Lower extremity limb salvage in diabetic patients: the impossible is possible
https://doi.org/10.14341/DM13245
Abstract
Lesions of the lower extremities in diabetes mellitus are a complex and urgent problem of modern medicine. The high prevalence of diabetes mellitus, significant difficulties in timely diagnosis, differential diagnosis and the choice of therapeutic tactics to preserve the supporting function of the limb determine the difficulties in managing diabetic patients. Over the past decades, significant changes have occurred in the structure of specialized medical care for diabetic foot patients which has significantly reduced the number of high amputations, improved the quality and life expectancy of patients. The article presents the results of the long-term experience of the Diabetic Foot department in the treatment of diabetic foot patients.
About the Authors
G. R. GalstyanRussian Federation
Gagik R. Galstyan, MD, PhD, Professor
11 Dm. Ulyanova street, 117292 Moscow
E. V. Artemova
Russian Federation
Ekaterina V. Artemova, MD
11 Dm. Ulyanova street, 117292 Moscow
P. S. Bardiugov
Russian Federation
Petr S. Bardiugov
11 Dm. Ulyanova street, 117292 Moscow
O. N. Bondarenko
Russian Federation
Olga N. Bondarenko, MD, PhD, leading research associate
11 Dm. Ulyanova street, 117292 Moscow
Z. N. Dzhemilova
Russian Federation
Zera N. Dzhemilova, MD
11 Dm. Ulyanova street, 117292 Moscow
L. P. Doronina
Russian Federation
Ludmila P. Doronina, MD, PhD
11 Dm. Ulyanova street, 117292 Moscow
D. N. Egorova
Russian Federation
Daria N. Egorova, MD, PhD, senior research associate
11 Dm. Ulyanova street, 117292 Moscow
E. L. Zaitseva
Russian Federation
Ekaterina L. Zaitseva, MD, PhD
11 Dm. Ulyanova street, 117292 Moscow
V. A. Mitish
Russian Federation
Valery V. Mitish, MD, PhD
11 Dm. Ulyanova street, 117292 Moscow
S. V. Sergeeva
Russian Federation
Svetlana V. Sergeeva, MD
11 Dm. Ulyanova street, 117292 Moscow
I. I. Sitkin
Russian Federation
Ivan I. Sitkin, MD, PhD, senior research associate
11 Dm. Ulyanova street, 117292 Moscow
A. Y. Tokmakova
Russian Federation
Alla Y. Tokmakova, MD, PhD
11 Dm. Ulyanova street, 117292 Moscow
M. V. Yaroslavceva
Russian Federation
Marianna V. Yaroslavceva, MD, PhD, senior researcher
11 Dm. Ulyanova street, 117292 Moscow
M. V. Shestakova
Russian Federation
Marina V. Shestakova, MD, PhD, Professor, Academician of the RAS
11 Dm. Ulyanova street, 117292 Moscow
References
1. Galstyan GR, Tokmakova AY, Egorova DN, et al. Clinical guidelines for diagnosis and treatment of diabetic foot syndrome. Wounds and wound infections. The prof. B.M. Kostyuchenok journal. 2015;2(3):63-83. (In Russ.) doi: https://doi.org/10.17650/2408-9613-2015-2-3-63-83
2. Dedov II, Shestakova MV, Vikulova OK, et al. Diabetes mellitus in the Russian Federation: dynamics of epidemiological indicators according to the Federal Register of Diabetes Mellitus for the period 2010–2022. Diabetes mellitus. 2023;26(2):104-123. (In Russ.) doi: https://doi.org/10.14341/DM13035
3. Kostyuchenok BM, Amiraslanov YA, Shcherba SG. Gnoinaya khirurgicheskaya infektsiya u bol’nykh sakharnym diabetom. Rany i ranevaya infektsiya. 2nd ed. Kuzin MI, Kostyuchenok BM, editors. Moscow: «Meditsina»; 1990. (In Russ.)
4. Pokrovskiy АV. The place of vascular surgery in treatment of diabetic patients. Annals of the Russian academy of medical sciences. 2012;67(1):27-30. (In Russ.) doi: https://doi.org/10.15690/vramn.v67i1.106
5. Diabetes care and research in Europe: the Saint Vincent declaration. Diabet Med. 1990;7(4):360
6. Dedov II, Shestakova MV, Suntsov YI, et al. Federal targeted programme ‘Prevention and Management of Socially Significant Diseases (2007-2012)’: results of the ‘Diabetes mellitus’ sub-programme. Diabetes mellitus. 2013;16(2S):1-48. (In Russ.) doi: https://doi.org/10.14341/2072-0351-3879
7. IWGDF Guidelines. IWGDF Guidelines on the prevention and management of diabetes-related foot disease. Available from: https://iwgdfguidelines.org/wp-content/uploads/2023/07/IWGDF-Guidelines-2023.pdf
8. Klinicheskie rekomendatsii [Internet. Rubrikator klinicheskikh rekomendatsii [dostup ot 10.01.2025. Available from: https://cr.minzdrav.gov.ru/clin-rec (In Russ.)
9. Armstrong DG, Tan TW, Boulton AJM, Bus SA. Diabetic Foot Ulcers: A Review. JAMA. 2023;330(1):62-75. doi: https://doi.org/10.1001/jama.2023.10578
10. Pop-Busui R, Boulton AJ, Feldman EL, et al. Diabetic Neuropathy: A Position Statement by the American Diabetes Association. Diabetes Care. 2017;40(1):136-154. doi: https://doi.org/10.2337/dc16-2042
11. Artemova EV, Dzhemilova ZN, Gorbacheva AM, et al. Neirogumoral’naya regulyatsiya reparatsii tkanei pri sakharnom diabete. Moscow: OOO Izdatel’stvo «KURS»; 2022. (In Russ.)
12. Jaiswal M, Divers J, Dabelea D, et al. Prevalence of and Risk Factors for Diabetic Peripheral Neuropathy in Youth With Type 1 and Type 2 Diabetes: SEARCH for Diabetes in Youth Study. Diabetes Care. 2017;40(9):1226-1232. doi: https://doi.org/10.2337/dc17-0179
13. Fitridge R, Chuter V, Mills J, et al. The intersocietal IWGDF, ESVS, SVS guidelines on peripheral artery disease in people with diabetes and a foot ulcer. Diabetes Metab Res Rev. 2024;40(3):e3686. doi: https://doi.org/10.1002/dmrr.3686
14. Boulton AJM. The pathway to ulceration: aetiopathogenesis. In: Boulton AJM, Cavanagh PR, Rayman G. The Diabetic Foot (4-th edition). Wiley;2008:51-67
15. Stoberock K, Kaschwich M, Nicolay SS, et al. The interrelationship between diabetes mellitus and peripheral arterial disease. Vasa. 2021;50(5):323-330. doi: https://doi.org/10.1024/0301-1526/a000925
16. Conte MS, Bradbury AW, Kolh P, et al. Global vascular guidelines on the management of chronic limb-threatening ischemia [published correction appears in J Vasc Surg. 2019 Aug;70(2):662. doi: 10.1016/j.jvs.2019.06.102. J Vasc Surg. 2019;69(6S):3S-125S.e40. doi: https://doi.org/10.1016/j.jvs.2019.02.016
17. Dedov II, Shestakova MV, Mayorov AY, et al. Standards of Specialized Diabetes Care / Edited by Dedov II, Shestakova MV, Mayorov AYu. 11th Edition. Diabetes mellitus. 2023;26(2S):1-157. (In Russ.) doi: https://doi.org/10.14341/DM13042
18. Bus SA, Sacco ICN, Monteiro-Soares M, et al. Guidelines on the prevention of foot ulcers in persons with diabetes (IWGDF 2023 update). Diabetes Metab Res Rev. 2024;e3651. doi: https://doi.org/10.1002/dmrr.3651
19. van Netten JJ, Raspovic A, Lavery LA, et al. Prevention of foot ulcers in persons with diabetes at risk of ulceration: A systematic review and meta-analysis. Diabetes Metab Res Rev. 2024;40(3):e3652. doi: https://doi.org/10.1002/dmrr.3652
20. Bus SA, Waaijman R, Arts M, et al. Effect of custom-made footwear on foot ulcer recurrence in diabetes: a multicenter randomized controlled trial. Diabetes Care. 2013;36(12):4109-4116. doi: https://doi.org/10.2337/dc13-0996
21. Norgren L, Hiatt WR, Dormandy JA, et al. Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II). J Vasc Surg. 2007;45 Suppl S:S5-S67. doi: https://doi.org/10.1016/j.jvs.2006.12.037
22. Galstyan GR, Vikulova OK, Isakov MA, et al. Trends in the epidemiology of diabetic foot and lower limb amputations in Russian Federation according to the Federal Diabetes Register (2013–2016). Diabetes mellitus. 2018;21(3):170-177. (In Russ.) doi: https://doi.org/10.14341/DM9688
23. Robson MC, Barbul A. Guidelines for the best care of chronic wounds. Wound Repair Regen. 2006;14(6):647-648. doi: https://doi.org/10.1111/j.1524-475X.2006.00173.x
24. Bondarenko ON, Galstyan GR, Dedov II. The clinical course of critical limb ischaemia and the role of endovascular revascularisation in patients with diabetes. Diabetes mellitus. 2015;18(3):57-69. (In Russ.) doi: https://doi.org/10.14341/DM2015357-69
25. Dzhemilova ZN, Galstyan GR. Assessment of tissue perfusion by indocyanine green fluorescein angiography in patients with neuroischemic diabetic foot syndrome after endovascular treatment. Pirogov Russian Journal of Surgery. 2023;9(2):43–53. (In Russ.) https://doi.org/10.17116/hirurgia202309243
26. Patent RU №2734275 C1/14.10.2020. Grachev P.V., Loshchenov V.B., Balyko I.A., et al. Sposob diagnostiki stepeni krovenapolnennosti biologicheskikh tkanei i otsenki parametrov krovotoka i limfotoka. (In Russ.)
27. Gerhard-Herman MD, Gornik HL, Barrett C, et al. 2016 AHA/ACC Guideline on the Management of Patients With Lower Extremity Peripheral Artery Disease: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines [published correction appears in Circulation. 2017 Mar 21;135(12):e791-e792. doi: 10.1161/CIR.0000000000000502. Circulation. 2017;135(12):e726-e779. doi: https://doi.org/10.1161/CIR.0000000000000471
28. Ahn SS, Concepcion B. Current status of atherectomy for peripheral arterial occlusive disease. World J Surg. 1996;20(6):635-643. doi: https://doi.org/10.1007/s002689900097
29. Rastan A, Sixt S, Schwarzwälder U, et al. Initial experience with directed laser atherectomy using the CLiRpath photoablation atherectomy system and bias sheath in superficial femoral artery lesions. J Endovasc Ther. 2007;14(3):365-373. doi: https://doi.org/10.1583/06-2046.1
30. Faglia E, Clerici G, Clerissi J, et al. Long-term prognosis of diabetic patients with critical limb ischemia: a population-based cohort study [published correction appears in Diabetes Care. 2009 Jul;32(7):1355. Luppattelli, Tommaso [corrected to Lupattelli, Tommaso. Diabetes Care. 2009;32(5):822-827. doi: https://doi.org/10.2337/dc08-1223
31. Uccioli L, Gandini R, Giurato L, et al. Long-term outcomes of diabetic patients with critical limb ischemia followed in a tertiary referral diabetic foot clinic. Diabetes Care. 2010;33(5):977-982. doi: https://doi.org/10.2337/dc09-0831
32. Meloni M, Izzo V, Giurato L, et al. Recurrence of Critical Limb Ischemia After Endovascular Intervention in Patients with Diabetic Foot Ulcers. Adv Wound Care (New Rochelle). 2018;7(6):171-176. doi: https://doi.org/10.1089/wound.2017.0778
33. Ayubova NL, Bondarenko ON, Galstyan GR, et al. Clinical outcomes of lower limb peripheral vascular disease after endovascular intervention in patients with diabetes mellitus, critical limb ischemia and chronic kidney disease. Diabetes mellitus. 2013;16(4):85-94. (In Russ.) doi: https://doi.org/10.14341/DM2013485-94
34. Adam DJ, Beard JD, Cleveland T, et al. Bypass versus angioplasty in severe ischaemia of the leg (BASIL): multicentre, randomised controlled trial. Lancet. 2005;366(9501):1925-1934. doi: https://doi.org/10.1016/S0140-6736(05)67704-5
35. 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;40(3):e3646. doi: https://doi.org/10.1002/dmrr.3646
36. Raspovic KM, Schaper NC, Gooday C, et al. Diagnosis and treatment of active charcot neuro-osteoarthropathy in persons with diabetes mellitus: A systematic review. Diabetes Metab Res Rev. 2024;40(3):e3653. doi: https://doi.org/10.1002/dmrr.3653
37. Ul’yanova IN, Yaroslavtseva MV, Galstyan GR. Diabeticheskaya neiroosteoartropatiya: osobennosti kostnogo metabolizma u patsientov s sakharnym diabetom. Meditsina kriticheskikh sostoyanii. 2009;(3):36-41. (In Russ.)
38. Yaroslavceva MV, Bondarenko ON, El-Taravi YA, et al. Etiopathogenetic features of bone metabolism in patients with diabetes mellitus and Charcot foot. Problems of Endocrinology. 2024;70(4):57-64. (In Russ.) doi: https://doi.org/10.14341/probl13362
39. Armstrong DG, Peters EJ. Charcot’s arthropathy of the foot. J Am Podiatr Med Assoc. 2002;92(7):390-394. doi: https://doi.org/10.7547/87507315-92-7-390
40. McEwen LN, Ylitalo KR, Herman WH, Wrobel JS. Prevalence and risk factors for diabetes-related foot complications in Translating Research Into Action for Diabetes (TRIAD). J Diabetes Complications. 2013;27(6):588-592. doi: https://doi.org/10.1016/j.jdiacomp.2013.08.003
41. Patent RF №2570970 C1/20.12.2015. Mitish VA, Paskhalova YS, Doronina LP, Garyaeva VV. Sposob khirurgicheskogo lecheniya diabeticheskoi neiroosteoartropatii srednego otdela stopy v stadii troficheskikh narushenii. (In Russ.)
42. Patent RF №2561286 C1/27.08.2015. Mitish VA., Paskhalova YS, Doronina LP, Garyaeva VV. Sposob khirurgicheskogo lecheniya diabeticheskoi neiroosteoartropatii srednego otdela stopy v stadii gnoinykh oslozhnenii. (In Russ.)
43. Kalandiya MM, Doronina LP, Mitish VA, et al. Long-term results of corrective surgical interventions in patients with diabetic midfoot neuroosteoarthropathy. Diabetes mellitus. 2023;26(5):464-472. (In Russ.) doi: https://doi.org/10.14341/DM13000
44. Ha J, Hester T, Foley R, et al. Charcot foot reconstruction outcomes: A systematic review. J Clin Orthop Trauma. 2020;11(3):357-368. doi: https://doi.org/10.1016/j.jcot.2020.03.025
45. Kwaadu KY. Charcot Reconstruction: Understanding and Treating the Deformed Charcot Neuropathic Arthropathic Foot. Clin Podiatr Med Surg. 2020;37(2):247-261. doi: https://doi.org/10.1016/j.cpm.2019.12.002
46. Cianni L, Bocchi MB, Vitiello R, et al. Arthrodesis in the Charcot foot: a systematic review. Orthop Rev (Pavia). 2020;12(Suppl 1):8670. doi: https://doi.org/10.4081/or.2020.8670
47. Hartig N, Krenn S, Trnka HJ. Operative Versorgung des Charcot-Fußes am Rückfuß : Langzeitergebnisse und systematischer Überblick [Surgical treatment of the Charcot foot : long-term results and systematic review. Orthopade. 2015;44(1):14-24. doi: https://doi.org/10.1007/s00132-014-3058-8
48. Stapleton JJ, Zgonis T. Surgical reconstruction of the diabetic Charcot foot: internal, external or combined fixation? Clin Podiatr Med Surg. 2012;29(3):425-433. doi: https://doi.org/10.1016/j.cpm.2012.04.003
49. Bardiugov PS, Parshikov MV, Galstyan GR, Yarygin NV. Indications for various options of foot deformities orthopedic correction in diabetic neuroosteoarthropathy. Diabetes mellitus. 2020;23(4):374-385. (In Russ.) doi: https://doi.org/10.14341/DM12271
50. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M. Growth factors and cytokines in wound healing. Wound Repair Regen. 2008;16(5):585-601. doi: https://doi.org/10.1111/j.1524-475X.2008.00410.x
51. Yang Q, Zhang Y, Yin H, Lu Y. Topical Recombinant Human Epidermal Growth Factor for Diabetic Foot Ulcers: A Meta-Analysis of Randomized Controlled Clinical Trials. Ann Vasc Surg. 2020;62:442-451. doi: https://doi.org/10.1016/j.avsg.2019.05.041
52. Zaitseva EL, Zhilyaev VM, Galstyan GR. Long-term Follow-up of treatment of chronic foot wounds with recombinant human epidermal growth factor in patients with different complications of diabetes mellitus. Diabetes mellitus. 2020;23(6):532-540. (In Russ.) doi: https://doi.org/10.14341/DM12701
53. Patent RF №2754383 C1/2021.09.01. Zaitseva EL, Doronina LP, Tokmakova AYu, Galstyan GR, Shestakova MV. Sposob lecheniya neinfitsirovannogo posleoperatsionnogo ranevogo defekta stopy pri otsutstvii priznakov kriticheskoi ishemii konechnosti u bol’nykh s neiropaticheskoi i neiroishemicheskoi formoi sindroma diabeticheskoi stopy. (In Russ.)
54. Albehairy A, Kyrillos F, Gawish H, et al. Autologous Mononuclear Versus Mesenchymal Stem Cells in Healing of Recalcitrant Neuropathic Diabetic Foot Ulcers. In: Diabetic Foot Study Group (DFSG) Berlin 2018; 2018 Oct 2. Available from: https://www.easd.org/media-centre/home.html#!resources/autologous-mononuclear-versus-mesenchymal-stem-cells-in-healing-of-recalcitrant-neuropathic-diabetic-foot-ulcers
55. Moon KC, Suh HS, Kim KB, et al. Potential of Allogeneic Adipose-Derived Stem Cell-Hydrogel Complex for Treating Diabetic Foot Ulcers. Diabetes. 2019;68(4):837-846. doi: https://doi.org/10.2337/db18-0699
56. Lonardi R, Leone N, Gennai S, Trevisi Borsari G, Covic T, Silingardi R. Autologous micro-fragmented adipose tissue for the treatment of diabetic foot minor amputations: a randomized controlled single-center clinical trial (MiFrAADiF). Stem Cell Res Ther. 2019;10(1):223. doi: https://doi.org/10.1186/s13287-019-1328-4
57. Dixon D, Edmonds M. Managing diabetic foot ulcers: pharmacotherapy for wound healing. Drugs. 2021;81(1):29-56. doi: https://doi.org/10.1007/s40265-020-01415-8
58. Mulder G, Tallis AJ, Marshall VT, et al. Treatment of nonhealing diabetic foot ulcers with a platelet-derived growth factor gene-activated matrix (GAM501): results of a phase 1/2 trial. Wound Repair Regen. 2009;17(6):772-779. doi: https://doi.org/10.1111/j.1524-475X.2009.00541.x
59. Kwon MJ, An S, Choi S, et al. Effective healing of diabetic skin wounds by using nonviral gene therapy based on minicircle vascular endothelial growth factor DNA and a cationic dendrimer. J Gene Med. 2012;14(4):272-278. doi: https://doi.org/10.1002/jgm.2618
Supplementary files
|
1. Figure 1. Outcome of comprehensive treatment in a patient with neuroischemic diabetic foot syndrome using percutaneous transluminal balloon angioplasty of lower leg and foot arteries. A — initial limb appearance and angiography; Б — clinical and angiographic treatment outcome. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(954KB)
|
Indexing metadata ▾ |
|
2. Figure 2. Surgical correction outcome of midfoot deformity in a patient with neuro-osteoarthropathy. A — pre-treatment foot appearance and multislice CT scan; Б — surgical stages; В — outcome after intervention. | |
Subject | ||
Type | Исследовательские инструменты | |
View
(540KB)
|
Indexing metadata ▾ |
|
3. Figure 3. Treatment outcome in a female patient with type 2 diabetes mellitus (aseptic necrosis of talus and medial malleolus, loss of limb support function, wound in the area of lateral malleolus apex communicating with a cavity). A — initial appearance and X-ray; B — clinical and radiographic result (secondary wound healing, bone ankylosis formation, restoration of limb support function). | |
Subject | ||
Type | Исследовательские инструменты | |
View
(595KB)
|
Indexing metadata ▾ |
Review
For citations:
Galstyan G.R., Artemova E.V., Bardiugov P.S., Bondarenko O.N., Dzhemilova Z.N., Doronina L.P., Egorova D.N., Zaitseva E.L., Mitish V.A., Sergeeva S.V., Sitkin I.I., Tokmakova A.Y., Yaroslavceva M.V., Shestakova M.V. Lower extremity limb salvage in diabetic patients: the impossible is possible. Diabetes mellitus. 2025;28(1):56-67. (In Russ.) https://doi.org/10.14341/DM13245

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND 4.0).