Magnetic Resonance Imaging of Accelerated Bone Remodeling

Bruno C. Vande Berg; Charbel Mourad; Patrick Omoumi; Jacques Malghem

doi:10.1055/s-0043-1761611

Seminars in Musculoskeletal Radiology, Table of Contents

Semin Musculoskelet Radiol 2023; 27(01): 114-123
DOI: 10.1055/s-0043-1761611

Review Article

Magnetic Resonance Imaging of Accelerated Bone Remodeling

Authors

Bruno C. Vande Berg

¹Department of Radiology, Musculoskeletal Section, Centre Hospitalier Chrétien, CHC, Clinique Mont Legia, Liege, Belgium
Charbel Mourad

²Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland

³Department of Diagnostic and Interventional Radiology, Hôpital Libanais Geitaoui- CHU, Beyrouth, Lebanon
Patrick Omoumi

²Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland
Jacques Malghem

⁴Department of Radiology, Cliniques Universitaires Saint-Luc Université Catholique de Louvain, Brussels, Belgium

Abstract

A regional acceleration of bone remodeling may possibly follow biomechanical insults to the bone. This review assesses the literature and clinical arguments supporting the hypothetical association between accelerated bone remodeling and bone marrow edema (BME)-like signal intensity on magnetic resonance imaging. BME-like signal is defined as a confluent ill-delimited area of bone marrow with a moderate decrease in signal intensity on fat-sensitive sequences and a high signal intensity on fat-suppressed fluid-sensitive sequences. In addition to this confluent pattern, a linear subcortical pattern and a patchy disseminated pattern have also been recognized on fat-suppressed fluid-sensitive sequences. These particular BME-like patterns may remain occult on T1-weighted spin-echo images. We hypothesize that these BME-like patterns, with particular characteristics in terms of distribution and signal, are associated with accelerated bone remodeling. Limitations in recognizing these BME-like patterns are also discussed.

Keywords

bone remodeling - regional acceleratory phenomenon - bone turnover - bone marrow edema - magnetic resonance imaging

Full Text

References

References
1 Raggatt LJ, Partridge NC. Cellular and molecular mechanisms of bone remodeling. J Biol Chem 2010; 285 (33) 25103-25108
2 Eriksen EF. Cellular mechanisms of bone remodeling. Rev Endocr Metab Disord 2010; 11 (04) 219-227
3 Frost HM. The regional acceleratory phenomenon: a review. Henry Ford Hosp Med J 1983; 31 (01) 3-9
4 Frost HM. From Wolff's law to the Utah paradigm: insights about bone physiology and its clinical applications. Anat Rec 2001; 262 (04) 398-419
5 Frost HM. Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 2003; 275 (02) 1081-1101
6 Allman RM, Brower AC. Circulatory patterns of deossification. Radiol Clin North Am 1981; 19 (04) 553-569
7 Wilson AJ, Murphy WA, Hardy DC, Totty WG. Transient osteoporosis: transient bone marrow edema?. Radiology 1988; 167 (03) 757-760
8 Gorbachova T, Amber I, Beckmann NM. et al. Nomenclature of subchondral nonneoplastic bone lesions. AJR Am J Roentgenol 2019; 213 (05) 963-982
9 Palmer W, Bancroft L, Bonar F. et al. Glossary of terms for musculoskeletal radiology. Skeletal Radiol 2020; 49 (1, Suppl 1): 1-33
10 Pathria MN, Chung CB, Resnick DL. Acute and stress-related injuries of bone and cartilage: pertinent anatomy, basic biomechanics, and imaging perspective. Radiology 2016; 280 (01) 21-38
11 Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol 2008; 3 (Suppl. 03) S131-S139
12 Sims NA, Martin TJ. Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit. Bonekey Rep 2014; 3: 481
13 Tong X, Chen X, Zhang S. et al. The effect of exercise on the prevention of osteoporosis and bone angiogenesis. BioMed Res Int 2019; 2019: 8171897
14 Kang JH, Lee HJ, Kim OH, Yun YJ, Seo YJ, Lee HJ. Biomechanical forces enhance directed migration and activation of bone marrow-derived dendritic cells. Sci Rep 2021; 11 (01) 12106
15 Xu R, Yallowitz A, Qin A. et al. Targeting skeletal endothelium to ameliorate bone loss. Nat Med 2018; 24 (06) 823-833
16 Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 2014; 507 (7492): 323-328
17 Kular J, Tickner J, Chim SM, Xu J. An overview of the regulation of bone remodelling at the cellular level. Clin Biochem 2012; 45 (12) 863-873
18 Zhu S, Yao F, Qiu H, Zhang G, Xu H, Xu J. Coupling factors and exosomal packaging microRNAs involved in the regulation of bone remodelling. Biol Rev Camb Philos Soc 2018; 93 (01) 469-480
19 Yao Z, Lafage-Proust MH, Plouët J, Bloomfield S, Alexandre C, Vico L. Increase of both angiogenesis and bone mass in response to exercise depends on VEGF. J Bone Miner Res 2004; 19 (09) 1471-1480
20 Frost HM. The Utah paradigm of skeletal physiology: an overview of its insights for bone, cartilage and collagenous tissue organs. J Bone Miner Metab 2000; 18 (06) 305-316
21 Tyrovola JB, Odont X. The “mechanostat theory” of Frost and the OPG/RANKL/RANK system. J Cell Biochem 2015; 116 (12) 2724-2729
22 Matheny JB, Goff MG, Pownder SL. et al. An in vivo model of a mechanically-induced bone marrow lesion. J Biomech 2017; 64: 258-261
23 Zhen G, Wen C, Jia X. et al. Inhibition of TGF-β signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med 2013; 19 (06) 704-712
24 Schneider R. Radionuclide techniques. In: Resnick D. ed. Diagnosis of Bone and Joint Disorders. 4th ed. Philadelphia, PA: WB Saunders; 2002: 319-424
25 Järvinen J, Niinimäki J, Karppinen J, Takalo R, Haapea M, Tervonen O. Does bone scintigraphy show Modic changes associated with increased bone turnover?. Eur J Radiol Open 2020; 7: 100222
26 Watkins L, MacKay J, Haddock B. et al. Evaluating the relationship between dynamic Na[18F]F-uptake parameters and MRI knee osteoarthritic findings. J Nucl Med 2020; 61 (Suppl. 01) 182-182
27 Jena A, Taneja S, Rana P. et al. Emerging role of integrated PET-MRI in osteoarthritis. Skeletal Radiol 2021; 50 (12) 2349-2363
28 Jarraya M, Roemer FW, Bäuerle T, Kogan F, Guermazi A. PET imaging in osteoarthritis. PET Clin 2023; 18 (01) 21-29
29 Shabestari M, Vik J, Reseland JE, Eriksen EF. Bone marrow lesions in hip osteoarthritis are characterized by increased bone turnover and enhanced angiogenesis. Osteoarthritis Cartilage 2016; 24 (10) 1745-1752
30 Shabestari M, Kise NJ, Landin MA. et al. Enhanced angiogenesis and increased bone turnover characterize bone marrow lesions in osteoarthritis at the base of the thumb. Bone Joint Res 2018; 7 (06) 406-413
31 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
32 Bergin D, Hochberg H, Zoga AC, Qazi N, Parker L, Morrison WB. Indirect soft-tissue and osseous signs on knee MRI of surgically proven meniscal tears. AJR Am J Roentgenol 2008; 191 (01) 86-92
33 Lance V, Heilmeier UR, Joseph GB, Steinbach L, Ma B, Link TM. MR imaging characteristics and clinical symptoms related to displaced meniscal flap tears. Skeletal Radiol 2015; 44 (03) 375-384
34 White LM, Powell TI, Tomlinson G, Boynton E. Increased subcortical patellar signal intensity at T2-weighted MR imaging: a subacute finding after knee injury. Radiology 2005; 236 (03) 952-957
35 Gondim Teixeira PA, Balaj C, Marie B. et al. Linear signal hyperintensity adjacent to the subchondral bone plate at the knee on T2-weighted fat-saturated sequences: imaging aspects and association with structural lesions. Skeletal Radiol 2014; 43 (11) 1589-1598
36 Gondim Teixeira PA, Savi de Tové KM, Abou Arab W. et al. Subchondral linear hyperintensity of the femoral head: MR imaging findings and associations with femoro-acetabular joint pathology. Diagn Interv Imaging 2017; 98 (03) 245-252
37 Bailey JF, Miller SL, Khieu K. et al. From the international space station to the clinic: how prolonged unloading may disrupt lumbar spine stability. Spine J 2018; 18 (01) 7-14
38 Pal CR, Tasker AD, Ostlere SJ, Watson MS. Heterogeneous signal in bone marrow on MRI of children's feet: a normal finding?. Skeletal Radiol 1999; 28 (05) 274-278
39 Foster K, Chapman S, Johnson K. MRI of the marrow in the paediatric skeleton. Clin Radiol 2004; 59 (08) 651-673
40 Taccone A, Oddone M, Dell'Acqua AD, Occhi M, Ciccone MA. MRI “road-map” of normal age-related bone marrow. II. Thorax, pelvis and extremities. Pediatr Radiol 1995; 25 (08) 596-606
41 Shabshin N, Schweitzer ME, Morrison WB, Carrino JA, Keller MS, Grissom LE. High-signal T2 changes of the bone marrow of the foot and ankle in children: red marrow or traumatic changes?. Pediatr Radiol 2006; 36 (07) 670-676
42 Ricci C, Cova M, Kang YS. et al. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 1990; 177 (01) 83-88
43 de Abreu MR, Wesselly M, Chung CB, Resnick D. Bone marrow MR imaging findings in disuse osteoporosis. Skeletal Radiol 2011; 40 (05) 571-575
44 Vande Berg B, Kirchgesner T, Mourad C, Acid S, Malghem J. Regional osteopenia or regional acceleratory phenomenon: what have we missed at MRI?. Diagn Interv Imaging 2021; 102 (09) 577-580
45 Schweitzer ME, White LM. Does altered biomechanics cause marrow edema?. Radiology 1996; 198 (03) 851-853
46 Sax AJ, Halpern EJ, Zoga AC, Roedl JB, Belair JA, Morrison WB. Predicting osteomyelitis in patients whose initial MRI demonstrated bone marrow edema without corresponding T1 signal marrow replacement. Skeletal Radiol 2020; 49 (08) 1239-1247
47 Smith SE, Murphey MD, Motamedi K, Mulligan ME, Resnik CS, Gannon FH. From the archives of the AFIP. Radiologic spectrum of Paget disease of bone and its complications with pathologic correlation. Radiographics 2002; 22 (05) 1191-1216
48 Steinbach LS, Suh KJ. Bone marrow edema pattern around the knee on magnetic resonance imaging excluding acute traumatic lesions. Semin Musculoskelet Radiol 2011; 15 (03) 208-220