Дифференциальная диагностика диабетической нейроостеоартропатии и остеомиелита стопы при помощи методов медицинской визуализации

Согласно современным представлениям, нейроостеоартропатия Шарко (стопа Шарко) рассматривается как асептический воспалительный процесс у лиц с дистальной полинейропатией, который приводит к повреждению костей и суставов. Чаще всего стопа Шарко формируется у пациентов с сахарным диабетом (СД) и поражает стопу и голеностопный сустав. Диабетическая нейроостеоартропатия (ДНОАП) подразделяется на активную и неактивную стадии. Типичная клиническая картина активной стадии диабетической нейроостеоартропатии представляет собой отек и гиперемию пораженной стопы с градиентом температур более 2 °C по сравнению с непораженной стопой. Неспецифическая клиническая картина активной стадии диабетической нейроостеоартропатии затрудняет постановку диагноза и часто приводит к необходимости дифференциальной диагностики активной стадии диабетической нейроостеоартропатии и остеомиелита, что является одним из наиболее сложных вопросов в клинической практике. Выявление на ранних стадиях этих состояний имеет решающее значение, поскольку лечение активной стадии диабетической нейроостеоартропатии может предотвратить необратимую деформацию стопы, а выявление остеомиелита позволит своевременно назначить антибиотикотерапию. Признаки изменений структур костей и стопы в активной стадии диабетической нейроостеоартропатии на изображениях, полученные методами компьютерной рентгеновской, магнитно-резонансной и эмиссионной томографии могут быть схожи с признаками остеомиелита, что определяет важность выбора метода визуализации при обследовании пациента и разработке эффективного алгоритма ранней диагностики ДНОАП. В данном обзоре основное внимание будет уделено отличительным признакам активной стадии диабетической нейроостеоартропатии и остеомиелита при использовании визуализирующих методов исследования.

1. International Diabetes Federation. IDF Diabetes Atlas 10th edition 2021. diabetesatlas.org. Published 2021. https://diabetesatlas.org/

2. Wukich DK, Schaper NC, Gooday C, et al. Guidelines on the diagnosis and treatment of active Charcot neuro-osteoarthropathy in persons with diabetes mellitus (IWGDF 2023). Diabetes Metab Res Rev. 2024. https://doi.org/10.1002/dmrr.3646

3. Dardari D. An overview of Charcot’s neuroarthropathy. J Clin Transl Endocrinol. 2020. https://doi.org/10.1016/j.jcte.2020.100239

4. Trieb K. The Charcot foot. The Bone & Joint Journal. 2016;98-B (9):1155-1159. https://doi.org/10.1302/0301-620x.98b9.37038

5. Rahman NA, Fauzi AA, Chung TY, Latif LA, Chan SC. Foot ulcers and their association with diabetic Charcot foot complications. Australian Journal of General Practice. 2020;49(1-2):48-53. https://doi.org/10.31128/ajgp-07-19-4991

6. Armstrong DG, Swerdlow MA, Armstrong AA, et al. Five year mortality and direct costs of care for people with diabetic foot complications are comparable to cancer. Journal of Foot and Ankle Research. 2020;13(1). https://doi.org/10.1186/s13047-020-00383-2

7. Jansen RB, Svendsen OL. A review of bone metabolism and developments in medical treatment of the diabetic Charcot foot. Journal of Diabetes and its Complications. 2018;32(7):708-712. https://doi.org/10.1016/j.jdiacomp.2018.04.010

8. Shone A, Burnside J, Chipchase S, Game F, Jeffcoate W. Probing the Validity of the Probe-to-Bone Test in the Diagnosis of Osteomyelitis of the Foot in Diabetes. Diabetes Care. 2006;29(4):945-945. https://doi.org/10.2337/diacare.29.04.06.dc05-2450

9. Jeffcoate WJ. Charcot foot syndrome. Diabetic Medicine. 2015;32(6):760-770. https://doi.org/10.1111/dme.12754

10. Trieb K. The Charcot foot. The Bone & Joint Journal. 2016;98-B (9):1155-1159. https://doi.org/10.1302/0301-620x.98b9.37038

11. Kloska A, Korzon-Burakowska A, Malinowska M, et al. The role of genetic factors and monocyte-to-osteoclast differentiation in the pathogenesis of Charcot neuroarthropathy. Diabetes Research and Clinical Practice. 2020; 166:108337. https://doi.org/10.1016/j.diabres.2020.108337

12. Aragón-Sánchez J. Treatment of Diabetic Foot Osteomyelitis: A Surgical Critique. The International Journal of Lower Extremity Wounds. 2010;9(1):37-59. https://doi.org/10.1177/1534734610361949

13. Lipsky BA, Uçkay İ. Treating Diabetic Foot Osteomyelitis: A Practical State-of-the-Art Update. Medicina. 2021;57(4):339. https://doi.org/10.3390/medicina57040339

14. Lew DP, Waldvogel FA. Osteomyelitis. The Lancet. 2004;364(9431):369-379. https://doi.org/10.1016/s0140-6736(04)16727-5

15. Giurato L, Meloni M, Izzo V, Uccioli L. Osteomyelitis in diabetic foot: A comprehensive overview. World Journal of Diabetes. 2017;8(4):135. https://doi.org/10.4239/wjd.v8.i4.135

16. Dobaria DG, Cohen HL. Osteomyelitis Imaging.; 2023. https://www.ncbi.nlm.nih.gov/books/NBK594242/

17. Korst GS, Ratliff HT, Torian J, Jimoh RO, Jupiter DC. Delayed Diagnosis of Charcot Foot: A Systematic Review. The Journal of Foot and Ankle Surgery. Published online February 2022. https://doi.org/10.1053/j.jfas.2022.01.008

18. Holmes C, Schmidt B, Munson M, Wrobel JS. Charcot stage 0: A review and consideratons for making the correct diagnosis early. Clinical Diabetes and Endocrinology. 2015;1(1). https://doi.org/10.1186/s40842-015-0018-0

19. Lam K, van Asten SAV, Nguyen T, La Fontaine J, Lavery LA. Diagnostic Accuracy of Probe to Bone to Detect Osteomyelitis in the Diabetic Foot: A Systematic Review. Clinical Infectious Diseases. 2016;63(7):944-948. https://doi.org/10.1093/cid/ciw445

20. IWGDF/IDSA Infection guideline (2023 update). IWGDF Guidelines. Published May 13, 2023. https://iwgdfguidelines.org/infection-guideline-2023/

21. Lavery LA, Crisologo PA, La Fontaine J, Bhavan K, Oz OK, Davis KE. Are We Misdiagnosing Diabetic Foot Osteomyelitis? Is the Gold Standard Gold? The Journal of Foot and Ankle Surgery. 2019;58(4):713-716. https://doi.org/10.1053/j.jfas.2018.12.010

22. Konarzewska A, Korzon-Burakowska A, Rzepecka-Wejs L, et al. Diabetic foot syndrome: Charcot arthropathy or osteomyelitis? Part I: Clinical picture and radiography. Journal of Ultrasonography. 2018;18(72):42-49. https://doi.org/10.15557/jou.2018.0007

23. Álvaro-Afonso FJ, Lázaro-Martínez JL, García-Morales E, et al. Cortical disruption is the most reliable and accurate plain radiographic sign in the diagnosis of diabetic foot osteomyelitis. Diabetic Medicine. 2019;36(2):258-259. https://doi.org/10.1111/dme.13824

24. Rubitschung K, Sherwood A, Crisologo AP, et al. Pathophysiology and Molecular Imaging of Diabetic Foot Infections. International Journal of Molecular Sciences. 2021;22(21):11552. https://doi.org/10.3390/ijms222111552

25. Marmolejo VS, Arnold JF, Ponticello M, Andersen CA. Charcot Foot: Clinical Clues, Diagnostic Strategies, and Treatment Principles. American Family Physician. 2018;97(9):594-599. https://www.aafp.org/pubs/afp/issues/2018/0501/p594.html

26. Ergen FB, Sanverdi SE, Oznur A. Charcot foot in diabetes and an update on imaging. Diabetic Foot & Ankle. 2013;4(1):21884. https://doi.org/10.3402/dfa.v4i0.21884

27. Leone A, Vitiello C, Gullì C, et al. Bone and soft tissue infections in patients with diabetic foot. La radiologia medica. 2019;125(2):177-187. https://doi.org/10.1007/s11547-019-01096-8

28. D’Angelo T, Albrecht MH, Caudo D, et al. Virtual non-calcium dual-energy CT: clinical applications. European Radiology Experimental. 2021;5(1). https://doi.org/10.1186/s41747-021-00228-y

29. Zuo T, Chen Y, Zheng H, et al. Detection of bone marrow edema in osteonecrosis of the femoral head using virtual noncalcium dual-energy computed tomography. European Journal of Radiology. 2021; 139:109681. https://doi.org/10.1016/j.ejrad.2021.109681

30. Mens MA, A de Geus, R.H.H. Wellenberg, et al. Preliminary evaluation of dual-energy CT to quantitatively assess bone marrow edema in patients with diabetic foot ulcers and suspected osteomyelitis. European Radiology. 2023;33(8):5645-5652. https://doi.org/10.1007/s00330-023-09479-2

31. Daneshvar K, Anwander H. Diagnostic Imaging of Diabetic Foot Disorders. Foot and Ankle Clinics. Published online August 2022. https://doi.org/10.1016/j.fcl.2022.01.002

32. Rosskopf AB, Loupatatzis C, Pfirrmann CWA, et al. The Charcot foot: a pictorial review. Insights into Imaging. 2019;10(1). https://doi.org/10.1186/s13244-019-0768-9

33. Diez AIG, Fuster D, Morata L, et al. 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. European Journal of Radiology. 2020; 132:109299. https://doi.org/10.1016/j.ejrad.2020.109299

34. Ferhat Cüce, Gökalp Tulum, Kerim Bora Yılmaz, Osman O, Ayşe Aralasmak. Radiomics method in the differential diagnosis of diabetic foot osteomyelitis and charcot neuroarthropathy. British Journal of Radiology. 2023;96(1148). https://doi.org/10.1259/bjr.20220758

35. Lauri C, Tamminga M, Glaudemans AWJM, et al. 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;40(8):1111-1120. https://doi.org/10.2337/dc17-0532

36. Lauri C, Leone A, Cavallini M, et al. Diabetic Foot Infections: The Diagnostic Challenges. Journal of Clinical Medicine. 2020;9(6):1779. https://doi.org/10.3390/jcm9061779

37. Изотопы: свойства, получение, применение / Под ред. В.Ю. Баранова. — М.: Физматлит, 2005. — Т. В 2 т. Т.2. — 728 с.

38. Van den Wyngaert T, Strobel K, Kampen WU, et al. The EANM practice guidelines for bone scintigraphy. European Journal of Nuclear Medicine and Molecular Imaging. 2016;43(9):1723-1738. https://doi.org/10.1007/s00259-016-3415-4

39. Baqer MM, Loutfi I. Optimal Imaging Positions for 3-Phase Bone Scanning of Patients with Bony Pathology of the Feet. Journal of Nuclear Medicine Technology. 2010;38(2):69-75. https://doi.org/10.2967/jnmt.109.070771

40. Shanmuga Sundaram P, Padma S, Kumar H, Nair V, Kumar S. Role of 99mTc MDP bone and 67Gallium imaging in evaluation of diabetic osteopathy. The Foot. 2007;17(2):94-101. https://doi.org/10.1016/j.foot.2006.11.004

41. Love C, Palestro CJ. Radionuclide Imaging of Infection. Journal of Nuclear Medicine Technology. 2004;32(2):47-57. https://tech.snmjournals.org/content/32/2/47

42. Shanmuga Sundaram P, Padma S, Kumar H, Nair V, Kumar S. Role of 99mTc MDP bone and 67Gallium imaging in evaluation of diabetic osteopathy. The Foot. 2007;17(2):94-101. https://doi.org/10.1016/j.foot.2006.11.004

43. Lee YJ, Sadigh S, Mankad K, Kapse N, Rajeswaran G. The imaging of osteomyelitis. Quantitative Imaging in Medicine and Surgery. 2016;6(2):184-198. https://doi.org/10.21037/qims.2016.04.01

44. de Vries EFJ, Roca M, Jamar F, Israel O, Signore A. Guidelines for the labelling of leucocytes with 99mTc-HMPAO. European Journal of Nuclear Medicine and Molecular Imaging. 2010;37(4):842-848. https://doi.org/10.1007/s00259-010-1394-4

45. Roca M, de Vries EFJ, Jamar F, Israel O, Signore A. Guidelines for the labelling of leucocytes with 111In-oxine. European Journal of Nuclear Medicine and Molecular Imaging. 2010;37(4):835-841. https://doi.org/10.1007/s00259-010-1393-5

46. Ahluwalia R, Bilal A, Petrova N, et al. The Role of Bone Scintigraphy with SPECT/CT in the Characterization and Early Diagnosis of Stage 0 Charcot Neuroarthropathy. Journal of Clinical Medicine. 2020;9(12):4123. https://doi.org/10.3390/jcm9124123

47. Ashraf MA, Goyal A. Fludeoxyglucose (18F). PubMed. 2021. https://www.ncbi.nlm.nih.gov/books/NBK557653/

48. The impact of infection and inflammation in oncologic 18F-FDG PET/CT imaging. Biomedicine & Pharmacotherapy. 2019;117:109168. https://doi.org/10.1016/j.biopha.2019.109168

49. Mbakaza O, Vangu MDTW. 18F-FDG PET/CT Imaging: Normal Variants, Pitfalls, and Artifacts Musculoskeletal, Infection, and Inflammation. Frontiers in Nuclear Medicine. 2022;2. https://doi.org/10.3389/fnume.2022.847810

50. 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. Nuclear Medicine Communications. 2016;37(3):259-262. https://doi.org/10.1097/mnm.0000000000000434

51. Rastogi A, Bhattacharya A, Prakash M, et al. Utility of PET/CT with fluorine-18-fluorodeoxyglucose-labeled autologous leukocytes for diagnosing diabetic foot osteomyelitis in patients with Charcot’s neuroarthropathy. Nuclear Medicine Communications. 2016;37(12):1253-1259. https://doi.org/10.1097/mnm.0000000000000603

52. Yandrapalli S, Puckett Y. SPECT Imaging. PubMed. Published 2020. https://www.ncbi.nlm.nih.gov/books/NBK564426/

53. Phillips WT, Gorzell BC, Martinez RA, et al. Fewer-Angle SPECT/CT Blood Pool Imaging for Infection and Inflammation. Journal of Nuclear Medicine Technology. 2020;49(1):39-43. https://doi.org/10.2967/jnmt.120.256933

54. Lauri C, Campagna G, Aloisi F, et al. How to combine CTA, 99mTc-WBC SPECT/CT, and [18F] FDG PET/CT in patients with suspected abdominal vascular endograft infections? European Journal of Nuclear Medicine and Molecular Imaging. 2023;50(11):3235-3250. https://doi.org/10.1007/s00259-023-06309-x

55. Anthony ML, Cravey KS, Atway SA. Development of Charcot Neuroarthropathy in Diabetic Patients who Received Kidney or Kidney-Pancreas Transplants. The Journal of Foot and Ankle Surgery. 2019;58(3):475-479. https://doi.org/10.1053/j.jfas.2018.09.022

56. Greco T, Mascio A, Comisi C, et al. RANKL-RANK-OPG Pathway in Charcot Diabetic Foot: Pathophysiology and Clinical-Therapeutic Implications. International Journal of Molecular Sciences. 2023;24(3):3014. https://doi.org/10.3390/ijms24033014

57. Сантоцкий М.И., Бухман А.И. Основы рентгенодиагностики и рентгенотерапии эндокринных болезней. — М., 1965. — С. 158

58. Bazina K.A., Kolosunin I.A., Kozlov S.A., Fomicheva T.V., Tsyganova T.V. Diabetic neuroosteoarthropathy (Charcot foot) and osteomyelitis (a literature review). Izvestiya vysshikh uchebnykh zavedeniy. 2021;2:49–68. https://doi:10.21685/2072-3032-2021-2-5

59. Демина А.Г., Бреговский В.Б., Карпова И.А. Ближайшие результаты лечения активной стадии стопы Шарко в амбулаторных условиях // Сахарный диабет. — 2020. — Т. 23. — №4. — С. 316-323. https://doi.org/10.14341/DM10363-9815

60. Bregovskiy VB. Radiology diagnostics of the diabetic Charcot neuroarthropathy. Translational Medicine. 2021;8(1):12-18. https://doi.org/10.18705/2311-4495-2021-8-1-12-18

61. Stupina TA, Mezentsev IN, Shchudlo MM, Migalkin NS, Sudnitsyn AS. Current issues of the pathomorphology of foot tissues in diabetic neuroosteoarthropathy, including complicated by osteomyelitis (literature review and results of own research). Orthopaedic Genius. 2022;28(2):282-288. https://doi.org/10.18019/1028-4427-2022-28-2-282-288

62. Teik Hin Tan, Boon Nang Lee. False negative 99m Tc-hydroxymethane diphosphonate three-phase bone scintigraphy and 99m Tc-besilesomab scan in detecting tibia osteomyelitis concomitant with necrotizing fasciitis. World journal of nuclear medicine. 2014;13(03):190-192. https://doi.org/10.4103/1450-1147.144820

63. Dutta P, Bhansali A, Mittal BR, Singh B, Masoodi SR. Instant 99mTc-Ciprofloxacin Scintigraphy for the Diagnosis of Osteomyelitis in the Diabetic Foot. Foot & Ankle International. 2006;27(9):716-722. https://doi.org/10.1177/107110070602700911

64. Dutta P, Bhansali A, Mittal BR, Singh B, Masoodi SR. Instant 99mTc-Ciprofloxacin Scintigraphy for the Diagnosis of Osteomyelitis in the Diabetic Foot. Foot & Ankle International. 2006;27(9):716-722. https://doi.org/10.1177/107110070602700911

65. Sallam A, El-Sharawy A. Role of Interleukin-6 (IL-6) and Indicators of Inflammation in the Pathogenesis of Diabetic Foot Ulcers. Australian Journal of Basic and Applied Sciences. 2012;6(6):430-435. https://www.ajbasweb.com/old/ajbas/2012/June/430-435.pdf

66. Scott P, Kozloff, Blazeski. Besilesomab for imaging inflammation and infection in peripheral bone in adults with suspected osteomyelitis. Reports in Medical Imaging. Published online August 2010:17. https://doi.org/10.2147/rmi.s9458

67. Albano D, Bosio G, Paghera B, Bertagna F. Comparison Between 99mTc-Sulesomab and 18F-FDG PET/CT in a Patient With Suspected Prosthetic Joint Infection. Clinical Nuclear Medicine. 2016;41(6): e298-e300. https://doi.org/10.1097/rlu.0000000000001217

68. Skehan SJ, White J, Evans JW, et al. Mechanism of accumulation of 99mTc-sulesomab in inflammation. PubMed. 2003;44(1):11-18.

69. Palestro CJ, Caprioli R, Love C, et al. Rapid diagnosis of pedal osteomyelitis in diabetics with a technetium-99m-labeled monoclonal antigranulocyte antibody. Journal of Foot & Ankle Surgery. 2003;42(1):2-8. https://doi.org/10.1053/jfas.2003.0420001