Download PDF
CC BY-NC-ND 4.0 · Semin Musculoskelet Radiol 2023; 27(01): 091-102
DOI: 10.1055/s-0043-1761496
Review Article

Axial Skeleton Bone Marrow Changes in Inflammatory Rheumatologic Disorders

Monique Reijnierse
1   Musculoskeletal Radiology, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

Magnetic resonance imaging (MRI) of the axial skeleton, spine, and sacroiliac (SI) joints is critical for the early detection and follow-up of inflammatory rheumatologic disorders such as axial spondyloarthritis, rheumatoid arthritis, and SAPHO/CRMO (synovitis, acne, pustulosis, hyperostosis, and osteitis/chronic recurrent multifocal osteomyelitis). To offer a valuable report to the referring physician, disease-specific knowledge is essential. Certain MRI parameters can help the radiologist provide an early diagnosis and lead to effective treatment. Awareness of these hallmarks may help avoid misdiagnosis and unnecessary biopsies. A bone marrow edema-like signal plays an important role in reports but is not disease specific. Age, sex, and history should be considered in interpreting MRI to prevent overdiagnosis of rheumatologic disease. Differential diagnoses—degenerative disk disease, infection, and crystal arthropathy—are addressed here. Whole-body MRI may be helpful in diagnosing SAPHO/CRMO.

Keywords

spondyloarthritis - magnetic resonance imaging - sacroiliitis - SAPHO - inflammatory rheumatologic disease


Publication History

Article published online:
03 March 2023

© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Bloem JL, Reijnierse M, Huizinga TWJ, van der Helm-van Mil AHM. MR signal intensity: staying on the bright side in MR image interpretation. RMD Open 2018; 4 (01) e000728
    CrossrefPubMedGoogle Scholar
  • 2 Stomp W, Krabben A, van der Heijde D. et al. Aiming for a shorter rheumatoid arthritis MRI protocol: can contrast-enhanced MRI replace T2 for the detection of bone marrow oedema?. Eur Radiol 2014; 24 (10) 2614-2622
    CrossrefPubMedGoogle Scholar
  • 3 Mayerhoefer ME, Breitenseher MJ, Kramer J, Aigner N, Norden C, Hofmann S. STIR vs. T1-weighted fat-suppressed gadolinium-enhanced MRI of bone marrow edema of the knee: computer-assisted quantitative comparison and influence of injected contrast media volume and acquisition parameters. J Magn Reson Imaging 2005; 22 (06) 788-793
    CrossrefPubMedGoogle Scholar
  • 4 Schmid MR, Hodler J, Vienne P, Binkert CA, Zanetti M. Bone marrow abnormalities of foot and ankle: STIR versus T1-weighted contrast-enhanced fat-suppressed spin-echo MR imaging. Radiology 2002; 224 (02) 463-469
    CrossrefPubMedGoogle Scholar
  • 5 Tamai M, Kawakami A, Uetani M. et al. Magnetic resonance imaging (MRI) detection of synovitis and bone lesions of the wrists and finger joints in early-stage rheumatoid arthritis: comparison of the accuracy of plain MRI-based findings and gadolinium-diethylenetriamine pentaacetic acid-enhanced MRI-based findings. Mod Rheumatol 2012; 22 (05) 654-658
    CrossrefPubMedGoogle Scholar
  • 6 Appel H, Loddenkemper C, Grozdanovic Z. et al. Correlation of histopathological findings and magnetic resonance imaging in the spine of patients with ankylosing spondylitis. Arthritis Res Ther 2006; 8 (05) R143
    CrossrefPubMedGoogle Scholar
  • 7 McQueen FM, Gao A, Ostergaard M. et al. High-grade MRI bone oedema is common within the surgical field in rheumatoid arthritis patients undergoing joint replacement and is associated with osteitis in subchondral bone. Ann Rheum Dis 2007; 66 (12) 1581-1587
    CrossrefPubMedGoogle Scholar
  • 8 Jimenez-Boj E, Nöbauer-Huhmann I, Hanslik-Schnabel B. et al. Bone erosions and bone marrow edema as defined by magnetic resonance imaging reflect true bone marrow inflammation in rheumatoid arthritis. Arthritis Rheum 2007; 56 (04) 1118-1124
    CrossrefPubMedGoogle Scholar
  • 9 McQueen FM. Bone marrow edema and osteitis in rheumatoid arthritis: the imaging perspective. Arthritis Res Ther 2012; 14 (05) 224-236
    CrossrefPubMedGoogle Scholar
  • 10 Zanetti M, Bruder E, Romero J, Hodler J. Bone marrow edema pattern in osteoarthritic knees: correlation between MR imaging and histologic findings. Radiology 2000; 215 (03) 835-840
    CrossrefPubMedGoogle Scholar
  • 11 Taljanovic MS, Graham AR, Benjamin JB. et al. Bone marrow edema pattern in advanced hip osteoarthritis: quantitative assessment with magnetic resonance imaging and correlation with clinical examination, radiographic findings, and histopathology. Skeletal Radiol 2008; 37 (05) 423-431
    CrossrefPubMedGoogle Scholar
  • 12 Craig JG, Amin MB, Wu K. et al. Osteomyelitis of the diabetic foot: MR imaging-pathologic correlation. Radiology 1997; 203 (03) 849-855
    CrossrefPubMedGoogle Scholar
  • 13 Assmann G, Simon P. The SAPHO syndrome—are microbes involved?. Best Pract Res Clin Rheumatol 2011; 25 (03) 423-434
    CrossrefPubMedGoogle Scholar
  • 14 Sudoł-Szopińska I, Jurik AG, Eshed I. et al. Recommendations of the ESSR Arthritis Subcommittee for the Use of Magnetic Resonance Imaging in Musculoskeletal Rheumatic Diseases. Semin Musculoskelet Radiol 2015; 19 (04) 396-411
    Article in Thieme ConnectPubMedGoogle Scholar
  • 15 Rudwaleit M, Jurik AG, Hermann KG. et al. Defining active sacroiliitis on magnetic resonance imaging (MRI) for classification of axial spondyloarthritis: a consensual approach by the ASAS/OMERACT MRI group. Ann Rheum Dis 2009; 68 (10) 1520-1527
    CrossrefPubMedGoogle Scholar
  • 16 de Hooge M, van den Berg R, Navarro-Compán V. et al. Magnetic resonance imaging of the sacroiliac joints in the early detection of spondyloarthritis: no added value of gadolinium compared with short tau inversion recovery sequence. Rheumatology (Oxford) 2013; 52 (07) 1220-1224
    CrossrefPubMedGoogle Scholar
  • 17 Özgen A. The value of the T2-weighted multipoint Dixon sequence in MRI of sacroiliac joints for the diagnosis of active and chronic sacroiliitis. AJR Am J Roentgenol 2017; 208 (03) 603-608
    CrossrefPubMedGoogle Scholar
  • 18 Eggers H, Börnert P. Chemical shift encoding-based water-fat separation methods. J Magn Reson Imaging 2014; 40 (02) 251-268
    CrossrefPubMedGoogle Scholar
  • 19 Lecouvet FE. Whole-body MR. Imaging: musculoskeletal applications. Radiology 2016; 279 (02) 345-365
    CrossrefPubMedGoogle Scholar
  • 20 Khan MA. Update on spondyloarthropathies. Ann Intern Med 2002; 136 (12) 896-907
    CrossrefPubMedGoogle Scholar
  • 21 Reijnierse M, Eshed I, Gaalen FV. Top-ten tips for effective imaging of axial spondyloarthritis. Semin Musculoskelet Radiol 2019; 23 (04) 376-391
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Rudwaleit M, van der Heijde D, Landewé R. et al. The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann Rheum Dis 2011; 70 (01) 25-31
    CrossrefPubMedGoogle Scholar
  • 23 Callhoff J, Sieper J, Weiß A, Zink A, Listing J. Efficacy of TNFα blockers in patients with ankylosing spondylitis and non-radiographic axial spondyloarthritis: a meta-analysis. Ann Rheum Dis 2015; 74 (06) 1241-1248
    CrossrefPubMedGoogle Scholar
  • 24 van der Heijde D, Schiff MH, Sieper J. et al; ATLAS Study Group. Adalimumab effectiveness for the treatment of ankylosing spondylitis is maintained for up to 2 years: long-term results from the ATLAS trial. Ann Rheum Dis 2009; 68 (06) 922-929
    CrossrefPubMedGoogle Scholar
  • 25 Feldtkeller E, Bruckel J, Khan MA. Scientific contributions of ankylosing spondylitis patient advocacy groups. Curr Opin Rheumatol 2000; 12 (04) 239-247
    CrossrefPubMedGoogle Scholar
  • 26 Dean LE, Jones GT, MacDonald AG, Downham C, Sturrock RD, Macfarlane GJ. Global prevalence of ankylosing spondylitis. Rheumatology (Oxford) 2014; 53 (04) 650-657
    CrossrefPubMedGoogle Scholar
  • 27 Ez-Zaitouni Z, Bakker PA, van Lunteren M. et al. The yield of a positive MRI of the spine as imaging criterion in the ASAS classification criteria for axial spondyloarthritis: results from the SPACE and DESIR cohorts. Ann Rheum Dis 2017; 76 (10) 1731-1736
    CrossrefPubMedGoogle Scholar
  • 28 Benjamin M, McGonagle D. The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites. J Anat 2001; 199 (Pt 5): 503-526
    CrossrefPubMedGoogle Scholar
  • 29 Schett G, Lories RJ, D'Agostino M-A. et al. Enthesitis: from pathophysiology to treatment. Nat Rev Rheumatol 2017; 13 (12) 731-741
    CrossrefPubMedGoogle Scholar
  • 30 Navarro-Compán V, Sepriano A, El-Zorkany B, van der Heijde D. Axial spondyloarthritis. Ann Rheum Dis 2021; 80 (12) 1511-1521
    CrossrefPubMedGoogle Scholar
  • 31 Resnick D. Ankylosing spondylitis. In: Resnick D. ed. Articular Diseases. Philadelphia, PA: WB Saunders; 2002. . Diagnosis of Bone and Joint Disorders; 4th ed, vol 2: 1023-1081
    Google Scholar
  • 32 Reijnierse M. Radiographic/MR imaging correlation of paravertebral ossifications in ligaments and bony vertebral outgrowths. Anatomy, early detection and clinical impact. Magn Reson Imaging Clin N Am 2019; 27 (04) 641-659
    CrossrefPubMedGoogle Scholar
  • 33 van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 1984; 27 (04) 361-368
    CrossrefPubMedGoogle Scholar
  • 34 Lambert RG, Bakker PA, van der Heijde D. et al. Defining active sacroiliitis on MRI for classification of axial spondyloarthritis: update by the ASAS MRI working group. Ann Rheum Dis 2016; 75 (11) 1958-1963
    CrossrefPubMedGoogle Scholar
  • 35 Schueller-Weidekamm C, Mascarenhas VV, Sudol-Szopinska I. et al. Imaging and interpretation of axial spondylarthritis: the radiologist's perspective—consensus of the Arthritis Subcommittee of the ESSR. Semin Musculoskelet Radiol 2014; 18 (03) 265-279
    Article in Thieme ConnectPubMedGoogle Scholar
  • 36 Weber U, Maksymowych WP, Chan SM. et al. Does evaluation of the ligamentous compartment enhance diagnostic utility of sacroiliac joint MRI in axial spondyloarthritis?. Arthritis Res Ther 2015; 17 (01) 246
    CrossrefPubMedGoogle Scholar
  • 37 Jans L, Coeman L, Van Praet L. et al. How sensitive and specific are MRI features of sacroiliitis for diagnosis of spondyloarthritis in patients with inflammatory back pain?. JBR-BTR 2014; 97 (04) 202-205
    PubMedGoogle Scholar
  • 38 Weber U, Pedersen SJ, Østergaard M, Rufibach K, Lambert RG, Maksymowych WP. Can erosions on MRI of the sacroiliac joints be reliably detected in patients with ankylosing spondylitis? A cross-sectional study. Arthritis Res Ther 2012; 14 (03) R124
    CrossrefPubMedGoogle Scholar
  • 39 Eshed I, Lidar M. Fat metaplasia in inflammatory sacroiliitis and in nonrheumatic conditions: a step toward better characterization. J Rheumatol 2018; 45 (07) 884-886
    CrossrefPubMedGoogle Scholar
  • 40 Ziegeler K, Eshkal H, Schorr C. et al. Age- and sex-dependent frequency of fat metaplasia and other structural changes of the sacroiliac joints in patients without axial spondyloarthritis: a retrospective, cross-sectional MRI study. J Rheumatol 2018; 45 (07) 915-921
    CrossrefPubMedGoogle Scholar
  • 41 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 (08) 1278-1288
    CrossrefPubMedGoogle Scholar
  • 42 Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010; 376 (9746): 1094-1108
    CrossrefPubMedGoogle Scholar
  • 43 Ajeganova S, van Steenbergen HW, van Nies JA, Burgers LE, Huizinga TW, van der Helm-van Mil AH. Disease-modifying antirheumatic drug-free sustained remission in rheumatoid arthritis: an increasingly achievable outcome with subsidence of disease symptoms. Ann Rheum Dis 2016; 75 (05) 867-873
    CrossrefPubMedGoogle Scholar
  • 44 van der Woude D, van der Helm-van Mil AHM. Update on the epidemiology, risk factors, and disease outcomes of rheumatoid arthritis. Best Pract Res Clin Rheumatol 2018; 32 (02) 174-187
    CrossrefPubMedGoogle Scholar
  • 45 den Hollander NK, Verstappen M, Sidhu N, van Mulligen E, Reijnierse M, van der Helm-van Mil AHM. Hand and foot MRI in contemporary undifferentiated arthritis: in which patients is MRI valuable to detect rheumatoid arthritis early? A large prospective study. Rheumatology (Oxford) 2022; 61 (10) 3963-3973
    CrossrefPubMedGoogle Scholar
  • 46 Nieuwenhuis WP, van Steenbergen HW, Stomp W. et al. The course of bone marrow edema in early undifferentiated arthritis and rheumatoid arthritis: a longitudinal magnetic resonance imaging study at bone level. Arthritis Rheumatol 2016; 68 (05) 1080-1088
    CrossrefPubMedGoogle Scholar
  • 47 Narváez JA, Narváez J, Serrallonga M. et al. Cervical spine involvement in rheumatoid arthritis: correlation between neurological manifestations and magnetic resonance imaging findings. Rheumatology (Oxford) 2008; 47 (12) 1814-1819
    CrossrefPubMedGoogle Scholar
  • 48 Reijnierse M, Helm-Mil AV, Eshed I, Schueller-Weidekamm C. Magnetic resonance imaging of rheumatoid arthritis: peripheral joints and spine. Semin Musculoskelet Radiol 2018; 22 (02) 127-146
    Article in Thieme ConnectPubMedGoogle Scholar
  • 49 Depasquale R, Kumar N, Lalam RK. et al. SAPHO: What radiologists should know. Clin Radiol 2012; 67 (03) 195-206
    CrossrefPubMedGoogle Scholar
  • 50 Magrey M, Khan MA. New insights into synovitis, acne, pustulosis, hyperostosis, and osteitis (SAPHO) syndrome. Curr Rheumatol Rep 2009; 11 (05) 329-333
    CrossrefPubMedGoogle Scholar
  • 51 Leone A, Cassar-Pullicino VN, Casale R, Magarelli N, Semprini A, Colosimo C. The SAPHO syndrome revisited with an emphasis on spinal manifestations. Skeletal Radiol 2015; 44 (01) 9-24
    CrossrefPubMedGoogle Scholar
  • 52 Zhang LH, Han SB, Song L. et al. Comparative analysis and differentiation between SAPHO syndrome and spondyloarthropathies using whole-spine MRI. Clin Radiol 2021; 76 (05) 394.e9-394.e14
    CrossrefPubMedGoogle Scholar
  • 53 McGauvran AM, Kotsenas AL, Diehn FE, Wald JT, Carr CM, Morris JM. SAPHO syndrome: imaging findings of vertebral involvement. AJNR Am J Neuroradiol 2016; 37 (08) 1567-1572
    CrossrefPubMedGoogle Scholar
  • 54 Shah A, Rosenkranz M, Thapa M. Review of spinal involvement in chronic recurrent multifocal osteomyelitis (CRMO): what radiologists need to know about CRMO and its imitators. Clin Imaging 2022; 81: 122-135
    CrossrefPubMedGoogle Scholar
  • 55 Arnoldi AP, Schlett CL, Douis H. et al. Whole-body MRI in patients with non-bacterial osteitis: radiological findings and correlation with clinical data. Eur Radiol 2017; 27 (06) 2391-2399
    CrossrefPubMedGoogle Scholar
  • 56 de Bruin F, ter Horst S, Bloem HL. et al. Prevalence of degenerative changes of the spine on magnetic resonance images and radiographs in patients aged 16-45 years with chronic back pain of short duration in the Spondyloarthritis Caught Early (SPACE) cohort. Rheumatology (Oxford) 2016; 55 (01) 56-65
    CrossrefPubMedGoogle Scholar
  • 57 Modic MT, Steinberg PM, Ross JS, Masaryk TJ, Carter JR. Degenerative disk disease: assessment of changes in vertebral body marrow with MR imaging. Radiology 1988; 166 (1 Pt 1): 193-199
    CrossrefPubMedGoogle Scholar
  • 58 de Bruin F, Treyvaud MO, Feydy A. et al. Prevalence of degenerative changes and overlap with spondyloarthritis-associated lesions in the spine of patients from the DESIR cohort. RMD Open 2018; 4 (01) e000657
    CrossrefPubMedGoogle Scholar
  • 59 Resnick D, Niwayama G. Radiographic and pathologic features of spinal involvement in diffuse idiopathic skeletal hyperostosis (DISH). Radiology 1976; 119 (03) 559-568
    CrossrefPubMedGoogle Scholar
  • 60 Reijnierse M, Schwabl C, Klauser A. Imaging of crystal disorders: calcium hydroxyapatite crystal deposition disease (HADD), calcium pyrophosphate dihydrate crystal deposition disease (CPPD), and gout. Pathophysiology, imaging and diagnosis. Radiol Clin North Am 2022; 60 (04) 641-656
    PubMedGoogle Scholar
  • 61 Weber U, Jurik AG, Zejden A. et al. Frequency and anatomic distribution of magnetic resonance imaging features in the sacroiliac joints of young athletes: exploring “background noise” toward a data-driven definition of sacroiliitis in early spondyloarthritis. Arthritis Rheumatol 2018; 70 (05) 736-745
    CrossrefPubMedGoogle Scholar
  • 62 Agten CA, Zubler V, Zanetti M. et al. Postpartum bone marrow edema at the sacroiliac joints may mimic sacroiliitis of axial spondyloarthritis on MRI. AJR Am J Roentgenol 2018; 211 (06) 1306-1312
    CrossrefPubMedGoogle Scholar
  • 63 Germann C, Kroismayr D, Brunner F, Pfirrmann CWA, Sutter R, Zubler V. Influence of pregnancy/childbirth on long-term bone marrow edema and subchondral sclerosis of sacroiliac joints. Skeletal Radiol 2021; 50 (08) 1617-1628
    CrossrefPubMedGoogle Scholar
  • 64 Kang Y, Hong SH, Kim JY. et al. Unilateral sacroiliitis: differential diagnosis between infectious sacroiliitis and spondyloarthritis based on MRI findings. AJR Am J Roentgenol 2015; 205 (05) 1048-1055
    CrossrefPubMedGoogle Scholar