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Imaging evaluation of inflammation in the musculoskeletal system: current concepts and perspectives

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Abstract

Inflammation is the non-specific stereotyped reaction of the musculoskeletal system to various types of aggression, such as infection, tumor, autoimmune diseases, or trauma. Precise evaluation and, increasingly, reliable quantification of inflammation are now key factors for optimal patient management, as targeted therapies (e.g., anti-angiogenesis, anti-macrophages, anti-cytokines) are emerging as everyday drugs. In current practice, inflammation is evaluated mostly using MRI and US on the basis of its non-specific extracellular component due to the increased volume of free water. Inflamed tissue is described as areas of low T1 signal and high T2 signal on magnetic resonance imaging or as hypoechogenic areas on ultrasound imaging, and the evaluation of the increased tissue vascularity can be performed using gadolinium-enhanced MRI or power Doppler US. Emerging new imaging tools, regrouped under the label “cellular and molecular imaging” and defined as the in vivo characterization and measurement of biologic processes at the cellular and molecular level, demonstrate the possible shift of medical imaging from a macroscopic and non-specific level to a microscopic and targeted scale. Cellular and molecular imaging now allows the investigation of specific pathways involved in inflammation (e.g., angiogenesis, cell proliferation, and recruitment, proteases generation, metabolism, gene expression). PET and SPECT imaging are the most commonly used “molecular” imaging modalities, but recent progress in MR, US, and optical imaging has been made. In the future, those techniques might enable a detection of inflammation at its very early stage, its quantification through the definition of biomarkers, and possibly demonstrate the response to therapy at molecular and cellular levels.

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References

  1. Stephenson TJ. Inflammation. In: Underwood JCE, editor. General and systemic pathology. 4th ed. London: Churchill Livingstone; 2004. p. 201–22.

    Google Scholar 

  2. Boyesen P, Haavardsholm EA, Ostergaard M, van der Heijde D, Sesseng S, Kvien TK. MRI in early rheumatoid arthritis: synovitis and bone marrow oedema are independent predictors of subsequent radiographic progression. Ann Rheum Dis. 2011;70(3):428–33.

    Article  PubMed  Google Scholar 

  3. Klarlund M, Ostergaard M, Jensen KE, Madsen JL, Skjodt H, Lorenzen I. Magnetic resonance imaging, radiography, and scintigraphy of the finger joints: one-year follow-up of patients with early arthritis. The TIRA Group. Ann Rheum Dis. 2000;59(7):521–8.

    Article  PubMed  CAS  Google Scholar 

  4. Bierry G, Huang AJ, Chang CY, Torriani M, Bredella MA. MRI findings of treated bacterial septic arthritis. Skeletal Radiol. 2012.

  5. Jaffer FA, Weissleder R. Molecular imaging in the clinical arena. JAMA. 2005;293(7):855–62.

    Article  PubMed  CAS  Google Scholar 

  6. Shinohara M, Mirakaj V, Serhan CN. Functional metabolomics reveals novel active products in the DHA metabolome. Front Immunol. 2012;81(3):Epub 17.

  7. Weissleder R, Pittet MJ. Imaging in the era of molecular oncology. Nature. 2008;452(7187):580–9.

    Article  PubMed  CAS  Google Scholar 

  8. Herfkens R, Davis P, Crooks L, Kaufman L, Price D, Miller T, et al. Nuclear magnetic resonance imaging of the abnormal live rat and correlations with tissue characteristics. Radiology. 1981;141(1):211–8.

    PubMed  CAS  Google Scholar 

  9. Gillams A, Chaddha B, Carter A. MR appearances of the temporal evolution and resolution of infectious spondylitis. AJR Am J Roentgenol. 1996;166(4):903–7.

    Article  PubMed  CAS  Google Scholar 

  10. Boks SS, Vroegindeweij D, Koes BW, Bernsen RMD, Hunink MGM, Bierma-Zeinstra SMA. MRI follow-up of posttraumatic bone bruises of the knee in general practice. Am J Roentgenol. 2007;189(3):556–62.

    Article  Google Scholar 

  11. Ostergaard M, Szkudlarek M. Ultrasonography: a valid method for assessing rheumatoid arthritis? Arthritis Rheum. 2005;52(3):681–6.

    Article  PubMed  Google Scholar 

  12. Taylor PC. VEGF and imaging of vessels in rheumatoid arthritis. Arthritis Res. 2002;4 Suppl 3:S99–107.

    Article  PubMed  Google Scholar 

  13. Ribbens C, Andre B, Marcelis S, Kaye O, Mathy L, Bonnet V, et al. Rheumatoid hand joint synovitis: gray-scale and power Doppler US quantifications following anti-tumor necrosis factor-alpha treatment: pilot study. Radiology. 2003;229(2):562–9.

    Article  PubMed  Google Scholar 

  14. Carr DH. The use of iron and gadolinium chelates as NMR contrast agents: animal and human studies. Physiol Chem Phys Med NMR. 1984;16(2):137–44.

    PubMed  CAS  Google Scholar 

  15. MacAdam AJ, Sharpe AH. Infectious diseases. In: Kumur V, Abbas AK, Fausto N, Aster J, editors. Robbins and cotran pathologic basis of disease. 8th ed. Philadelphia: Saunders; 2010. p. 1246–79.

    Google Scholar 

  16. Fernandez-Madrid F, Karvonen RL, Teitge RA, Miller PR, An T, Negendank WG. Synovial thickening detected by MR imaging in osteoarthritis of the knee confirmed by biopsy as synovitis. Magn Reson Imaging. 1995;13(2):177–83.

    Article  PubMed  CAS  Google Scholar 

  17. Mohana-Borges AVR, Chung CB, Resnick D. Monoarticular arthritis. Radiol Clin N Am. 2004;42(1):135–49.

    Article  PubMed  Google Scholar 

  18. Ostergaard M, Peterfy C, Conaghan P, McQueen F, Bird P, Ejbjerg B, et al. OMERACT Rheumatoid Arthritis Magnetic Resonance Imaging Studies. Core set of MRI acquisitions, joint pathology definitions, and the OMERACT RA-MRI scoring system. J Rheumatol. 2003;30(6):1385–6.

    PubMed  Google Scholar 

  19. Cimmino MA, Innocenti S, Livrone F, Magnaguagno F, Silvestri E, Garlaschi G. Dynamic gadolinium-enhanced magnetic resonance imaging of the wrist in patients with rheumatoid arthritis can discriminate active from inactive disease. Arthritis Rheum. 2003;48(5):1207–13.

    Article  PubMed  Google Scholar 

  20. Conaghan PG, O’Connor P, McGonagle D, Astin P, Wakefield RJ, Gibbon WW, et al. Elucidation of the relationship between synovitis and bone damage: a randomized magnetic resonance imaging study of individual joints in patients with early rheumatoid arthritis. Arthritis Rheum. 2003;48(1):64–71.

    Article  PubMed  Google Scholar 

  21. Kalden-Nemeth D, Grebmeier J, Antoni C, Manger B, Wolf F, Kalden JR. NMR monitoring of rheumatoid arthritis patients receiving anti-TNF-alpha monoclonal antibody therapy. Rheumatol Int. 1997;16(6):249–55.

    Article  PubMed  CAS  Google Scholar 

  22. Brown AK, Quinn MA, Karim Z, Conaghan PG, Peterfy CG, Hensor E, et al. Presence of significant synovitis in rheumatoid arthritis patients with disease-modifying antirheumatic drug-induced clinical remission: evidence from an imaging study may explain structural progression. Arthritis Rheum. 2006;54(12):3761–73.

    Article  PubMed  CAS  Google Scholar 

  23. Frosch M, Foell D, Ganser G, Roth J. Arthrosonography of hip and knee joints in the follow up of juvenile rheumatoid arthritis. Ann Rheum Dis. 2003;62(3):242–4.

    Article  PubMed  CAS  Google Scholar 

  24. Brasch RC, Weinmann HJ, Wesbey GE. Contrast-enhanced NMR imaging: animal studies using gadolinium-DTPA complex. AJR Am J Roentgenol. 1984;142(3):625–30.

    Article  PubMed  CAS  Google Scholar 

  25. Ross JS, Delamarter R, Hueftle MG, Masaryk TJ, Aikawa M, Carter J, et al. Gadolinium-DTPA-enhanced MR imaging of the postoperative lumbar spine: time course and mechanism of enhancement. AJR Am J Roentgenol. 1989;152(4):825–34.

    Article  PubMed  CAS  Google Scholar 

  26. Wilson SR, Burns PN, Muradali D, Wilson JA, Lai X. Harmonic hepatic US with microbubble contrast agent: initial experience showing improved characterization of hemangioma, hepatocellular carcinoma, and metastasis. Radiology. 2000;215(1):153–61.

    PubMed  CAS  Google Scholar 

  27. Platzgummer H, Schueller G, Grisar J, Weber M, Schueller-Weidekamm C. Quantification of synovitis in rheumatoid arthritis: do we really need quantitative measurement of contrast-enhanced ultrasound? Eur J Radiol. 2009;71(2):237–41.

    Article  PubMed  Google Scholar 

  28. Szkudlarek M, Court-Payen M, Strandberg C, Klarlund M, Klausen T, Ostergaard M. Contrast-enhanced power Doppler ultrasonography of the metacarpophalangeal joints in rheumatoid arthritis. Eur Radiol. 2003;13(1):163–8.

    PubMed  Google Scholar 

  29. Ostergaard M, Stoltenberg M, Lovgreen-Nielsen P, Volck B, Sonne-Holm S, Lorenzen I. Quantification of synovitis by MRI: correlation between dynamic and static gadolinium-enhanced magnetic resonance imaging and microscopic and macroscopic signs of synovial inflammation. Magn Reson Imaging. 1998;16(7):743–54.

    Article  PubMed  CAS  Google Scholar 

  30. Tamai K, Yamato M, Yamaguchi T, Ohno W. Dynamic magnetic resonance imaging for the evaluation of synovitis in patients with rheumatoid arthritis. Arthritis Rheum. 1994;37(8):1151–7.

    Article  PubMed  CAS  Google Scholar 

  31. Kubassova OA, Boyle RD, Radjenovic A. Quantitative analysis of dynamic contrast-enhanced MRI datasets of the metacarpophalangeal joints. Acad Radiol. 2007;14(10):1189–200.

    Article  PubMed  Google Scholar 

  32. van Dijke CF, Peterfy CG, Brasch RC, Lang P, Roberts TP, Shames D, et al. MR imaging of the arthritic rabbit knee joint using albumin-(Gd-DTPA)30 with correlation to histopathology. Magn Reson Imaging. 1999;17(2):237–45.

    Article  PubMed  Google Scholar 

  33. Meier R, Krug C, Golovko D, Boddington S, Piontek G, Rudelius M, et al. Indocyanine green-enhanced imaging of antigen-induced arthritis with an integrated optical imaging/radiography system. Arthritis Rheum. 2010;62(8):2322–7.

    Article  PubMed  Google Scholar 

  34. Werner SG, Langer HE, Ohrndorf S, Bahner M, Schott P, Schwenke C, et al. Inflammation assessment in patients with arthritis using a novel in vivo fluorescence optical imaging technology. Ann Rheum Dis. 2012;71(4):504–10.

    Article  PubMed  Google Scholar 

  35. Meier RTK, Moog P, Noël PB, Ahari C, Sievert M, Dorn F, et al. Detection of synovitis in the hands of patients with rheumatologic disorders: diagnostic performance of optical imaging in comparison with magnetic resonance imaging. Arthritis Rheum. 2012;64(8):2489–98.

    Article  PubMed  Google Scholar 

  36. Weissleder R. Molecular imaging: exploring the next frontier. Radiology. 1999;212(3):609–14.

    PubMed  CAS  Google Scholar 

  37. Hoffman JM, Gambhir SS. Molecular imaging: the vision and opportunity for radiology in the future. Radiology. 2007;244(1):39–47.

    Article  PubMed  Google Scholar 

  38. Mahmood U, Weissleder R. Some tools for molecular imaging. Acad Radiol. 2002;9(6):629–31.

    Article  PubMed  Google Scholar 

  39. Becker W, Goldenberg DM, Wolf F. The use of monoclonal antibodies and antibody fragments in the imaging of infectious lesions. Semin Nucl Med. 1994;24(2):142–53.

    Article  PubMed  CAS  Google Scholar 

  40. Weissleder R, Lee AS, Fischman AJ, Reimer P, Shen T, Wilkinson R, et al. Polyclonal human immunoglobulin G labeled with polymeric iron oxide: antibody MR imaging. Radiology. 1991;181(1):245–9.

    PubMed  CAS  Google Scholar 

  41. Huang X, Lee S, Chen X. Design of “smart” probes for optical imaging of apoptosis. Am J Nucl Med Mol Imaging. 2011;1(1):3–17.

    PubMed  CAS  Google Scholar 

  42. Bremer C, Ntziachristos V, Weitkamp B, Theilmeier G, Heindel W, Weissleder R. Optical imaging of spontaneous breast tumors using protease sensing ‘smart’ optical probes. Investig Radiol. 2005;40(6):321–7.

    Article  CAS  Google Scholar 

  43. Weissleder R, Elizondo G, Wittenberg J, Lee AS, Josephson L, Brady TJ. Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology. 1990;175(2):494–8.

    PubMed  CAS  Google Scholar 

  44. Choi SH, Cho HR, Kim HS, Kim YH, Kang KW, Kim H, et al. Imaging and quantification of metastatic melanoma cells in lymph nodes with a ferritin MR reporter in living mice. NMR Biomed. 2012;25(5):737–45.

    Article  PubMed  Google Scholar 

  45. Lallemand C, Kavrochorianou N, Steenholdt C, Bendtzen K, Ainsworth MA, Meritet JF, et al. Reporter gene assay for the quantification of the activity and neutralizing antibody response to TNFalpha antagonists. J Immunol Methods. 2011;373(1–2):229–39.

    Article  PubMed  CAS  Google Scholar 

  46. Dannenberg Jr AM. Macrophages in inflammation and infection. N Engl J Med. 1975;293(10):489–93.

    Article  PubMed  Google Scholar 

  47. Li J, Hsu HC, Yang P, Wu Q, Li H, Edgington LE, et al. Treatment of arthritis by macrophage depletion and immunomodulation: testing an apoptosis-mediated therapy in a humanized death receptor mouse model. Arthritis Rheum. 2012;64(4):1098–109.

    Article  PubMed  CAS  Google Scholar 

  48. Long DM, Multer FK, Greenburg AG, Peskin GW, Lasser EC, Wickham WG, et al. Tumor imaging with x-rays using macrophage uptake of radiopaque fluorocarbon emulsions. Surgery. 1978;84(1):104–12.

    PubMed  CAS  Google Scholar 

  49. Bierry G, Jehl F, Boehm N, Robert P, Prevost G, Dietemann JL, et al. Macrophage activity in infected areas of an experimental vertebral osteomyelitis model: USPIO-enhanced MR imaging–feasibility study. Radiology. 2008;248(1):114–23.

    Article  PubMed  Google Scholar 

  50. Hauger O, Grenier N, Deminere C, Lasseur C, Delmas Y, Merville P, et al. USPIO-enhanced MR imaging of macrophage infiltration in native and transplanted kidneys: initial results in humans. Eur Radiol. 2007;17(11):2898–907.

    Article  PubMed  Google Scholar 

  51. Bierry G, Jehl F, Neuville A, Lefevre S, Robert P, Kremer S, et al. MRI of macrophages in infectious knee synovitis. AJR Am J Roentgenol. 2010;194(6):W521–6.

    Article  PubMed  Google Scholar 

  52. Lutz AM, Seemayer C, Corot C, Gay RE, Goepfert K, Michel BA, et al. Detection of synovial macrophages in an experimental rabbit model of antigen-induced arthritis: ultrasmall superparamagnetic iron oxide-enhanced MR imaging. Radiology. 2004;233(1):149–57.

    Article  PubMed  Google Scholar 

  53. Lefevre S, Ruimy D, Jehl F, Neuville A, Robert P, Sordet C, et al. Septic arthritis: monitoring with USPIO-enhanced macrophage MR imaging. Radiology. 2011;258(3):722–8.

    Article  PubMed  Google Scholar 

  54. Gent YY, Voskuyl AE, Kloet RW, van Schaardenburg D, Hoekstra OS, Dijkmans BA, et al. Macrophage positron emission tomography imaging as a biomarker for preclinical rheumatoid arthritis: findings of a prospective pilot study. Arthritis Rheum. 2012;64(1):62–6.

    Article  PubMed  Google Scholar 

  55. Turk MJ, Breur GJ, Widmer WR, Paulos CM, Xu LC, Grote LA, et al. Folate-targeted imaging of activated macrophages in rats with adjuvant-induced arthritis. Arthritis Rheum. 2002;46(7):1947–55.

    Article  PubMed  Google Scholar 

  56. Matteson EL, Lowe VJ, Prendergast FG, Crowson CS, Moder KG, Morgenstern DE, et al. Assessment of disease activity in rheumatoid arthritis using a novel folate targeted radiopharmaceutical Folatescan. Clin Exp Rheumatol. 2009;27(2):253–9.

    PubMed  CAS  Google Scholar 

  57. Nakajima A, Seroogy CM, Sandora MR, Tarner IH, Costa GL, Taylor-Edwards C, et al. Antigen-specific T cell-mediated gene therapy in collagen-induced arthritis. J Clin Investig. 2001;107(10):1293–301.

    Article  PubMed  CAS  Google Scholar 

  58. Marcus C, Thakur ML, Huynh TV, Louie JS, Leibling M, Minami C, et al. Imaging rheumatic joint diseases with anti-T lymphocyte antibody OKT-3. Nucl Med Commun. 1994;15(10):824–30.

    Article  PubMed  CAS  Google Scholar 

  59. Martins FP, Gutfilen B, de Souza SA, de Azevedo MN, Cardoso LR, Fraga R, et al. Monitoring rheumatoid arthritis synovitis with 99mTc-anti-CD3. Br J Radiol. 2008;81(961):25–9.

    Article  PubMed  CAS  Google Scholar 

  60. Yeh TC, Zhang W, Ildstad ST, Ho C. Intracellular labeling of T-cells with superparamagnetic contrast agents. Magn Reson Med. 1993;30(5):617–25.

    Article  PubMed  CAS  Google Scholar 

  61. Tran L, Huitema AD, van Rijswijk MH, Dinant HJ, Baars JW, Beijnen JH, et al. CD20 antigen imaging with 124I-rituximab PET/CT in patients with rheumatoid arthritis. Hum Antibodies. 2011;20:29–35.

    PubMed  CAS  Google Scholar 

  62. Cascao R, Rosario HS, Souto-Carneiro MM, Fonseca JE. Neutrophils in rheumatoid arthritis: more than simple final effectors. Autoimmun Rev. 2010;9(8):531–5.

    Article  PubMed  CAS  Google Scholar 

  63. Jorgensen C, Apparailly F, Couret I, Canovas F, Jacquet C, Sany J. Interleukin-4 and interleukin-10 are chondroprotective and decrease mononuclear cell recruitment in human rheumatoid synovium in vivo. Immunology. 1998;93(4):518–23.

    Article  PubMed  CAS  Google Scholar 

  64. Taylor PC, Peters AM, Paleolog E, Chapman PT, Elliott MJ, McCloskey R, et al. Reduction of chemokine levels and leukocyte traffic to joints by tumor necrosis factor alpha blockade in patients with rheumatoid arthritis. Arthritis Rheum. 2000;43(1):38–47.

    Article  PubMed  CAS  Google Scholar 

  65. Gross S, Gammon ST, Moss BL, Rauch D, Harding J, Heinecke JW, et al. Bioluminescence imaging of myeloperoxidase activity in vivo. Nat Med. 2009;15(4):455–61.

    Article  PubMed  CAS  Google Scholar 

  66. Babior BM. The respiratory burst of phagocytes. J Clin Investig. 1984;73(3):599–601.

    Article  PubMed  CAS  Google Scholar 

  67. Matsui T, Nakata N, Nagai S, Nakatani A, Takahashi M, Momose T, et al. Inflammatory cytokines and hypoxia contribute to 18F-FDG uptake by cells involved in pannus formation in rheumatoid arthritis. J Nucl Med Off Publ Soc Nucl Med. 2009;50(6):920–6.

    CAS  Google Scholar 

  68. Beckers C, Ribbens C, Andre B, Marcelis S, Kaye O, Mathy L, et al. Assessment of disease activity in rheumatoid arthritis with (18)F-FDG PET. J Nucl Med Off Publ Soc Nucl Med. 2004;45(6):956–64.

    CAS  Google Scholar 

  69. Palmer WE, Rosenthal DI, Schoenberg OI, Fischman AJ, Simon LS, Rubin RH, et al. Quantification of inflammation in the wrist with gadolinium-enhanced MR imaging and PET with 2-[F-18]-fluoro-2-deoxy-D-glucose. Radiology. 1995;196(3):647–55.

    PubMed  CAS  Google Scholar 

  70. Kubota K, Ito K, Morooka M, Mitsumoto T, Kurihara K, Yamashita H, et al. Whole-body FDG-PET/CT on rheumatoid arthritis of large joints. Ann Nucl Med. 2009;23(9):783–91.

    Article  PubMed  Google Scholar 

  71. Golman K, Olsson LE, Axelsson O, Mansson S, Karlsson M, Petersson JS. Molecular imaging using hyperpolarized 13C. Br J Radiol. 2003;76(Spec No 2):S118–27.

    Article  PubMed  CAS  Google Scholar 

  72. MacKenzie JD, Yen YF, Mayer D, Tropp JS, Hurd RE, Spielman DM. Detection of inflammatory arthritis by using hyperpolarized 13C-pyruvate with MR imaging and spectroscopy. Radiology. 2011;259(2):414–20.

    Article  PubMed  Google Scholar 

  73. Ostergaard M, Hansen M, Stoltenberg M, Gideon P, Klarlund M, Jensen KE, et al. Magnetic resonance imaging-determined synovial membrane volume as a marker of disease activity and a predictor of progressive joint destruction in the wrists of patients with rheumatoid arthritis. Arthritis Rheum. 1999;42(5):918–29.

    Article  PubMed  CAS  Google Scholar 

  74. Roivainen A, Parkkola R, Yli-Kerttula T, Lehikoinen P, Viljanen T, Mottonen T, et al. Use of positron emission tomography with methyl-11C-choline and 2-18F-fluoro-2-deoxy-D-glucose in comparison with magnetic resonance imaging for the assessment of inflammatory proliferation of synovium. Arthritis Rheum. 2003;48(11):3077–84.

    Article  PubMed  CAS  Google Scholar 

  75. Thakur ML, Zhang K, Paudyal B, Devakumar D, Covarrubias MY, Cheng C, et al. Targeting apoptosis for optical imaging of infection. Mol Imaging Biol MIB Off Publ Acad Mol Imaging. 2012;14(2):163–71.

    Article  Google Scholar 

  76. Post AM, Katsikis PD, Tait JF, Geaghan SM, Strauss HW, Blankenberg FG. Imaging cell death with radiolabeled annexin V in an experimental model of rheumatoid arthritis. J Nucl Med Off Publ Soc Nucl Med. 2002;43(10):1359–65.

    CAS  Google Scholar 

  77. Wunder A, Schellenberger E, Mahmood U, Bogdanov Jr A, Muller-Ladner U, Weissleder R, et al. Methotrexate-induced accumulation of fluorescent annexin V in collagen-induced arthritis. Mol Imaging. 2005;4(1):1–6.

    PubMed  Google Scholar 

  78. van Loo G, Beyaert R. Negative regulation of NF-kappaB and its involvement in rheumatoid arthritis. Arthritis Res Ther. 2011;13(3):221.

    Article  PubMed  Google Scholar 

  79. Carlsen H, Moskaug JO, Fromm SH, Blomhoff R. In vivo imaging of NF-kappa B activity. J Immunol. 2002;168(3):1441–6.

    PubMed  CAS  Google Scholar 

  80. Izmailova ES, Paz N, Alencar H, Chun M, Schopf L, Hepperle M, et al. Use of molecular imaging to quantify response to IKK-2 inhibitor treatment in murine arthritis. Arthritis Rheum. 2007;56(1):117–28.

    Article  PubMed  CAS  Google Scholar 

  81. Walsh DA. Angiogenesis and arthritis. Rheumatology (Oxford). 1999;38(2):103–12.

    Article  CAS  Google Scholar 

  82. Ballara S, Taylor PC, Reusch P, Marme D, Feldmann M, Maini RN, et al. Raised serum vascular endothelial growth factor levels are associated with destructive change in inflammatory arthritis. Arthritis Rheum. 2001;44(9):2055–64.

    Article  PubMed  CAS  Google Scholar 

  83. Levashova Z, Backer M, Backer JM, Blankenberg FG. Imaging vascular endothelial growth factor (VEGF) receptors in turpentine-induced sterile thigh abscesses with radiolabeled single-chain VEGF. J Nucl Med Off Publ Soc Nucl Med. 2009;50(12):2058–63.

    Google Scholar 

  84. Nagengast WB, Lub-de Hooge MN, Oosting SF, den Dunnen WF, Warnders FJ, Brouwers AH, et al. VEGF-PET imaging is a noninvasive biomarker showing differential changes in the tumor during sunitinib treatment. Cancer Res. 2011;71(1):143–53.

    Article  PubMed  CAS  Google Scholar 

  85. Jubeli E, Moine L, Vergnaud-Gauduchon J, Barratt G. E-selectin as a target for drug delivery and molecular imaging. J Control Release Of J Control Release Soc. 2012;158(2):194–206.

    Article  CAS  Google Scholar 

  86. Chapman PT, Jamar F, Keelan ET, Peters AM, Haskard DO. Use of a radiolabeled monoclonal antibody against E-selectin for imaging of endothelial activation in rheumatoid arthritis. Arthritis Rheum. 1996;39(8):1371–5.

    Article  PubMed  CAS  Google Scholar 

  87. Robinson SD, Hodivala-Dilke KM. The role of beta3-integrins in tumor angiogenesis: context is everything. Curr Opin Cell Biol. 2011;23(5):630–7.

    Article  PubMed  CAS  Google Scholar 

  88. Firestein GS. Starving the synovium: angiogenesis and inflammation in rheumatoid arthritis. J Clin Investig. 1999;103(1):3–4.

    Article  PubMed  CAS  Google Scholar 

  89. Sipkins DA, Cheresh DA, Kazemi MR, Nevin LM, Bednarski MD, Li KC. Detection of tumor angiogenesis in vivo by alphaVbeta3-targeted magnetic resonance imaging. Nat Med. 1998;4(5):623–6.

    Article  PubMed  CAS  Google Scholar 

  90. Mohammed FF, Smookler DS, Khokha R. Metalloproteinases, inflammation, and rheumatoid arthritis. Ann Rheum Dis. 2003;62 Suppl 2:ii43–7.

    PubMed  CAS  Google Scholar 

  91. Raymond SB, Skoch J, Hills ID, Nesterov EE, Swager TM, Bacskai BJ. Smart optical probes for near-infrared fluorescence imaging of Alzheimer’s disease pathology. Eur J Nucl Med Mol Imaging. 2008;35 Suppl 1:S93–8.

    Article  PubMed  Google Scholar 

  92. Wunder A, Tung CH, Muller-Ladner U, Weissleder R, Mahmood U. In vivo imaging of protease activity in arthritis: a novel approach for monitoring treatment response. Arthritis Rheum. 2004;50(8):2459–65.

    Article  PubMed  CAS  Google Scholar 

  93. Yoshihara Y, Nakamura H, Obata K, Yamada H, Hayakawa T, Fujikawa K, et al. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis. Ann Rheum Dis. 2000;59(6):455–61.

    Article  PubMed  CAS  Google Scholar 

  94. Ouimet T, Lancelot E, Hyafil F, Rienzo M, Deux F, Lemaitre M, et al. Molecular and cellular targets of the MRI contrast agent p947 for atherosclerosis imaging. Mol Pharm. 2012;9(4):850–61.

    Article  PubMed  CAS  Google Scholar 

  95. Amirbekian V, Aguinaldo JG, Amirbekian S, Hyafil F, Vucic E, Sirol M, et al. Atherosclerosis and matrix metalloproteinases: experimental molecular MR imaging in vivo. Radiology. 2009;251(2):429–38.

    Article  PubMed  Google Scholar 

  96. Barrera P, Oyen WJ, Boerman OC, van Riel PL. Scintigraphic detection of tumour necrosis factor in patients with rheumatoid arthritis. Ann Rheum Dis. 2003;62(9):825–8.

    Article  PubMed  CAS  Google Scholar 

  97. Chianelli M, D’Alessandria C, Conti F, Priori R, Valesini G, Annovazzi A, et al. New radiopharmaceuticals for imaging rheumatoid arthritis. Q J Nucl Med Mol Imaging. 2006;50(3):217–25.

    PubMed  CAS  Google Scholar 

  98. Barrera P, van der Laken CJ, Boerman OC, Oyen WJ, van de Ven MT, van Lent PL, et al. Radiolabelled interleukin-1 receptor antagonist for detection of synovitis in patients with rheumatoid arthritis. Rheumatology (Oxford). 2000;39(8):870–4.

    Article  CAS  Google Scholar 

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  1. Department of Radiology, University Hospital of Strasbourg, 10 Avenue Molière, 67098, Strasbourg, France

    Guillaume Bierry & Jean-Louis Dietemann

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Bierry, G., Dietemann, JL. Imaging evaluation of inflammation in the musculoskeletal system: current concepts and perspectives. Skeletal Radiol 42, 1347–1359 (2013). https://doi.org/10.1007/s00256-013-1636-1

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