Magnetic Resonance Imaging Biomarkers of Bone and Soft Tissue Tumors

Abstract

Magnetic resonance imaging (MRI) is essential in the management of musculoskeletal (MSK) tumors. This review delves into the diverse MRI modalities, focusing on anatomical, functional, and metabolic sequences that provide essential biomarkers for tumor detection, characterization, disease extent determination, and assessment of treatment response. MRI's multimodal capabilities offer a range of biomarkers that enhance MSK tumor evaluation, aiding in better patient management.

Keywords

magnetic resonance imaging - biomarker - sarcoma - bone tumor - soft tissue tumor

Publication History

Article published online:
08 February 2024

• References

• 1 Shiga NT, Del Grande F, Lardo O, Fayad LM. Imaging of primary bone tumors: determination of tumor extent by non-contrast sequences. Pediatr Radiol 2013; 43 (08) 1017-1023
• 2 Ahlawat S, Fritz J, Morris CD, Fayad LM. Magnetic resonance imaging biomarkers in musculoskeletal soft tissue tumors: review of conventional features and focus on nonmorphologic imaging. J Magn Reson Imaging 2019; 50 (01) 11-27
• 3 Fayad LM, Mugera C, Soldatos T, Flammang A, del Grande F. Technical innovation in dynamic contrast-enhanced magnetic resonance imaging of musculoskeletal tumors: an MR angiographic sequence using a sparse k-space sampling strategy. Skeletal Radiol 2013; 42 (07) 993-1000
• 4 Dreizin D, Ahlawat S, Del Grande F, Fayad LM. Gradient-echo in-phase and opposed-phase chemical shift imaging: role in evaluating bone marrow. Clin Radiol 2014; 69 (06) 648-657
• 5 Kumar NM, Ahlawat S, Fayad LM. Chemical shift imaging with in-phase and opposed-phase sequences at 3 T: what is the optimal threshold, measurement method, and diagnostic accuracy for characterizing marrow signal abnormalities?. Skeletal Radiol 2018; 47 (12) 1661-1671
• 6 Vilanova JC, Baleato-Gonzalez S, Romero MJ, Carrascoso-Arranz J, Luna A. Assessment of musculoskeletal malignancies with functional MR imaging. Magn Reson Imaging Clin N Am 2016; 24 (01) 239-259
• 7 Subhawong TK, Jacobs MA, Fayad LM. Diffusion-weighted MR imaging for characterizing musculoskeletal lesions. Radiographics 2014; 34 (05) 1163-1177
• 8 Zeitoun R, Shokry AM, Ahmed Khaleel S, Mogahed SM. Osteosarcoma subtypes: magnetic resonance and quantitative diffusion weighted imaging criteria. J Egypt Natl Canc Inst 2018; 30 (01) 39-44
• 9 Leplat C, Hossu G, Chen B. et al. Contrast-enhanced 3-T perfusion MRI with quantitative analysis for the characterization of musculoskeletal tumors: is it worth the trouble?. AJR Am J Roentgenol 2018; 211 (05) 1092-1098
• 10 Subhawong TK, Wang X, Durand DJ. et al. Proton MR spectroscopy in metabolic assessment of musculoskeletal lesions. AJR Am J Roentgenol 2012; 198 (01) 162-172
• 11 Samet J, Weinstein J, Fayad LM. MRI and clinical features of Langerhans cell histiocytosis (LCH) in the pelvis and extremities: can LCH really look like anything?. Skeletal Radiol 2016; 45 (05) 607-613
• 12 Zanchetta E, Ciniselli CM, Bardelli A. et al. Magnetic resonance imaging patterns of tumor response to chemotherapy in desmoid-type fibromatosis. Cancer Med 2021; 10 (13) 4356-4365
• 13 Gross AM, Dombi E, Wolters PL. et al. Long-term safety and efficacy of selumetinib in children with neurofibromatosis type 1 on a phase 1/2 trial for inoperable plexiform neurofibromas. Neuro Oncol 2023; 25 (10) 1883-1894
• 14 Shimizu K, Hamada S, Sakai T. et al. MRI characteristics predict the efficacy of meloxicam treatment in patients with desmoid-type fibromatosis. J Med Imaging Radiat Oncol 2019; 63 (06) 751-757
• 15 Soldatos T, Ahlawat S, Montgomery E, Chalian M, Jacobs MA, Fayad LM. Multiparametric assessment of treatment response in high-grade soft-tissue sarcomas with anatomic and functional MR imaging sequences. Radiology 2016; 278 (03) 831-840
• 16 de Castro Luna R, Kumar NM, Fritz J, Ahlawat S, Fayad LM. MRI evaluation of soft tissue tumors: comparison of a fast, isotropic, 3D T2-weighted fat-saturated sequence with a conventional 2D T2-weighted fat-saturated sequence for tumor characteristics, resolution, and acquisition time. Eur Radiol 2022; 32 (12) 8670-8680
• 17 Ahlawat S, Morris C, Fayad LM. Three-dimensional volumetric MRI with isotropic resolution: improved speed of acquisition, spatial resolution and assessment of lesion conspicuity in patients with recurrent soft tissue sarcoma. Skeletal Radiol 2016; 45 (05) 645-652
• 18 Fritz J, Raithel E, Thawait GK, Gilson W, Papp DF. Six-fold acceleration of high-spatial resolution 3D SPACE MRI of the knee through incoherent k-space undersampling and iterative reconstruction—first experience. Invest Radiol 2016; 51 (06) 400-409
• 19 Jones BC, Ahlawat S, Fayad LM. 3D MRI in musculoskeletal oncology. Semin Musculoskelet Radiol 2021; 25 (03) 418-424
• 20 Li S, Huang X, Li G. et al. Exponential subtraction in 3D ultrashort echo time imaging to visualize short T2 tissues in tibia. Acta Radiol 2020; 61 (06) 760-767
• 21 Gulati V, Chhabra A. Qualitative and quantitative MRI techniques for the evaluation of musculoskeletal neoplasms. Semin Roentgenol 2022; 57 (03) 291-305
• 22 Fayad LM, Jacobs MA, Wang X, Carrino JA, Bluemke DA. Musculoskeletal tumors: how to use anatomic, functional, and metabolic MR techniques. Radiology 2012; 265 (02) 340-356
• 23 Suh CH, Yun SJ, Jin W, Park SY, Ryu CW, Lee SH. Diagnostic performance of in-phase and opposed-phase chemical-shift imaging for differentiating benign and malignant vertebral marrow lesions: a meta-analysis. AJR Am J Roentgenol 2018; 211 (04) W188-W197
• 24 Jahanvi V, Kelkar A. Chemical shift imaging: an indispensable tool in diagnosing musculoskeletal pathologies. SA J Radiol 2021; 25 (01) 2061
• 25 Thawait SK, Marcus MA, Morrison WB, Klufas RA, Eng J, Carrino JA. Research synthesis: what is the diagnostic performance of magnetic resonance imaging to discriminate benign from malignant vertebral compression fractures? Systematic review and meta-analysis. Spine 2012; 37 (12) E736-E744
• 26 Ragab Y, Emad Y, Gheita T. et al. Differentiation of osteoporotic and neoplastic vertebral fractures by chemical shift in-phase and out-of phase MR imaging. Eur J Radiol 2009; 72 (01) 125-133
• 27 Kenneally BE, Gutowski CJ, Reynolds AW, Morrison WB, Abraham JA. Utility of opposed-phase magnetic resonance imaging in differentiating sarcoma from benign bone lesions. J Bone Oncol 2015; 4 (04) 110-114
• 28 Del Grande F, Tatizawa-Shiga N, Jalali Farahani S, Chalian M, Fayad LM. Chemical shift imaging: preliminary experience as an alternative sequence for defining the extent of a bone tumor. Quant Imaging Med Surg 2014; 4 (03) 173-180
• 29 Baur A, Reiser MF. Diffusion-weighted imaging of the musculoskeletal system in humans. Skeletal Radiol 2000; 29 (10) 555-562
• 30 van Rijswijk CSP, Kunz P, Hogendoorn PCW, Taminiau AHM, Doornbos J, Bloem JL. Diffusion-weighted MRI in the characterization of soft-tissue tumors. J Magn Reson Imaging 2002; 15 (03) 302-307
• 31 Raya JG, Duarte A, Wang N. et al. Applications of diffusion-weighted MRI to the musculoskeletal system. J Magn Reson Imaging 2023 July 21 (Epub ahead of print)
• 32 Costa FM, Ferreira EC, Vianna EM. Diffusion-weighted magnetic resonance imaging for the evaluation of musculoskeletal tumors. Magn Reson Imaging Clin N Am 2011; 19 (01) 159-180
• 33 Hong JH, Jee WH, Jung CK, Jung JY, Shin SH, Chung YG. Soft tissue sarcoma: adding diffusion-weighted imaging improves MR imaging evaluation of tumor margin infiltration. Eur Radiol 2019; 29 (05) 2589-2597
• 34 Ahlawat S, Khandheria P, Subhawong TK, Fayad LM. Differentiation of benign and malignant skeletal lesions with quantitative diffusion weighted MRI at 3T. Eur J Radiol 2015; 84 (06) 1091-1097
• 35 Pozzi G, Albano D, Messina C. et al. Solid bone tumors of the spine: diagnostic performance of apparent diffusion coefficient measured using diffusion-weighted MRI using histology as a reference standard. J Magn Reson Imaging 2018; 47 (04) 1034-1042
• 36 Dallaudière B, Lecouvet F, Vande Berg B. et al. Diffusion-weighted MR imaging in musculoskeletal diseases: current concepts. Diagn Interv Imaging 2015; 96 (04) 327-340
• 37 Dietrich O, Geith T, Reiser MF, Baur-Melnyk A. Diffusion imaging of the vertebral bone marrow. NMR Biomed 2017; 30 (03) e3333
• 38 Rao A, Sharma C, Parampalli R. Role of diffusion-weighted MRI in differentiating benign from malignant bone tumors. BJR Open 2019; 1 (01) 20180048
• 39 Tamai K, Koyama T, Saga T. et al. The utility of diffusion-weighted MR imaging for differentiating uterine sarcomas from benign leiomyomas. Eur Radiol 2008; 18 (04) 723-730
• 40 Wang Q, Xiao X, Liang Y. et al. Diagnostic performance of diffusion MRI for differentiating benign and malignant nonfatty musculoskeletal soft tissue tumors: a systematic review and meta-analysis. J Cancer 2021; 12 (24) 7399-7412
• 41 Razek A, Nada N, Ghaniem M, Elkhamary S. Assessment of soft tissue tumours of the extremities with diffusion echoplanar MR imaging. Radiol Med (Torino) 2012; 117 (01) 96-101
• 42 Lee SY, Jee WH, Jung JY. et al. Differentiation of malignant from benign soft tissue tumours: use of additive qualitative and quantitative diffusion-weighted MR imaging to standard MR imaging at 3.0 T. Eur Radiol 2016; 26 (03) 743-754
• 43 Oka K, Yakushiji T, Sato H. et al. Usefulness of diffusion-weighted imaging for differentiating between desmoid tumors and malignant soft tissue tumors. J Magn Reson Imaging 2011; 33 (01) 189-193
• 44 Liu Y, Wu J, Shen Q. et al. Magnetic resonance imaging features of prostatic stromal tumour of uncertain malignant potential. J Med Imaging Radiat Oncol 2022; 66 (08) 1065-1072
• 45 Del Grande F, Ahlawat S, Subhawong T, Fayad LM. Characterization of indeterminate soft tissue masses referred for biopsy: what is the added value of contrast imaging at 3.0 Tesla?. J Magn Reson Imaging 2017; 45 (02) 390-400
• 46 Kransdorf MJ. Benign soft-tissue tumors in a large referral population: distribution of specific diagnoses by age, sex, and location. AJR Am J Roentgenol 1995; 164 (02) 395-402
• 47 Yun JS, Lee MH, Lee SM. et al. Peripheral nerve sheath tumor: differentiation of malignant from benign tumors with conventional and diffusion-weighted MRI. Eur Radiol 2021; 31 (03) 1548-1557
• 48 Demehri S, Belzberg A, Blakeley J, Fayad LM. Conventional and functional MR imaging of peripheral nerve sheath tumors: initial experience. AJNR Am J Neuroradiol 2014; 35 (08) 1615-1620
• 49 Matsumine A, Kusuzaki K, Nakamura T. et al. Differentiation between neurofibromas and malignant peripheral nerve sheath tumors in neurofibromatosis 1 evaluated by MRI. J Cancer Res Clin Oncol 2009; 135 (07) 891-900
• 50 Bhargava R, Parham DM, Lasater OE, Chari RS, Chen G, Fletcher BD. MR imaging differentiation of benign and malignant peripheral nerve sheath tumors: use of the target sign. Pediatr Radiol 1997; 27 (02) 124-129
• 51 Ahlawat S, Fayad LM. Imaging cellularity in benign and malignant peripheral nerve sheath tumors: utility of the “target sign” by diffusion weighted imaging. Eur J Radiol 2018; 102: 195-201
• 52 Kim JH, Choe J, Kim HK, Lee HY. MRI-based stepwise approach to anterior mediastinal cystic lesions for diagnosis and further management. Korean J Radiol 2023; 24 (01) 62-78
• 53 Subhawong TK, Durand DJ, Thawait GK, Jacobs MA, Fayad LM. Characterization of soft tissue masses: can quantitative diffusion weighted imaging reliably distinguish cysts from solid masses?. Skeletal Radiol 2013; 42 (11) 1583-1592
• 54 Pekcevik Y, Kahya MO, Kaya A. Characterization of soft tissue tumors by diffusion-weighted imaging. Iran J Radiol 2015; 12 (03) e15478
• 55 Morán LM, Vega J, Gómez-León N, Royuela A. Myxomas and myxoid liposarcomas of the extremities: our preliminary findings in conventional, perfusion, and diffusion magnetic resonance. Acta Radiol Open 2022; 11 (10) 20 584601221131481
• 56 Arslan S, Ergen FB, Aydın GB. et al. Different attenuation models of diffusion-weighted MR imaging for the differentiation of benign and malignant musculoskeletal tumors. J Magn Reson Imaging 2022; 55 (02) 594-607
• 57 Nagata S, Nishimura H, Uchida M. et al. Diffusion-weighted imaging of soft tissue tumors: usefulness of the apparent diffusion coefficient for differential diagnosis. Radiat Med 2008; 26 (05) 287-295
• 58 Genovese E, Canì A, Rizzo S, Angeretti MG, Leonardi A, Fugazzola C. Comparison between MRI with spin-echo echo-planar diffusion-weighted sequence (DWI) and histology in the diagnosis of soft-tissue tumours. Radiol Med (Torino) 2011; 116 (04) 644-656
• 59 Uhl M, Saueressig U, Koehler G. et al. Evaluation of tumour necrosis during chemotherapy with diffusion-weighted MR imaging: preliminary results in osteosarcomas. Pediatr Radiol 2006; 36 (12) 1306-1311
• 60 Hayashida Y, Yakushiji T, Awai K. et al. Monitoring therapeutic responses of primary bone tumors by diffusion-weighted image: initial results. Eur Radiol 2006; 16 (12) 2637-2643
• 61 Dudeck O, Zeile M, Pink D. et al. Diffusion-weighted magnetic resonance imaging allows monitoring of anticancer treatment effects in patients with soft-tissue sarcomas. J Magn Reson Imaging 2008; 27 (05) 1109-1113
• 62 Wang CS, Du LJ, Si MJ. et al. Noninvasive assessment of response to neoadjuvant chemotherapy in osteosarcoma of long bones with diffusion-weighted imaging: an initial in vivo study. PLoS One 2013; 8 (08) e72679
• 63 Setiawati R, Novariyanto B, Rahardjo P, Mustokoweni S, Guglielmi G. Characteristic of apparent diffusion coefficient and time intensity curve analysis of dynamic contrast enhanced MRI in osteosarcoma histopathologic subtypes. Int J Med Sci 2023; 20 (02) 163-171
• 64 Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986; 161 (02) 401-407
• 65 Jin B, Yang J, Zhen J. et al. Intravoxel incoherent motion and dynamic contrast-enhanced magnetic resonance imaging can differentiate between atypical cartilaginous tumors and high-grade chondrosarcoma: correlation with histological vessel characteristics. J Comput Assist Tomogr 2023 August 9 (Epub ahead of print)
• 66 Lim HK, Jee WH, Jung JY. et al. Intravoxel incoherent motion diffusion-weighted MR imaging for differentiation of benign and malignant musculoskeletal tumours at 3 T. Br J Radiol 2018; 91 (1082): 20170636
• 67 Wu G, Liu X, Xiong Y, Ran J, Li X. Intravoxel incoherent motion and diffusion kurtosis imaging for discriminating soft tissue sarcoma from vascular anomalies. Medicine (Baltimore) 2018; 97 (50) e13641
• 68 Zhan J, Hao D, Wang D. et al. Standard diffusion-weighted, intravoxel incoherent motion, and dynamic contrast-enhanced MRI of musculoskeletal tumours: correlations with Ki67 proliferation status. Clin Radiol 2021; 76 (12) 941.e11-941.e18
• 69 Li X, Liu Y, Tao J. et al. Value of intravoxel incoherent motion and diffusion kurtosis imaging in predicting peritumoural infiltration of soft-tissue sarcoma: a prospective study based on MRI-histopathology comparisons. Clin Radiol 2021; 76 (07) 532-539
• 70 Niu J, Li W, Wang H. et al. Intravoxel incoherent motion diffusion-weighted imaging of bone marrow in patients with acute myeloid leukemia: a pilot study of prognostic value. J Magn Reson Imaging 2017; 46 (02) 476-482
• 71 Baidya Kayal E, Kandasamy D, Khare K, Bakhshi S, Sharma R, Mehndiratta A. Intravoxel incoherent motion (IVIM) for response assessment in patients with osteosarcoma undergoing neoadjuvant chemotherapy. Eur J Radiol 2019; 119: 108635
• 72 Drapé JL. Advances in magnetic resonance imaging of musculoskeletal tumours. Orthop Traumatol Surg Res 2013; 99 (1, Suppl): S115-S123
• 73 Ioannidis GS, Nikiforaki K, Karantanas A. Statistical and spatial correlation between diffusion and perfusion MR imaging parameters: a study on soft tissue sarcomas. Phys Med 2019; 65: 59-66
• 74 Petralia G, Summers PE, Agostini A. et al. Dynamic contrast-enhanced MRI in oncology: how we do it. Radiol Med (Torino) 2020; 125 (12) 1288-1300
• 75 Saha A, Peck KK, Karimi S, Lis E, Holodny AI. Dynamic contrast-enhanced MR perfusion: role in diagnosis and treatment follow-up in patients with vertebral body tumors. Neuroimaging Clin N Am 2023; 33 (03) 477-486
• 76 Walker-Samuel S, Leach MO, Collins DJ. Evaluation of response to treatment using DCE-MRI: the relationship between initial area under the gadolinium curve (IAUGC) and quantitative pharmacokinetic analysis. Phys Med Biol 2006; 51 (14) 3593-3602
• 77 Dyke JP, Panicek DM, Healey JH. et al. Osteogenic and Ewing sarcomas: estimation of necrotic fraction during induction chemotherapy with dynamic contrast-enhanced MR imaging. Radiology 2003; 228 (01) 271-278
• 78 Del Grande F, Subhawong T, Weber K, Aro M, Mugera C, Fayad LM. Detection of soft-tissue sarcoma recurrence: added value of functional MR imaging techniques at 3.0 T. Radiology 2014; 271 (02) 499-511
• 79 Notley M, Yu J, Fulcher AS, Turner MA, Cockrell CH, Nguyen D. Pictorial review. Diagnosis of recurrent prostate cancer and its mimics at multiparametric prostate MRI. Br J Radiol 2015; 88 (1054): 20150362
• 80 Erber BM, Reidler P, Goller SS. et al. Impact of dynamic contrast enhanced and diffusion-weighted MR imaging on detection of early local recurrence of soft tissue sarcoma. J Magn Reson Imaging 2023; 57 (02) 622-630
• 81 Franiel T, Hamm B, Hricak H. Dynamic contrast-enhanced magnetic resonance imaging and pharmacokinetic models in prostate cancer. Eur Radiol 2011; 21 (03) 616-626
• 82 Ocak I, Bernardo M, Metzger G. et al. Dynamic contrast-enhanced MRI of prostate cancer at 3 T: a study of pharmacokinetic parameters. AJR Am J Roentgenol 2007; 189 (04) 849
• 83 Song XL, Ren JL, Zhao D, Wang L, Ren H, Niu J. Radiomics derived from dynamic contrast-enhanced MRI pharmacokinetic protocol features: the value of precision diagnosis ovarian neoplasms. Eur Radiol 2021; 31 (01) 368-378
• 84 Li X, Welch EB, Chakravarthy AB. et al. Statistical comparison of dynamic contrast-enhanced MRI pharmacokinetic models in human breast cancer. Magn Reson Med 2012; 68 (01) 261-271
• 85 Huang W, Beckett BR, Tudorica A. et al. Evaluation of soft tissue sarcoma response to preoperative chemoradiotherapy using dynamic contrast-enhanced magnetic resonance imaging. Tomography 2016; 2 (04) 308-316
• 86 Fayad LM, Salibi N, Wang X. et al. Quantification of muscle choline concentrations by proton MR spectroscopy at 3 T: technical feasibility. AJR Am J Roentgenol 2010; 194 (01) W73-W79
• 87 Fayad LM, Wang X, Salibi N. et al. A feasibility study of quantitative molecular characterization of musculoskeletal lesions by proton MR spectroscopy at 3 T. AJR Am J Roentgenol 2010; 195 (01) W69-W75
• 88 Deshmukh S, Subhawong T, Carrino JA, Fayad L. Role of MR spectroscopy in musculoskeletal imaging. Indian J Radiol Imaging 2014; 24 (03) 210-216
• 89 Isaac A, Lecouvet F, Dalili D. et al. Detection and characterization of musculoskeletal cancer using whole-body magnetic resonance imaging. Semin Musculoskelet Radiol 2020; 24 (06) 726-750
• 90 Messiou C, Hillengass J, Delorme S. et al. Guidelines for acquisition, interpretation, and reporting of whole-body MRI in myeloma: Myeloma Response Assessment and Diagnosis System (MY-RADS). Radiology 2019; 291 (01) 5-13
• 91 Sun M, Cheng J, Ren C. et al. Quantitative whole-body MR imaging for assessment of tumor burden in patients with multiple myeloma: correlation with prognostic biomarkers. Quant Imaging Med Surg 2021; 11 (08) 3767-3780
• 92 Sun M, Cheng J, Ren C. et al. Evaluation of diffuse bone marrow infiltration pattern in monoclonal plasma cell diseases by quantitative whole-body magnetic resonance imaging. Acad Radiol 2022; 29 (04) 490-500
• 93 Takasu M, Kondo S, Akiyama Y. et al. Assessment of early treatment response on MRI in multiple myeloma: comparative study of whole-body diffusion-weighted and lumbar spinal MRI. PLoS One 2020; 15 (02) e0229607
• 94 Pasoglou V, Van Nieuwenhove S, Peeters F, Duchêne G, Kirchgesner T, Lecouvet FE. 3D Whole-body MRI of the musculoskeletal system. Semin Musculoskelet Radiol 2021; 25 (03) 441-454
• 95 Johnston EW, Latifoltojar A, Sidhu HS. et al. Multiparametric whole-body 3.0-T MRI in newly diagnosed intermediate- and high-risk prostate cancer: diagnostic accuracy and interobserver agreement for nodal and metastatic staging. Eur Radiol 2019; 29 (06) 3159-3169
• 96 Lecouvet FE, Pasoglou V, Van Nieuwenhove S. et al. Shortening the acquisition time of whole-body MRI: 3D T1 gradient echo Dixon vs fast spin echo for metastatic screening in prostate cancer. Eur Radiol 2020; 30 (06) 3083-3093
• 97 Ahlawat S, Blakeley JO, Langmead S, Belzberg AJ, Fayad LM. Current status and recommendations for imaging in neurofibromatosis type 1, neurofibromatosis type 2, and schwannomatosis. Skeletal Radiol 2020; 49 (02) 199-219