Possibilities of modern radiological modalities in the diagnosis of complicated diabetic foot syndrome

Document Type : Review Article

Authors

1 Department of Radiology and Radiotherapy, Siberian State Medical University, Tomsk, Russian Federation

2 Department Endocrinology and Diabetology, Siberian State Medical University, Tomsk, Russian Federation

Abstract

The issue of establishing the diagnosis and differential diagnosis of diabetic foot syndrome (DFS), including at the early stages, is of great relevance, which can be achieved by expanding information on current trends in the visualization of this frequent and severe complication of diabetes mellitus. The authors analyzed, systematized and summarized the modern pilot data on the use of high-tech medical imaging methods in DFS mainly over the past 7 years. An expert analytical assessment of the possibilities of molecular pathogen-specific visualization of pathological processes in DFS using modern methods of SPECT and PET is given. To solve the fundamental and applied aspects of diagnosing DFS, the possibilities of using high-energy radionuclides in bacterial infection were analyzed. The most important literature data of foot perfusion in patients with diabetes mellitus and limb ischemia using new modalities of MRI and hybrid diagnostic methods (SPECT/CT and PET/CT) are systematized, which contributes to a new understanding of the response to revascularization and healing of foot ulcers. This article is aimed at substantiating the multiparametric approach for DFS, as well as the selection, development and implementation of innovative diagnostic strategies in diagnosing DFS and its complications as part of the development of personalized medicine.

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  1. Ertuğrul B, Uçkay I, Schöni M, Peter-Riesch B, Lipsky BA. Management of diabetic foot infections in the light of recent literature and new international guidelines. Expert Rev Anti Infect Ther. 2020 Apr;18(4):293-305.
  2. Yammine K, Hayek F, Assi C. A meta-analysis of mortality after minor amputation among patients with diabetes and/or peripheral vascular disease. J Vasc Surg. 2020 Dec;72(6):2197-207.
  3. Dardari D. An overview of Charcot's neuroarthropathy. J Clin Transl Endocrinol. 2020 Oct 28;22:100239.
  4. Gazzaruso C, Gallotti P, Pujia A, Montalcini T, Giustina A, Coppola A. Predictors of healing, ulcer recurrence and persistence, amputation and mortality in type 2 diabetic patients with diabetic foot: a 10-year retrospective cohort study. Endocrine. 2021 Jan;71(1):59-68.
  5. Lázaro-Martínez JL, García-Madrid M, García-Álvarez Y, Álvaro-Afonso FJ, Sanz-Corbalán I, García-Morales E. Conservative surgery for chronic diabetic foot osteomyelitis: Procedures and recommendations. J Clin Orthop Trauma. 2020 Dec 15;16:86-98.
  6. Rubitschung K, Sherwood A, Crisologo AP, Bhavan K, Haley RW, Wukich DK, Castellino L, Hwang H, La Fontaine J, Chhabra A, Lavery L, Öz OK. Pathophysiology and molecular imaging of diabetic foot infections. Int J Mol Sci. 2021 Oct 26;22(21):11552.
  7. Casali M, Lauri C, Altini C, Bertagna F, Cassarino G, Cistaro A, Erba AP, Ferrari C, Mainolfi CG, Palucci A, Prandini N, Baldari S, Bartoli F, Bartolomei M, D'Antonio A, Dondi F, Gandolfo P, Giordano A, Laudicella R, Massollo M, Nieri A, Piccardo A, Vendramin L, Muratore F, Lavelli V, Albano D, Burroni L, Cuocolo A, Evangelista L, Lazzeri E, Quartuccio N, Rossi B, Rubini G, Sollini M, Versari A, Signore A. State of the art of 18F-FDG PET/CT application in inflammation and infection: a guide for image acquisition and interpretation. Clin Transl Imaging. 2021;9(4):299-339.
  8. Fridman R, Bar-David T, Kamen S, Staron RB, Leung DK, Rasiej MJ. Imaging of diabetic foot infections. Clin Podiatr Med Surg. 2014 Jan;31(1):43-56.
  9. Lauri C, Glaudemans AWJM, Signore A. Leukocyte imaging of the diabetic foot. Curr Pharm Des. 2018;24(12):1270-6.
  10. Signore A, Jamar F, Israel O, Buscombe J, Martin-Comin J, Lazzeri E. Clinical indications, image acquisition and data interpretation for white blood cells and anti-granulocyte monoclonal antibody scintigraphy: an EANM procedural guideline. Eur J Nucl Med Mol Imaging. 2018 Sep;45(10):1816-31.
  11. Lauri C, Tamminga M, Glaudemans AWJM, Juárez Orozco LE, Erba PA, Jutte PC, Lipsky BA, IJzerman MJ, Signore A, Slart RHJA. Detection of osteomyelitis in the diabetic foot by imaging techniques: a systematic review and meta-analysis comparing MRI, white blood cell scintigraphy, and FDG-PET. Diabetes Care. 2017 Aug;40(8):1111-20.
  12. Lauri C, Leone A, Cavallini M, Signore A, Giurato L, Uccioli L. Diabetic foot infections: the diagnostic challenges. J Clin Med. 2020 Jun 8;9(6):1779.
  13. Ahmed N, Fatima S, Saeed MA, Zia M, Irfan Ullah J. 99m Tc-Ceftizoxime: synthesis, characterization and its use in diagnosis of diabetic foot osteomyelitis. J Med Imaging Radiat Oncol. 2019 Feb;63(1):61-8.
  14. Lauri C, Glaudemans AWJM, Campagna G, Keidar Z, Muchnik Kurash M, Georga S, Arsos G, Noriega-Álvarez E, Argento G, Kwee TC, Slart RHJA, Signore A. Comparison of white blood cell scintigraphy, FDG PET/CT and MRI in suspected diabetic foot infection: results of a large retrospective multicenter study. J Clin Med. 2020 May 30;9(6):1645.
  15. Ankrah AO, Klein HC, Elsinga PH. New imaging tracers for the infected diabetic foot (nuclear and optical imaging). Curr Pharm Des. 2018;24(12):1287-303.
  16. Ruiz-Bedoya CA, Gordon O, Mota F, Abhishek S, Tucker EW, Ordonez AA, Jain SK. Molecular imaging of diabetic foot infections: new tools for old questions. Int J Mol Sci. 2019 Nov 28;20(23):5984.
  17. Koźmiński P, Gawęda W, Rzewuska M, Kopatys A, Kujda S, Dudek MK, Halik PK, Królicki L, Gniazdowska E. Physicochemical and biological study of 99mTc and 68Ga radiolabelled ciprofloxacin and evaluation of [99mTc]Tc-CIP as potential diagnostic radiopharmaceutical for diabetic foot syndrome imaging. Tomography. 2021 Dec;7(4):829-42.
  18. Yang C, Ren C, Zhou J, Liu J, Zhang Y, Huang F, Ding D, Xu B, Liu J. Dual fluorescent- and isotopic-labelled self-assembling vancomycin for in vivo imaging of bacterial infections. Angew Chem Int Ed Engl. 2017 Feb 20;56(9):2356-60.
  19. Ahluwalia R, Bilal A, Petrova N, Boddhu K, Manu C, Vas P, Bates M, Corcoran B, Reichert I, Mulholland N, Kavarthapu V, Vivian G, Edmonds M. The role of bone scintigraphy with SPECT/CT in the characterization and early diagnosis of stage 0 charcot neuroarthropathy. J Clin Med. 2020 Dec 21;9(12):4123.
  20. Vouillarmet J, Moret M, Morelec I, Michon P, Dubreuil J. Application of white blood cell SPECT/CT to predict remission after a 6 or 12 week course of antibiotic treatment for diabetic foot osteomyelitis. Diabetologia. 2017 Dec;60(12):2486-2494.
  21. Jeffcoate WJ. Osteomyelitis of the foot: non-surgical management, SPECT/CT scanning and minimising the duration of antibiotic use. Diabetologia. 2017 Dec;60(12):2337-40.
  22. 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 Oct;131:109215.
  23. Yang H, Zhuang H, Rubello D, Alavi A. Mild-to-moderate hyperglycemia will not decrease the sensitivity of 18F-FDG PET imaging in the detection of pedal osteomyelitis in diabetic patients. Nucl Med Commun. 2016 Mar;37(3):259-62.
  24. Glaudemans AWJM, Jutte PC, Cataldo MA, Cassar-Pullicino V, Gheysens O, Borens O, Trampuz A, Wörtler K, Petrosillo N, Winkler H, Signore A, Sconfienza LM. Consensus document for the diagnosis of peripheral bone infection in adults: a joint paper by the EANM, EBJIS, and ESR (with ESCMID endorsement). Eur J Nucl Med Mol Imaging. 2019 Apr;46(4):957-70.
  25. Diez AIG, Fuster D, Morata L, Torres F, Garcia R, Poggio D, Sotes S, Del Amo M, Isern-Kebschull J, Pomes J, Soriano A, Brugnara L, Tomas X. Comparison of the diagnostic accuracy of diffusion-weighted and dynamic contrast-enhanced MRI with 18F-FDG PET/CT to differentiate osteomyelitis from Charcot neuro-osteoarthropathy in diabetic foot. Eur J Radiol. 2020 Nov;132:109299.
  26. Senneville EM, Lipsky BA, van Asten SAV, Peters EJ. Diagnosing diabetic foot osteomyelitis. Diabetes Metab Res Rev. 2020 Mar;36 Suppl 1:e3250.
  27. Torigian DA, Kjær A, Zaidi H, Alavi A. PET/MR imaging: clinical applications. PET Clin. 2016 Oct;11(4):xi-xii.
  28. Udodov V.D., Zorkaltsev M.A., Zavadovskaya V.D., Zamyshevskaya M.A., Grigorev E.G., Kurazhov A.P. Hybrid SPECT-WBC/MRI in the diagnosis of diabetic foot syndrome. Med Vis. 2016;(2):36-42.
  29. Meacock L, Petrova NL, Donaldson A, Isaac A, Briody A, Ramnarine R, Edmonds ME, Elias DA. Novel semiquantitative bone marrow oedema score and fracture score for the magnetic resonance imaging assessment of the active charcot foot in diabetes. J Diabetes Res. 2017;2017:8504137.
  30. Alvelo JL, Papademetris X, Mena-Hurtado C, Jeon S, Sumpio BE, Sinusas AJ, Stacy MR. Radiotracer imaging allows for noninvasive detection and quantification of abnormalities in angiosome foot perfusion in diabetic patients with critical limb ischemia and nonhealing wounds. Circ Cardiovasc Imaging. 2018 May;11(5):e006932.
  31. Mahendra M, Singh R. Diagnostic accuracy and surgical utility of MRI in complicated diabetic foot. J Clin Diagn Res. 2017 Jul;11(7):RC01-4.
  32. Misra S, Shishehbor MH, Takahashi EA, Aronow HD, Brewster LP, Bunte MC, Kim ESH, Lindner JR, Rich K; American Heart Association Council on peripheral vascular disease; council on clinical cardiology; and council on cardiovascular and stroke nursing. perfusion assessment in critical limb ischemia: principles for understanding and the development of evidence and evaluation of devices: a scientific statement from the American Heart Association. Circulation. 2019 Sep 17;140(12):e657-72.
  33. Chou TH, Atway SA, Bobbey AJ, Sarac TP, Go MR, Stacy MR. SPECT/CT imaging: a noninvasive approach for evaluating serial changes in angiosome foot perfusion in critical limb ischemia. Adv Wound Care (New Rochelle). 2020 Mar 1;9(3):103-10.