Skip to main content
SpringerLink
Log in

Neuropathic Diabetic Foot Ulceration

  • Chapter
  • First Online:
Limb Salvage of the Diabetic Foot

  • 645 Accesses

Abstract

Diabetic foot ulceration (DFU) is one of the most feared complications of diabetes; it leads to significant morbidity and confers an increased risk of lower extremity amputation. Neuropathic DFU, defined as ulceration occurring in neuropathic feet without co-existent peripheral vascular disease, is perhaps the most common type, occurring in 50–60% of DFU patients. A complex interplay between neuropathy, foot deformities, changes in plantar pressure and extrinsic factors such as footwear leading to the development of neuropathic DFU has been identified. Ulceration on the plantar foot with subtle but significant local soft tissue and bone damage are clinical hallmarks. The management of neuropathic DFU is reliant on early referral to a specialist foot clinic allowing expert assessment, wound care delivery, aggressive treatment of any infection, and importantly, appropriate offloading. Limb-threatening infections may require urgent debridement of all infected tissue. The consequent tissue defect may benefit from application of topical negative pressure wound therapy and access to early wound closure techniques. In those with significant foot deformities, surgical deformity correction may be indicated to prevent ulcer recurrence. At the same time, it is important to appreciate and treat any comorbidities that may interfere with wound healing. All patients with neuropathic DFU should receive education to improve compliance with treatment, promote ulcer healing and prevent recurrence.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Armstrong DG, Boulton AJM, Bus SA. Diabetic foot ulcers and their recurrence. N Engl J Med. 2017;376:2367–75.

    Article  PubMed  Google Scholar 

  2. Huang DY, Wilkins CJ, Evans DR, Ammar T, Deane C, Vas PR, et al. The diabetic foot: the importance of coordinated care. Semin Intervent Radiol. 2014;31:307–12.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ghanassia E, Villon L, dit Dieudonné J-FT, Boegner C, Avignon A, Sultan A. long-term outcome and disability of diabetic patients hospitalized for diabetic foot ulcers a 6.5-year follow-up study. Diabetes Care. 2008;31:1288–92.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Winkley K, Stahl D, Chalder T, Edmonds ME, Ismail K. Quality of life in people with their first diabetic foot ulcer: a prospective cohort study. J Am Podiatr Med Assoc. 2009;99:406–14.

    Article  PubMed  Google Scholar 

  5. Moulik PK, Mtonga R, Gill GV. Amputation and mortality in new-onset diabetic foot ulcers stratified by etiology. Diabetes Care. 2003;26:491–4.

    Article  PubMed  Google Scholar 

  6. Brownrigg J, Davey J, Holt P, Davis W, Thompson M, Ray K. The association of ulceration of the foot with cardiovascular and all-cause mortality in patients with diabetes: a meta-analysis. Diabetologia. 2012;55:2906–12.

    Article  CAS  PubMed  Google Scholar 

  7. Kerr M, Barron E, Chadwick P, Evans T, Kong WM, Rayman G et al. The cost of diabetic foot ulcers and amputations to the National Health Service in England. Diabet Med. 2019;36(8):995–1002.

    Google Scholar 

  8. Hex N, Bartlett C, Wright D, Taylor M, Varley D. Estimating the current and future costs of Type 1 and Type 2 diabetes in the UK, including direct health costs and indirect societal and productivity costs. Diabet Med. 2012;29:855–62.

    Article  CAS  PubMed  Google Scholar 

  9. Rice JB, Desai U, Cummings AKG, Birnbaum HG, Skornicki M, Parsons NB. Burden of diabetic foot ulcers for medicare and private insurers. Diabetes Care. 2014;37:651–8.

    Article  PubMed  Google Scholar 

  10. Crawford F, McCowan C, Dimitrov BD, Woodburn J, Wylie GH, Booth E. The risk of foot ulceration in people with diabetes screened in community settings: findings from a cohort study. QJM. 2011;104:403–10.

    Article  CAS  PubMed  Google Scholar 

  11. Abbott CA, Carrington AL, Ashe H, Bath S, Every LC, Griffiths J, et al. The north-west diabetes foot care study: incidence of, and risk factors for, new diabetic foot ulceration in a community-based patient cohort. Diabet Med. 2002;19:377–84.

    Article  CAS  PubMed  Google Scholar 

  12. Henriksson F, Agardh CD, Berne C, Bolinder J, Lönnqvist F, Stenström P, et al. Direct medical costs for patients with type 2 diabetes in Sweden. J Intern Med. 2000;248:387–96.

    Article  CAS  PubMed  Google Scholar 

  13. Boulton AJ, Kirsner RS, Vileikyte L. Neuropathic diabetic foot ulcers. N Engl J Med. 2004;351:48–55.

    Article  CAS  PubMed  Google Scholar 

  14. Abbott CA, Vileikyte L, Williamson S, Carrington AL, Boulton AJ. Multicenter study of the incidence of and predictive risk factors for diabetic neuropathic foot ulceration. Diabetes Care. 1998;21:1071–5.

    Article  CAS  PubMed  Google Scholar 

  15. Margolis DJ, Malay DS, Hoffstad OJ, Leonard CE, MaCurdy T, Lopez de Nava K. Prevalence of diabetes, diabetic foot ulcer, and lower extremity amputation among Medicare beneficiaries, 2006 to 2008: Data Points Publication Series [Internet]. Rockville, MD: Agency for Healthcare Research and Quality (US); 2011.

    Google Scholar 

  16. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, et al. High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study. Diabetologia. 2007;50:18–25.

    Article  CAS  PubMed  Google Scholar 

  17. Reiber GE, Vileikyte L, Boyko EJ, del Aguila M, Smith DG, Lavery LA, et al. Causal pathways for incident lower-extremity ulcers in patients with diabetes from two settings. Diabetes Care. 1999;22:157–62.

    Article  CAS  PubMed  Google Scholar 

  18. Kumar S, Ashe HA, Parnell LN, Fernando DJS, Tsigos C, Young RJ, et al. The prevalence of foot ulceration and its correlates in type 2 diabetic patients: a population-based study. Diabetic Med. 1994;11:480–4.

    Article  CAS  PubMed  Google Scholar 

  19. Ince P, Game FL, Jeffcoate WJ. Rate of healing of neuropathic ulcers of the foot in diabetes and its relationship to ulcer duration and ulcer area. Diabetes Care. 2007;30:660–3.

    Article  PubMed  Google Scholar 

  20. Moura Neto A, Zantut-Wittmann DE, Fernandes TD, Nery M, Parisi MC. Risk factors for ulceration and amputation in diabetic foot: study in a cohort of 496 patients. Endocrine. 2013;44:119–24.

    Article  CAS  PubMed  Google Scholar 

  21. Fabrin J, Larsen K, Holstein PE. Long-term follow-up in diabetic charcot feet with spontaneous onset. Diabetes Care. 2000;23:796–800.

    Article  CAS  PubMed  Google Scholar 

  22. Boyko EJ, Ahroni JH, Stensel V, Forsberg RC, Davignon DR, Smith DG. A prospective study of risk factors for diabetic foot ulcer. The seattle diabetic foot study. Diabetes Care. 1999;22:1036–42.

    Article  CAS  PubMed  Google Scholar 

  23. Young MJ, Breddy JL, Veves A, Boulton AJ. The prediction of diabetic neuropathic foot ulceration using vibration perception thresholds. A prospective study. Diabetes Care. 1994;17:557–60.

    Article  CAS  PubMed  Google Scholar 

  24. Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Diabetic neuropathic foot ulcers: the association of wound size, wound duration, and wound grade on healing. Diabetes Care. 2002;25:1835–9.

    Article  PubMed  Google Scholar 

  25. Marston WA. Risk factors associated with healing chronic diabetic foot ulcers: the importance of hyperglycemia. Ostomy Wound Manage. 2006;52:26–8, 30, 32 passim.

    PubMed  Google Scholar 

  26. Duzgun AP, Satır HZ, Ozozan O, Saylam B, Kulah B, Coskun F. Effect of hyperbaric oxygen therapy on healing of diabetic foot ulcers. J Foot Ankle Surg. 2008;47:515–9.

    Article  PubMed  Google Scholar 

  27. Apelqvist J, Larsson J, Agardh CD. The influence of external precipitating factors and peripheral neuropathy on the development and outcome of diabetic foot ulcers. J Diabet Complications. 1990;4:21–5.

    Article  CAS  PubMed  Google Scholar 

  28. Ndip A, Rutter MK, Vileikyte L, Vardhan A, Asari A, Jameel M, et al. Dialysis treatment is an independent risk factor for foot ulceration in patients with diabetes and stage 4 or 5 chronic kidney disease. Diabetes Care. 2010;33:1811–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Margolis DJ, Kantor J, Santanna J, Strom BL, Berlin JA. Risk factors for delayed healing of neuropathic diabetic foot ulcers: a pooled analysis. Arch Dermatol. 2000;136:1531–5.

    CAS  PubMed  Google Scholar 

  30. Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Diabetic neuropathic foot ulcers: predicting which ones will not heal. Am J Med. 2003;115:627–31.

    Article  PubMed  Google Scholar 

  31. Markuson M, Hanson D, Anderson J, Langemo D, Hunter S, Thompson P, Paulson R, Rustvang D. The relationship between hemoglobin A(1c) values and healing time for lower extremity ulcers in individuals with diabetes. Adv Skin Wound Care. 2009;22(8):365–72. https://doi.org/10.1097/01.ASW.0000358639.45784.cd.

    Article  PubMed  Google Scholar 

  32. Winkley K, Stahl D, Chalder T, Edmonds ME, Ismail K. Risk factors associated with adverse outcomes in a population-based prospective cohort study of people with their first diabetic foot ulcer. J Diabetes Complicat. 2007;21:341–9.

    Article  Google Scholar 

  33. Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Armstrong DG, Harkless LB, Boulton AJM. The effects of ulcer size and site, patient’s age, sex and type and duration of diabetes on the outcome of diabetic foot ulcers. Diabet Med. 2001;18:133–8.

    Article  CAS  PubMed  Google Scholar 

  34. Yosuf MK, Mahadi SI, Mahmoud SM, Widatalla AH, Ahmed ME. Diabetic neuropathic forefoot and heel ulcers: management, clinical presentation and outcomes. J Wound Care. 2015;24:420–5.

    Article  CAS  PubMed  Google Scholar 

  35. Tone A, Nguyen S, Devemy F, Topolinski H, Valette M, Cazaubiel M. Six-week versus twelve-week antibiotic therapy for nonsurgically treated diabetic foot osteomyelitis: a multicenter open-label controlled randomized study. Diabet Care. 2015;38:302–7.

    Article  Google Scholar 

  36. Jagadish M, McNally MM, Heidel RE, Teffeteller S, Arnold JD, Freeman M. Diabetic foot ulcers: the importance of patient comorbidity recognition and total contact casting in successful wound care. Am Surg. 2016;82:733–6.

    PubMed  Google Scholar 

  37. Dubsky M, Jirkovska A, Bem R, Fejfarova V, Skibova J, Schaper NC, et al. Risk factors for recurrence of diabetic foot ulcers: prospective follow-up analysis in the Eurodiale subgroup. Int Wound J. 2013;10:555–61.

    Article  PubMed  Google Scholar 

  38. Waaijman R, de Haart M, Arts ML, Wever D, Verlouw AJ, Nollet F, et al. Risk factors for plantar foot ulcer recurrence in neuropathic diabetic patients. Diabet Care. 2014;37:1697–705.

    Article  Google Scholar 

  39. Molines-Barroso RJ, Lázaro-Martínez JL, Aragón-Sánchez J, García-Morales E, Beneit-Montesinos JV, Álvaro-Afonso FJ. Analysis of transfer lesions in patients who underwent surgery for diabetic foot ulcers located on the plantar aspect of the metatarsal heads. Diabet Med. 2013;30:973–6.

    Article  CAS  PubMed  Google Scholar 

  40. Siersma V, Thorsen H, Holstein PE, Kars M, Apelqvist J, Jude EB. Health-related quality of life predicts major amputation and death, but not healing, in people with diabetes presenting with foot ulcers: the Eurodiale study. Diabet Care. 2014;37:694–700.

    Article  Google Scholar 

  41. Pecoraro RE, Reiber GE, Burgess EM. Pathways to diabetic limb amputation: basis for prevention. Diabet Care. 1990;13:513–21.

    Article  CAS  Google Scholar 

  42. Parisi MC, Moura Neto A, Menezes FH, Gomes MB, Teixeira RM, de Oliveira JE. Baseline characteristics and risk factors for ulcer, amputation and severe neuropathy in diabetic foot at risk: the BRAZUPA study. Diabetol Metab Syndr. 2016;8:25.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Jiang Y, Ran X, Jia L, Yang C, Wang P, Ma J. Epidemiology of type 2 diabetic foot problems and predictive factors for amputation in China. Int J Low Extrem Wounds. 2015;14:19–27.

    Article  PubMed  Google Scholar 

  44. Shojaiefard A, Khorgami Z, Larijani B. Independent risk factors for amputation in diabetic foot. Int J Diabetes Dev Ctries. 2008;28:32–7.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Pemayun TG, Naibaho RM, Novitasari D, Amin N, Minuljo TT. Risk factors for lower extremity amputation in patients with diabetic foot ulcers: a hospital-based case-control study. Diabet Foot Ankle. 2015;6:29629.

    Article  PubMed  Google Scholar 

  46. Reiber GE, Pecoraro RE, Koepsell TD. Risk factors for amputation in patients with diabetes mellitus. A case-control study. Ann Intern Med. 1992;117:97–105.

    Article  CAS  PubMed  Google Scholar 

  47. Rajamani K, Colman PG, Li LP, Best JD, Voysey M, D’Emden MC. Effect of fenofibrate on amputation events in people with type 2 diabetes mellitus (FIELD study): a prespecified analysis of a randomised controlled trial. Lancet. 2009;373:1780–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Lavery LA, Lavery DC, Hunt NA, La Fontaine J, Ndip A, Boulton AJ. Amputations and foot-related hospitalisations disproportionately affect dialysis patients. Int Wound J. 2015;12:523–6.

    Article  PubMed  Google Scholar 

  49. Chen IW, Yang HM, Chiu CH, Yeh JT, Huang CH, Huang YY. Clinical Characteristics and Risk Factor Analysis for Lower-Extremity Amputations in Diabetic Patients With Foot Ulcer Complicated by Necrotizing Fasciitis. Medicine (Baltimore). 2015;94:e1957.

    Article  Google Scholar 

  50. Carlson T, Reed JF 3rd. A case-control study of the risk factors for toe amputation in a diabetic population. Int J Low Extrem Wounds. 2003;2:19–21.

    Article  PubMed  Google Scholar 

  51. Quilici MT, Del Fiol Fde S, Vieira AE, Toledo MI. Risk Factors for Foot Amputation in Patients Hospitalized for Diabetic Foot Infection. J Diabetes Res. 2016;2016:8931508.

    PubMed  Google Scholar 

  52. Holman N, Young RJ, Jeffcoate WJ. Variation in the incidence of amputation in the lower limb in England. Diabetologia. 2012 Jul;55(7):1919–25. https://doi.org/10.1007/s00125-012-2468-6.

    Article  CAS  PubMed  Google Scholar 

  53. Boulton AJM. The pathway to ulceration: aetiopathogenesis. In: The foot in diabetes. Hoboken, NJ: Wiley; 2006. p. 51–67.

    Chapter  Google Scholar 

  54. Gardner SE, Haleem A, Jao Y-L, Hillis SL, Femino JE, Phisitkul P, Heilmann KP, et al. Cultures of diabetic foot ulcers without clinical signs of infection do not predict outcomes. Diabetes Care. 2014;37:2693–701.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Edmonds M. Diabetic foot ulcers: practical treatment recommendations. Drugs. 2006;66:913–29.

    Article  PubMed  Google Scholar 

  56. Bus S, Netten J, Lavery L, Monteiro-Soares M, Rasmussen A, Jubiz Y. IWGDF guidance on the prevention of foot ulcers in at-risk patients with diabetes. Diabetes Metab Res Rev. 2016;32:16–24.

    Article  PubMed  Google Scholar 

  57. Jeffcoate W, Young B. National diabetic foot audit of England and Wales yields its first dividends. Diabet Med. 2016;33:1464–5.

    Article  CAS  PubMed  Google Scholar 

  58. Jeffcoate WJ, Vileikyte L, Boyko EJ, Armstrong DG, Boulton AJM. Current challenges and opportunities in the prevention and management of diabetic foot ulcers. Diabet Care. 2018;41:645–52.

    Article  Google Scholar 

  59. Vas PR, Sharma S, Rayman G. Distal sensorimotor neuropathy: improvements in diagnosis. Rev Diabet Stud. 2015;12:29–47.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA. 2005;293:217–28.

    Article  CAS  PubMed  Google Scholar 

  61. Dros J, Wewerinke A, Bindels PJ, van Weert HC. Accuracy of monofilament testing to diagnose peripheral neuropathy: a systematic review. Ann Fam Med. 2009;7:555–8.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Tan LS. The clinical use of the 10g monofilament and its limitations: a review. Diabet Res Clin Pract. 2010;90:1–7.

    Article  Google Scholar 

  63. American Diabetes Association. 11. Microvascular complications and foot care: Standards of Medical Care in Diabetes—2019. Diabetes Care 2019;42(Suppl. 1):S124–S138.

    Google Scholar 

  64. Willits I, Cole H, Jones R, Dimmock P, Arber M, Craig J. VibraTip for testing vibration perception to detect diabetic peripheral neuropathy: a NICE medical technology guidance. Appl Health Econ Health Policy. 2015;13(4):315–24.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Pop-Busui R, Boulton AJM, Feldman EL, Bril V, Freeman R, Malik RA. Diabetic Neuropathy: A Position Statement by the American Diabetes Association. Diabetes Care. 2017;40:136–54.

    Google Scholar 

  66. Rayman G, Vas PR, Baker N, Taylor CG Jr, Gooday C, Alder AI. The Ipswich touch test: a simple and novel method to identify inpatients with diabetes at risk of foot ulceration. Diabetes Care. 2011;34:1517–8.

    PubMed  PubMed Central  Google Scholar 

  67. American Diabetes Association. Peripheral arterial disease in people with diabetes. Diabetes Care. 2003;26:3333–41.

    Article  Google Scholar 

  68. Boyko EJ, Ahroni JH, Davignon D, Stensel V, Prigeon RL, Smith DG. Diagnostic utility of the history and physical examination for peripheral vascular disease among patients with diabetes mellitus. J Clin Epidemiol. 1997;50:659–68.

    Article  CAS  PubMed  Google Scholar 

  69. Armstrong DW, Tobin C, Matangi MF. The accuracy of the physical examination for the detection of lower extremity peripheral arterial disease. Can J Cardiol. 2010;26:e346–50.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Hinchliffe RJ, Brownrigg JR, Apelqvist J, Boyko EJ, Fitridge R, Mills JL, et al. IWGDF guidance on the diagnosis, prognosis and management of peripheral artery disease in patients with foot ulcers in diabetes. Diabetes Metab Res Rev. 2016;32(Suppl 1):37–44.

    Article  PubMed  Google Scholar 

  71. Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ, Armstrong DG. Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis. 2012;54:e132–73.

    Google Scholar 

  72. Peters EJ. Pitfalls in diagnosing diabetic foot infections. Diabetes Metab Res Rev. 2016;32:254–60.

    Article  PubMed  Google Scholar 

  73. Berendt AR, Peters EJ, Bakker K, Embil JM, Eneroth M, Hinchliffe RJ. Diabetic foot osteomyelitis: a progress report on diagnosis and a systematic review of treatment. Diabetes Metab Res Rev. 2008;24(Suppl 1):S145–61.

    Article  PubMed  Google Scholar 

  74. Lipsky BA. Osteomyelitis of the foot in diabetic patients. Clin Infect Dis. 1997;25:1318–26.

    Article  CAS  PubMed  Google Scholar 

  75. Balsells M, Viade J, Millan M, Garcia JR, Garcia-Pascual L, del Pozo C, et al. Prevalence of osteomyelitis in non-healing diabetic foot ulcers: usefulness of radiologic and scintigraphic findings. Diabetes Res Clin Pract. 1997;38:123–7.

    Article  CAS  PubMed  Google Scholar 

  76. Lipsky BA. Medical treatment of diabetic foot infections. Clin Infect Dis. 2004;39:S104–14.

    Article  PubMed  Google Scholar 

  77. Barwick AL, Tessier JW, Janse de Jonge X, Ivers JR, Chuter VH. Peripheral sensory neuropathy is associated with altered postocclusive reactive hyperemia in the diabetic foot. BMJ Open Diabet Res Care. 2016;4(1):e000235. https://doi.org/10.1136/bmjdrc-2016-000235. eCollection 2016

    Article  Google Scholar 

  78. Edmonds M. Modern treatment of infection and ischaemia to reduce major amputation in the diabetic foot. Curr Pharm Des. 2013;19:5008–15.

    Article  CAS  PubMed  Google Scholar 

  79. Edmonds ME, Foster AV. Diabetic foot ulcers. BMJ. 2006;332:407–10.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Spichler A, Hurwitz BL, Armstrong DG, Lipsky BA. Microbiology of diabetic foot infections: from Louis Pasteur to ‘crime scene investigation’. BMC Med. 2015;13:2. https://doi.org/10.1186/s12916-014-0232-0.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Lipsky BA, Aragon-Sanchez J, Diggle M, Embil J, Kono S, Lavery L. IWGDF guidance on the diagnosis and management of foot infections in persons with diabetes. Diabetes Metab Res Rev. 2016;32(Suppl 1):45–74.

    Article  PubMed  Google Scholar 

  82. Slater R, Lazarovitch T, Boldur I, Ramot Y, Buchs A, Weiss M. Swab cultures accurately identify bacterial pathogens in diabetic foot wounds not involving bone. Diabet Med. 2004;21:705–9.

    Article  CAS  PubMed  Google Scholar 

  83. Gjødsbøl K, Skindersoe ME, Christensen JJ, Karlsmark T, Jørgensen B, Jensen AM. No need for biopsies: comparison of three sample techniques for wound microbiota determination. Int Wound J. 2012;9:295–302.

    Article  PubMed  Google Scholar 

  84. O’Meara S, Nelson E, Golder S, Dalton J, Craig D, Iglesias C. Systematic review of methods to diagnose infection in foot ulcers in diabetes. Diabet Med. 2006;23:341–7.

    Google Scholar 

  85. Sanverdi SE, Ergen BF, Oznur A. Current challenges in imaging of the diabetic foot. Diabet Foot Ankle. 2012;3

    Google Scholar 

  86. Peterson N, Widnall J, Evans P, Jackson G, Platt S. Diagnostic imaging of diabetic foot disorders. Foot Ankle Int. 2016;38:86–95.

    Article  PubMed  Google Scholar 

  87. Dinh T, Snyder G, Veves A. Review papers. Current techniques to detect foot infection in the diabetic patient. Int J Low Extrem Wounds. 2010;9(1):24–30. https://doi.org/10.1177/1534734610363004.

    Article  PubMed  Google Scholar 

  88. Kapoor A, Page S, LaValley M, Gale DR, Felson DT. Magnetic resonance imaging for diagnosing foot osteomyelitis: a meta-analysis. Arch Intern Med. 2007;167:125–32.

    Article  PubMed  Google Scholar 

  89. Lin Z, Vasudevan A, Tambyah PA. Use of erythrocyte sedimentation rate and c-reactive protein to predict osteomyelitis recurrence. J Orthop Surg. 2016;24:77–83.

    Article  CAS  Google Scholar 

  90. Paisey RB, Darby T, George AM, Waterson M, Hewson P, Paisey CF. Prediction of protective sensory loss, neuropathy and foot ulceration in type 2 diabetes. BMJ Open Diabetes Res Care. 2016;4(1):e000163. https://doi.org/10.1136/bmjdrc-2015-000163. eCollection 2016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Christman AL, Selvin E, Margolis DJ, Lazarus GS, Garza LA. Hemoglobin A1c predicts healing rate in diabetic wounds. J Invest Dermatol. 2011;131:2121–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Boulton AJ, Betts RP, Franks CI, Newrick PG, Ward JD, Duckworth T. Abnormalities of foot pressure in early diabetic neuropathy. Diabet Med. 1987;4:225–8.

    Article  CAS  PubMed  Google Scholar 

  93. Caselli A, Pham H, Giurini JM, Armstrong DG, Veves A. The forefoot-to-rearfoot plantar pressure ratio is increased in severe diabetic neuropathy and can predict foot ulceration. Diabetes Care. 2002;25:1066–71.

    Article  PubMed  Google Scholar 

  94. Veves A, Murray HJ, Young MJ, Boulton AJ. The risk of foot ulceration in diabetic patients with high foot pressure: a prospective study. Diabetologia. 1992;35:660–3.

    Article  CAS  PubMed  Google Scholar 

  95. Wallace C, Reiber GE, LeMaster J, Smith DG, Sullivan K, Hayes S, et al. Incidence of falls, risk factors for falls, and fall-related fractures in individuals with diabetes and a prior foot ulcer. Diabetes Care. 2002;25:1983–6.

    Article  PubMed  Google Scholar 

  96. Vas PRJ, Ahluwalia R, Manas AB, Manu CA, Kavarthapu V, Edmonds ME. Undiagnosed severe sleep apnoea and diabetic foot ulceration—a case series based hypothesis: a hitherto under emphasized factor in failure to heal. Diabet Med. 2016;33:e1–4.

    Google Scholar 

  97. Zhang SS, Tang ZY, Fang P, Qian HJ, Xu L, Ning G. Nutritional status deteriorates as the severity of diabetic foot ulcers increases and independently associates with prognosis. Exp Ther Med. 2013;5:215–22.

    Article  CAS  PubMed  Google Scholar 

  98. Chuan F, Zhang M, Yao Y, Tian W, He X, Zhou B. Anemia in patients with diabetic foot ulcer. Int J Low Extremity Wound. 2016;15:220–6.

    Article  Google Scholar 

  99. Ismail K, Winkley K, Stahl D, Chalder T, Edmonds M. A cohort study of people with diabetes and their first foot ulcer: the role of depression on mortality. Diabetes Care. 2007;30:1473–9.

    Article  PubMed  Google Scholar 

  100. Natovich R, Kushnir T, Harman-Boehm I, Margalit D, Siev-Ner I, Tsalichin D. Cognitive dysfunction: part and parcel of the diabetic foot. Diabetes Care. 2016;39:1202–7.

    Article  PubMed  Google Scholar 

  101. Hingorani A, LaMuraglia GM, Henke P, Meissner MH, Loretz L, al ZKM. The management of diabetic foot: a clinical practice guideline by the Society for Vascular Surgery in collaboration with the American Podiatric Medical Association and the Society for Vascular Medicine. J Vasc Surg. 2016;63:3S–21S.

    Article  PubMed  Google Scholar 

  102. Game FL, Attinger C, Hartemann A, Hinchliffe RJ, Londahl M, Price PE, et al. IWGDF guidance on use of interventions to enhance the healing of chronic ulcers of the foot in diabetes. Diabetes Metab Res Rev. 2016;32(Suppl 1):75–83.

    Article  PubMed  Google Scholar 

  103. Armstrong DG, Lavery LA. Negative pressure wound therapy after partial diabetic foot amputation: a multicentre, randomised controlled trial. Lancet. 2005;366:1704–10.

    Article  PubMed  Google Scholar 

  104. Blume PA, Walters J, Payne W, Ayala J, Lantis J. Comparison of negative pressure wound therapy using vacuum-assisted closure with advanced moist wound therapy in the treatment of diabetic foot ulcers: a multicenter randomized controlled trial. Diabetes Care. 2008;31:631–6.

    Article  PubMed  Google Scholar 

  105. NICE: Diabetic foot problems: prevention and management. 2015

    Google Scholar 

  106. Sherman RA. Mechanisms of maggot-induced wound healing: what do we know, and where do we go from here? Evid Based. Complement Alternat Med. 2014;2014:592419.

    Google Scholar 

  107. Sherman RA. Maggot therapy for treating diabetic foot ulcers unresponsive to conventional therapy. Diabetes Care. 2003;26:446–51.

    Article  PubMed  Google Scholar 

  108. Sheehan P. Early change in wound area as a predictor of healing in diabetic foot ulcers: knowing “when to say when”. Plast Reconstruct Surg. 200(117):245S–7S.

    Google Scholar 

  109. Snyder RJ, Cardinal M, Dauphinée DM, Stavosky J. A post-hoc analysis of reduction in diabetic foot ulcer size at 4 weeks as a predictor of healing by 12 weeks. Ostom Wound Manag. 2010;56(3):44–50.

    Google Scholar 

  110. Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Healing diabetic neuropathic foot ulcers: are we getting better? Diabet Med. 2005;22:172–6.

    Article  CAS  PubMed  Google Scholar 

  111. Blume PA, Donegan R, Schmidt BM. The role of plastic surgery for soft tissue coverage of the diabetic foot and ankle. Clin Podiatr Med Surg. 2014;31:127–50.

    Article  PubMed  Google Scholar 

  112. Schaper NC, Van Netten JJ, Apelqvist J, Lipsky BA, Bakker K. Prevention and management of foot problems in diabetes: a summary guidance for daily practice 2015, based on the IWGDF guidance documents. Diabetes Metab Res Rev. 2016;32(Suppl 1):7–15.

    Article  PubMed  Google Scholar 

  113. Morona JK, Buckley ES, Jones S, Reddin EA, Merlin TL. Comparison of the clinical effectiveness of different off-loading devices for the treatment of neuropathic foot ulcers in patients with diabetes: a systematic review and meta-analysis. Diabetes Metab Res Rev. 2013;29:183–93.

    Article  PubMed  Google Scholar 

  114. Gotz J, Lange M, Dullien S, Grifka J, Hertel G, Baier C, et al. Off-loading strategies in diabetic foot syndrome-evaluation of different devices. Int Orthop. 2017;41:239–46.

    Article  PubMed  Google Scholar 

  115. Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet. 2003;361:1545–51.

    Article  PubMed  Google Scholar 

  116. Frykberg RG, Bevilacqua NJ, Habershaw G. Surgical off-loading of the diabetic foot. J Vasc Surg. 2010;52:44S–58S.

    Article  PubMed  Google Scholar 

  117. La Fontaine J, Lavery LA, Hunt NA, Murdoch DP. The role of surgical off-loading to prevent recurrent ulcerations. Int J Low Extrem Wounds. 2014;13:320–34.

    Article  PubMed  Google Scholar 

  118. Scott JE, Hendry GJ, Locke J. Effectiveness of percutaneous flexor tenotomies for the management and prevention of recurrence of diabetic toe ulcers: a systematic review. J Foot Ankle Res. 2016;9:25. https://doi.org/10.1186/s13047-016-0159-0.

    Article  PubMed  PubMed Central  Google Scholar 

  119. Dallimore SM, Kaminski MR. Tendon lengthening and fascia release for healing and preventing diabetic foot ulcers: a systematic review and meta-analysis. J Foot Ankle Res. 2015;8:33.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Siebachmeyer M, Boddu K, Bilal A, Hester TW, Hardwick T, Fox TP et al. Outcome of one-stage correction of deformities of the ankle and hindfoot and fusion in Charcot neuroarthropathy using a retrograde intramedullary hindfoot arthrodesis nail. Bone Joint J. 2015;97-B:76–82.

    Google Scholar 

  121. Wukich DK, Raspovic KM, Hobizal KB, Sadoskas D. Surgical management of Charcot neuroarthropathy of the ankle and hindfoot in patients with diabetes. Diabetes Metab Res Rev. 2016;32:292–6.

    Article  PubMed  Google Scholar 

  122. Hatipoglu M, Mutluoglu M, Turhan V, Uzun G, Lipsky BA, Sevim E. J Diabetes Complications. 2016;30(5):910–6. https://doi.org/10.1016/j.jdiacomp.2016.02.013.

    Article  PubMed  Google Scholar 

  123. Rastogi A, Sukumar S, Hajela A, Mukherjee S, Dutta P, Bhadada SK, et al. The microbiology of diabetic foot infections in patients recently treated with antibiotic therapy: a prospective study from India. J Diabetes Complications. 2017;31(2):407–12. https://doi.org/10.1016/j.jdiacomp.2016.11.001.

    Article  PubMed  Google Scholar 

  124. Bowling FL, Jude EB, Boulton AJM. MRSA and diabetic foot wounds: contaminating or infecting organisms? Curr Diabet Rep. 2009;9:440–4.

    Article  Google Scholar 

  125. Lipsky BA. Diabetic foot infections: current treatment and delaying the ‘post-antibiotic era’. Diabetes Metab Res Rev. 2016;32(Suppl 1):246–53.

    Article  PubMed  Google Scholar 

  126. Vas PRJ, Edmonds M, Kavarthapu V, Rashid H, Ahluwalia R, Pankhurst C, et al. The diabetic foot attack: “Tis Too Late to Retreat!”. Int J Low Extrem Wounds. 2018;17:7–13.

    Article  PubMed  Google Scholar 

  127. Uckay I, Gariani K, Dubois-Ferriere V, Suva D, Lipsky BA. Diabetic foot infections: recent literature and cornerstones of management. Curr Opin Infect Dis. 2016;29:145–52.

    Article  PubMed  Google Scholar 

  128. Selva Olid A, Solà I, Barajas-Nava LA, Gianneo OD, Bonfill Cosp X, Lipsky BA. Systemic antibiotics for treating diabetic foot infections. Cochrane Database Syst Rev. 2015;9:CD009061. https://doi.org/10.1002/14651858.CD009061.pub2.

    Article  Google Scholar 

  129. Lázaro-Martínez JL, Aragón-Sánchez J, García-Morales E. Antibiotics versus conservative surgery for treating diabetic foot osteomyelitis: a randomized comparative trial. Diabetes Care. 2014;37:789–95.

    Article  PubMed  Google Scholar 

  130. Hasan R, Firwana B, Elraiyah T, Domecq JP, Prutsky G, Nabhan M, et al. A systematic review and meta-analysis of glycemic control for the prevention of diabetic foot syndrome. J Vasc Surg. 63:22S–8S.e22

    Google Scholar 

  131. McGuire H, Longson D, Adler A, Farmer A, Lewin I. Management of type 2 diabetes in adults: summary of updated NICE guidance. BMJ: 2016;353:i1575. https://doi.org/10.1136/bmj.i1575.

  132. Standards of medical care in diabetes—2016: summary of revisions. Diabetes Care. 2016;39:S4–5.

    Google Scholar 

  133. Viswanathan V, Madhavan S, Rajasekar S, Chamukuttan S, Ambady R. Amputation prevention initiative in South India: positive impact of foot care education. Diabetes Care. 2005;28:1019–21.

    Article  PubMed  Google Scholar 

  134. Malone JM, Snyder M, Anderson G, Bernhard VM, Holloway GA Jr, Bunt TJ. Prevention of amputation by diabetic education. Am J Surg. 1989;158:520–3; discussion 523–524.

    Article  CAS  PubMed  Google Scholar 

  135. van Netten JJ, Price PE, Lavery LA, Monteiro-Soares M, Rasmussen A, Jubiz Y. Prevention of foot ulcers in the at-risk patient with diabetes: a systematic review. Diabetes Metab Res Rev. 2016;32(Suppl 1):84–98.

    Article  PubMed  Google Scholar 

  136. Dorresteijn JA, Kriegsman DM, Assendelft WJ, Valk GD. Patient education for preventing diabetic foot ulceration. Cochrane Database Syst Rev. 2014:CD001488.

    Google Scholar 

  137. Edmonds ME, Blundell MP, Morris ME, Thomas EM, Cotton LT, Watkins PJ. Improved survival of the diabetic foot: the role of a specialized foot clinic. Q J Med. 1986;60:763–71.

    CAS  PubMed  Google Scholar 

  138. Krishnan S, Nash F, Baker N, Fowler D, Rayman G. Reduction in diabetic amputations over 11 years in a defined U.K. population: benefits of multidisciplinary team work and continuous prospective audit. Diabetes Care. 2008;31:99–101.

    Article  PubMed  Google Scholar 

  139. McCabe CJ, Stevenson RC, Dolan AM. Evaluation of a diabetic foot screening and protection programme. Diabet Med. 1998;15:80–4.

    Article  CAS  PubMed  Google Scholar 

  140. Hedetoft C, Rasmussen A, Fabrin J, Kolendorf KK. Four-fold increase in foot ulcers in type 2 diabetic subjects without an increase in major amputations by a multidisciplinary setting. Diabetes Res Clin Pract. 2009;83:353–7.

    Article  PubMed  Google Scholar 

  141. Diabetes UK: Putting Feet First. Fast track for a foot attack: preventing amputations. London: Diabetes UK; 2013.

    Google Scholar 

  142. Van Acker K, Weyler J, De Leeuw I. The diabetic foot project of Flanders, the Northern part of Belgium: implementation of the St. Vincent Consensus. Acta Clinica Belgica. 2001;56:21–31.

    Google Scholar 

  143. Xu Z, Ran X. Diabetic foot care in China: challenges and strategy. Lancet Diabet Endocr. 2016;4:297–8.

    Article  Google Scholar 

  144. Viswanathan V, Rao VN. Managing diabetic foot infection in India. Int J Low Extrem Wounds. 2013;12:158–66.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Diabetic Foot Clinic, King’s College Hospital NHS Foundation Trust, London, UK

    Prashanth R. J. Vas, Jody Lucas, Sobia Arshad & Michael E. Edmonds

Authors
  1. Prashanth R. J. Vas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jody Lucas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sobia Arshad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael E. Edmonds
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Prashanth R. J. Vas .

Editor information

Editors and Affiliations

  1. King’s College Hospital, London, UK

    Michael E. Edmonds

  2. School of Medicine, Yale University, New Haven, CT, USA

    Bauer E. Sumpio

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Vas, P.R.J., Lucas, J., Arshad, S., Edmonds, M.E. (2019). Neuropathic Diabetic Foot Ulceration. In: Edmonds, M., Sumpio, B. (eds) Limb Salvage of the Diabetic Foot. Springer, Cham. https://doi.org/10.1007/978-3-319-17918-6_4

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-17918-6_4

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-17917-9

  • Online ISBN: 978-3-319-17918-6

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation