Semin Musculoskelet Radiol 2023; 27(01): 103-113
DOI: 10.1055/s-0043-1761497
Review Article

The Many Faces of Marrow Necrosis

Charbel Mourad
1   Department of Diagnostic and Interventional Radiology, Hôpital Libanais Geitaoui - CHU, Beyrouth, Lebanon
2   Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland
,
Patrick Omoumi
2   Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland
,
Bruno Vande Berg
3   Department of Radiology, Musculoskeletal Section, Centre Hospitalier Chretien, CHC, Clinique Mont Legia, Liege, Belgium
› Author Affiliations

Abstract

Depending on the age and location within the skeleton, bone marrow can be mostly fatty or hematopoietic, and both types can be affected by marrow necrosis. This review article highlights the magnetic resonance imaging findings of disorders in which marrow necrosis is the dominant feature.

Fatty marrow necrosis is detected on T1-weighted images that show an early and specific finding: the reactive interface. Collapse is a frequent complication of epiphyseal necrosis and detected on fat-suppressed fluid-sensitive sequences or using conventional radiographs. Nonfatty marrow necrosis is less frequently diagnosed. It is poorly visible on T1-weighted images, and it is detected on fat-suppressed fluid-sensitive images or by the lack of enhancement after contrast injection.

Pathologies historically “misnamed” as osteonecrosis but do not share the same histologic or imaging features of marrow necrosis are also highlighted.



Publication History

Article published online:
03 March 2023

© 2023. Thieme. All rights reserved.

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

 
  • References

  • 1 Gorbachova T, Amber I, Beckmann NM. et al. Nomenclature of subchondral nonneoplastic bone lesions. AJR Am J Roentgenol 2019; 213 (05) 963-982
  • 2 Phemister DB. Repair of bone in the presence of aseptic necrosis resulting from fractures, transplantations, and vascular obstruction. JBJS 1930; 12 (04) 769-787
  • 3 Ficat RP. Aseptic necrosis of the femur head. Pathogenesis: the theory of circulation. [in French]. Acta Orthop Belg 1981; 47 (02) 198-199
  • 4 Nixon JE. Avascular necrosis of bone: a review. J R Soc Med 1983; 76 (08) 681-692
  • 5 Taleisnik J, Kelly PJ. The extraosseous and intraosseous blood supply of the scaphoid bone. J Bone Joint Surg Am 1966; 48 (06) 1125-1137
  • 6 Steinmann SP, Adams JE. Scaphoid fractures and nonunions: diagnosis and treatment. J Orthop Sci 2006; 11 (04) 424-431
  • 7 Anderson SE, Steinbach LS, Tschering-Vogel D, Martin M, Nagy L. MR imaging of avascular scaphoid nonunion before and after vascularized bone grafting. Skeletal Radiol 2005; 34 (06) 314-320
  • 8 Cheema HS, Cheema AN. Radiographic evaluation of vascularity in scaphoid nonunions: a review. World J Orthop 2020; 11 (11) 475-482
  • 9 Megerle K, Worg H, Christopoulos G, Schmitt R, Krimmer H. Gadolinium-enhanced preoperative MRI scans as a prognostic parameter in scaphoid nonunion. J Hand Surg Eur Vol 2011; 36 (01) 23-28
  • 10 Rancy SK, Swanstrom MM, DiCarlo EF, Sneag DB, Lee SK, Wolfe SW. Scaphoid Nonunion Consortium. Success of scaphoid nonunion surgery is independent of proximal pole vascularity. J Hand Surg Eur Vol 2018; 43 (01) 32-40
  • 11 Cerezal L, Abascal F, Canga A, García-Valtuille R, Bustamante M, del Piñal F. Usefulness of gadolinium-enhanced MR imaging in the evaluation of the vascularity of scaphoid nonunions. AJR Am J Roentgenol 2000; 174 (01) 141-149
  • 12 Schoierer O, Bloess K, Bender D. et al. Dynamic contrast-enhanced magnetic resonance imaging can assess vascularity within fracture non-unions and predicts good outcome. Eur Radiol 2014; 24 (02) 449-459
  • 13 Larribe M, Gay A, Freire V, Bouvier C, Chagnaud C, Souteyrand P. Usefulness of dynamic contrast-enhanced MRI in the evaluation of the viability of acute scaphoid fracture. Skeletal Radiol 2014; 43 (12) 1697-1703
  • 14 Ng AW, Griffith JF, Taljanovic MS, Li A, Tse WL, Ho PC. Is dynamic contrast-enhanced MRI useful for assessing proximal fragment vascularity in scaphoid fracture delayed and non-union?. Skeletal Radiol 2013; 42 (07) 983-992
  • 15 Büchler U, Nagy L. The issue of vascularity in fractures and non-union of the scaphoid. J Hand Surg [Br] 1995; 20 (06) 726-735
  • 16 Ito H, Kaneda K, Matsuno T. Osteonecrosis of the femoral head. Simple varus intertrochanteric osteotomy. J Bone Joint Surg Br 1999; 81 (06) 969-974
  • 17 Pascart T, Falgayrac G, Migaud H. et al. Region-specific Raman spectroscopy analysis of the femoral head reveals that trabecular bone is unlikely to contribute to non-traumatic osteonecrosis. Sci Rep 2017; 7 (01) 97
  • 18 Glimcher MJ, Kenzora JE. Nicolas Andry award. The biology of osteonecrosis of the human femoral head and its clinical implications: 1. Tissue biology. Clin Orthop Relat Res 1979; 138 (138) 284-309
  • 19 Cultot A, Norberciak L, Coursier R. et al. Bone perfusion and adiposity beyond the necrotic zone in femoral head osteonecrosis: a quantitative MRI study. Eur J Radiol 2020; 131: 109206
  • 20 Chan WP, Liu YJ, Huang GS. et al. Relationship of idiopathic osteonecrosis of the femoral head to perfusion changes in the proximal femur by dynamic contrast-enhanced MRI. AJR Am J Roentgenol 2011; 196 (03) 637-643
  • 21 Murphey MD, Foreman KL, Klassen-Fischer MK, Fox MG, Chung EM, Kransdorf MJ. From the radiologic pathology archives imaging of osteonecrosis: radiologic-pathologic correlation. Radiographics 2014; 34 (04) 1003-1028
  • 22 Catto M. Ischaemia of bone. J Clin Pathol Suppl (R Coll Pathol) 1977; 11: 78-93
  • 23 Zhang YZ, Cao XY, Li XC. et al. Accuracy of MRI diagnosis of early osteonecrosis of the femoral head: a meta-analysis and systematic review. J Orthop Surg Res 2018; 13 (01) 167
  • 24 Mitchell DG, Rao VM, Dalinka MK. et al. Femoral head avascular necrosis: correlation of MR imaging, radiographic staging, radionuclide imaging, and clinical findings. Radiology 1987; 162 (03) 709-715
  • 25 Min BW, Song KS, Cho CH, Lee SM, Lee KJ. Untreated asymptomatic hips in patients with osteonecrosis of the femoral head. Clin Orthop Relat Res 2008; 466 (05) 1087-1092
  • 26 Zhao FC, Guo KJ, Li ZR. Osteonecrosis of the femoral head in SARS patients: seven years later. Eur J Orthop Surg Traumatol 2013; 23 (06) 671-677
  • 27 Kenzora JE, Glimcher MJ. Pathogenesis of idiopathic osteonecrosis: the ubiquitous crescent sign. Orthop Clin North Am 1985; 16 (04) 681-696
  • 28 Kubo Y, Motomura G, Utsunomiya T. et al. Distribution of femoral head subchondral fracture site relates to contact pressures, age, and acetabular structure. AJR Am J Roentgenol 2020; 215 (02) 448-457
  • 29 Kubo Y, Motomura G, Ikemura S. et al. The effect of the anterior boundary of necrotic lesion on the occurrence of collapse in osteonecrosis of the femoral head. Int Orthop 2018; 42 (07) 1449-1455
  • 30 Utsunomiya T, Motomura G, Ikemura S. et al. Effects of sclerotic changes on stress concentration in early-stage osteonecrosis: a patient-specific, 3D finite element analysis. J Orthop Res 2018; 36 (12) 3169-3177
  • 31 Gao F, Han J, He Z, Li Z. Radiological analysis of cystic lesion in osteonecrosis of the femoral head. Int Orthop 2018; 42 (07) 1615-1621
  • 32 Yang JW, Koo KH, Lee MC. et al. Mechanics of femoral head osteonecrosis using three-dimensional finite element method. Arch Orthop Trauma Surg 2002; 122 (02) 88-92
  • 33 Karasuyama K, Yamamoto T, Motomura G, Sonoda K, Kubo Y, Iwamoto Y. The role of sclerotic changes in the starting mechanisms of collapse: a histomorphometric and FEM study on the femoral head of osteonecrosis. Bone 2015; 81: 644-648
  • 34 Brown TD, Hild GL. Pre-collapse stress redistributions in femoral head osteonecrosis—a three-dimensional finite element analysis. J Biomech Eng 1983; 105 (02) 171-176
  • 35 Brown TD, Mutschler TA, Ferguson Jr AB. A non-linear finite element analysis of some early collapse processes in femoral head osteonecrosis. J Biomech 1982; 15 (09) 705-715
  • 36 Magid D, Fishman EK, Scott Jr WW. et al. Femoral head avascular necrosis: CT assessment with multiplanar reconstruction. Radiology 1985; 157 (03) 751-756
  • 37 Stevens K, Tao C, Lee SU. et al. Subchondral fractures in osteonecrosis of the femoral head: comparison of radiography, CT, and MR imaging. AJR Am J Roentgenol 2003; 180 (02) 363-368
  • 38 Mourad CJ, Libert F, Gangji V, Michoux N, Vande Berg BC. Collapse-related bone changes at multidetector CT in ARCO 1-2 osteonecrotic femoral heads: correlation with clinical and MRI data. Eur Radiol 2023; 32 (02) 1486-1495
  • 39 Koo KH, Ahn IO, Kim R. et al. Bone marrow edema and associated pain in early-stage osteonecrosis of the femoral head: prospective study with serial MR images. Radiology 1999; 213 (03) 715-722
  • 40 Lafforgue P, Dahan E, Chagnaud C, Schiano A, Kasbarian M, Acquaviva PC. Early-stage avascular necrosis of the femoral head: MR imaging for prognosis in 31 cases with at least 2 years of follow-up. Radiology 1993; 187 (01) 199-204
  • 41 Shimizu K, Moriya H, Akita T, Sakamoto M, Suguro T. Prediction of collapse with magnetic resonance imaging of avascular necrosis of the femoral head. J Bone Joint Surg Am 1994; 76 (02) 215-223
  • 42 Takatori Y, Kokubo T, Ninomiya S, Nakamura S, Morimoto S, Kusaba I. Avascular necrosis of the femoral head. Natural history and magnetic resonance imaging. J Bone Joint Surg Br 1993; 75 (02) 217-221
  • 43 Sugano N, Atsumi T, Ohzono K, Kubo T, Hotokebuchi T, Takaoka K. The 2001 revised criteria for diagnosis, classification, and staging of idiopathic osteonecrosis of the femoral head. J Orthop Sci 2002; 7 (05) 601-605
  • 44 Ohzono K, Saito M, Sugano N, Takaoka K, Ono K. The fate of nontraumatic avascular necrosis of the femoral head. A radiologic classification to formulate prognosis. Clin Orthop Relat Res 1992; (277) 73-78
  • 45 Sugano N, Takaoka K, Ohzono K, Matsui M, Masuhara K, Ono K. Prognostication of nontraumatic avascular necrosis of the femoral head. Significance of location and size of the necrotic lesion. Clin Orthop Relat Res 1994; (303) 155-164
  • 46 Meier R, Kraus TM, Schaeffeler C. et al. Bone marrow oedema on MR imaging indicates ARCO stage 3 disease in patients with AVN of the femoral head. Eur Radiol 2014; 24 (09) 2271-2278
  • 47 Ejindu VC, Hine AL, Mashayekhi M, Shorvon PJ, Misra RR. Musculoskeletal manifestations of sickle cell disease. Radiographics 2007; 27 (04) 1005-1021
  • 48 Malizos KN, Siafakas MS, Fotiadis DI, Karachalios TS, Soucacos PN. An MRI-based semiautomated volumetric quantification of hip osteonecrosis. Skeletal Radiol 2001; 30 (12) 686-693
  • 49 Styles LA, Vichinsky EP. Core decompression in avascular necrosis of the hip in sickle-cell disease. Am J Hematol 1996; 52 (02) 103-107
  • 50 Rao VM, Mitchell DG, Rifkin MD. et al. Marrow infarction in sickle cell anemia: correlation with marrow type and distribution by MRI. Magn Reson Imaging 1989; 7 (01) 39-44
  • 51 Khedr SA, Hassaan MA, Shabana AA, Gaballah AH, Mokhtar DA. Musculoskeletal manifestations of sickle cell disease, diagnosis with whole body MRI. Egypt J Radiol Nucl Med 2012; 43 (01) 77-84
  • 52 Kosaraju V, Harwani A, Partovi S. et al. Imaging of musculoskeletal manifestations in sickle cell disease patients. Br J Radiol 2017; 90 (1073): 20160130-20160130
  • 53 Geith T, Stellwag AC, E Müller P, Reiser M, Baur-Melnyk A. Is bone marrow edema syndrome a precursor of hip or knee osteonecrosis? Results of 49 patients and review of the literature. Diagn Interv Radiol 2020; 26 (04) 355-362
  • 54 Ahlbäck S, Bauer GC, Bohne WH. Spontaneous osteonecrosis of the knee. Arthritis Rheum 1968; 11 (06) 705-733
  • 55 Gorbachova T, Melenevsky Y, Cohen M, Cerniglia BW. Osteochondral lesions of the knee: differentiating the most common entities at MRI. Radiographics 2018; 38 (05) 1478-1495
  • 56 Yamamoto T, Bullough PG. Spontaneous osteonecrosis of the knee: the result of subchondral insufficiency fracture. J Bone Joint Surg Am 2000; 82 (06) 858-866
  • 57 Blaine ES. Spondylitis traumatica tarda (Kummell's disease). Radiology, November 1, 1930. Available at: pubs.rsna.org/doi/10.1148/15.5.551. Accessed June 19, 2022
  • 58 Kümmell H. Ueber die traumatischen Erkrankungen der Wirbelsäule1). Dtsch Med Wochenschr 1895; 21 (11) 180-181
  • 59 Maldague BE, Noel HM, Malghem JJ. The intravertebral vacuum cleft: a sign of ischemic vertebral collapse. Radiology 1978; 129 (01) 23-29
  • 60 Libicher M, Appelt A, Berger I. et al. The intravertebral vacuum phenomenon as specific sign of osteonecrosis in vertebral compression fractures: results from a radiological and histological study. Eur Radiol 2007; 17 (09) 2248-2252
  • 61 Laredo JD. Expert's comment concerning Grand Rounds case entitled “Kümmell's disease: delayed post-traumatic osteonecrosis of the vertebral body” (by R. Ma, R. Chow, F. H. Shen). Eur Spine J 2010; 19 (07) 1071-1072
  • 62 Laredo JD, Goumont V, Cywiner-Golenzer C, Bard M, Roucoules J, Ryckewaert A. Vertebral compression with intrasomatic vacuum images. Apropos of 2 cases with histological control by trocar biopsy. [in French]. Rev Rhum Mal Osteoartic 1985; 52 (06) 373-379
  • 63 Marx RE, Stern D. Oral and Maxillofacial Pathology: A Rationale for Diagnosis and Treatment. 2nd ed.. Chicago, IL: Quintessence; 2012
  • 64 Kühl S, Walter C, Acham S, Pfeffer R, Lambrecht JT. Bisphosphonate-related osteonecrosis of the jaws—a review. Oral Oncol 2012; 48 (10) 938-947
  • 65 Favia G, Pilolli GP, Maiorano E. Histologic and histomorphometric features of bisphosphonate-related osteonecrosis of the jaws: an analysis of 31 cases with confocal laser scanning microscopy. Bone 2009; 45 (03) 406-413
  • 66 Holtmann H, Lommen J, Kübler NR. et al. Pathogenesis of medication-related osteonecrosis of the jaw: a comparative study of in vivo and in vitro trials. J Int Med Res 2018; 46 (10) 4277-4296