Musculoskeletal System


Mission statement

The MSK group is conducting research related to Muscle energetics, Quantitative muscle MRI and Quantitative MSK MRI. A transversal project is devoted to muscle segmentation.

Regarding Muscle energetics, experiments are conducted in both humans and animal models. The corresponding topics are related to standardisation of results and protocols, metabolic effects of training, impact of muscle pathologies, metabolic control, muscle fatigue and functional effects of electrostimulation.

Quantitative investigation of muscle using MRI is mainly performed in collaboration with the Neurology Department of Prof. Attarian (Timone Hospital). The aim is to assess the validity of outcome measures for the follow-up of natural history of rare disorders affecting muscle and also to assess the efficiency of therapeutic strategy.

The MSK program is devoted to the quantitative and functional analysis of cartilage in both rheumatoid and osteo-arthritis using quantitative MRI approaches. Another topic is dedicated to microstructural analysis of bone at ultra high-field.

The transversal project related to segmentation mainly addresses the issue of an optimal supervised segmentation of individual muscles using a variety of approaches i.e. multi-atlas- based, registration-based, artificial intelligence-based…

Through national and international collaborations, we develop a multidiscplinary approach of muscle and joint function using different non invasive techniques and investigating a variety of physiological and pathophysiological conditions.

The muscle Group at CRMBM is a multidisciplinary team composed of biochemists, physiologists, physicists and clinicians.

Research Topics

AMU-MWI Industrial Chair

Publications

Matias, Alexs A., Corinna F. Serviente, Stephen T. Decker, Muhammet Enes Erol, Gaia Giuriato, Yann Le Fur, Rajakumar Nagarajan, David Bendahan, and Gwenael Layec. “Repeatability of Alkaline Inorganic Phosphate Quantification in the Skeletal Muscle Using 31P-Magnetic Resonance Spectroscopy at 3 T.” NMR in Biomedicine, September 3, 2024, e5255. https://doi.org/10.1002/nbm.5255.
Varoquaux, Arthur, Nicolas Fakhry, Ugo Scemama, and David Taïeb. “Differentiation of Vagal from Carotid Paraganglioma on Unenhanced PET/CT: The ‘Sweet Potato’ Shape on PET.” European Journal of Nuclear Medicine and Molecular Imaging, June 3, 2024. https://doi.org/10.1007/s00259-024-06776-w.
Sallustio, V., M. Rossi, M. Mandrone, F. Rossi, I. Chiocchio, T. Cerchiara, E. Longo, et al. “A Promising Eco-Sustainable Wound Dressing Based on Cellulose Extracted from Spartium Junceum L. and Impregnated with Glycyrrhiza Glabra L Extract: Design, Production and Biological Properties.” International Journal of Biological Macromolecules 272, no. Pt 2 (June 3, 2024): 132883. https://doi.org/10.1016/j.ijbiomac.2024.132883.
White, McKenzie S., Augustin C. Ogier, Thomas L. Chenevert, Elizabeth Zucker, Luke Stoneback, Constance P. Michel, Riann M. Palmieri-Smith, and Lindsey K. Lepley. “Beyond Weakness: Exploring Intramuscular Fat and Quadriceps Atrophy in ACLR Recovery.” Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society, June 1, 2024. https://doi.org/10.1002/jor.25910.
Macchi, Robin, Yoko Kunimasa, Pascale Chavet, Baptiste Corcelle, Laura Pomportes, Camille Fazzari, Arnaud Hays, et al. “Effect of a Graded Running Race on Lower Limb Muscle Damage, Jump Performance and Muscle Soreness in Men and Women.” Scandinavian Journal of Medicine & Science in Sports 34, no. 5 (May 2024): e14643. https://doi.org/10.1111/sms.14643.
Galli, Ricardo A., Tamara C. Borsboom, Charlotte Gineste, Lorenza Brocca, Maira Rossi, Darren T. Hwee, Fady I. Malik, et al. “Tirasemtiv Enhances Submaximal Muscle Tension in an Acta1:P.Asp286Gly Mouse Model of Nemaline Myopathy.” The Journal of General Physiology 156, no. 4 (April 1, 2024): e202313471. https://doi.org/10.1085/jgp.202313471.
Michel, Constance P., Laurent A. Messonnier, Benoit Giannesini, Christophe Vilmen, Joevin Sourdon, Yann Le Fur, and David Bendahan. “Endurance Training and Hydroxyurea Have Synergistic Effects on Muscle Function and Energetics in Sickle Cell Disease Mice.” Blood Cells, Molecules & Diseases 107 (March 29, 2024): 102853. https://doi.org/10.1016/j.bcmd.2024.102853.
Monestier, Laura, Jean Del Grande, Ralph Haddad, Laure Santini, Justin Michel, Arthur Varoquaux, and Nicolas Fakhry. “Correlation between MRI (DWI and DCE) and Cellularity of Parotid Gland Pleomorphic Adenomas.” European Archives of Oto-Rhino-Laryngology: Official Journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS): Affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery, March 18, 2024. https://doi.org/10.1007/s00405-024-08562-8.
Brui, Ekaterina A., Zilya Badrieva, Charles-Alexis de Mayenne, Stanislas Rapacchi, Thomas Troalen, and David Bendahan. “Mitigating Slice Cross-Talk in Multi-Slice Multi-Echo Spin Echo T2 Mapping.” Magnetic Resonance in Medicine 91, no. 5 (2024): 2089–2103. https://doi.org/10.1002/mrm.29987.
Guenoun, Daphne, Theo Wirth, Damien Roche, Constance P. Michel, Pierre Daudé, Augustin C. Ogier, Christophe Chagnaud, et al. “Ultra-High Field Magnetic Resonance Imaging of the Quadriceps Tendon Enthesis in Healthy Subjects.” Surgical and Radiologic Anatomy 45, no. 8 (August 1, 2023): 1049–54. https://doi.org/10.1007/s00276-023-03175-y.
Vladimirov, Nikita, Ekaterina Brui, Anatoliy Levchuk, Walid Al-Haidri, Vladimir Fokin, Aleksandr Efimtcev, and David Bendahan. “CNN-Based Fully Automatic Wrist Cartilage Volume Quantification in MR Images: A Comparative Analysis between Different CNN Architectures.” Magnetic Resonance in Medicine 90, no. 2 (August 2023): 737–51. https://doi.org/10.1002/mrm.29671.
Graber, Matthieu, Farah Cadour, Ahmed Ali El Ahmadi, Idir Khati, Jean Del Grande, Christophe Chagnaud, Nicolas Fakhry, Maxime Guye, and Arthur Varoquaux. “Adding Automated Decision-Tree Models to Multiparametric MRI for Parotid Tumours Improves Clinical Performance.” European Journal of Radiology 166 (July 20, 2023): 110999. https://doi.org/10.1016/j.ejrad.2023.110999.
Ogier, Augustin C., Stanislas Rapacchi, and Marc-Emmanuel Bellemare. “Four-Dimensional Reconstruction and Characterization of Bladder Deformations.” Computer Methods and Programs in Biomedicine 237 (April 29, 2023): 107569. https://doi.org/10.1016/j.cmpb.2023.107569.
Michel, Constance P., David Bendahan, Benoit Giannesini, Christophe Vilmen, Yann Le Fur, and Laurent A. Messonnier. “Effects of Hydroxyurea on Skeletal Muscle Energetics and Force Production in a Sickle Cell Disease Murine Model.” Journal of Applied Physiology 134, no. 2 (February 2023): 415–25. https://doi.org/10.1152/japplphysiol.00333.2022.
Heskamp, Linda, Augustin Ogier, David Bendahan, and Arend Heerschap. “Author Correction: Whole-Muscle Fat Analysis Identifies Distal Muscle End as Disease Initiation Site in Facioscapulohumeral Muscular Dystrophy.” Communications Medicine 3, no. 1 (January 12, 2023): 6. https://doi.org/10.1038/s43856-023-00236-6.
Chivet, Mathilde, Maximilian McCluskey, Anne Sophie Nicot, Julie Brocard, Mathilde Beaufils, Diane Giovannini, Benoit Giannesini, et al. “Huntingtin Regulates Calcium Fluxes in Skeletal Muscle.” The Journal of General Physiology 155, no. 1 (January 2, 2023): e202213103. https://doi.org/10.1085/jgp.202213103.
Durelle, Clémence, Emilien Delmont, Constance Michel, Amira Trabelsi, Marc-Adrien Hostin, Augustin Ogier, David Bendahan, and Shahram Attarian. “Quantification of Muscle Involvement in Familial Amyloid Polyneuropathy Using MRI.” European Journal of Neurology 30, no. 10 (2023): 3286–95. https://doi.org/10.1111/ene.15970.
Nassar, Jannette, Amira Trabelsi, Rula Amer, Yann Le Fur, Shahram Attarian, Dvir Radunsky, Tamar Blumenfeld-Katzir, Hayit Greenspan, David Bendahan, and Noam Ben-Eliezer. “Estimation of Subvoxel Fat Infiltration in Neurodegenerative Muscle Disorders Using Quantitative Multi-T2 Analysis.” NMR in Biomedicine 36, no. 9 (2023): e4947. https://doi.org/10.1002/nbm.4947.
Hostin, Marc-Adrien, Augustin C. Ogier, Constance P. Michel, Yann Le Fur, Maxime Guye, Shahram Attarian, Etienne Fortanier, Marc-Emmanuel Bellemare, and David Bendahan. “The Impact of Fatty Infiltration on MRI Segmentation of Lower Limb Muscles in Neuromuscular Diseases: A Comparative Study of Deep Learning Approaches.” Journal of Magnetic Resonance Imaging 58, no. 6 (2023): 1826–35. https://doi.org/10.1002/jmri.28708.
Poullain, François, Pierre Champsaur, Vanessa Pauly, Paul Knoepflin, Thomas Le Corroller, Maud Creze, Martine Pithioux, David Bendahan, and Daphne Guenoun. “Vertebral Trabecular Bone Texture Analysis in Opportunistic MRI and CT Scan Can Distinguish Patients with and without Osteoporotic Vertebral Fracture: A Preliminary Study.” European Journal of Radiology 158 (December 6, 2022): 110642. https://doi.org/10.1016/j.ejrad.2022.110642.
Heskamp, Linda, Augustin Ogier, David Bendahan, and Arend Heerschap. “Whole-Muscle Fat Analysis Identifies Distal Muscle End as Disease Initiation Site in Facioscapulohumeral Muscular Dystrophy.” Communications Medicine 2, no. 1 (December 1, 2022): 155. https://doi.org/10.1038/s43856-022-00217-1.
Knoepflin, Paul, Martine Pithioux, David Bendahan, François Poullain, Thomas Le Corroller, Cyprien Fabre, Vanessa Pauly, et al. “Texture Parameters Measured by UHF-MRI and CT Scan Provide Information on Bone Quality in Addition to BMD: A Biomechanical Ex Vivo Study.” Diagnostics 12, no. 12 (December 2022): 3143. https://doi.org/10.3390/diagnostics12123143.
Soldati, Enrico, Flavy Roseren, Daphne Guenoun, Lucia Mancini, Emilio Catelli, Silvia Prati, Giorgia Sciutto, et al. “Multiscale Femoral Neck Imaging and Multimodal Trabeculae Quality Characterization in an Osteoporotic Bone Sample.” Materials (Basel, Switzerland) 15, no. 22 (November 14, 2022): 8048. https://doi.org/10.3390/ma15228048.
Mayoly, Alice, Marie Witters, Elisabeth Jouve, Cécilia Bec, Aurélie Iniesta, Najib Kachouh, Julie Veran, et al. “Intra Articular Injection of Autologous Microfat and Platelets-Rich Plasma in the Treatment of Wrist Osteoarthritis: A Pilot Study.” Journal of Clinical Medicine 11, no. 19 (September 29, 2022): 5786. https://doi.org/10.3390/jcm11195786.
Meimoun, Laura, Émilie Pecchi, Christophe Vilmen, David Bendahan, and Benoît Giannesini. “Effect of Citrulline Malate Supplementation on Muscle Function and Bioenergetics during Short-Term Repeated Bouts of Fatiguing Exercise.” Journal of Sports Sciences 40, no. 17 (September 2, 2022): 1981–90. https://doi.org/10.1080/02640414.2022.2123527.
Katirtzidou, Eirini, Olivier Rager, Arthur Damien Varoquaux, Antoine Poncet, Vincent Lenoir, Nicolas Dulguerov, Alexandra Platon, Valentina Garibotto, Habib Zaidi, and Minerva Becker. “Detection of Distant Metastases and Distant Second Primary Cancers in Head and Neck Squamous Cell Carcinoma: Comparison of [18F]FDG PET/MRI and [18F]FDG PET/CT.” Insights into Imaging 13, no. 1 (July 28, 2022): 121. https://doi.org/10.1186/s13244-022-01261-0.
Amer, Rula, Jannette Nassar, Amira Trabelsi, David Bendahan, Hayit Greenspan, and Noam Ben-Eliezer. “Quantification of Intra-Muscular Adipose Infiltration in Calf/Thigh MRI Using Fully and Weakly Supervised Semantic Segmentation.” Bioengineering 9, no. 7 (July 14, 2022): 315. https://doi.org/10.3390/bioengineering9070315.
Cadour, Farah, Jennifer Cautela, Stanislas Rapacchi, Arthur Varoquaux, Paul Habert, François Arnaud, Alexis Jacquier, et al. “Cardiac MRI Features and Prognostic Value in Immune Checkpoint Inhibitor–Induced Myocarditis.” Radiology 303, no. 3 (June 2022): 512–21. https://doi.org/10.1148/radiol.211765.
Brui, Ekaterina, Anna Mikhailovskaya, Georgiy Solomakha, Alexander Efimtcev, Anna Andreychenko, and Alena Shchelokova. “Volumetric Wireless Coil for Wrist MRI at 1.5 T as a Practical Alternative to Tx/Rx Extremity Coil: A Comparative Study.” Journal of Magnetic Resonance (San Diego, Calif.: 1997) 339 (June 2022): 107209. https://doi.org/10.1016/j.jmr.2022.107209.
Boutray, Marie de, Mélanie Pons, Nicolas Graillon, Cyrille Chossegros, Anthony Reyre, Christophe Chagnaud, and Arthur Varoquaux. “Stensen’s Duct Stenosis Balloon Dilatation: Long-Term Evaluation of Clinical Outcomes and Quality of Life Impacts.” Otolaryngology–Head and Neck Surgery, May 3, 2022, 01945998221097636. https://doi.org/10.1177/01945998221097636.
Shpringer, Guy, David Bendahan, and Noam Ben-Eliezer. “Accelerated Reconstruction of Dictionary-Based T2 Relaxation Maps Based on Dictionary Compression and Gradient Descent Search Algorithms.” Magnetic Resonance Imaging 87 (April 2022): 56–66. https://doi.org/10.1016/j.mri.2021.12.006.
Micieli, Evy, Davide Voci, Nicola Mumoli, Daniela Mastroiacovo, Alexandru Grigorean, Michael Obadia, Nicolas Menjot de Champfleur, et al. “Transient Perivascular Inflammation of the Carotid Artery (TIPIC) Syndrome.” VASA. Zeitschrift Fur Gefasskrankheiten 51, no. 2 (March 2022): 71–77. https://doi.org/10.1024/0301-1526/a000989.
Jourdan, Arthur, Stanislas Rapacchi, Maxime Guye, David Bendahan, Catherine Masson, and Thierry Bège. “Dynamic-MRI Quantification of Abdominal Wall Motion and Deformation during Breathing and Muscular Contraction.” Computer Methods and Programs in Biomedicine 217 (January 29, 2022): 106667. https://doi.org/10.1016/j.cmpb.2022.106667.
Trojani, Marie-Charlotte, Fréderic Chorin, Pauline Gerus, Véronique Breuil, Constance Michel, Sandrine Guis, David Bendahan, and Christian Roux. “Concentric or Eccentric Physical Activity for Patients with Symptomatic Osteoarthritis of the Knee: A Randomized Prospective Study.” Therapeutic Advances in Musculoskeletal Disease 14 (2022): 1759720X221102805. https://doi.org/10.1177/1759720X221102805.
Michel, Constance P., Laurent A. Messonnier, Benoit Giannesini, Benjamin Chatel, Christophe Vilmen, Yann Le Fur, and David Bendahan. “Effects of Hydroxyurea on Skeletal Muscle Energetics and Function in a Mildly Anemic Mouse Model.” Frontiers in Physiology 13 (2022): 915640. https://doi.org/10.3389/fphys.2022.915640.
Brui, Ekaterina A., Stanislas Rapacchi, David Bendahan, and Anna E. Andreychenko. “Comparative Analysis of SINC-Shaped and SLR Pulses Performance for Contiguous Multi-Slice Fast Spin-Echo Imaging Using Metamaterial-Based MRI.” Magnetic Resonance Materials in Physics, Biology and Medicine 34, no. 6 (December 1, 2021): 929–38. https://doi.org/10.1007/s10334-021-00937-w.
Park, Jae Mo, Sonal Josan, Ralph E. Hurd, James Graham, Peter J. Havel, David Bendahan, Dirk Mayer, Youngran Chung, Daniel M. Spielman, and Thomas Jue. “Hyperpolarized NMR Study of the Impact of Pyruvate Dehydrogenase Kinase Inhibition on the Pyruvate Dehydrogenase and TCA Flux in Type 2 Diabetic Rat Muscle.” Pflügers Archiv - European Journal of Physiology 473, no. 11 (November 1, 2021): 1761–73. https://doi.org/10.1007/s00424-021-02613-3.
Arsovic, Emina, Marion Montava, Nicolas Fakhry, Jean-Pierre Lavieille, Karel Pacak, David Taïeb, and Arthur Varoquaux. “Quantitative Biomarkers Allow the Diagnosis of Head and Neck Paraganglioma on Multiparametric MRI.” European Journal of Radiology 143 (October 2021): 109911. https://doi.org/10.1016/j.ejrad.2021.109911.
Chatel, Benjamin, Sylvie Ducreux, Zeina Harhous, Nadia Bendridi, Isabelle Varlet, Augustin C. Ogier, Monique Bernard, et al. “Impaired Aerobic Capacity and Premature Fatigue Preceding Muscle Weakness in the Skeletal Muscle Tfam-Knockout Mouse Model.” Disease Models & Mechanisms 14, no. 9 (September 15, 2021): dmm048981. https://doi.org/10.1242/dmm.048981.
Soldati, Enrico, Jerome Vicente, Daphne Guenoun, David Bendahan, and Martine Pithioux. “Validation and Optimization of Proximal Femurs Microstructure Analysis Using High Field and Ultra-High Field MRI.” Diagnostics (Basel, Switzerland) 11, no. 9 (September 2, 2021): 1603. https://doi.org/10.3390/diagnostics11091603.
Fournel, Joris, Axel Bartoli, David Bendahan, Maxime Guye, Monique Bernard, Elisa Rauseo, Mohammed Y. Khanji, Steffen E. Petersen, Alexis Jacquier, and Badih Ghattas. “Medical Image Segmentation Automatic Quality Control: A Multi-Dimensional Approach.” Medical Image Analysis 74 (August 12, 2021): 102213. https://doi.org/10.1016/j.media.2021.102213.
Guedj, E., J. Y. Campion, P. Dudouet, E. Kaphan, F. Bregeon, H. Tissot-Dupont, S. Guis, et al. “18F-FDG Brain PET Hypometabolism in Patients with Long COVID.” European Journal of Nuclear Medicine and Molecular Imaging 48, no. 9 (August 2021): 2823–33. https://doi.org/10.1007/s00259-021-05215-4.
Winter, Josine M. de, Charlotte Gineste, Elisa Minardi, Lorenza Brocca, Maira Rossi, Tamara Borsboom, Alan H. Beggs, et al. “Acute and Chronic Tirasemtiv Treatment Improves in Vivo and in Vitro Muscle Performance in Actin-Based Nemaline Myopathy Mice.” Human Molecular Genetics 30, no. 14 (June 26, 2021): 1305–20. https://doi.org/10.1093/hmg/ddab112.
Velier, Mélanie, Stéphane Priet, Romain Appay, Thérèse Atieh, Hubert Lepidi, Gilles Kaplanski, Pierre André Jarrot, et al. “Severe and Irreversible Pancytopenia Associated With SARS-CoV-2 Bone Marrow Infection in a Patient With Waldenstrom Macroglobulinemia.” Clinical Lymphoma, Myeloma & Leukemia 21, no. 6 (June 2021): e503–5. https://doi.org/10.1016/j.clml.2021.01.005.
Soldati, Enrico, Francesca Rossi, Jerome Vicente, Daphne Guenoun, Martine Pithioux, Stefano Iotti, Emil Malucelli, and David Bendahan. “Survey of MRI Usefulness for the Clinical Assessment of Bone Microstructure.” International Journal of Molecular Sciences 22, no. 5 (March 2, 2021): 2509. https://doi.org/10.3390/ijms22052509.
Chatel, Benjamin, Emmanuelle Bernit, Christophe Vilmen, Constance Michel, David Bendahan, and Laurent A. Messonnier. “In Vivo Muscle Function and Energetics in Women with Sickle Cell Anemia or Trait: A 31P-Magnetic Resonance Spectroscopy Study.” Journal of Applied Physiology (Bethesda, Md.: 1985) 130, no. 3 (March 1, 2021): 737–45. https://doi.org/10.1152/japplphysiol.00790.2020.
Molto, Anna, Laure Gossec, Serge Poiraudeau, Pascal Claudepierre, Martin Soubrier, Françoise Fayet, Daniel Wendling, et al. “Evaluation of the Impact of a Nurse-Led Program of Patient Self-Assessment and Self-Management in Axial Spondyloarthritis: Results of a Prospective, Multicentre, Randomized, Controlled Trial (COMEDSPA).” Rheumatology (Oxford, England) 60, no. 2 (February 1, 2021): 888–95. https://doi.org/10.1093/rheumatology/keaa480.
Secondulfo, Laura, Augustin C. Ogier, Jithsa R. Monte, Vincent L. Aengevaeren, David Bendahan, Aart J. Nederveen, Gustav J. Strijkers, and Melissa T. Hooijmans. “Supervised Segmentation Framework for Evaluation of Diffusion Tensor Imaging Indices in Skeletal Muscle.” NMR in Biomedicine 34, no. 1 (January 2021): e4406. https://doi.org/10.1002/nbm.4406.
Vergez, S., N. Fakhry, C. Cartier, T. Kennel, M. Courtade-Saidi, E. Uro-Coste, A. Varoquaux, et al. “Guidelines of the French Society of Otorhinolaryngology–Head and Neck Surgery (SFORL), Part I: Primary Treatment of Pleomorphic Adenoma.” European Annals of Otorhinolaryngology, Head and Neck Diseases 138, no. 4 (2021): 269–74. https://doi.org/10.1016/j.anorl.2020.09.002.
Baboudjian, Michael, Mehdi Mhatli, Adel Bourouina, Bastien Gondran-Tellier, Vassili Anastay, Lea Perez, Pauline Proye, et al. “Is Minor Surgery Safe during the COVID-19 Pandemic? A Multi-Disciplinary Study.” PloS One 16, no. 5 (2021): e0251122. https://doi.org/10.1371/journal.pone.0251122.