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Neuropathic osteoarthropathy with and without superimposed osteomyelitis in patients with a diabetic foot

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Abstract

Soft tissue and bone infection involving the foot is one of the most common long-term complications of diabetes mellitus, implying a serious impairment in quality of life for patients in the advanced stages of the disease. Neuropathic osteoarthropathy often coexists and differentiating between these two entities is commonly challenging, but crucial, as the management may differ substantially. The importance of correct diagnosis cannot be understated and effective management requires a multidisciplinary approach owing to the complicated nature of therapy in such patients. A missed diagnosis has a high likelihood of major morbidity for the patient, including limb amputation, and over-diagnosis results in a great socioeconomic challenge for healthcare systems, the over-utilization of healthcare resources, and the unwise use of antibiotics. Diagnosis is largely based on clinical signs supplemented by various imaging modalities such as radiography, MR imaging, and hybrid imaging techniques such as F-18 fluorodeoxyglucose-positron emission tomography. In the interests of the management of diabetic foot complications, this review article is aimed on the one hand at providing radiologists with important clinical knowledge, and on the other hand to equip clinicians with relevant radiological semiotics.

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References

  1. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014;103(2):137–49.

    Article  CAS  PubMed  Google Scholar 

  2. Ahmadi ME, Morrison WB, Carrino JA, Schweitzer ME, Raikin SM, Ledermann HP. Neuropathic arthropathy of the foot with and without superimposed osteomyelitis: MR imaging characteristics. Radiology. 2006;238(2):622–31.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Lipsky BA, Berendt AR, Deery HG, et al. Diagnosis and treatment of diabetic foot infections. Clin Infect Dis. 2004;39(7):885–910.

    Article  PubMed  Google Scholar 

  5. Donovan A, Schweitzer ME. Use of MR imaging in diagnosing diabetes-related pedal osteomyelitis. Radiographics. 2010;30(3):723–36.

    Article  PubMed  Google Scholar 

  6. Tan PL, The J. MRI of the diabetic foot: differentiation of infection from neuropathic change. Br J Radiol. 2007;80:939–48.

    Article  CAS  PubMed  Google Scholar 

  7. Jeffcoate WJ. Theories concerning the pathogenesis of the acute Charcot foot suggest future therapy. Curr Diab Rep. 2005;5(6):430–5.

    Article  PubMed  Google Scholar 

  8. Charcot JM. Sur quelques arthropathies qui paraissent dépendre d’une lesion du cerveau ou de la moëlle épinière. Arch Physiol Norm Pathol. 1868;1:161–78.

  9. Jones EA, Manaster BJ, May DA, Disler DG. Neuropathic osteoarthropathy: diagnostic dilemmas and differential diagnosis. Radiographics. 2000;20:279–93.

    Article  Google Scholar 

  10. Sella EJ, Barrette C. Staging of Charcot neuroarthropathy along the medial column of the foot in the diabetic patient. J Foot Ankle Surg. 1999;38:34–40.

    Article  CAS  PubMed  Google Scholar 

  11. Schwarz GS, Berenyi MR, Siegel MW. Atrophic arthropathy and diabetic neuritis. AJR Am J Roentgenol. 1969;106:523–9.

    Article  CAS  Google Scholar 

  12. Jeffcoate WJ. Abnormalities of vasomotor regulation in the pathogenesis of the acute Charcot foot of diabetes mellitus. Int J Low Extrem Wounds. 2005;4:133–7.

    Article  PubMed  Google Scholar 

  13. Trepman E, Nihal A, Pinzur MS. Current topics review: Charcot neuroarthropathy of the foot and ankle. Foot Ankle Int. 2005;26:46–63.

    PubMed  Google Scholar 

  14. Jeffcoate W. The causes of the Charcot syndrome. Clin Podiatr Med Surg. 2008;25:29–42.

    Article  PubMed  Google Scholar 

  15. Petrova NL, Petrov PK, Edmonds ME, Shanahan CM. Inhibition of TNF-α reverses the pathological resorption pit profile of osteoclasts from patients with acute Charcot osteoarthropathy. J Diabetes Res. 2015;2015:917945.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jirkovská A, Kasalický P, Bouček P, Hosová J, Skibová J. Calcaneal ultrasonometry in patients with Charcot osteoarthropathy and its relationship with densitometry in the lumbar spine and femoral neck and with markers of bone turnover. Diabet Med. 2001;18(6):495–500.

    Article  PubMed  Google Scholar 

  17. Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet. 2005;366(9502):2058–61.

    Article  CAS  PubMed  Google Scholar 

  18. Rogers LC, Frykberg RG, Armstrong DG, et al. The Charcot foot in diabetes. Diabetes Care. 2011;34(9):2123–9.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Uccioli L, Sinistro A, Almerighi C, et al. Proinflammatory modulation of the surface and cytokine phenotype of monocytes in patients with acute Charcot foot. Diabetes Care. 2010;33:350–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Eichenholtz SN. Charcot joints. Springfield, IL: Thomas CC; 1966. p. 7–8.

    Google Scholar 

  21. Shibata T, Tada K, Hashizume C. The results of arthrodesis of the ankle for leprotic neuroarthropathy. J Bone Joint Surg. 1990;72:749–56.

    CAS  PubMed  Google Scholar 

  22. Chantelau EA, Grützner G. Is the Eichenholtz classification still valid for the diabetic Charcot foot? Swiss Med Wkly. 2014;144:w13948.

    PubMed  Google Scholar 

  23. Sanders LJ, Frykberg RG. Diabetic neuropathic osteoarthropathy: the Charcot foot. In: Frykberg RG, editor. The high risk foot in diabetes mellitus. New York: Churchill Livingstone; 1991. p. 297–338.

    Google Scholar 

  24. Brodsky JW. Evaluation of the diabetic foot. Instr Course Lect. 1999;48:289–303.

    CAS  PubMed  Google Scholar 

  25. Rajbhandari SM, Jenkins RC, Davies C, Tesfaye S. Charcot neuroarthropathy in diabetes mellitus. Diabetologia. 2002;45:1085–96.

    Article  CAS  PubMed  Google Scholar 

  26. Rogers LC, Bevilacqua NJ. The diagnosis of Charcot foot. Clin Podiatr Med Surg. 2008;25(1):43–51.

    Article  PubMed  Google Scholar 

  27. Jeffcoate W, Lima J, Nobrega L. The Charcot foot. Diabet Med. 2000;17:253–8.

    Article  CAS  PubMed  Google Scholar 

  28. Wukich DK, Sung W. Charcot arthropathy of the foot and ankle: modern concepts and management review. J Diabetes Complicat. 2009;23:409–26.

    Article  PubMed  Google Scholar 

  29. Cofield RH, Morrison MJ, Beabout JW. Diabetic neuroarthropathy in the foot: patient characteristics and patterns of radiographic change. Foot Ankle. 1983;4:15–22.

    Article  CAS  PubMed  Google Scholar 

  30. Petrova NL, Foster AV, Edmonds ME. Difference in presentation of Charcot osteoarthropathy in type 1 compared with type 2 diabetes. Diabetes Care. 2004;27(5):1235–6.

    Article  PubMed  Google Scholar 

  31. Rathur HM, Boulton AJ. The diabetic foot. Clin Dermatol. 2007;25:109–20.

    Article  PubMed  Google Scholar 

  32. Johnson JTH. Neuropathic fractures and joint injuries. Pathogenesis and rationale for prevention and treatment. J Bone Joint Surg Am. 1967;49-A:1–30.

    Google Scholar 

  33. Sommer TC, Lee TH. Charcot foot: the diagnostic dilemma. Am Fam Physician. 2001;64(9):1591–8.

    CAS  PubMed  Google Scholar 

  34. Mendelson EB, Fisher MR, Deschler TW, et al. Osteomyelitis in the diabetic foot: a difficult diagnostic challenge. Radiographics. 1983;3:248–61.

    Article  Google Scholar 

  35. Nguyen VD, Keh RA, Daehler RW. Freiberg's disease in diabetes mellitus. Skeletal Radiol. 1991;20:425–8.

    Article  CAS  PubMed  Google Scholar 

  36. Kathol MH, el-Khoury GY, Moore TE, et al. Calcaneal insufficiency avulsion fractures in patients with diabetes mellitus. Radiology. 1991;180:725–9.

    Article  CAS  PubMed  Google Scholar 

  37. Boulton AJM. The pathway to foot ulceration in diabetes. In: Boulton AJM, editor. The diabetic foot. Philadelphia: Elsevier; 2013. p. 775–90.

    Google Scholar 

  38. Ctercteko GC, Dhanendran M, Hutton WC, Le Quesne LP. Vertical forces acting on the feet of diabetic patients with neuropathic ulceration. Br J Surg. 1981;68(9):608–14.

    Article  CAS  PubMed  Google Scholar 

  39. 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  PubMed Central  Google Scholar 

  40. Chantelau E, Poll LW. Evaluation of the diabetic Charcot foot by MR imaging or plain radiography—an observational study. Exp Clin Endocrinol Diabetes. 2006;114:428–31.

    Article  CAS  PubMed  Google Scholar 

  41. Yablon CM, Duggal N, Wu JS, Shetty SK, Dawson F, Hochman MG. A review of Charcot neuroarthropathy of the midfoot and hindfoot: what every radiologist needs to know. Curr Probl Diagn Radiol. 2010;39(5):187–99.

    Article  PubMed  Google Scholar 

  42. Wukich DK, Raspovic KM, Hobizal KB, Rosario B. Radiographic analysis of diabetic midfoot Charcot neuroarthropathy with and without midfoot ulceration. Foot Ankle Int. 2014;35(11):1108–15.

    Article  PubMed  Google Scholar 

  43. Schon LC, Easley ME, Cohen I, et al. The acquired midtarsus deformity classification system–interobserver reliability and intraobserver reproducibility. Foot Ankle Int. 2002;23:30–6.

    Article  PubMed  Google Scholar 

  44. Schon LC, Weinfeld SB, Horton GA, Resch S. Radiographic and clinical classification of acquired midtarsus deformities. Foot Ankle Int. 1998;19:394–404.

    Article  CAS  PubMed  Google Scholar 

  45. Sinacore DR, Gutekunst DJ, Hastings MK, et al. Neuropathic midfoot deformity: associations with ankle and subtalar joint motion. J Foot Ankle Res. 2013;6:11.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bevan WP, Tomlinson MP. Radiographic measures as a predictor of ulcer formation in diabetic Charcot midfoot. Foot Ankle Int. 2008;29:568–73.

    Article  PubMed  Google Scholar 

  47. Hastings MK, Johnson JE, Strube MJ, et al. Progression of foot deformity in Charcot neuropathic osteoarthropathy. J Bone Joint Surg Am. 2013;95:1206–13.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Loredo R, Rahal A, Garcia G, Metter D. Imaging of the diabetic foot diagnostic dilemmas. Foot Ankle Spec. 2010;3:249–64.

    Article  PubMed  Google Scholar 

  49. Ergen FB, Sanverdi SE, Oznur A. Charcot foot in diabetes and an update on imaging. Diabet Foot Ankle. 2013;4:21884.

    Article  Google Scholar 

  50. Morrison WB, Ledermann HP. Work-up of the diabetic foot. Radiol Clin N Am. 2002;40:1171–92.

    Article  PubMed  Google Scholar 

  51. Roug IK, Pierre-Jerome C. MRI spectrum of bone changes in the diabetic foot. Eur J Radiol. 2012;81(7):1625–9.

    Article  PubMed  Google Scholar 

  52. 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 

  53. Frykberg RG. Mendeszoon E. Management of the diabetic Charcot foot. Diabetes Metab Res Rev. 2000;16 Suppl 1:S59–65.

    Article  PubMed  Google Scholar 

  54. McGill M, Molyneaux L, Bolton T, Ioannou K, Uren R, Yue DK. Response of Charcot’s arthropathy to contact casting: assessment by quantitative techniques. Diabetologia. 2000;43:481–4.

    Article  CAS  PubMed  Google Scholar 

  55. Gouveri E, Papanas N. Charcot osteoarthropathy in diabetes: a brief review with an emphasis on clinical practice. World J Diabetes. 2011;2:59–65.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Van Der Ven A, Chapman CB, Bowker JH. Charcot neuroarthropathy of the foot and ankle. J Am Acad Orthop Surg. 2009;17:562–71.

    Article  PubMed  Google Scholar 

  57. De Souza LJ. Charcot neuroarthropathy and immobilization in a weight-bearing total contact cast. J Bone Joint Surg Am. 2008;90:754–9.

    Article  PubMed  Google Scholar 

  58. Mueller MJ, Diamond JE, Sinacore DR, et al. Total contact casting in treatment of diabetic plantar ulcers: controlled clinical trial. Diabetes Care. 1989;12:384–8.

    Article  CAS  PubMed  Google Scholar 

  59. Caravaggi C, Faglia E, De Giglio R, et al. 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 

  60. 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 

  61. Madan SS, Pai DR. Charcot neuroarthropathy of the foot and ankle. Orthop Surg. 2013;5(2):86–93.

    Article  PubMed  Google Scholar 

  62. Pinzur MS, Lio T, Posner M. Treatment of Eichenholtz stage I Charcot foot arthropathy with a weight-bearing total contact cast. Foot Ankle Int. 2006;27:324–9.

    PubMed  Google Scholar 

  63. Sinacore DR. Acute Charcot arthropathy in patients with diabetes mellitus: healing times by foot location. J Diabetes Complicat. 1998;12:287–93.

    Article  CAS  PubMed  Google Scholar 

  64. Nabuurs-Franssen MH, Sleegers R, Huijberts MS, et al. Total contact casting of the diabetic foot in daily practice: a prospective follow-up study. Diabetes Care. 2005;28(2):243–7.

    Article  PubMed  Google Scholar 

  65. Raymakers JTFJ, Houben AJ, Van der Heyden JJ, Tordoir JHM, Kitslaar PJEHM, Schaper NC. The effect of diabetes and severe ischemia on the penetration of ceftazidime into tissues of the limb. Diabet Med. 2001;18:229–34.

    Article  CAS  PubMed  Google Scholar 

  66. Wu SC, Jensen JL, Weber AK, Robinson DE, Armstrong DG. Use of pressure offloading devices in diabetic foot ulcers. Do we practice what we preach? Diabetes Care. 2008;31(11):2118–9.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Mehta JA, Brown C, Sargeant N Charcot restraint orthotic walker. Foot Ankle Int. 1998;19:619–23.

    Article  CAS  PubMed  Google Scholar 

  68. Guse ST, Alvine FG. Treatment of diabetic foot ulcers and Charcot neuroarthropathy using the patellar tendon-bearing brace. Foot Ankle Int. 1997;18:675–7.

    Article  CAS  PubMed  Google Scholar 

  69. Boninger ML, Leonard Jr JA. Use of bivalved ankle- foot orthosis in neuropathic foot and ankle lesions. J Rehabil Res Dev. 1996;33:16–22.

    CAS  PubMed  Google Scholar 

  70. Jude EB, Selby PL, Burgess J, et al. Bisphosphonates in the treatment of Charcot neuroarthropathy: a double-blind randomised controlled trial. Diabetologia. 2001;44:2032–7.

    Article  CAS  PubMed  Google Scholar 

  71. Bem R, Jirkovská A, Fejfarová V, Skibová J, Jude EB. Intranasal calcitonin in the treatment of acute Charcot neuroosteoarthropathy: a randomized controlled trial. Diabetes Care. 2006;29:1392–4.

    Article  CAS  PubMed  Google Scholar 

  72. Rogers MJ, Gordon S, Benford HL, et al. Cellular and molecular mechanisms of action of bisphosphonates. Cancer. 2000;88(12 Suppl):2961–78.

    Article  CAS  PubMed  Google Scholar 

  73. Boulton AJ, Jeffcoate WJ, Jones TL, Ulbrecht JS. International collaborative research on Charcot’s disease. Lancet. 2009;373:105–6.

    Article  PubMed  Google Scholar 

  74. Pinzur M. Surgical versus accommodative treatment for Charcot arthropathy of the midfoot. Foot Ankle Int. 2004;25:545–9.

    Article  PubMed  Google Scholar 

  75. Simon SR, Tejwani SG, Wilson DL, Santner TJ, Denniston NL. Arthrodesis as an early alternative to nonoperative management of Charcot arthropathy of the diabetic foot. J Bone Joint Surg Am. 2000;82-A:939–50.

    CAS  PubMed  Google Scholar 

  76. 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  PubMed Central  Google Scholar 

  77. Roukis TS, Stapleton JJ, Zgonis T. Addressing psychosocial aspects of care for patients with diabetes undergoing limb salvage surgery. Clin Podiatr Med Surg. 2007;24(3):601–10.

    Article  PubMed  Google Scholar 

  78. Stapleton JJ, Zgonis T. Surgical reconstruction of the diabetic Charcot foot: internal, external or combined fixation? Clin Podiatr Med Surg. 2012;29(3):425–33.

    Article  PubMed  Google Scholar 

  79. Laurinaviciene R, Kirketerp-Moeller K, Holstein PE. Exostectomy for chronic midfoot plantar ulcer in Charcot deformity. J Wound Care. 2008;17:53–9.

    Article  CAS  PubMed  Google Scholar 

  80. Zarutsky E, Rush SM, Schuberth JM. The use of circular wire external fixation in the treatment of salvage ankle arthrodesis. J Foot Ankle Surg. 2005;44:22–31.

    Article  PubMed  Google Scholar 

  81. Burns PR, Wukich DK. Surgical reconstruction of the Charcot rear foot and ankle. Clin Podiatr Med Surg. 2008;25:95–120.

    Article  PubMed  Google Scholar 

  82. Mueller MJ, Sinacore DR, Hastings MK, Strube MJ, Johnson JE. Impact of Achilles tendon lengthening on functional limitations and perceived disability in people with a neuropathic plantar ulcer. Diabetes Care. 2004;27:1559–64.

    Article  PubMed  Google Scholar 

  83. Ertugrul BM, Savk O, Ozturk B, Cobanoglu M, Oncu S, Sakarya S. The diagnosis of diabetic foot osteomyelitis: examination findings and laboratory values. Med Sci Monit. 2009;15:CR307–312.

    PubMed  Google Scholar 

  84. Newman LG, Waller J, Palestro CJ, et al. Unsuspected osteomyelitis in diabetic foot ulcers. Diagnosis and monitoring by leukocyte scanning with indium in 111 oxyquinoline. JAMA. 1991;266:1246–51.

    Article  CAS  PubMed  Google Scholar 

  85. Butalia S, Palda VA, Sargeant RJ, Detsky AS, Mourad O. Does this patient with diabetes have osteomyelitis of the lower extremity? JAMA. 2008;299(7):806–13.

    Article  CAS  PubMed  Google Scholar 

  86. Grayson ML, Gibbons GW, Balogh K, Levin E, Karchmer AW. Probing to bone in infected pedal ulcers. A clinical sign of underlying osteomyelitis in diabetic patients. JAMA. 1995;273:721–3.

    Article  CAS  PubMed  Google Scholar 

  87. Aragon-Sanchez J, Lipsky BA, Lazaro-Martinez JL. Diagnosing diabetic foot osteomyelitis: is the combination of probe-to-bone test and plain radiography sufficient for high-risk inpatients? Diabet Med. 2011;28:191–4.

    Article  CAS  PubMed  Google Scholar 

  88. Lavery LA, Armstrong DG, Peters EJ, Lipsky BA. Probe-to bone test for diagnosing diabetic foot osteomyelitis: reliable or relic? Diabetes Care. 2007;30:270–4.

    Article  PubMed  Google Scholar 

  89. Morales Lozano R, Gonzalez Fernandez ML, Martinez Hernandez D, Beneit Montesinos JV, Guisado Jimenez S, Gonzalez Jurado MA. Validating the probe-to-bone test and other tests for diagnosing chronic osteomyelitis in the diabetic foot. Diabetes Care. 2010;33:2140–5.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Vartanians VM, Karchmer AW, Giurini JM, Rosenthal DI. Is there a role for imaging in the management of patients with diabetic foot? Skeletal Radiol. 2009;38(7):633–6.

    Article  PubMed  Google Scholar 

  91. Ledermann HP, Schweitzer ME, Morrison WB. Nonenhancing tissue on MR imaging of pedal infection: characterization of necrotic tissue and associated limitations for diagnosis of osteomyelitis and abscess. AJR Am J Roentgenol. 2002;178(1):215–22.

    Article  PubMed  Google Scholar 

  92. Callegari L, Leonardi A, Bini A, et al. Ultrasound-guided removal of foreign bodies: personal experience. Eur Radiol. 2009;19:1273–9.

    Article  PubMed  Google Scholar 

  93. Schweitzer ME, Daffner RH, Weissman BN, et al. ACR appropriateness criteria on suspected osteomyelitis in patients with diabetes mellitus. J Am Coll Radiol. 2008;5:881–6.

    Article  PubMed  Google Scholar 

  94. Klauser AS, Tagliafico A, Allen GM, et al. Clinical indications for musculoskeletal ultrasound: a Delphi-based consensus paper of the European Society of Musculoskeletal Radiology. Eur Radiol. 2012;22:1140–8.

    Article  PubMed  Google Scholar 

  95. 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(2):125–32.

    Article  PubMed  Google Scholar 

  96. Morrison WB, Schweitzer ME, Batte WG, Radack DP, Russel KM. Osteomyelitis of the foot: relative importance of primary and secondary MR imaging signs. Radiology. 1998;207(3):625–32.

    Article  CAS  PubMed  Google Scholar 

  97. Karchevsky M, Schweitzer ME, Morrison WB, et al. MRI findings of septic arthritis and associated osteomyelitis in adults. AJR Am J Roentgenol. 2004;182:119–22.

    Article  PubMed  Google Scholar 

  98. Graif M, Schweitzer ME, Deely D, et al. The septic versus nonseptic inflamed joint: MRI characteristics. Skeletal Radiol. 1999;28:616–20.

    Article  CAS  PubMed  Google Scholar 

  99. Bancroft LW. MR imaging of infectious processes of the knee. Radiol Clin N Am. 2007;45:931–41.

    Article  PubMed  Google Scholar 

  100. 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(3):257–68.

    Article  PubMed  Google Scholar 

  101. Clouse ME, Gramm HF, Legg M, et al. Diabetic osteoarthropathy. Clinical and roentgenographic observations in 90 cases. Am J Roentgenol Radium Ther Nucl Med. 1974;121:22–34.

    Article  CAS  PubMed  Google Scholar 

  102. Papanas N, Zissimopoulos A, Maltezos E. The role of nuclear medicine in the diagnosis of common and specific diabetic infections. Hell J Nucl Med. 2010;13:150–7.

    PubMed  Google Scholar 

  103. Croll SD, Nicholas GG, Osborne MA, Wasser TE, Jones S. Role of magnetic resonance imaging in the diagnosis of osteomyelitis in diabetic foot infections. J Vasc Surg. 1996;24(2):266–70.

    Article  CAS  PubMed  Google Scholar 

  104. Enderle MD, Coerper S, Schweizer HP, et al. Correlation of imaging techniques to histopathology in patients with diabetic foot syndrome and clinical suspicion of chronic osteomyelitis. The role of high-resolution ultrasound. Diabetes Care. 1999;22(2):294–9.

    Article  CAS  PubMed  Google Scholar 

  105. Aslangul E, M'bemba J, Caillat-Vigneron N, Coignard S, Larger E, Boitard C, et al. Diagnosing diabetic foot osteomyelitis in patients without signs of soft tissue infection by coupling hybrid 67Ga SPECT/CT with bedside percutaneous bone puncture. Diabetes Care. 2013;36(8):2203–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Heiba SI, Kolker D, Mocherla B, et al. The optimized evaluation of diabetic foot infection by dual isotope SPECT/CT imaging protocol. J Foot Ankle Surg. 2010;49:529–36.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  108. Gnanasegaran G, Vijayanathan S, Fogelman I. Diagnosis of infection in the diabetic foot using (18)F-FDG PET/CT: a sweet alternative? Eur J Nucl Med Mol Imaging. 2012;39(10):1525–7.

    Article  PubMed  Google Scholar 

  109. Palestro CJ. FDG-PET in musculoskeletal infections. Semin Nucl Med. 2013;43(5):367–76.

    Article  PubMed  Google Scholar 

  110. Vouillarmet J, Morelec I, Thivolet C. Assessing diabetic foot osteomyelitis remission with white blood cell SPECT/CT imaging. Diabet Med. 2014;31(9):1093–9.

    Article  CAS  PubMed  Google Scholar 

  111. Revest M, Patrat-Delon S, Devillers A, Tattevin P, Michelet C. Contribution of 18fluoro-deoxyglucose PET/CT for the diagnosis of infectious diseases. Med Mal Infect. 2014;44(6):251–60.

    Article  CAS  PubMed  Google Scholar 

  112. Zhuang HM, Cortes-Blanco A, Pourdehnad M, et al. Do high glucose levels have differential effect on FDG uptake in inflammatory and malignant disorders? Nucl Med Commun. 2001;22:1123–8.

    Article  CAS  PubMed  Google Scholar 

  113. Hopfner S, Krolak C, Kessler S, et al. 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.

    PubMed  Google Scholar 

  114. Rabkin Z, Israel O, Keidar Z. Do hyperglycemia and diabetes affect the incidence of false negative 18F-FDG-PET/CT studies in patients evaluated for infection or inflammation and cancer? A comparative analysis. J Nucl Med 2010;51:1015–20.

    Article  PubMed  Google Scholar 

  115. Israel O, Sconfienza LM, Lipsky BA. Diagnosing diabetic foot infection: the role of imaging and a proposed flow chart for assessment. Q J Nucl Med Mol Imaging. 2014;58(1):33–45.

    CAS  PubMed  Google Scholar 

  116. Treglia G, Sadeghi R, Annunziata S, Caldarella C, Bertagna F, Giovanella L. Diagnostic performance of fluorine-18-fluorodeoxyglucose positron emission tomography for the diagnosis of osteomyelitis related to diabetic foot: a systematic review and a meta-analysis. Foot (Edinb). 2013;23:140–8.

    Article  Google Scholar 

  117. Kagna O, Srour S, Melamed E, Militianu D, Keidar Z. FDG PET/CT imaging in the diagnosis of osteomyelitis in the diabetic foot. Eur J Nucl Med Mol Imaging. 2012;39(10):1545–50.

    Article  PubMed  Google Scholar 

  118. Basu S, Chryssikos T, Houseni M, et al. Potential role of FDG PET in the setting of diabetic neuroosteoarthropathy: can it differentiate uncomplicated Charcot’s neuroarthropathy from osteomyelitis and soft-tissue infection? Nucl Med Commun. 2007;28:465–72.

    Article  PubMed  Google Scholar 

  119. Nawaz A, Torigian DA, Siegelman ES, Basu S, Chryssikos T, Alavi A. Diagnostic performance of FDG-PET, MRI, and plain film radiography (PFR) for the diagnosis of osteomyelitis in the diabetic foot. Mol Imaging Biol. 2010;12(3):335–42.

    Article  PubMed  Google Scholar 

  120. Schwegler B, Stumpe KD, Weishaupt D, et al. Unsuspected osteomyelitis is frequent in persistent diabetic foot ulcer and better diagnosed by MRI than by 18F-FDG PET or 99mTc-MOAB. J Intern Med. 2008;263:99–106.

    CAS  PubMed  Google Scholar 

  121. Familiari D, Glaudemans AW, Vitale V, et al. Can sequential 18F-FDG PET/CT replace WBC imaging in the diabetic foot? J Nucl Med. 2011;52(7):1012–9.

    Article  PubMed  Google Scholar 

  122. Palestro CJ. 18F-FDG and diabetic foot infections: the verdict is... J Nucl Med. 2011;52(7):1009–11.

    Article  PubMed  Google Scholar 

  123. 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(3):789–95.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  125. Jeffcoate WJ, Lipsky BA. Controversies in diagnosing and managing osteomyelitis of the foot in diabetes. Clin Infect Dis. 2004;39 Suppl 2:S115–122.

    Article  PubMed  Google Scholar 

  126. Embil JM, Rose G, Trepman E, et al. Oral antimicrobial therapy for diabetic foot osteomyelitis. Foot Ankle Int. 2006;27:771–9.

    PubMed  Google Scholar 

  127. Game FL, Jeffcoate WJ. Primarily non-surgical management of osteomyelitis of the foot in diabetes. Diabetologia. 2008;51:962–7.

    Article  CAS  PubMed  Google Scholar 

  128. Hartemann-Heurtier A, Senneville E. Diabetic foot osteomyelitis. Diabetes Metab. 2008;34:87–95.

    Article  CAS  PubMed  Google Scholar 

  129. Murdoch DP, Armstrong DG, Dacus JB, Laughlin TJ, Morgan CB, Lavery LA. The natural history of great toe amputations. J Foot Ankle Surg. 1997;36:204–8; discussion 256.

    Article  CAS  PubMed  Google Scholar 

  130. Lipsky BA, Berendt AR, Cornia PB, et al. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis. 2012;54(12):e132–173.

    Article  PubMed  Google Scholar 

  131. Aragón-Sánchez J. Treatment of diabetic foot osteomyelitis: a surgical critique. Int J Low Extrem Wounds. 2010;9:37–59.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Radiology, School of Medicine, Catholic University, Largo A. Gemelli 1, 00168, Rome, Italy

    Antonio Leone, Alessia Semprini, Laura Tonetti, Nicola Magarelli & Cesare Colosimo

  2. Department of Diagnostic Imaging, The Robert Jones and Agnes Hunt Orthopaedic and District Hospital, Oswestry, Shropshire, UK

    Victor N. Cassar-Pullicino

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  1. Antonio Leone
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  2. Victor N. Cassar-Pullicino
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  3. Alessia Semprini
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Correspondence to Antonio Leone.

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Leone, A., Cassar-Pullicino, V.N., Semprini, A. et al. Neuropathic osteoarthropathy with and without superimposed osteomyelitis in patients with a diabetic foot. Skeletal Radiol 45, 735–754 (2016). https://doi.org/10.1007/s00256-016-2339-1

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  • DOI: https://doi.org/10.1007/s00256-016-2339-1

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