The Increasing Spectrum of Indications of Whole-Body MRI Beyond Oncology: Imaging Answers to Clinical Needs

Abstract

Whole-body coverage using MRI was developed almost 2 decades ago. The first applications focused on the investigation of the skeleton to detect neoplastic disease, mainly metastases from solid cancers, and involvement by multiple myeloma and lymphoma. But the extensive coverage of the whole musculoskeletal system, combined with the exquisite sensitivity of MRI to tissue alteration in relation to different pathologic conditions, mainly inflammation, has led to the identification of a growing number of indications outside oncology. Seronegative rheumatisms, systemic sclerosis, inflammatory diseases involving muscles or fascias, and multifocal osseous, vascular, or neurologic diseases represent currently validated or emerging indications of whole-body MRI (WB-MRI). We first illustrate the most valuable indications of WB-MRI in seronegative rheumatisms that include providing significant diagnostic information in patients with negative or ambiguous MRI of the sacroiliac joints and the lumbar spine, assessing disease activity in advanced (ankylosed) central disease, and evaluating the peripherally dominant forms of spondyloarthropathy. Then we review the increasing indications of WB-MRI in other rheumatologic and nonneoplastic disorders, underline the clinical needs, and illustrate the role of WB-MRI in the positive diagnosis and evaluation of disease burden, therapeutic decisions, and treatment monitoring.

Keywords

MRI - diffusion-weighted MRI - whole-body MRI - rheumatisms - spondyloarthropathy - systemic sclerosis - myositis - treatment - inflammation - biomarker

^* P. Omoumi and M. Stoenoiu contributed equally to this work.

• References

• 1 Johnson KM, Leavitt GD, Kayser HW. Total-body MR imaging in as little as 18 seconds. Radiology 1997; 202 (1) 262-267
• 2 Horvath LJ, Burtness BA, McCarthy S, Johnson KM. Total-body echo-planar MR imaging in the staging of breast cancer: comparison with conventional methods—early experience. Radiology 1999; 211 (1) 119-128
• 3 Eustace S, Tello R, DeCarvalho V , et al. A comparison of whole-body turboSTIR MR imaging and planar 99mTc-methylene diphosphonate scintigraphy in the examination of patients with suspected skeletal metastases. AJR Am J Roentgenol 1997; 169 (6) 1655-1661
• 4 Lauenstein TC, Goehde SC, Herborn CU , et al. Whole-body MR imaging: evaluation of patients for metastases. Radiology 2004; 233 (1) 139-148
• 5 Pasoglou V, Michoux N, Peeters F , et al. Whole-body 3D T1-weighted MR imaging in patients with prostate cancer: feasibility and evaluation in screening for metastatic disease. Radiology 2015; 275 (1) 155-166
• 6 Lecouvet FE, Larbi A, Pasoglou V , et al. MRI for response assessment in metastatic bone disease. Eur Radiol 2013; 23 (7) 1986-1997
• 7 Lecouvet FE, Talbot JN, Messiou C, Bourguet P, Liu Y, de Souza NM ; EORTC Imaging Group Monitoring the response of bone metastases to treatment with Magnetic Resonance Imaging and nuclear medicine techniques: a review and position statement by the European Organisation for Research and Treatment of Cancer imaging group. Eur J Cancer 2014; 50 (15) 2519-2531
• 8 Baur-Melnyk A, Buhmann S, Becker C , et al. Whole-body MRI versus whole-body MDCT for staging of multiple myeloma. AJR Am J Roentgenol 2008; 190 (4) 1097-1104
• 9 van Ufford HM, Kwee TC, Beek FJ , et al. Newly diagnosed lymphoma: initial results with whole-body T1-weighted, STIR, and diffusion-weighted MRI compared with 18F-FDG PET/CT. AJR Am J Roentgenol 2011; 196 (3) 662-669
• 10 Lecouvet FE, El Mouedden J, Collette L , et al. Can whole-body magnetic resonance imaging with diffusion-weighted imaging replace Tc 99m bone scanning and computed tomography for single-step detection of metastases in patients with high-risk prostate cancer?. Eur Urol 2012; 62 (1) 68-75
• 11 Althoff CE, Appel H, Rudwaleit M , et al. Whole-body MRI as a new screening tool for detecting axial and peripheral manifestations of spondyloarthritis. Ann Rheum Dis 2007; 66 (7) 983-985
• 12 Fritz J, Tzaribatchev N, Claussen CD, Carrino JA, Horger MS. Chronic recurrent multifocal osteomyelitis: comparison of whole-body MR imaging with radiography and correlation with clinical and laboratory data. Radiology 2009; 252 (3) 842-851
• 13 Schanz S, Henes J, Ulmer A , et al. Magnetic resonance imaging findings in patients with systemic scleroderma and musculoskeletal symptoms. Eur Radiol 2013; 23 (1) 212-221
• 14 Weckbach S. Whole-body MRI for inflammatory arthritis and other multifocal rheumatoid diseases. Semin Musculoskelet Radiol 2012; 16 (5) 377-388
• 15 Castro TC, Lederman H, Terreri MT, Caldana WI, Kaste SC, Hilário MO. The use of joint-specific and whole-body MRI in osteonecrosis: a study in patients with juvenile systemic lupus erythematosus. Br J Radiol 2011; 84 (1003) 621-628
• 16 Schmidt GP, Reiser MF, Baur-Melnyk A. Whole-body imaging of bone marrow. Semin Musculoskelet Radiol 2009; 13 (2) 120-133
• 17 Schmidt GP, Baur-Melnyk A, Herzog P , et al. High-resolution whole-body magnetic resonance image tumor staging with the use of parallel imaging versus dual-modality positron emission tomography-computed tomography: experience on a 32-channel system. Invest Radiol 2005; 40 (12) 743-753
• 18 Lecouvet FE, Simon M, Tombal B, Jamart J, Vande Berg BC, Simoni P. Whole-body MRI (WB-MRI) versus axial skeleton MRI (AS-MRI) to detect and measure bone metastases in prostate cancer (PCa). Eur Radiol 2010; 20 (12) 2973-2982
• 19 Rennie WJ, Dhillon SS, Conner-Spady B, Maksymowych WP, Lambert RG. Magnetic resonance imaging assessment of spinal inflammation in ankylosing spondylitis: standard clinical protocols may omit inflammatory lesions in thoracic vertebrae. Arthritis Rheum 2009; 61 (9) 1187-1193
• 20 Weckbach S, Schewe S, Michaely HJ, Steffinger D, Reiser MF, Glaser C. Whole-body MR imaging in psoriatic arthritis: additional value for therapeutic decision making. Eur J Radiol 2011; 77 (1) 149-155
• 21 Poggenborg RP, Eshed I, Østergaard M , et al. Enthesitis in patients with psoriatic arthritis, axial spondyloarthritis and healthy subjects assessed by ‘head-to-toe’ whole-body MRI and clinical examination. Ann Rheum Dis 2015; 74 (5) 823-829
• 22 Poggenborg RP, Wiell C, Bøyesen P , et al. No overall damage progression despite persistent inflammation in adalimumab-treated psoriatic arthritis patients: results from an investigator-initiated 48-week comparative magnetic resonance imaging, computed tomography and radiography trial. Rheumatology (Oxford) 2014; 53 (4) 746-756
• 23 Khan MA. Newer clinical and radiographic features of seronegative spondyloarthropathies. Curr Opin Rheumatol 1989; 1 (2) 139-143
• 24 Althoff CE, Sieper J, Song IH , et al. Active inflammation and structural change in early active axial spondyloarthritis as detected by whole-body MRI. Ann Rheum Dis 2013; 72 (6) 967-973
• 25 Barkham N, Keen HI, Coates LC , et al. Clinical and imaging efficacy of infliximab in HLA-B27-Positive patients with magnetic resonance imaging-determined early sacroiliitis. Arthritis Rheum 2009; 60 (4) 946-954
• 26 Rudwaleit M, Schwarzlose S, Hilgert ES, Listing J, Braun J, Sieper J. MRI in predicting a major clinical response to anti-tumour necrosis factor treatment in ankylosing spondylitis. Ann Rheum Dis 2008; 67 (9) 1276-1281
• 27 Rudwaleit M, Landewé R, van der Heijde D , et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part I): classification of paper patients by expert opinion including uncertainty appraisal. Ann Rheum Dis 2009; 68 (6) 770-776
• 28 Rudwaleit M, van der Heijde D, Landewé R , et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis 2009; 68 (6) 777-783
• 29 Mandl P, Navarro-Compán V, Terslev L , et al; European League Against Rheumatism (EULAR). EULAR recommendations for the use of imaging in the diagnosis and management of spondyloarthritis in clinical practice. Ann Rheum Dis 2015; 74 (7) 1327-1339
• 30 Aydin SZ, Maksymowych WP, Bennett AN, McGonagle D, Emery P, Marzo-Ortega H. Validation of the ASAS criteria and definition of a positive MRI of the sacroiliac joint in an inception cohort of axial spondyloarthritis followed up for 8 years. Ann Rheum Dis 2012; 71 (1) 56-60
• 31 Hermann KG, Baraliakos X, van der Heijde DM , et al; Assessment in SpondyloArthritis international Society (ASAS). Descriptions of spinal MRI lesions and definition of a positive MRI of the spine in axial spondyloarthritis: a consensual approach by the ASAS/OMERACT MRI study group. Ann Rheum Dis 2012; 71 (8) 1278-1288
• 32 Landewé RB, Hermann KG, van der Heijde DM , et al. Scoring sacroiliac joints by magnetic resonance imaging. A multiple-reader reliability experiment. J Rheumatol 2005; 32 (10) 2050-2055
• 33 Krohn M, Braum LS, Sieper J , et al. Erosions and fatty lesions of sacroiliac joints in patients with axial spondyloarthritis: evaluation of different MRI techniques and two scoring methods. J Rheumatol 2014; 41 (3) 473-480
• 34 Maksymowych WP, Inman RD, Salonen D , et al. Spondyloarthritis Research Consortium of Canada magnetic resonance imaging index for assessment of spinal inflammation in ankylosing spondylitis. Arthritis Rheum 2005; 53 (4) 502-509
• 35 Maksymowych WP, Inman RD, Salonen D , et al. Spondyloarthritis research Consortium of Canada magnetic resonance imaging index for assessment of sacroiliac joint inflammation in ankylosing spondylitis. Arthritis Rheum 2005; 53 (5) 703-709
• 36 Mager AK, Althoff CE, Sieper J, Hamm B, Hermann KG. Role of whole-body magnetic resonance imaging in diagnosing early spondyloarthritis. Eur J Radiol 2009; 71 (2) 182-188
• 37 Weber U, Pfirrmann CW, Kissling RO, Hodler J, Zanetti M. Whole body MR imaging in ankylosing spondylitis: a descriptive pilot study in patients with suspected early and active confirmed ankylosing spondylitis. BMC Musculoskelet Disord 2007; 8: 20
• 38 Weber U, Hodler J, Kubik RA , et al. Sensitivity and specificity of spinal inflammatory lesions assessed by whole-body magnetic resonance imaging in patients with ankylosing spondylitis or recent-onset inflammatory back pain. Arthritis Rheum 2009; 61 (7) 900-908
• 39 Weber U, Hodler J, Jurik AG , et al. Assessment of active spinal inflammatory changes in patients with axial spondyloarthritis: validation of whole body MRI against conventional MRI. Ann Rheum Dis 2010; 69 (4) 648-653
• 40 Bennett AN, Marzo-Ortega H, Rehman A, Emery P, McGonagle D ; Leeds Spondyloarthropathy Group. The evidence for whole-spine MRI in the assessment of axial spondyloarthropathy. Rheumatology (Oxford) 2010; 49 (3) 426-432
• 41 Eshed I, Bollow M, McGonagle DG , et al. MRI of enthesitis of the appendicular skeleton in spondyloarthritis. Ann Rheum Dis 2007; 66 (12) 1553-1559
• 42 Muche B, Bollow M, François RJ, Sieper J, Hamm B, Braun J. Anatomic structures involved in early- and late-stage sacroiliitis in spondylarthritis: a detailed analysis by contrast-enhanced magnetic resonance imaging. Arthritis Rheum 2003; 48 (5) 1374-1384
• 43 Karpitschka M, Godau-Kellner P, Kellner H , et al. Assessment of therapeutic response in ankylosing spondylitis patients undergoing anti-tumour necrosis factor therapy by whole-body magnetic resonance imaging. Eur Radiol 2013; 23 (7) 1773-1784
• 44 Chary-Valckenaere I, d'Agostino MA, Loeuille D. Role for imaging studies in ankylosing spondylitis. Joint Bone Spine 2011; 78 (2) 138-143
• 45 Bredella MA, Steinbach LS, Morgan S, Ward M, Davis JC. MRI of the sacroiliac joints in patients with moderate to severe ankylosing spondylitis. AJR Am J Roentgenol 2006; 187 (6) 1420-1426
• 46 Gezmis E, Donmez FY, Agildere M. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol 2013; 82 (12) 2316-2321
• 47 Bozgeyik Z, Ozgocmen S, Kocakoc E. Role of diffusion-weighted MRI in the detection of early active sacroiliitis. AJR Am J Roentgenol 2008; 191 (4) 980-986
• 48 Weber U, Zubler V, Zhao Z , et al. Does spinal MRI add incremental diagnostic value to MRI of the sacroiliac joints alone in patients with non-radiographic axial spondyloarthritis?. Ann Rheum Dis 2015; 74 (6) 985-992
• 49 van der Heijde D, Sieper J, Maksymowych WP , et al. Spinal inflammation in the absence of sacroiliac joint inflammation on magnetic resonance imaging in patients with active nonradiographic axial spondyloarthritis. Arthritis Rheum (Munch) 2014; 66 (3) 667-673
• 50 Guérin-Pfyffer S, Guillaume-Czitrom S, Tammam S, Koné-Paut I. Evaluation of chronic recurrent multifocal osteitis in children by whole-body magnetic resonance imaging. Joint Bone Spine 2012; 79 (6) 616-620
• 51 Coates LC, Hodgson R, Conaghan PG, Freeston JE. MRI and ultrasonography for diagnosis and monitoring of psoriatic arthritis. Best Pract Res Clin Rheumatol 2012; 26 (6) 805-822
• 52 Chamot AM, Benhamou CL, Kahn MF, Beraneck L, Kaplan G, Prost A. Acne-pustulosis-hyperostosis-osteitis syndrome. Results of a national survey. 85 cases [in French]. Rev Rhum Mal Osteoartic 1987; 54 (3) 187-196
• 53 Crouzet J, Claudepierre P, Aribi EH , et al. Two cases of discitis due to Propionibacterium acnes. Rev Rhum Engl Ed 1998; 65 (1) 68-71
• 54 Earwaker JW, Cotten A. SAPHO: syndrome or concept? Imaging findings. Skeletal Radiol 2003; 32 (6) 311-327
• 55 Parlier-Cuau C, Laredo J. Vertebral involvement in SAPHO syndrome [in French]. J Radiol 2010; 91 (9 Pt 2): 1068-1078
• 56 Magrey M, Khan MA. New insights into synovitis, acne, pustulosis, hyperostosis, and osteitis (SAPHO) syndrome. Curr Rheumatol Rep 2009; 11 (5) 329-333
• 57 Sundaram M, McDonald D, Engel E, Rotman M, Siegfried EC. Chronic recurrent multifocal osteomyelitis: an evolving clinical and radiological spectrum. Skeletal Radiol 1996; 25 (4) 333-336
• 58 Jurik AG. Chronic recurrent multifocal osteomyelitis. Semin Musculoskelet Radiol 2004; 8 (3) 243-253
• 59 Mammen AL. Skeletal muscle involvement. In: Varga J, Denton CP, Wigley FM, eds. Scleroderma: From Pathogenesis to Comprehensive Management. London, UK: Springer; 2012: 525-529
• 60 Avouac J, Walker UA, Hachulla E , et al; the EUSTAR collaborators*; the EUSTAR collaborators. Joint and tendon involvement predict disease progression in systemic sclerosis: a EUSTAR prospective study. Ann Rheum Dis 2014;
• 61 West SG, Killian PJ, Lawless OJ. Association of myositis and myocarditis in progressive systemic sclerosis. Arthritis Rheum 1981; 24 (5) 662-668
• 62 Abdel-Magied RA, Lotfi A, AbdelGawad EA. Magnetic resonance imaging versus musculoskeletal ultrasonography in detecting inflammatory arthropathy in systemic sclerosis patients with hand arthralgia. Rheumatol Int 2013; 33 (8) 1961-1966
• 63 Akbayrak E, Dinser R, Müller-Ladner U, Tarner IH. Low-field magnetic resonance imaging study on carpal arthritis in systemic sclerosis—low-grade erosive arthritis of carpal bones is an unexpected and frequent disease manifestation. Arthritis Res Ther 2013; 15 (1) R2
• 64 Schanz S, Henes J, Ulmer A , et al. Response evaluation of musculoskeletal involvement in patients with deep morphea treated with methotrexate and prednisolone: a combined MRI and clinical approach. AJR Am J Roentgenol 2013; 200 (4) W376-W382
• 65 Ranque B, Authier FJ, Le-Guern V , et al. A descriptive and prognostic study of systemic sclerosis-associated myopathies. Ann Rheum Dis 2009; 68 (9) 1474-1477
• 66 Bohan A, Peter JB. Polymyositis and dermatomyositis (first of two parts). N Engl J Med 1975; 292 (7) 344-347
• 67 Bohan A, Peter JB. Polymyositis and dermatomyositis (second of two parts). N Engl J Med 1975; 292 (8) 403-407
• 68 Shelly MJ, Bolster F, Foran P, Crosbie I, Kavanagh EC, Eustace SJ. Whole-body magnetic resonance imaging in skeletal muscle disease. Semin Musculoskelet Radiol 2010; 14 (1) 47-56
• 69 Farber JM, Buckwalter KA. MR imaging in nonneoplastic muscle disorders of the lower extremity. Radiol Clin North Am 2002; 40 (5) 1013-1031
• 70 Yoshida K, Kurosaka D, Joh K , et al. Fasciitis as a common lesion of dermatomyositis, demonstrated early after disease onset by en bloc biopsy combined with magnetic resonance imaging. Arthritis Rheum 2010; 62 (12) 3751-3759
• 71 Cantwell C, Ryan M, O'Connell M , et al. A comparison of inflammatory myopathies at whole-body turbo STIR MRI. Clin Radiol 2005; 60 (2) 261-267
• 72 Walker UA. Imaging tools for the clinical assessment of idiopathic inflammatory myositis. Curr Opin Rheumatol 2008; 20 (6) 656-661
• 73 Del Grande F, Carrino JA, Del Grande M, Mammen AL, Christopher Stine L. Magnetic resonance imaging of inflammatory myopathies. Top Magn Reson Imaging 2011; 22 (2) 39-43
• 74 Mercuri E, Pichiecchio A, Allsop J, Messina S, Pane M, Muntoni F. Muscle MRI in inherited neuromuscular disorders: past, present, and future. J Magn Reson Imaging 2007; 25 (2) 433-440
• 75 Brennan DD, Whelan PF, Robinson K , et al. Rapid automated measurement of body fat distribution from whole-body MRI. AJR Am J Roentgenol 2005; 185 (2) 418-423
• 76 Shulman LE. Diffuse fasciitis with eosinophilia: a new syndrome?. Trans Assoc Am Physicians 1975; 88: 70-86
• 77 Kirchgesner T, Dallaudière B, Omoumi P , et al. Eosinophilic fasciitis: typical abnormalities, variants and differential diagnosis of fasciae abnormalities using MR imaging. Diagn Interv Imaging 2015; 96 (4) 341-348
• 78 Baumann F, Brühlmann P, Andreisek G, Michel BA, Marincek B, Weishaupt D. MRI for diagnosis and monitoring of patients with eosinophilic fasciitis. AJR Am J Roentgenol 2005; 184 (1) 169-174
• 79 Moulton SJ, Kransdorf MJ, Ginsburg WW, Abril A, Persellin S. Eosinophilic fasciitis: spectrum of MRI findings. AJR Am J Roentgenol 2005; 184 (3) 975-978
• 80 Sekine T, Amano Y, Hidaka F , et al. Hepatosplenic and muscular sarcoidosis: characterization with MR imaging. Magn Reson Med Sci 2012; 11 (2) 83-89
• 81 Wieërs G, Lhommel R, Lecouvet F, Van den Bergh P, Lambert M. A tiger man. Lancet 2012; 380 (9856) 1859
• 82 Mangino D, Stover DE. Sarcoidosis presenting as metastatic bony disease. A case report and review of the literature on vertebral body sarcoidosis. Respiration 2004; 71 (3) 292-294
• 83 Kuzyshyn H, Feinstein D, Kolasinski SL, Eid H. Osseous sarcoidosis: a case series. Rheumatol Int 2015; 35 (5) 925-933
• 84 Atkin KL, Ditchfield MR. The role of whole-body MRI in pediatric oncology. J Pediatr Hematol Oncol 2014; 36 (5) 342-352
• 85 Dallaudière B, Kerger J, Malghem J, Galant C, Lecouvet FE. Adult onset asynchronous multifocal eosinophilic granuloma of bone: an 11-year follow-up. Acta Radiol Open 2015; 4 (2) 2047981614552217
• 86 Mueller WP, Melzer HI, Schmid I, Coppenrath E, Bartenstein P, Pfluger T. The diagnostic value of 18F-FDG PET and MRI in paediatric histiocytosis. Eur J Nucl Med Mol Imaging 2013; 40 (3) 356-363
• 87 Miettunen PM, Lafay-Cousin L, Guilcher GM, Nettel-Aguirre A, Moorjani V. Widespread osteonecrosis in children with leukemia revealed by whole-body MRI. Clin Orthop Relat Res 2012; 470 (12) 3587-3595
• 88 Schmidt GP, Reiser MF, Baur-Melnyk A. Whole-body imaging of the musculoskeletal system: the value of MR imaging. Skeletal Radiol 2007; 36 (12) 1109-1119
• 89 Nguyen R, Jett K, Harris GJ, Cai W, Friedman JM, Mautner VF. Benign whole body tumor volume is a risk factor for malignant peripheral nerve sheath tumors in neurofibromatosis type 1. J Neurooncol 2014; 116 (2) 307-313
• 90 Van Meerbeeck SF, Verstraete KL, Janssens S, Mortier G. Whole body MR imaging in neurofibromatosis type 1. Eur J Radiol 2009; 69 (2) 236-242
• 91 Teixeira SR, Elias Junior J, Nogueira-Barbosa MH, Guimarães MD, Marchiori E, Santos MK. Whole-body magnetic resonance imaging in children: state of the art. Radiol Bras 2015; 48 (2) 111-120