Abstract
Purpose
We endeavored to determine which characteristics of diabetic ulcers portend the strongest risk for osteomyelitis in patients whose initial T1-weighted imaging was normal. By determining which features have a greater risk for osteomyelitis, clinicians can treat patients more aggressively to reduce the sequela of inadequately treated osteomyelitis.
Materials and methods
We performed a retrospective analysis of MR imaging from 60 pedal ulcers with suspected osteomyelitis. Ulcer dimensions and depth were measured. Ratios of marrow ROI/joint fluid ROI on T2/STIR sequences were obtained. Progression to osteomyelitis on subsequent MRI was characterized by loss of normal marrow signal on T1-weighted images. Statistical analysis was performed with a two-sample t test and Cox proportional hazard model. A p value < 0.05 was used as the threshold for statistical significance.
Results
Sixty MR exams were identified. Thirty-four progressed to osteomyelitis. Marrow ROI/joint fluid ratios averaged 65% in the osteomyelitis group, and 45% in the non-osteomyelitis group, p < 0.001. ROI ratios > 53% had a 6.5-fold increased risk of osteomyelitis, p < 0.001. Proximity to bone averaged 6 mm in the osteomyelitis group and 9 mm in the non-osteomyelitis group, p = 0.02. Ulcer size averaged 4 cm2 in the osteomyelitis group versus 2.4 cm2 in the non-osteomyelitis group, p = 0.07. Ulcers greater than 3 cm2 has a 2-fold increase in the risk of osteomyelitis, p = 0.04.
Conclusion
Increasing bone marrow ROI signal/joint fluid ratios on T2/STIR images were the strongest risk factors for developing osteomyelitis, while ulcer size and depth are weaker predictors.
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References
Centers for Disease Control and Prevention (CDC). National Diabetes Statistics Report, 2017. July 2017:1–20.
Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA. 2005;293(2):217–28. https://doi.org/10.1001/jama.293.2.217.
Mutluoglu M, Sivrioglu AK, Eroglu M, et al. The implications of the presence of osteomyelitis on outcomes of infected diabetic foot wounds. Scand J Infect Dis. 2013;45(7):497–503. https://doi.org/10.3109/00365548.2013.765589.
Aulivola B, Hile CN, Hamdan AD, et al. Major lower extremity amputation: outcome of a modern series. Arch Surg. 2004;139(4):395–9 discussion399.
Schaper NC, Apelqvist J, Bakker K. Reducing lower leg amputations in diabetes: a challenge for patients, healthcare providers and the healthcare system. Diabetologia. 2012;55(7):1869–72.
Newman LG. Unsuspected osteomyelitis in diabetic foot ulcers. JAMA. 1991;266(9):1246–51. https://doi.org/10.1001/jama.1991.03470090080036.
Barshes NR, Mindru C, Ashong C, Rodriguez-Barradas M, Trautner BW. Treatment failure and leg amputation among patients with foot osteomyelitis. Int J Low Extrem Wounds. 2016;15(4):303–12. https://doi.org/10.1177/1534734616661058.
Noor S, Khan RU, Ahmad J. Understanding diabetic foot infection and its management. Diabetes Metab Syndr. 2017;11(2):149–56. https://doi.org/10.1016/j.dsx.2016.06.023.
Zeun P, Gooday C, Nunney I, Dhatariya K. Predictors of outcomes in diabetic foot osteomyelitis treated initially with conservative (nonsurgical) medical management. Int J Low Extrem Wounds. 2016;15(1):19–25. https://doi.org/10.1177/1534734615596892.
Dinh MT, Abad CL, Safdar N. Diagnostic accuracy of the physical examination and imaging tests for osteomyelitis underlying diabetic foot ulcers: meta-analysis. Clin Infect Dis. 2008;47(4):519–27. https://doi.org/10.1086/590011.
Donovan A, Schweitzer ME. Current concepts in imaging diabetic pedal osteomyelitis. Radiol Clin N Am. 2008;46(6):1105–24. https://doi.org/10.1016/j.rcl.2008.08.004.
Kapoor A, Page S, Lavalley M, Gale DR, Felson DT. Magnetic resonance imaging for diagnosing foot osteomyelitis: a meta-analysis. Arch Intern Med. 2007;167(2):125–32. https://doi.org/10.1001/archinte.167.2.125.
Mahendra M. Diagnostic accuracy and surgical utility of MRI in complicated diabetic foot. JCDR. 2017:1–4. doi:https://doi.org/10.7860/JCDR/2017/25902.10154.
Duryea D, Bernard S, Flemming D, Walker E, French C. Outcomes in diabetic foot ulcer patients with isolated T2 marrow signal abnormality in the underlying bone: should the diagnosis of “osteitis” be changed to ‘early osteomyelitis’?. Skelet Radiol 2017: 1–7. doi:https://doi.org/10.1007/s00256-017-2666-x.
Craig J, Amin M, Wu K, et al. Osteomyelftis ofthe diabetic foot: MR imaging-pathologic correlation. Radiology. 1997;203:849–55.
Morrison WB, Schweitzer ME, Batte WG, Radack DP, Russel KM. Osteomyelitis of the foot: relative importance of primary and secondary MR imaging signs. Radiology. 1998;207(3):625–32. https://doi.org/10.1148/radiology.207.3.9609883.
Donovan A, Schweitzer ME. Use of MR imaging in diagnosing diabetes-related pedal osteomyelitis. RadioGraphics. 2010;30(3):723–36. https://doi.org/10.1148/rg.303095111.
Toledano T, Fatone E, 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):257–68. https://doi.org/10.1055/s-0031-1278425.
Roug IK, Pierre-Jerome C. MRI spectrum of bone changes in the diabetic foot. Eur J Radiol. 2012;81(7):1625–9. https://doi.org/10.1016/j.ejrad.2011.04.048.
Johnson PW, Collins MS, Wenger DE. Diagnostic utility of T1-weighted MRI characteristics in evaluation of osteomyelitis of the foot. Am J Roentgenol. 2009;192(1):96–100. https://doi.org/10.2214/AJR.08.1376.
Collins MS, Schaar MM, Wenger DE, Mandrekar JN. T1-weighted MRI characteristics of pedal osteomyelitis. Am J Roentgenol. 2005;185:386–93.
McCarthy E, Morrison WB, Zoga A. MR imaging of the diabetic foot. Magn Reson Imaging Clin N Am. 2017;25(1):183–94. https://doi.org/10.1016/j.mric.2016.08.005.
Lavery LA, Peters EJG, Armstrong DG, Wendel CS, Murdoch DP, Lipsky BA. Risk factors for developing osteomyelitis in patients with diabetic foot wounds. Diabetes Res Clin Pract. 2009;83(3):347–52. https://doi.org/10.1016/j.diabres.2008.11.030.
Butalia S, Palda VA, Sargeant RJ, Detsky AS, Mourad O. Does this patient with diabetes have osteomyelitis of the lower extremity? JAMA. 2008;299(7):806–13. https://doi.org/10.1001/jama.299.7.806.
Lipsky BA, Aragón-Sánchez J, Diggle M, et al. IWGDF guidance on the diagnosis and management of foot infections in persons with diabetes. Diabetes Metab Res Rev. 2016;32(Suppl 1):45–74. https://doi.org/10.1002/dmrr.2699.
Newman LG, Waller J, Palestro CJ, et al. Unsuspected osteomyelitis in diabetic foot ulcers. Diagnosis and monitoring by leukocyte scanning with indium in 111 oxyquinoline. JAMA. 1991;266(9):1246–51.
Markanday A. Diagnosing diabetic foot osteomyelitis: narrative review and a suggested 2-step score-based diagnostic pathway for clinicians. Open Forum Infect Dis. 2014;1(2):1–6. https://doi.org/10.1093/ofid/ofu060.
Malhotra R, Chan CS-Y, Nather A. Osteomyelitis in the diabetic foot. Diabet Foot Ankle. 2014;5(1):24445. https://doi.org/10.3402/dfa.v5.24445.
Grayson ML, Gibbons GW, Balogh K, Levin E, Karchmer AW. Probing to bone in infected pedal ulcers. A clinical sign of underlying osteomyelitis in diabetic patients. JAMA. 1995;273(9):721–3.
Ang MT, Wong GR, Wong DR, Clements W, Joseph T. Diagnostic yield of computed tomography-guided biopsy and aspiration for vertebral osteomyelitis. J Med Imaging Radiat Oncol. 2019;63:589–95.
Czuczman GJ, Marrero DE, Huang AJ, et al. Diagnostic yield of repeat CT-guided biopsy for suspected infectious spondylodiscitis. Skelet Radiol. 2018;47(10):1403–10.
Hoang D, Fisher S, Oz OK, La Fontaine J, Chhabra A. Percutaneous CT guided bone biopsy for suspected osteomyelitis: diagnostic yield and impact on patient’s treatment change and recovery. Eur J Radiol. 2019;114:85–91.
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Sax, A.J., Halpern, E.J., Zoga, A.C. et al. Predicting osteomyelitis in patients whose initial MRI demonstrated bone marrow edema without corresponding T1 signal marrow replacement. Skeletal Radiol 49, 1239–1247 (2020). https://doi.org/10.1007/s00256-020-03396-x
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DOI: https://doi.org/10.1007/s00256-020-03396-x