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DOI: 10.1055/s-0043-1761494
Bone Marrow Changes and Lesions of Diabetic Foot and Ankle Disease: Conventional and Advanced Magnetic Resonance Imaging
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Abstract
Diabetic foot and ankle complications contribute to substantial mortality and morbidity. Early detection and treatment can lead to better patient outcomes. The primary diagnostic challenge for radiologists is distinguishing Charcot's neuroarthropathy from osteomyelitis. Magnetic resonance imaging (MRI) is the preferred imaging modality for assessing diabetic bone marrow alterations and for identifying diabetic foot complications. Several recent technical advances in MRI, such as the Dixon technique, diffusion-weighted imaging, and dynamic contrast-enhanced imaging, have led to improved image quality and increased capability to add more functional and quantitative information.
We discuss the bone marrow abnormalities encountered in daily radiologic assessment: osteopenia, reactive bone marrow edema-like signal, insufficiency fractures, Charcot's neuroarthropathy, osteomyelitis, serous marrow atrophy, digital ischemia, and bone infarcts, along with their pathophysiology and the conventional and advanced imaging techniques used for a comprehensive marrow evaluation.
Keywords
diabetes mellitus - bone marrow - foot and ankle - magnetic resonance imaging - Charcot's neuroarthropathyPublication History
Article published online:
03 March 2023
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References
- 1 Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. Lancet 2005; 366 (9498): 1719-1724
- 2 Jeffcoate WJ, Macfarlane RM, Fletcher EM. The description and classification of diabetic foot lesions. Diabet Med 1993; 10 (07) 676-679
- 3 Roug IK, Pierre-Jerome C. MRI spectrum of bone changes in the diabetic foot. Eur J Radiol 2012; 81 (07) 1625-1629
- 4 Singh J, Lalam R. Bone, Joint and Spinal Infections. In: Andreas A. et al, editors Grainger & Allison's Diagnostic Radiology. 7th edition. Elsevier Limited; 2021: 1184-1222
- 5 Toledano TR, Fatone EA, Weis A, Cotten A, Beltran J. MRI evaluation of bone marrow changes in the diabetic foot: a practical approach. Semin Musculoskelet Radiol 2011; 15 (03) 257-268
- 6 Rogers LC, Frykberg RG, Armstrong DG. et al. The Charcot foot in diabetes. Diabetes Care 2011; 34 (09) 2123-2129
- 7 Baker JC, Demertzis JL, Rhodes NG, Wessell DE, Rubin DA. Diabetic musculoskeletal complications and their imaging mimics. Radiographics 2012; 32 (07) 1959-1974
- 8 Lipsky BA, Berendt AR, Cornia PB. et al. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. J Am Podiatr Med Assoc 2013; 103 (01) 2-7
- 9 Berg BV. et al. General Principles of MRI of the Bone Marrow. Chapter 71. In: Pope TL, Bloem HL, Beltran J. et al, editors. Musculoskeletal Imaging. 2nd edition. Philadelphia: Saunders: Elsevier; 2008: 868-868
- 10 Moore SG, Dawson KL. Red and yellow marrow in the femur: age-related changes in appearance at MR imaging. Radiology 1990; 175 (01) 219-223
- 11 Moon C, Liu J. The effects of type 1 vs. type 2 diabetes on bone metabolism. Orthop Surg 2020; 3: 5
- 12 Sundararaghavan V, Mazur MM, Evans B, Liu J, Ebraheim NA. Diabetes and bone health: latest evidence and clinical implications. Ther Adv Musculoskelet Dis 2017; 9 (03) 67-74
- 13 Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet 2005; 366 (9502): 2058-2061
- 14 Rubitschung K, Sherwood A, Crisologo AP. et al. Pathophysiology and molecular imaging of diabetic foot infections. Int J Mol Sci 2021; 22 (21) 11552
- 15 Llewellyn A, Kraft J, Holton C, Harden M, Simmonds M. Imaging for detection of osteomyelitis in people with diabetic foot ulcers: a systematic review and meta-analysis. Eur J Radiol 2020; 131: 109215
- 16 Konin GP. et al. Diabetic Pedal Infection. In: Pope TL, Bloem HL, Beltran J. et al, editors. 2nd edition Musculoskeletal Imaging. Philadelphia: Saunders: Elsevier; 2008: 805-814
- 17 Gosangi B, Mandell JC, Weaver MJ. et al. Bone marrow edema at dual-energy CT: a game changer in the emergency department. Radiographics 2020; 40 (03) 859-874
- 18 Dreizin D, Ahlawat S, Del Grande F, Fayad LM. Gradient-echo in-phase and opposed-phase chemical shift imaging: role in evaluating bone marrow. Clin Radiol 2014; 69 (06) 648-657
- 19 Pezeshk P, Alian A, Chhabra A. Role of chemical shift and Dixon based techniques in musculoskeletal MR imaging. Eur J Radiol 2017; 94: 93-100
- 20 Omoumi P. The Dixon method in musculoskeletal MRI: from fat-sensitive to fat-specific imaging. Skeletal Radiol 2022; 51 (07) 1365-1369
- 21 Guerini H, Omoumi P, Guichoux F. et al. Fat suppression with Dixon techniques in musculoskeletal magnetic resonance imaging: a pictorial review. Semin Musculoskelet Radiol 2015; 19 (04) 335-347
- 22 Del Grande F, Santini F, Herzka DA. et al. Fat-suppression techniques for 3-T MR imaging of the musculoskeletal system. Radiographics 2014; 34 (01) 217-233
- 23 Abdel Razek AAK, Samir S. Diagnostic performance of diffusion-weighted MR imaging in differentiation of diabetic osteoarthropathy and osteomyelitis in diabetic foot. Eur J Radiol 2017; 89: 221-225
- 24 Desai S, Wadhwa V, Thakur U, Chhabra A. Role of diffusion weighted magnetic resonance imaging in diabetic foot and ankle disease. Biomed J Sci Tech Res 2021; 39 (03) 12
- 25 Costa FM, Canella C, Gasparetto E. Advanced magnetic resonance imaging techniques in the evaluation of musculoskeletal tumors. Radiol Clin North Am 2011; 49 (06) 1325-1358 , vii–viii
- 26 Herneth AM, Friedrich K, Weidekamm C. et al. Diffusion weighted imaging of bone marrow pathologies. Eur J Radiol 2005; 55 (01) 74-83
- 27 Liao D, Xie L, Han Y. et al. Dynamic contrast-enhanced magnetic resonance imaging for differentiating osteomyelitis from acute neuropathic arthropathy in the complicated diabetic foot. Skeletal Radiol 2018; 47 (10) 1337-1347
- 28 Jackuliak P, Payer J. Osteoporosis, fractures, and diabetes. Int J Endocrinol 2014; 2014: 820615
- 29 de Abreu MR, Wesselly M, Chung CB, Resnick D. Bone marrow MR imaging findings in disuse osteoporosis. Skeletal Radiol 2011; 40 (05) 571-575
- 30 Price P. The diabetic foot: quality of life. Clin Infect Dis 2004; 39 (Suppl. 02) S129-S131
- 31 Leone A, Cassar-Pullicino VN, Semprini A, Tonetti L, Magarelli N, Colosimo C. Neuropathic osteoarthropathy with and without superimposed osteomyelitis in patients with a diabetic foot. Skeletal Radiol 2016; 45 (06) 735-754
- 32 Sanders LJ, Frykberg RG. Diabetic neuropathic osteoarthropathy: charcot foot. The High Risk Foot in Diabetes Mellitus. (Frykberg RG. ed.), Churchill Livingstone, New York 1991
- 33 Rosskopf AB, Loupatatzis C, Pfirrmann CWA, Böni T, Berli MC. The Charcot foot: a pictorial review. Insights Imaging 2019; 10 (01) 77
- 34 Jones EA, Manaster BJ, May DA, Disler DG. Neuropathic osteoarthropathy: diagnostic dilemmas and differential diagnosis. Radiographics 2000; 20 (Spec No, suppl_1) S279-S293
- 35 Helms Clyde A. Arthritis. Chapter 6. In: Helms Clyde A. editor. Fundamentals of Skeletal Radiology, 5th Edition. Elsevier Inc.; 2020: 119-150
- 36 McCarthy E, Morrison WB, Zoga AC. MR imaging of the diabetic foot. Magn Reson Imaging Clin N Am 2017; 25 (01) 183-194
- 37 Berli MC, Higashigaito K, Götschi T, Pfirrmann CWA, Sutter R, Rosskopf AB. The “Balgrist Score” for evaluation of Charcot foot: a predictive value for duration of off-loading treatment. Skeletal Radiol 2021; 50 (02) 311-320
- 38 Zampa V, Bargellini I, Rizzo L. et al. Role of dynamic MRI in the follow-up of acute Charcot foot in patients with diabetes mellitus. Skeletal Radiol 2021; 40 (08) 991-999
- 39 Renner N, Wirth SH, Osterhoff G, Böni T, Berli M. Outcome after protected full weightbearing treatment in an orthopedic device in diabetic neuropathic arthropathy (Charcot arthropathy): a comparison of unilaterally and bilaterally affected patients. BMC Musculoskelet Disord 2016; 17 (01) 504
- 40 Ledermann HP, Morrison WB, Schweitzer ME. MR image analysis of pedal osteomyelitis: distribution, patterns of spread, and frequency of associated ulceration and septic arthritis. Radiology 2002; 223 (03) 747-755
- 41 Collins MS, Schaar MM, Wenger DE, Mandrekar JN. T1-weighted MRI characteristics of pedal osteomyelitis. AJR Am J Roentgenol 2005; 185 (02) 386-393
- 42 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
- 43 Ahmadi ME, Morrison WB, Carrino JA, Schweitzer ME, Raikin SM, Ledermann HP. Neuropathic arthropathy of the foot with and without superimposed osteomyelitis: MR imaging characteristics. Radiology 2006; 238 (02) 622-631
- 44 Singer AD, Umpierrez M, Kakarala A. et al. Performance of a rapid two-sequence screening protocol for osteomyelitis of the foot. Skeletal Radiol 2020; 49 (06) 977-984
- 45 Dallimore SM, Puli N, Kim D, Kaminski MR. Infrared dermal thermometry is highly reliable in the assessment of patients with Charcot neuroarthropathy. J Foot Ankle Res 2020; 13 (01) 56
- 46 Ledermann HP, Schweitzer ME, Morrison WB. Nonenhancing tissue on MR imaging of pedal infection: characterization of necrotic tissue and associated limitations for diagnosis of osteomyelitis and abscess. AJR Am J Roentgenol 2002; 178 (01) 215-222
- 47 Fujii M, Armstrong DG, Terashi H. Efficacy of magnetic resonance imaging in diagnosing diabetic foot osteomyelitis in the presence of ischemia. J Foot Ankle Surg 2013; 52 (06) 717-723
- 48 Ruhl KM, Katoh M, Langer S. et al. Time-resolved 3D MR angiography of the foot at 3 T in patients with peripheral arterial disease. AJR Am J Roentgenol 2008; 190 (06) W360–W364
- 49 Liu X, Fan Z, Zhang N. et al. Unenhanced MR angiography of the foot: initial experience of using flow-sensitive dephasing-prepared steady-state free precession in patients with diabetes. Radiology 2014; 272 (03) 885-894