM, Thompson MW, Ruell PA, Bryant GJ, Fonda JS, Harmer AR, Janse de Jonge XA, Hunter SK (2001) Effect of 10-day cast immobilization on sarcoplasmic reticulum calcium regulation in humans. Acta Physiol Scand 172:141–147CrossRefPubMed
33.
Zurück zum Zitat Vandenborne K, Elliott MA, Walter GA, Abdus S, Okereke E, Shaffer M, Tahernia D, Esterhai JL (1998) Longitudinal study of skeletal muscle adaptations during immobilization and rehabilitation. Muscle Nerve 21:1006–1012CrossRefPubMed Vandenborne K, Elliott MA, Walter GA, Abdus S, Okereke E, Shaffer M, Tahernia D, Esterhai JL (1998) Longitudinal study of skeletal muscle adaptations during immobilization and rehabilitation. Muscle Nerve 21:1006–1012CrossRefPubMed
34.
Zurück zum Zitat Willis TA, Hollingsworth KG, Coombs A, Sveen M-L, Andersen S, Stojkovic T, Eagle M, Mayhew A, de Sousa PL, Dewar L, Morrow JM, Sinclair CDJ, Thornton JS, Bushby K, Lochmuller H, Hanna MG, Hogrel J-Y, Carlier PG, Vissing J, Straub V (2014) Quantitative magnetic resonance imaging in limb-girdle muscular dystrophy 2I: A multinational cross-sectional study. PLoS one 9:e90377CrossRefPubMedPubMedCentral Willis TA, Hollingsworth KG, Coombs A, Sveen M-L, Andersen S, Stojkovic T, Eagle M, Mayhew A, de Sousa PL, Dewar L, Morrow JM, Sinclair CDJ, Thornton JS, Bushby K, Lochmuller H, Hanna MG, Hogrel J-Y, Carlier PG, Vissing J, Straub V (2014) Quantitative magnetic resonance imaging in limb-girdle muscular dystrophy 2I: A multinational cross-sectional study. PLoS one 9:e90377CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Hollingsworth KG, Garrood P, Eagle M, Bushby K, Straub V (2013) Magnetic resonance imaging in Duchenne muscular dystrophy: Longitudinal assessment of natural history over 18 months: short reports. Muscle Nerve 48:586–588CrossRefPubMed Hollingsworth KG, Garrood P, Eagle M, Bushby K, Straub V (2013) Magnetic resonance imaging in Duchenne muscular dystrophy: Longitudinal assessment of natural history over 18 months: short reports. Muscle Nerve 48:586–588CrossRefPubMed
36.
Zurück zum Zitat Maden-Wilkinson TM, Degens H, Jones DA, McPhee JS (2013) Comparison of MRI and DXA to measure muscle size and age-related atrophy in thigh muscles. J Musculoskelet Neuronal Interact 13:320–328PubMed Maden-Wilkinson TM, Degens H, Jones DA, McPhee JS (2013) Comparison of MRI and DXA to measure muscle size and age-related atrophy in thigh muscles. J Musculoskelet Neuronal Interact 13:320–328PubMed
37.
Zurück zum Zitat Hogrel J-Y, Barnouin Y, Azzabou N, Butler-Browne G, Voit T, Moraux A, Leroux G, Behin A, McPhee JS, Carlier PG (2015) NMR imaging estimates of muscle volume and intramuscular fat infiltration in the thigh: Variations with muscle, gender, and age. Age. doi:10.1007/s11357-015-9798-5 Hogrel J-Y, Barnouin Y, Azzabou N, Butler-Browne G, Voit T, Moraux A, Leroux G, Behin A, McPhee JS, Carlier PG (2015) NMR imaging estimates of muscle volume and intramuscular fat infiltration in the thigh: Variations with muscle, gender, and age. Age. doi:10.​1007/​s11357-015-9798-5
Metadaten
Titel
Volume measurements of individual muscles in human quadriceps femoris using atlas-based segmentation approaches
verfasst von
Arnaud Le Troter
Alexandre Fouré
Maxime Guye
Sylviane Confort-Gouny
Jean-Pierre Mattei
Julien Gondin
Emmanuelle Salort-Campana
David Bendahan
Publikationsdatum
16.03.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Magnetic Resonance Materials in Physics, Biology and Medicine / Ausgabe 2/2016
Print ISSN: 0968-5243
Elektronische ISSN: 1352-8661
DOI
https://doi.org/10.1007/s10334-016-0535-6

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