Advertisement

Rheumatology International

, Volume 32, Issue 3, pp 575–584 | Cite as

Bone marrow lesions: a universal bone response to injury?

  • Erik Fink Eriksen
  • Johan Diederich Ringe
Review

Abstract

The ever increasing use of magnetic resonance imaging in clinical practice has led to the recognition of a new entity, bone marrow lesions (BMLs). These lesions are characterized by excessive water signals in the marrow space and have emerged as a central component of many different diseases affecting the musculoskeletal system. BMLs have in particular been associated with a wide variety of inflammatory and non-inflammatory rheumatologic conditions and are not only considered significant sources of pain, but also linked to the worsening of patient prognosis in many disease states. In this review, we summarize the current knowledge on BMLs with an emphasis on the clinical and histological features of this entity in inflammatory and non-inflammatory disease and provide a unifying hypothesis based on the appearance with various imaging technologies. We also try to pair this hypothesis with the apparent beneficial effects of various treatment regimens, mainly within the group of bone antiresorptive drugs (calcitonin, bisphosphonates) on symptoms associated with BMLs.

Keywords

Bone marrow lesions Bone marrow edema Bone histomorphometry Osteoarthritis Rheumatoid arthritis Bisphosphonates Tendinitis Sudeks atrophy Calcitonin MRI Ultrasound 

References

  1. 1.
    Roemer FW, Frobell R, Hunter DJ, Crema MD, Fischer W, Bohndorf K, Guermazi A (2009) MRI-detected subchondral bone marrow signal alterations of the knee joint: terminology, imaging appearance, relevance and radiological differential diagnosis. Osteoarthr Cartil 17(9):1115–1131PubMedCrossRefGoogle Scholar
  2. 2.
    Starr AM, Wessely MA, Albastaki U, Pierre-Jerome C, Kettner NW (2008) Bone marrow edema: pathophysiology, differential diagnosis, and imaging. Acta Radiol 49(7):771–786PubMedCrossRefGoogle Scholar
  3. 3.
    Wakefield RJ, McGonagle D, Tan AL, Evangelisto A, Emery P (2004) Ultrasound detection of knee patellar enthesitis. Ann Rheum Dis 63(6):753–754PubMedGoogle Scholar
  4. 4.
    Kamel M, Eid H, Mansour R (2003) Ultrasound detection of heel enthesitis: a comparison with magnetic resonance imaging. J Rheumatol 30(4):774–778PubMedGoogle Scholar
  5. 5.
    Thiryayi WA, Thiryayi SA, Freemont AJ (2008) Histopathological perspective on bone marrow oedema, reactive bone change and haemorrhage. Eur J Radiol 67(1):62–67PubMedCrossRefGoogle Scholar
  6. 6.
    Stabler A, Reiser MF (2001) Imaging of spinal infection. Radiol Clin North Am 39(1):115–135PubMedCrossRefGoogle Scholar
  7. 7.
    Arndt WF III, Truax AL, Barnett FM, Simmons GE, Brown DC (1996) MR diagnosis of bone contusions of the knee: comparison of coronal T2-weighted fast spin-echo with fat saturation and fast spin-echo STIR images with conventional STIR images. AJR Am J Roentgenol 166(1):119–124PubMedGoogle Scholar
  8. 8.
    Plenk H, Jr., Hofmann S, Eschberger J, Gstettner M, Kramer J, Schneider W, Engel A (1997) Histomorphology and bone morphometry of the bone marrow edema syndrome of the hip. Clin Orthop Relat Res (334):73–84Google Scholar
  9. 9.
    Martig S, Boisclair J, Konar M, Spreng D, Lang J (2007) MRI characteristics and histology of bone marrow lesions in dogs with experimentally induced osteoarthritis. Vet Radiol Ultrasound 48(2):105–112PubMedCrossRefGoogle Scholar
  10. 10.
    Yamamoto T, Schneider R, Bullough PG (2001) Subchondral insufficiency fracture of the femoral head: histopathologic correlation with MRI. Skeletal Radiol 30(5):247–254PubMedCrossRefGoogle Scholar
  11. 11.
    Kim SY, Koo KH, Suh KT, Kim YS, Cho YJ, Min BW, Ha YC, Choi JA (2005) Fatty marrow conversion of the proximal femoral metaphysis in transient bone marrow edema syndrome. Arch Orthop Trauma Surg 125(6):390–395PubMedCrossRefGoogle Scholar
  12. 12.
    Newberg AH, Wetzner SM (1994) Bone bruises: their patterns and significance. Semin Ultrasound CT MR 15(5):396–409PubMedCrossRefGoogle Scholar
  13. 13.
    Ryu KN, Jin W, Ko YT, Yoon Y, Oh JH, Park YK, Kim KS (2000) Bone bruises: MR characteristics and histological correlation in the young pig. Clin Imaging 24(6):371–380PubMedCrossRefGoogle Scholar
  14. 14.
    Berger CE, Kroner AH, Kristen KH, Grabmeier GF, Kluger R, Minai-Pour MB, Leitha T, Engel A (2006) Transient bone marrow edema syndrome of the knee: clinical and magnetic resonance imaging results at 5 years after core decompression. Arthroscopy 22(8):866–871PubMedCrossRefGoogle Scholar
  15. 15.
    Berger CE, Kroner AH, Minai-Pour MB, Ogris E, Engel A (2003) Biochemical markers of bone metabolism in bone marrow edema syndrome of the hip. Bone 33(3):346–351PubMedCrossRefGoogle Scholar
  16. 16.
    Radke S, Battmann A, Jatzke S, Eulert J, Jakob F, Schutze N (2006) Expression of the angiomatrix and angiogenic proteins CYR61, CTGF, and VEGF in osteonecrosis of the femoral head. J Orthop Res 24(5):945–952PubMedCrossRefGoogle Scholar
  17. 17.
    Kanbe K, Inoue K, Inoue Y, Suzuki Y (2008) Histological changes in bone marrow after treatment of infliximab for rheumatoid arthritis. Clin Rheumatol 27(4):497–501PubMedCrossRefGoogle Scholar
  18. 18.
    Schett G (2009) Bone marrow edema. Ann N Y Acad Sci 1154:35–40PubMedCrossRefGoogle Scholar
  19. 19.
    Appel H, Kuhne M, Spiekermann S, Kohler D, Zacher J, Stein H, Sieper J, Loddenkemper C (2006) Immunohistochemical analysis of hip arthritis in ankylosing spondylitis: evaluation of the bone-cartilage interface and subchondral bone marrow. Arthritis Rheum 54(6):1805–1813PubMedCrossRefGoogle Scholar
  20. 20.
    Voormolen MH, van Rooij WJ, van der Graaf Y, Lohle PN, Lampmann LE, Juttmann JR, Sluzewski M (2006) Bone marrow edema in osteoporotic vertebral compression fractures after percutaneous vertebroplasty and relation with clinical outcome. AJNR Am J Neuroradiol 27(5):983–988PubMedGoogle Scholar
  21. 21.
    Straten VH, Franssen MJ, den Broeder AA, Obradov M, van den Hoogen FH (2009) Regional migratory osteoporosis in a patient with ankylosing spondylitis. Scand J Rheumatol 38(1):63–65PubMedCrossRefGoogle Scholar
  22. 22.
    Guardiano SA, Katz J, Schwartz AM, Brindle K, Curiel R (2004) Fracture complicating the bone marrow edema syndrome. J Clin Rheumatol 10(5):269–274PubMedCrossRefGoogle Scholar
  23. 23.
    Adriaensen ME, Mulhall KJ, Borghans RA, Magill P, and Kavanagh EC (2009) Transient osteoporosis of the hip and spontaneous osteonecrosis of the knee: a common aetiology? Ir J Med Sci. doi: 10.1007/s11845-009-0407-4
  24. 24.
    Karantanas AH, Drakonaki E, Karachalios T, Korompilias AV, Malizos K (2008) Acute non-traumatic marrow edema syndrome in the knee: MRI findings at presentation, correlation with spinal DEXA and outcome. Eur J Radiol 67(1):22–33PubMedCrossRefGoogle Scholar
  25. 25.
    Morrison WB, Carrino JA, Schweitzer ME, Sanders TG, Raiken DP, Johnson CE (2001) Subtendinous bone marrow edema patterns on MR images of the ankle: association with symptoms and tendinopathy. AJR Am J Roentgenol 176(5):1149–1154PubMedGoogle Scholar
  26. 26.
    Flemming DJ, Murphey MD, Shekitka KM, Temple HT, Jelinek JJ, Kransdorf MJ (2003) Osseous involvement in calcific tendinitis: a retrospective review of 50 cases. AJR Am J Roentgenol 181(4):965–972PubMedGoogle Scholar
  27. 27.
    Riley GM (2007) Magnetic resonance imaging in the evaluation of sports injuries of the foot and ankle: a pictorial essay. J Am Podiatr Med Assoc 97(1):59–67PubMedGoogle Scholar
  28. 28.
    Hoy G, Wood T, Phillips N, Connell D, Hughes DC (2006) When physiology becomes pathology: the role of magnetic resonance imaging in evaluating bone marrow oedema in the humerus in elite tennis players with an upper limb pain syndrome. Br J Sports Med 40(8):710–713PubMedCrossRefGoogle Scholar
  29. 29.
    Blankenbaker DG, Ullrick SR, Davis KW, De Smet AA, Haaland B, Fine JP (2008) Correlation of MRI findings with clinical findings of trochanteric pain syndrome. Skeletal Radiol 37(10):903–909PubMedCrossRefGoogle Scholar
  30. 30.
    Richards PJ, McCall IW, Day C, Belcher J, MaVulli N (2009) Longitudinal microvascularity in Achilles tendinopathy (power Doppler ultrasound, magnetic resonance imaging time-intensity curves and the Victorian Institute of Sport Assessment-Achilles questionnaire):a pilot study. Skeletal Radiol 39(6):509–521Google Scholar
  31. 31.
    Sanders TG, Medynski MA, Feller JF, Lawhorn KW (2000) Bone contusion patterns of the knee at MR imaging: footprint of the mechanism of injury. Radiographics 20 Spec No:S135–S151Google Scholar
  32. 32.
    Chantelau E, Richter A, Ghassem-Zadeh N, Poll LW (2007) “Silent” bone stress injuries in the feet of diabetic patients with polyneuropathy: a report on 12 cases. Arch Orthop Trauma Surg 127(3):171–177PubMedCrossRefGoogle Scholar
  33. 33.
    Yonetani Y, Nakamura N, Natsuume T, Shiozaki Y, Tanaka Y, Horibe S (2009) Histological evaluation of juvenile osteochondritis dissecans of the knee: a case series. Knee Surg Sports Traumatol Arthrosc 18(6):723–730Google Scholar
  34. 34.
    Choi YS, Cohen NA, Potter HG, Mintz DN (2007) Magnetic resonance imaging in the evaluation of osteochondritis dissecans of the patella. Skeletal Radiol 36(10):929–935PubMedCrossRefGoogle Scholar
  35. 35.
    Elias I, Jung JW, Raikin SM, Schweitzer MW, Carrino JA, Morrison WB (2006) Osteochondral lesions of the talus: change in MRI findings over time in talar lesions without operative intervention and implications for staging systems. Foot Ankle Int 27(3):157–166PubMedGoogle Scholar
  36. 36.
    Bennell KL, Creaby MW, Wrigley TV, Bowles KA, Hinman RS, Cicuttini F, Hunter DJ (2009) Bone marrow lesions are related to dynamic knee loading in medial knee osteoarthritis. Ann Rheum Dis 69(6):1151–1154Google Scholar
  37. 37.
    Roemer FW, Guermazi A, Javaid MK, Lynch JA, Niu J, Zhang Y, Felson DT, Lewis CE, Torner J, Nevitt MC (2009) Change in MRI-detected subchondral bone marrow lesions is associated with cartilage loss: the MOST Study. A longitudinal multicentre study of knee osteoarthritis. Ann Rheum Dis 68(9):1461–1465Google Scholar
  38. 38.
    vies-Tuck ML, Wluka AE, Wang Y, English DR, Giles GG, Cicuttini F (2009) The natural history of bone marrow lesions in community-based adults with no clinical knee osteoarthritis. Ann Rheum Dis 68(6):904–908CrossRefGoogle Scholar
  39. 39.
    Felson DT (2004) An update on the pathogenesis and epidemiology of osteoarthritis. Radiol Clin North Am 42(1):1–9, vGoogle Scholar
  40. 40.
    Felson DT, McLaughlin S, Goggins J, LaValley MP, Gale ME, Totterman S, Li W, Hill C, Gale D (2003) Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med 139(5 Pt 1):330–336Google Scholar
  41. 41.
    Scher C, Craig J, Nelson F (2008) Bone marrow edema in the knee in osteoarthrosis and association with total knee arthroplasty within a three-year follow-up. Skeletal Radiol 37(7):609–617PubMedCrossRefGoogle Scholar
  42. 42.
    Taljanovic MS, Graham AR, Benjamin JB, Gmitro AF, Krupinski EA, Schwartz SA, Hunter TB, Resnick DL (2008) 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 37(5):423–431PubMedCrossRefGoogle Scholar
  43. 43.
    Garnero P, Aronstein WS, Cohen SB, Conaghan PG, Cline GA, Christiansen C, Beary JF, Meyer JM, Bingham CO III (2008) Relationships between biochemical markers of bone and cartilage degradation with radiological progression in patients with knee osteoarthritis receiving risedronate: the Knee Osteoarthritis Structural Arthritis randomized clinical trial. Osteoarthr Cartil 16(6):660–666PubMedCrossRefGoogle Scholar
  44. 44.
    Garnero P, Mazieres B, Gueguen A, Abbal M, Berdah L, Lequesne M, Nguyen M, Salles JP, Vignon E, Dougados M (2005) Cross-sectional association of 10 molecular markers of bone, cartilage, and synovium with disease activity and radiological joint damage in patients with hip osteoarthritis: the ECHODIAH cohort. J Rheumatol 32(4):697–703PubMedGoogle Scholar
  45. 45.
    Garnero P, Peterfy C, Zaim S, Schoenharting M (2005) Bone marrow abnormalities on magnetic resonance imaging are associated with type II collagen degradation in knee osteoarthritis: a three-month longitudinal study. Arthritis Rheum 52(9):2822–2829PubMedCrossRefGoogle Scholar
  46. 46.
    Aaron RK, Dyke JP, Ciombor DM, Ballon D, Lee J, Jung E, Tung GA (2007) Perfusion abnormalities in subchondral bone associated with marrow edema, osteoarthritis, and avascular necrosis. Ann N Y Acad Sci 1117:124–137PubMedCrossRefGoogle Scholar
  47. 47.
    Dore D, Quinn S, Ding C, Winzenberg T, Jones G (2009) Correlates of subchondral BMD: a cross-sectional study. J Bone Miner Res 24(12):2007–2015PubMedCrossRefGoogle Scholar
  48. 48.
    Beuf O, Ghosh S, Newitt DC, Link TM, Steinbach L, Ries M, Lane N, Majumdar S (2002) Magnetic resonance imaging of normal and osteoarthritic trabecular bone structure in the human knee. Arthritis Rheum 46(2):385–393PubMedCrossRefGoogle Scholar
  49. 49.
    Majumdar S, Issever AS, Burghardt A, Lotz J, Arfelli F, Rigon L, Heitner G, Menk RH (2004) Diffraction enhanced imaging of articular cartilage and comparison with micro-computed tomography of the underlying bone structure. Eur Radiol 14(8):1440–1448PubMedCrossRefGoogle Scholar
  50. 50.
    Haavardsholm EA, Boyesen P, Ostergaard M, Schildvold A, Kvien TK (2008) Magnetic resonance imaging findings in 84 patients with early rheumatoid arthritis: bone marrow oedema predicts erosive progression. Ann Rheum Dis 67(6):794–800PubMedCrossRefGoogle Scholar
  51. 51.
    Olech E, Crues JV, III, Yocum DE, Merrill JT (2009) Bone marrow edema is the most specific finding for rheumatoid arthritis (RA) on noncontrast magnetic resonance imaging of the hands and wrists: a comparison of patients with RA and healthy controls. J Rheumatol 37(2):265–274Google Scholar
  52. 52.
    Haavardsholm EA, Ostergaard M, Hammer HB, Boyesen P, Boonen A, van der HD, Kvien TK (2009) Monitoring anti-TNFalpha treatment in rheumatoid arthritis: responsiveness of magnetic resonance imaging and ultrasonography of the dominant wrist joint compared with conventional measures of disease activity and structural damage. Ann Rheum Dis 68(10):1572–1579PubMedCrossRefGoogle Scholar
  53. 53.
    Eshed I, Althoff CE, Feist E, Minden K, Schink T, Hamm B, Hermann KG (2008) Magnetic resonance imaging of hindfoot involvement in patients with spondyloarthritides: comparison of low-field and high-field strength units. Eur J Radiol 65(1):140–147PubMedCrossRefGoogle Scholar
  54. 54.
    Erdem CZ, Tekin NS, Sarikaya S, Erdem LO, Gulec S (2008) MR imaging features of foot involvement in patients with psoriasis. Eur J Radiol 67(3):521–525PubMedCrossRefGoogle Scholar
  55. 55.
    Low AH, Lax M, Johnson SR, Lee P (2009) Magnetic resonance imaging of the hand in systemic sclerosis. J Rheumatol 36(5):961–964PubMedCrossRefGoogle Scholar
  56. 56.
    Ito H, Matsuno T, Minami A (2006) Relationship between bone marrow edema and development of symptoms in patients with osteonecrosis of the femoral head. AJR Am J Roentgenol 186(6):1761–1770PubMedCrossRefGoogle Scholar
  57. 57.
    Tanaka Y, Mima H, Yonetani Y, Shiozaki Y, Nakamura N, Horibe S (2009) Histological evaluation of spontaneous osteonecrosis of the medial femoral condyle and short-term clinical results of osteochondral autografting: a case series. Knee 16(2):130–135PubMedCrossRefGoogle Scholar
  58. 58.
    Javier RM, Moser T, Dietemann JL, Sparsa L, Natarajan-Ame S, Chenard MP, Kuntz JL (2008) Multiple vertebral osteonecrosis. Joint Bone Spine 75(3):341–344PubMedCrossRefGoogle Scholar
  59. 59.
    Nishida Y, Saito Y, Yokota T, Kanda T, Mizusawa H (2009) Skeletal muscle MRI in complex regional pain syndrome. Intern Med 48(4):209–212PubMedCrossRefGoogle Scholar
  60. 60.
    Tan PL, Teh J (2007) MRI of the diabetic foot: differentiation of infection from neuropathic change. Br J Radiol 80(959):939–948PubMedCrossRefGoogle Scholar
  61. 61.
    Carter JD, Kedar RP, Anderson SR, Osorio AH, Albritton NL, Gnanashanmugam S, Valeriano J, Vasey FB, Ricca LR (2009) An analysis of MRI and ultrasound imaging in patients with gout who have normal plain radiographs. Rheumatology (Oxford) 48(11):1442–1446CrossRefGoogle Scholar
  62. 62.
    Bui-Mansfield LT, Moak M (2005) Magnetic resonance appearance of bone marrow edema associated with hydroxyapatite deposition disease without cortical erosion. J Comput Assist Tomogr 29(1):103–107PubMedCrossRefGoogle Scholar
  63. 63.
    Agarwala S, Jain D, Joshi VR, Sule A (2005) Efficacy of alendronate, a bisphosphonate, in the treatment of AVN of the hip. A prospective open-label study.[erratum appears in Rheumatology (Oxford) 2005 Apr;44(4):569]. Rheumatology 44(3):352–359PubMedCrossRefGoogle Scholar
  64. 64.
    Lai KA, Shen WJ, Yang CY, Shao CJ, Hsu JT, Lin RM (2005) The use of alendronate to prevent early collapse of the femoral head in patients with nontraumatic osteonecrosis. A randomized clinical study. J Bone & Joint Surgery—American Volume 87(10):2155–2159Google Scholar
  65. 65.
    Ringe JD, Dorst A, Faber H (2005) Effective and rapid treatment of painful localized transient osteoporosis (bone marrow edema) with intravenous ibandronate. Osteoporos Int 16(12):2063–2068PubMedCrossRefGoogle Scholar
  66. 66.
    Maksymowych WP, Lambert R, Jhangri GS, Leclercq S, Chiu P, Wong B, Aaron S, Russell AS (2001) Clinical and radiological amelioration of refractory peripheral spondyloarthritis by pulse intravenous pamidronate therapy. J Rheumatol 28(1):144–155PubMedGoogle Scholar
  67. 67.
    Manicourt DH, Brasseur JP, Boutsen Y, Depreseux G, Devogelaer JP (2004) Role of alendronate in therapy for posttraumatic complex regional pain syndrome type I of the lower extremity. Arthritis Rheum 50(11):3690–3697PubMedCrossRefGoogle Scholar
  68. 68.
    Coleman RE (2004) Bisphosphonates: clinical experience. Oncologist 9(Suppl 4):14–27Google Scholar
  69. 69.
    Laktasic-Zerjavic N, Curkovic B, Babic-Naglic D, Potocki K, Prutki M, Soldo-Juresa D (2007) [Transient osteoporosis of the hip in pregnancy. Successful treatment with calcitonin: a case report]. Z Rheumatol 66(6):510–513Google Scholar
  70. 70.
    Nuti R, Vattimo A, Martini G, Turchetti V, Righi GA (1987) Carbocalcitonin treatment in Sudeck’s atrophy. Clin Orthop Relat Res (215):217–222Google Scholar
  71. 71.
    Jager M, Tillmann FP, Thornhill TS, Mahmoudi M, Blondin D, Hetzel GR, Zilkens C, Krauspe R (2008) Rationale for prostaglandin I2 in bone marrow oedema–from theory to application. Arthritis Res Ther 10(5):R120PubMedCrossRefGoogle Scholar
  72. 72.
    Aigner N, Petje G, Schneider W, Meizer R, Wlk M, Kotsaris S, Knahr K, Landsiedl F (2005) Bone marrow edema syndrome of the femoral head: treatment with the prostacyclin analogue iloprost vs. core decompression: an MRI-controlled study. Wien Klin Wochenschr 117(4):130–135Google Scholar
  73. 73.
    Meizer R, Radda C, Stolz G, Kotsaris S, Petje G, Krasny C, Wlk M, Mayerhofer M, Landsiedl F, Aigner N (2005) MRI-controlled analysis of 104 patients with painful bone marrow edema in different joint localizations treated with the prostacyclin analogue iloprost. Wien Klin Wochenschr 117(7–8):278–286PubMedCrossRefGoogle Scholar
  74. 74.
    Hirose W, Nishikawa K, Hirose M, Nanki T, Sugimoto H (2009) Response of early active rheumatoid arthritis to tumor necrosis factor inhibitors: evaluation by magnetic resonance imaging. Mod Rheumatol 19(1):20–26PubMedCrossRefGoogle Scholar
  75. 75.
    Marzo-Ortega H, McGonagle D, Emery P (2002) Etanercept treatment in resistant spondyloarthropathy: imaging, duration of effect and efficacy on reintroduction. Clin Exp Rheumatol 20(6 Suppl 28):S175–S177Google Scholar
  76. 76.
    Maksymowych WP, Inman RD, Salonen D, Dhillon SS, Williams M, Stone M, Conner-Spady B, Palsat J, Lambert RG (2005) Spondyloarthritis research Consortium of Canada magnetic resonance imaging index for assessment of sacroiliac joint inflammation in ankylosing spondylitis. Arthritis Rheum 53(5):703–709PubMedCrossRefGoogle Scholar
  77. 77.
    Marzo-Ortega H, McGonagle D, Rhodes LA, Tan AL, Conaghan PG, O’Connor P, Tanner SF, Fraser A, Veale D, Emery P (2007) Efficacy of infliximab on MRI-determined bone oedema in psoriatic arthritis. Ann Rheum Dis 66(6):778–781PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of EndocrinologyOslo University HospitalOsloNorway
  2. 2.Medizinische Klinik IV, Klinikum LeverkusenUniversity of CologneCologneGermany

Personalised recommendations