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Diabetic Foot Ulcers

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Ulcers of the Lower Extremity
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Abstract

“Diabetic foot” is one of the most common and feared complications associated with diabetes. It is estimated that almost 15 % of people with diabetes will develop foot ulcers requiring medical care during their lifetime. Diabetic foot ulcers are a major cause of hospital admission and thus impose a large financial burden on healthcare systems. Diabetic patients who develop foot ulcers are at greater risk of dying prematurely than those without this complication [1] (Fig. 1); in particular, not only ischemic diabetic foot ulcers but also neuropathic ulcerations are related to increased mortality in individuals with diabetes [2] (Fig. 2).

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References

  1. Boyko EJ, Ahroni JH, Smith DG, Davignon D. Increased mortality associated with diabetic foot ulcer. Diabet Med. 1996;13:967–72.

    Article  CAS  PubMed  Google Scholar 

  2. Chammas NK, Hill RL, Foster AV, Edmonds ME. Is neuropathic ulceration the key to understanding increased mortality due to ischaemic heart disease in diabetic foot ulcer patients? A population approach using a proportionate model. J Int Med Res. 2002;30:553–9.

    Article  CAS  PubMed  Google Scholar 

  3. Uccioli L. Advances in the treatment of peripheral vascular disease in diabetes and reduction of major amputations. Int J Low Extrem Wounds. 2011;10:72–4.

    Article  PubMed  Google Scholar 

  4. Vamos EP, Bottle A, Edmonds ME, Valabhji J, Majeed A, Millett C. Changes in the incidence of lower extremity amputations in individuals with and without diabetes in England between 2004 and 2008. Diabetes Care. 2010;33:2592–7.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Li Y, Burrows NR, Gregg EW, Albright A, Geiss LS. Declining rates of hospitalization for nontraumatic lower-extremity amputation in the diabetic population aged 40 years or older: U.S., 1988–2008. Diabetes Care. 2012;35:273–7.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Centers for Disease Control and Prevention (CDC). Hospital discharge rates for nontraumatic lower extremity amputation by diabetes status–United States, 1997. MMWR Morb Mortal Wkly Rep. 2001;50:954–8.

    Google Scholar 

  7. Sanders LJ, Robbins JM, Edmonds ME. History of the team approach to amputation prevention: pioneers and milestones. J Vasc Surg. 2010;52(Suppl):3S–16.

    Article  PubMed  Google Scholar 

  8. Faglia E, Favales F, Aldeghi A, Calia P, Quarantiello A, Barbano P, et al. Change in major amputation rate in a center dedicated to diabetic foot care during the 1980s: prognostic determinants for major amputation. J Diabetes Complications. 1998;12:96–102.

    Article  CAS  PubMed  Google Scholar 

  9. Lombardo FL, Maggini M, De Bellis A, Seghieri G, Anichini R. Lower extremity amputations in persons with and without diabetes in Italy: 2001–2010. PLoS One. 2014;9(1):e86405.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Faglia E, Clerici G, Mantero M, Caminiti M, Quarantiello A, Curci V, Morabito A. Incidence of critical limb ischemia and amputation outcome in contralateral limb in diabetic patients hospitalized for unilateral critical limb ischemia during 1999–2003 and followed-up until 2005. Diabetes Res Clin Pract. 2007;77:445–50.

    Article  PubMed  Google Scholar 

  11. Edmonds ME. Progress in the care of diabetic foot. Lancet. 1999;354:270–2.

    Article  CAS  PubMed  Google Scholar 

  12. 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 

  13. Rathur HM, Boulton AJ. The neuropathic diabetic foot. Nat Clin Pract Endocrinol Metab. 2007;3:14–25.

    Article  PubMed  Google Scholar 

  14. Adler AI, Boyko EJ, Ahroni JH, Smith DG. Lower-extremity amputation in diabetes. The independent effects of peripheral vascular disease, sensory neuropathy, and foot ulcers. Diabetes Care. 1999;22:1029–35.

    Article  CAS  PubMed  Google Scholar 

  15. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, Edmonds M, Holstein P, Jirkovska A, Mauricio D, Ragnarson Tennvall G, Reike H, Spraul M, Uccioli L, Urbancic V, Van Acker K, van Baal J, van Merode F, Schaper N. 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 

  16. Prompers L, Schaper N, Apelqvist J, Edmonds M, Jude E, Mauricio D, Uccioli L, Urbancic V, Bakker K, Holstein P, Jirkovska A, Piaggesi A, Ragnarson-Tennvall G, Reike H, Spraul M, Van Acker K, Van Baal J, Van Merode F, Ferreira I, Huijberts M. Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study. Diabetologia. 2008;51:747–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. American Diabetes Association/American Academy of Neurology: report and recommendations of the San Antonio Conference on diabetic neuropathy. Diabetes Care. 1988;11:592–7.

    Google Scholar 

  18. Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, Lauria G, Malik RA, Spallone V, Vinik A, Bernardi L, Valensi P, Toronto Diabetic Neuropathy Expert Group. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33:2285–93.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Bril V, England JD, Franklin GM, Backonja M, Cohen JA, Del Toro DR, Feldman EL, Iverson DJ, Perkins B, Russell JW, Zochodne DW, American Academy of Neurology, American Asociation of Neuromuscular and Electrodiagnostic Medicine, American Academy of Physical Medicine and Rehabilitation. Evidence-based guideline: treatment of painful diabetic neuropathy–report of the American Association of Neuromuscular and Electrodiagnostic Medicine, the American Academy of Neurology, and the American Academy of Physical Medicine & Rehabilitation. Muscle Nerve. 2011;43:910–7.

    Article  PubMed  Google Scholar 

  20. Boulton AJ, Malik RA, Arezzo JC, Sosenko JM. Diabetic somatic neuropathies. Diabetes Care. 2004;27:1458–86.

    Article  PubMed  Google Scholar 

  21. Maser RE, Lenhard MJ. Cardiovascular autonomic neuropathy due to diabetes mellitus: clinical manifestations, consequences, and treatment. J Clin Endocrinol Metab. 2005;90:5896–903.

    Article  CAS  PubMed  Google Scholar 

  22. Spallone V, Morganti R. Neuropatia diabetica. In: Uccioli L, editor. Il piede diabetico. Società Editrice Universo. Roma; 2008. p. 53–106.

    Google Scholar 

  23. Dyck PJ. Severity and staging of diabetic polyneuropathy. In: Gries FA, Cameron NE, Low PA, Ziegler D, editors. Textbook of diabetic neuropathy. Stuttgart: Thieme; 2003. p. 170–5.

    Google Scholar 

  24. Boulton AJ. Guidelines for diagnosis and outpatient management of diabetic peripheral neuropathy. European Association for the Study of Diabetes, Neurodiab. Diabetes Metab. 1998;24 Suppl 3:55–65.

    PubMed  Google Scholar 

  25. Nather A, Neo SH, Chionh SB, Liew SC, Sim EY, Chew JL. Assessment of sensory neuropathy in diabetic patients without diabetic foot problems. J Diabetes Complications. 2008;22:126–31.

    Article  PubMed  Google Scholar 

  26. Modawal A, Fley J, Shukla R, Rudawsky D, Welge J, Yang J. Use of monofilament in the detection of foot lesions in older adults. J Foot Ankle Surg. 2006;45:76–81.

    Article  PubMed  Google Scholar 

  27. Feng Y, Schlösser FJ, Sumpio BE. The Semmes Weinstein monofilament examination as a screening tool for diabetic peripheral neuropathy. J Vasc Surg. 2009;50:675–82.

    Article  PubMed  Google Scholar 

  28. Van Deursen RW, Sanchez MM, Derr JA, Becker MB, Ulbrecht JS, Cavanagh PR. Vibration perception threshold testing in patients with diabetic neuropathy: ceiling effects and reliability. Diabet Med. 2001;18:469–75.

    Article  PubMed  Google Scholar 

  29. Manivannam M, Periyasamy R, Narayanamurtty VB. Vibration perception threshold and the law of mobility in diabetic mellitus patients. Prim Care Dibetes. 2009;3:17–21.

    Article  Google Scholar 

  30. Reulen JP, Lansbergen MD, Verstraete E, Spaans F. Comparison of thermal threshold tests to assess small nerve fiber function: limits vs. levels. Clin Neurophysiol. 2003;114:556–63.

    Article  CAS  PubMed  Google Scholar 

  31. Bagavathiappan S, Philip J, Jayakumar T, Raj B, Rao PN, Varalakshmi M, Mohan V. Correlation between plantar foot temperature and diabetic neuropathy: a case study by using an infrared thermal imaging technique. J Diabetes Sci Technol. 2010;4:1386–92.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Ziegler D, Mayer P, Wiefels K, Gries FA. Evaluation of thermal, pain, and vibration sensation thresholds in newly diagnosed type 1 diabetic patients. J Neurol Neurosurg Psychiatry. 1988;11:1420–4.

    Article  Google Scholar 

  33. Sosenko JM, Kato M, Soto R, Bild DE. Comparison of quantitative sensory threshold measures for their association with foot ulceration in diabetic patients. Diabetes Care. 1990;13:1057–61.

    Article  CAS  PubMed  Google Scholar 

  34. Miralles-García JM, de Pablos-Velasco P, Cabrerizo L, Pérez M, López-Gómez V, Sociedad Española de Endocrinología y Nutrición. Prevalence of distal diabetic polyneuropathy using quantitative sensory methods in a population with diabetes of more than 10 years’ disease duration. Endocrinol Nutr. 2010;57:414–20.

    Article  PubMed  Google Scholar 

  35. Zinman LH, Bril V, Perkins BA. Cooling detection thresholds in the assessment of diabetic sensory polyneuropathy: comparison of CASE IV and Medoc instruments. Diabetes Care. 2004;27:1674–9.

    Article  PubMed  Google Scholar 

  36. Ziegler D, Siekierka-Kleiser E, Meyer B, Schweers M. Validation of a novel screening device (NeuroQuick) for quantitative assessment of small nerve fiber dysfunction as an early feature of diabetic polyneuropathy. Diabetes Care. 2005;28:1169–74.

    Article  PubMed  Google Scholar 

  37. Bus SA, Yang QX, Wang JH, Smith MB, Wunderlich R, Cavanagh PR. Intrinsic muscle atrophy and toe deformity in the diabetic neuropathic foot: a magnetic resonance imaging study. Diabetes Care. 2002;25:1444–50.

    Article  PubMed  Google Scholar 

  38. Bus SA, Maas M, Cavanagh PR, Michels RP, Levi M. Plantar fat-pad displacement in neuropathic diabetic patients with toe deformity: a magnetic resonance imaging study. Diabetes Care. 2004;27:2376–81.

    Article  PubMed  Google Scholar 

  39. Cavanagh PR, Ulbrecht JS, Caputo GM. Biomechanical aspects of diabetic foot disease: aetiology, treatment and prevention. Diabet Med. 1996;13 Suppl 1:517–22.

    Google Scholar 

  40. Schnider SL, Kohn RR. Glucosylation of human collagen in aging and diabetes mellitus. J Clin Invest. 1980;66:1179–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Giacomozzi C, D’Ambrogi E, Uccicoli L, Macellari V. Does the thickening of Achilles tendon and plantar fascia contribute to the alteration of diabetic foot loading? Clin Biomech (Bristol, Avon). 2005;20:532–39.

    Google Scholar 

  42. Carrington AL, Shaw JE, Van Schie CH, Abbott CA, Vileikyte L, Boulton AJ. Can motor nerve conduction velocity predict foot problems in diabetic subjects over a 6-year outcome period? Diabetes Care. 2002;25:2010–5.

    Article  PubMed  Google Scholar 

  43. Kanji JN, Anglin RE, Hunt DI, Panju A. Does this patient with diabetes have large -fiber peripheral neuropathy? JAMA. 2010;303:1526–32.

    Article  CAS  PubMed  Google Scholar 

  44. Freeman R. Autonomic peripheral neuropathy. Lancet. 2005;365:1259–70.

    Article  CAS  PubMed  Google Scholar 

  45. Tentolouris N, Voulgari C, Liatis S, Kokkinos A, Eleftheriadou I, Makrilakis K, Marinou K, Katsilambros N. Moisture status of the skin of the feet assessed by the visual test neuropad correlates with foot ulceration in diabetes. Diabetes Care. 2010;33:1112–4.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Quattrini C, Jeziorska M, Tavakoli M, Begum P, Boulton AJ, Malik RA. The Neuropad test: a visual indicator test for human diabetic neuropathy. Diabetologia. 2008;51:1046–50.

    Article  CAS  PubMed  Google Scholar 

  47. Spallone V, Morganti R, Siampli M, Fedele T, D’Amato C, Cacciotti L, Maiello MR. Neuropad as a diagnostic tool for diabetic autonomic and sensorimotor neuropathy. Diabet Med. 2009;26:686–92.

    Article  CAS  PubMed  Google Scholar 

  48. Tentolouris N, Marinou K, Kokotis P, Karanti A, Diakoumopoulou E, Katsilambros N. Sudomotor dysfunction is associated with foot ulceration in diabetes. Diabet Med. 2009;26:302–5.

    Article  CAS  PubMed  Google Scholar 

  49. Spallone V, Bellavere F, Scionti L, Maule S, Quadri R, Bax G, Melga P, Viviani GL, Esposito K, Morganti R, Cortelli P, Diabetic Neuropathy Study Group of the Italian Society of Diabetology. Recommendations for the use of cardiovascular tests in diagnosing diabetic autonomic neuropathy. Nutr Metab Cardiovasc Dis. 2011;21:69–78.

    Article  CAS  PubMed  Google Scholar 

  50. Stevens MJ, Edmonds ME, Douglas SLE, Watkins PJ. the influence of neuropathy on the microvascular response to local heating in the human diabetic foot. Clin Sci. 1991;80:249.

    Article  CAS  PubMed  Google Scholar 

  51. Hamady MS, Yu DF, Sayer GL, Edmonds ME, Walters HL, Sidhu PS. Lower limb arteriovenous communications in diabetes mellitus: a potential reason for aggravation of ischemic symptoms. Cardiovasc Intervent Radiol. 2006;29:745–51.

    Article  PubMed  Google Scholar 

  52. Wheeler SG, Ahroni JH, Boyko EJ. Prospective study of autonomic neuropathy as a predictor of mortality in patients with diabetes. Diabetes Res Clin Pract. 2002;58:131–8.

    Article  PubMed  Google Scholar 

  53. Astrup AS, Tarnow L, Rossing P, Hansen BV, Hilsted J, Parving HH. Cardiac autonomic neuropathy predicts cardiovascular morbidity and mortality in type 1 diabetic patients with diabetic nephropathy. Diabetes Care. 2006;29:334–9.

    Article  PubMed  Google Scholar 

  54. Delbrigde L, Ctercteko GC, Fowler C. The aetioligy of neuropathic ulceration in the diabetic foot. Br J Surg. 1985;72:1–6.

    Article  Google Scholar 

  55. Boulton AJ. Diabetic neuropathy: classification, measurement and treatment. Curr Opin Endocrinol Diabetes Obes. 2007;14:141–5.

    Article  PubMed  Google Scholar 

  56. Caputo GM, Ulbrecht JS, Cavanagh PR. The total contact cast: a method for treating neuropathic diabetic ulcers. Am Fam Physician. 1997;55:605–11.

    CAS  PubMed  Google Scholar 

  57. Boulton AJ, Bowker JH, Gadia M, Lemerman R, Caswell K, Skyler JS, Sosenko JM. Use of plaster casts in the management of diabetic neuropathic foot ulcers. Diabetes Care. 1986;9:149–52.

    Article  CAS  PubMed  Google Scholar 

  58. Nabuurs-Fransenn M, Sleegers R, Huijberts MSP, Wijnen W, Sanders AP, Walenkamp G, Schaper NC. Total contact casting of the diabetic foot in daily practice: a prospective follow-up study. Diabetes Care. 2005;28:243–7.

    Article  Google Scholar 

  59. Sinacore DR. Total contact casting for diabetic neuropathic ulcers. Phys Ther. 1996;76:296–301.

    Article  CAS  PubMed  Google Scholar 

  60. Caravaggi C, Faglia E, De Giglio R, Mantero M, Quarantiello A, Sommariva E, Gino M, Pritelli C, Morabito A. Effectiveness and safety of a nonremovable fiberglass off-bearing cast versus a therapeutic shoe in the treatment of neuropathic foot ulcers: a randomized study. Diabetes Care. 2000;23:1746–51.

    Article  CAS  PubMed  Google Scholar 

  61. Armstrong DG, Nguyen HC, Lavery LA, van Schie CH, Boulton AJ, Harkless LB. Off-loading the diabetic foot wound: a randomized clinical trial. Diabetes Care. 2001;24:1019–22.

    Article  CAS  PubMed  Google Scholar 

  62. Katz IA, Harlan A, Miranda-Palma B, Prieto-Sanchez L, Armstrong DG, Bowker JH, Mizel MS, Boulton AJ. A randomized trial of two irremovable off-loading devices in the management of plantar neuropathic diabetic foot ulcers. Diabetes Care. 2005;28:555–9.

    Article  PubMed  Google Scholar 

  63. Cavanagh PR, Bus SA. Off-loading the diabetic foot for ulcer prevention and healing. J Vasc Surg. 2010;52(3 Suppl):37S–43.

    Article  PubMed  Google Scholar 

  64. Piaggesi A, Macchiarini S, Rizzo L, Palumbo F, Tedeschi A, Nobili LA, Leporati E, Scire V, Teobaldi I, Del Prato S. An off-the-shelf instant contact casting device for the management of diabetic foot ulcers: a randomized prospective trial versus traditional fiberglass cast. Diabetes Care. 2007;30:586–90.

    Article  PubMed  Google Scholar 

  65. Faglia E, Caravaggi C, Clerici G, Sganzaroli A, Curci V, Vailati W, Simonetti D, Sommalvico F. Effectiveness of removable walker cast versus nonremovable fiberglass off-bearing cast in the healing of diabetic plantar foot ulcer: a randomized controlled trial. Diabetes Care. 2010;33:1419–23.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Piaggesi A, Schipani E, Campi F, Romanelli M, Baccetti F, Arvia C, Navalesi R. Conservative surgical approach versus non-surgical management for diabetic neuropathic foot ulcers: a randomized trial. Diabet Med. 1998;15:412–7.

    Article  CAS  PubMed  Google Scholar 

  67. Sanders LJ, Frykberg RG. Charcot neuroarthropathy of the foot. In: Bowker JH, Pfeifer MA, editors. Levin and O’Neal’s the diabetic foot. 6th ed. St. Louis: Mosby; 2001. p. 439–65.

    Google Scholar 

  68. Rogers LC, Frykberg RG, Armstrong DG, Boulton AJ, Edmonds M, Van GH, Hartemann A, Game F, Jeffcoate W, Jirkovska A, Jude E, Morbach S, Morrison WB, Pinzur M, Pitocco D, Sanders L, Wukich DK, Uccioli L. The Charcot foot in diabetes. Diabetes Care. 2011;34:2123–9.

    Article  PubMed  PubMed Central  Google Scholar 

  69. 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 

  70. Petrova NL, Foster AV, Edmonds ME. Difference in presentation of charcot osteoarthropathy in type 1 compared with type 2 diabetes. Diabetes Care. 2004;27:1235–6.

    Article  PubMed  Google Scholar 

  71. Pitocco D, Zelano G, Gioffrè G, Di Stasio E, Zaccardi F, Martini F, Musella T, Scavone G, Galli M, Caputo S, Mancini L, Ghirlanda G. Association between osteoprotegerin G1181C and T245G polymorphisms and diabetic charcot neuroarthropathy: a case-control study. Diabetes Care. 2009;32:1694–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Korzon-Burakowska A, Jakóbkiewicz-Banecka J, Fiedosiuk A, Petrova N, Koblik T, Gabig-Cimińska M, Edmonds M, Małecki MT, Węgrzyn G. Osteoprotegerin gene polymorphism in diabetic Charcot neuroarthropathy. Diabet Med. 2011;29(6):771–5.

    Article  CAS  Google Scholar 

  73. Ndip A, Williams A, Jude EB, Serracino-Inglott F, Richardson S, Smyth JV, Boulton AJ, Alexander MY. The RANKL/RANK/OPG signaling pathway mediates medial arterial calcification in diabetic Charcot neuroarthropathy. Diabetes. 2011;60:2187–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Mabilleau G, Petrova NL, Edmonds ME, Sabokbar A. Increased osteoclastic activity in acute Charcot’s osteoarthropathy: the role of receptor activator of nuclear factor-kappaB ligand. Diabetologia. 2008;51:1035–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Aggarwal BB, Gupta SC, Kim JH. Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood. 2012;119:651–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Toledano TR, Fatone EA, Weis A, Cotten A, Beltran J. MRI evaluation of bone marrow changes in the diabetic foot: a practical approach. Semin Musculoskelet Radiol. 2011;15:257–68.

    Article  PubMed  Google Scholar 

  77. Gaeta M, Mileto A, Mazzeo A, Minutoli F, Di Leo R, Settineri N, Donato R, Ascenti G, Blandino A. MRI findings, patterns of disease distribution, and muscle fat fraction calculation in five patients with Charcot-Marie-Tooth type 2 F disease. Skeletal Radiol. 2011;41(5):515–24.

    Article  PubMed  Google Scholar 

  78. Zampa V, Bargellini I, Rizzo L, Turini F, Ortori S, Piaggesi A, Bartolozzi C. Role of dynamic MRI in the follow-up of acute Charcot foot in patients with diabetes mellitus. Skeletal Radiol. 2011;40:991–9.

    Article  PubMed  Google Scholar 

  79. Chantelau E, Richter A, Ghassem-Zadeh N, Poll LW. “Silent” bone stress injuries in the feet of diabetic patients with polyneuropathy: a report on 12 cases. Arch Orthop Trauma Surg. 2007;127:171–7.

    Article  CAS  PubMed  Google Scholar 

  80. Ledermann HP, Morrison WB. Differential diagnosis of pedal osteomyelitis and diabetic neuroarthropathy: MR Imaging. Semin Musculoskelet Radiol. 2005;9:272–83.

    Article  PubMed  Google Scholar 

  81. Palestro CJ, Mehta HH, Patel M, Freeman SJ, Harrington WN, Tomas MB, Marwin SE. Marrow versus infection in the Charcot joint: indium-111 leukocyte and technetium-99m sulfur colloid scintigraphy. J Nucl Med. 1998;39:346–50.

    CAS  PubMed  Google Scholar 

  82. Tomas MB, Patel M, Marwin SE, Palestro CJ. The diabetic foot. Br J Radiol. 2000;73:443–50.

    Article  CAS  PubMed  Google Scholar 

  83. Palestro CJ, Love C. Nuclear medicine and diabetic foot infections. Semin Nucl Med. 2009;39:52–65.

    Article  PubMed  Google Scholar 

  84. Pickwell KM, van Kroonenburgh MJ, Weijers RE, van Hirtum PV, Huijberts MS, Schaper NC. F-18 FDG PET/CT scanning in Charcot disease: a brief report. Clin Nucl Med. 2011;36:8–10.

    Article  PubMed  Google Scholar 

  85. Höpfner S, Krolak C, Kessler S, Tiling R, Brinkbäumer K, Hahn K, Dresel S. Preoperative imaging of Charcot neuroarthropathy in diabetic patients: comparison of ring PET, hybrid PET, and magnetic resonance imaging. Foot Ankle Int. 2004;25:890–5.

    Article  PubMed  Google Scholar 

  86. Frykberg RG, Eneroth M. Principles of conservative management. In: Frykberg RG, editor. The diabetic Charcot foot: principles and management. Brooklandville: Data Trace Publishing Company; 2010. p. 93–116.

    Google Scholar 

  87. Jostel A, Jude EB. Medical treatment of Charcot neuroosteoarthropathy. Clin Podiatr Med Surg. 2008;25:63–9. vi–vii.

    Article  PubMed  Google Scholar 

  88. Armstrong DG, Todd WF, Lavery LA, Harkless LB, Bushman TR. The natural history of acute Charcot’s arthropathy in a diabetic foot specialty clinic. Diabet Med. 1997;14:357–63.

    Article  CAS  PubMed  Google Scholar 

  89. Giurini JM, Chrzan JS, Gibbons GW, Habershaw GM. Charcot’s disease in diabetic patients. Correct diagnosis can prevent progressive deformity. Postgrad Med. 1991;89:163–9.

    Article  CAS  PubMed  Google Scholar 

  90. Chantelau E. The perils of procrastination: effects of early vs. delayed detection and treatment of incipient Charcot fracture. Diabet Med. 2005;22:1707–12.

    Article  CAS  PubMed  Google Scholar 

  91. Eichenholtz SN. Charcot joints. Springfield: Charles C Thomas; 1966.

    Google Scholar 

  92. Parhouse N, Le Quesne PM. Impaired neurogenic vascular response in patients with diabetic and neurogenic foot lesions. N Engl J Med. 1989;39:346–50.

    Google Scholar 

  93. Mittlmeier T, Klaue K, Haar P, Beck M. Should one consider primary surgical reconstruction in charcot arthropathy of the feet? Clin Orthop Relat Res. 2010;468:1002–11.

    Article  PubMed  Google Scholar 

  94. Pinzur MS. Surgical management: history and general principles. In: Frykberg RG, editor. The diabetic Charcot foot: principles and management. Brooklandville: Data Trace Publishing Company; 2010. p. 165–88.

    Google Scholar 

  95. Johnson AR, Yoon P. Limb salvage in an unstable ankle fracture of a diabetic patient with Charcot arthropathy. Foot Ankle Spec. 2010;3:184–9.

    Article  PubMed  Google Scholar 

  96. Sohn MW, Stuck RM, Pinzur M, Lee TA, Budiman-Mak E. Lower-extremity amputation risk after charcot arthropathy and diabetic foot ulcer. Diabetes Care. 2010;33:98–100.

    Article  PubMed  Google Scholar 

  97. Iversen MM, Tell GS, Riise T, Hanestad BR, Østbye T, Graue M, Midthjell K. History of foot ulcer increases mortality among individuals with diabetes: ten-year follow-up of the Nord-Trøndelag Health Study, Norway. Diabetes Care. 2009;32:2193–9.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Gazis A, Pound N, Macfarlane R, Treece K, Game F, Jeffcoate W. Mortality in patients with diabetic neuropathic osteoarthropathy (Charcot foot). Diabet Med. 2004;21:1243–6.

    Article  CAS  PubMed  Google Scholar 

  99. Sohn MW, Lee TA, Stuck RM, Frykberg RG, Budiman-Mak E. Mortality risk of Charcot arthropathy compared with that of diabetic foot ulcer and diabetes alone. Diabetes Care. 2009;32:816–21.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Pecoraro E, Reiber E, Burges M. Pathways to diabetic limb amputation. Diabetes Care. 1990;3:513–5.

    Article  Google Scholar 

  101. LoGerfo FW, Gibbons GW, Pomposelli Jr FB, Campbell DR, Miller A, Freeman DV, Quist WC. Trends in the care of the diabetic foot. Expanded role of arterial reconstruction. Arch Surg. 1992;127:617–20.

    Article  CAS  PubMed  Google Scholar 

  102. Pomposelli FB, Campbell DR. Vascular surgery for the diabetic foot. In: Veves A, Giurini JM, LoGerfo FW, editors. The diabetic foot. Humana Press; 2002. p. 411–28. Totowa, NJ.

    Google Scholar 

  103. Hirsch AT, Criqui MH, Treat-Jacobson D, Regensteiner JG, Creager MA, Olin JW, Krook SH, Hunninghake DB, Comerota AJ, Walsh ME, McDermott MM, Hiatt WR. Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA. 2001;19:1317–24.

    Article  Google Scholar 

  104. American Diabetes Association. Peripheral arterial disease in people with diabetes. Diabetes Care. 2003;26:333–41.

    Article  Google Scholar 

  105. Kannel WB, McGee DL. Update on some epidemiologic features of intermittent claudication: the Framingham Study. J Am Geriatr Soc. 1985;33:13–8.

    Article  CAS  PubMed  Google Scholar 

  106. Abbot RD, Brand FN, Kannel WB. Epidemiology of some peripheral arterial findings in diabetic man and women: experiences from the Framingham Study. Am J Med. 1990;88:376–81.

    Article  Google Scholar 

  107. Ostchega Y, Paulose-Ram R, Dillon CF, Gu Q, Hughes JP. Prevalence of peripheral arterial disease and risk factors in persons aged 60 and older: data from the National Health and Nutrition Examination Survey 1999–2004. J Am Geriatr Soc. 2007;55:583–9.

    Article  PubMed  Google Scholar 

  108. Walters DP, Gatling W, Mullee MA, Hill RD. The prevalence, detection, and epidemiological correlates of peripheral vascular disease: a comparison of diabetic and non-diabetic subjects in a English community. Diabetic Med. 1992;9:710–5.

    Article  CAS  PubMed  Google Scholar 

  109. Donahue RP, Orchard TJ. Diabetes mellitus and macrovascular complications. An epidemiological perspective. Diabetes Care. 1992;15:1141–55.

    Article  CAS  PubMed  Google Scholar 

  110. Hiatt RH, Hoag S, Hamman RF. Effect of diagnostic criteria on the prevalence of peripheral arterial disease. The San Luis Valley Diabetes Study. Circulation. 1995;91:1472–9.

    Article  CAS  PubMed  Google Scholar 

  111. Jude EB, Eleftheriadou I, Tentolouris N. Peripheral arterial disease in diabetes-a review. Diabet Med. 2010;27:4–14.

    Article  CAS  PubMed  Google Scholar 

  112. Elhadd TA, Robb R, Jung RT, Stonebridge PA, Belch JJF. Pilot study of prevalence of asymptomatic peripheral arterial occlusive disease in patients with diabetes attending a hospital clinic. Practical Diabetes Int. 1999;16:163–6.

    Article  Google Scholar 

  113. Faglia E, Caravaggi C, Marchetti R, Mingardi R, Morabito A, Piaggesi A, Uccioli L, Ceriello A, SCAR (SCreening for ARteriopathy) Study Group. Screening for peripheral arterial disease by means of the ankle-brachial index in newly diagnosed Type 2 diabetic patients. Diabet Med. 2005;22:1310–4.

    Article  CAS  PubMed  Google Scholar 

  114. Walters DP, Gatling W, Mullee MA, Hill RD. The distribution and severity of diabetic foot disease: a community study with comparison to a non-diabetic group. Diabet Med. 1992;9:354–8.

    Article  CAS  PubMed  Google Scholar 

  115. Kallio M, Forsblom C, Groop PH, Groop L, Lepantalo M. Development of new peripheral arterial occlusive disease in patients with type 2 diabetes during a mean follow-up of 11 years. Diabetes Care. 2003;26:1241–5.

    Article  PubMed  Google Scholar 

  116. Criqui MH, Ninomiya JK, Wingard DL, Ji M, Fronek A. Progression of peripheral arterial disease predicts cardiovascular disease morbidity and mortality. J Am Coll Cardiol. 2008;18:1736–42.

    Article  Google Scholar 

  117. McDermott MM, Kerwin DR, Liu K, Martin GJ, O’Brien E, Kaplan H, Greenland P. Prevalence and significance of unrecognized lower extremity peripheral arterial disease in general medicine practice. J Gen Intern Med. 2001;16:384–90.

    Article  CAS  PubMed  Google Scholar 

  118. Khan NA, Rahim SA, Anand SS, Simel DL, Panju A. Does the clinical examination predict lower extremity peripheral arterial disease? JAMA. 2006;295:536–46.

    Article  CAS  PubMed  Google Scholar 

  119. Mayfield JA, Reiber GE, Sanders LJ, Janisse D, Pogach M. Preventive foot care in people with diabetes. Diabetes Care. 1998;21:2161–77.

    Article  CAS  PubMed  Google Scholar 

  120. Brearley S, Shearman CP, Simms MH. Peripheral pulse palpation: an unreliable physical sign. Ann R Coll Surg Engl. 1992;74:169–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Caruana MF, Bradbury AW, Adam DJ. The validity, reliability, reproducibilily and extended utility of ankle to brachial pressure index in current vascular surgical practice. Eur J Vasc Endovasc Surg. 2005;29:443–51.

    Article  CAS  PubMed  Google Scholar 

  122. Everhart JE, Pettitt DJ, Knowler WC, Rose FA, Bennett PH. Medial arterial calcification and its association with mortality and complications of diabetes. Diabetologia. 1988;31:16–23.

    CAS  PubMed  Google Scholar 

  123. Young MJ, Adams JE, Anderson GF, Boulton AJ, Cavanagh PR. Medial arterial calcification in the feet of diabetic patients and matched non-diabetic control subjects. Diabetologia. 1993;36:615–21.

    Article  CAS  PubMed  Google Scholar 

  124. Jeffcoate WJ, Rasmussen LM, Hofbauer LC, Game FL. Medial arterial calcification in diabetes and its relationship to neuropathy. Diabetologia. 2009;52:2478–88.

    Article  CAS  PubMed  Google Scholar 

  125. Faglia E, Clerici G, Clerissi J, Gabrielli L, Losa S, Mantero M, et al. Early and five- year amputation and survival rate of diabetic patients with critical limb ischemia: data of a cohort study of 564 patients. Eur J Vasc Endovasc Surg. 2006;32:484–90.

    Article  CAS  PubMed  Google Scholar 

  126. Aerden D, Massaad D, von Kemp K, van Tussenbroek F, Debing E, Keymeulen B, Van den Brande P. The ankle-brachial index and the diabetic foot: a troublesome marriage. Ann Vasc Surg. 2011;25:770–7.

    Article  PubMed  Google Scholar 

  127. Resnick HE, Lindsay RS, McDermott MM, Devereux RB, Jones KL, Fabsitz RR, Howard BV. Relationship of high and low ankle brachial index to all-cause and cardiovascular disease mortality: the Strong Heart Study. Circulation. 2004;109:733–9.

    Article  PubMed  Google Scholar 

  128. Wagner FW. The dysvascular foot: a system for diagnosis and treatment. Foot Ankle. 1981;2:64–122.

    Article  PubMed  Google Scholar 

  129. Armstrong DG, Lavery LA, Harkless LB. Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care. 1998;21:855–9.

    Article  CAS  PubMed  Google Scholar 

  130. Peters EJ, Lavery LA, International Working Group on the Diabetic Foot. Effectiveness of the diabetic foot risk classification system of the International Working Group on the Diabetic Foot. Diabetes Care. 2001;24:1442–7.

    Article  CAS  PubMed  Google Scholar 

  131. Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FGR on behalf of the TASC II Working Group. Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II). Eur J Vasc Endovasc Surg. 2007;33(Suppl):S73–108.

    Google Scholar 

  132. Ramaswami G, Al-Kutoubi A, Nicolaides AN, Dhanjil S, Griffin M, Belcaro G, et al. The role of duplex scanning in the diagnosis of lower limb arterial disease. Ann Vasc Surg. 1999;13:494–500.

    Article  CAS  PubMed  Google Scholar 

  133. Bradbury AW, Adam DJ. Diagnosis of peripheral arterial disease of the lower limb. BMJ. 2007;334:1229–30.

    Article  PubMed  PubMed Central  Google Scholar 

  134. Collins R, Cranny G, Burch J, Aguiar-Ibáñez R, Craig D, Wright K, Berry E, Gough M, Kleijnen J, Westwood M. A systematic review of duplex ultrasound, magnetic resonance angiography and computed tomography angiography for the diagnosis and assessment of symptomatic, lower limb peripheral arterial disease. Health Technol Assess. 2007;11:1–184.

    Google Scholar 

  135. Heijenbrok-Kal MH, Kock MC, Hunink MG. Lower extremity arterial disease: multidetector CT angiography meta-analysis. Radiology. 2007;245(2):433–9. Epub 2007 Sep 11.

    Article  PubMed  Google Scholar 

  136. Kreitner KF, Kalden P, Neufang A, Düber C, Krummenauer F, Küstner E, Laub G, Thelen M. Diabetes and peripheral arterial occlusive disease: prospective comparison of contrast-enhanced three-dimensional MR angiography with conventional digital subtraction angiography. AJR Am J Roentgenol. 2000;174:171–9.

    Article  CAS  PubMed  Google Scholar 

  137. Meyer BC, Werncke T, Foert E, Kruschewski M, Hopfenmüller W, Ribbe C, Wolf KJ, Albrecht T. Do the cardiovascular risk profile and the degree of arterial wall calcification influence the performance of MDCT angiography of lower extremity arteries? Eur Radiol. 2010;20:497–505.

    Article  CAS  PubMed  Google Scholar 

  138. Parfrey PS, Griffiths SM, Barrett BJ, Paul MD, Genge M, Withers J, Farid N, McManamon PJ. Contrast material-induced renal failure in patients with diabetes mellitus, renal insufficiency, or both. N Engl J Med. 1989;320:143–9.

    Article  CAS  PubMed  Google Scholar 

  139. Amini M, Salarifar M, Amirbaigloo A, Masoudkabir F, Esfahani F. N-acetylcysteine does not prevent contrast-induced nephropathy after cardiac catheterization in patients with diabetes mellitus and chronic kidney disease: a randomized clinical trial. Trials. 2009;29:10–45.

    Google Scholar 

  140. Sterner G, Nyman U, Valdes T. Low risk of contrast-medium-induced nephropathy with modern angiography techniques. J Intern Med. 2001;250:429–34.

    Article  CAS  PubMed  Google Scholar 

  141. Zaytseva NV, Shamkhalova MS, Shestakova MV, Matskeplishvili ST, Tugeeva EF, Buziashvili UI, Deev AD, Dedov II. Contrast-induced nephropathy in patients with type 2 diabetes during coronary angiography: risk-factors and prognostic value. Diabetes Res Clin Pract. 2009;86 Suppl 1:S63–9.

    Article  PubMed  Google Scholar 

  142. Pannu N, Wiebe N, Tonelli M, Alberta Kidney Disease Network. Prophylaxis strategies for contrast-induced nephropathy. JAMA. 2006;21(295):2765–79.

    Article  Google Scholar 

  143. Holt S. Radiocontrast media-induced renal injury–saline is effective in prevention. Nephron Clin Pract. 2003;93:C5–6.

    Article  PubMed  Google Scholar 

  144. Eickhoff JH. Changes in the number of lower limb amputations during a period of increasing vascular surgery activity. Results of a nation-wide study, Denmark, 1977–1990. Eur J Surg. 1993;159:469–73.

    CAS  PubMed  Google Scholar 

  145. Muhs BE, Gagne P, Sheehan P. Peripheral arterial disease: clinical assessment and indications for revascularization in the patient with diabetes. Curr Diab Rep. 2005;5:24–9.

    Article  PubMed  Google Scholar 

  146. Hallett Jr JW, Byrne J, Gayari MM, Il Strup DM, Jacobsen SJ, Gray DT. Impact of arterial surgery and balloon angioplasty on amputation: a population-based study of 1155 procedures between 1973 and 1992. J Vasc Surg. 1997;25:29–38.

    Article  PubMed  Google Scholar 

  147. Abou-Zamzam Jr AM, Gomez NR, Molkara A, Banta JE, Teruya TH, Killeen JD, et al. A prospective analysis of critical limb ischemia: factors leading to major primary amputation versus revascularization. Ann Vasc Surg. 2007;21:458–63.

    Article  PubMed  Google Scholar 

  148. Wunderlich RP, Peters EJ, Lavery LA. Systemic hyperbaric oxygen therapy: lower-extremity wound healing and the diabetic foot. Diabetes Care. 2000;23:1551–5.

    Article  CAS  PubMed  Google Scholar 

  149. Löndahl M, Katzman P, Nilsson A, Hammarlund C. Hyperbaric oxygen therapy facilitates healing of chronic foot ulcers in patients with diabetes. Diabetes Care. 2010;33:998–1003.

    Article  PubMed  PubMed Central  Google Scholar 

  150. The ICAI. Study Group Prostanoids for chronic critical leg ischemia. A randomized, controlled, open-label trial with prostaglandin E1. Ischemia Cronica degli Arti Inferiori. Ann Intern Med. 1999;130:412–21.

    Article  Google Scholar 

  151. Petrakis IE, Sciacca V. Epidural spinal cord electrical stimulation in diabetic critical lower limb ischemia. J Diabetes Complications. 1999;13:293–9.

    Article  CAS  PubMed  Google Scholar 

  152. Ouriel K. Peripheral arterial disease. Lancet. 2001;358:1257–64.

    Article  CAS  PubMed  Google Scholar 

  153. Adam DJ, Raptis S, Fitridge RA. Trends in the presentation and surgical management of the acute diabetic foot. Eur J Vasc Endovasc Surg. 2006;31:151–6.

    Article  CAS  PubMed  Google Scholar 

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Clerici, G., Faglia, E. (2016). Diabetic Foot Ulcers. In: Khanna, A., Tiwary, S. (eds) Ulcers of the Lower Extremity. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2635-2_12

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