Generic placeholder image

Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Review Article

Charcot Neuroarthropathy: From the Laboratory to the Bedside

Author(s): Dario Pitocco*, Giuseppe Scavone, Mauro Di Leo, Raffaele Vitiello, Alessandro Rizzi, Linda Tartaglione, Federica Costantini, Andrea Flex, Marco Galli, Salvatore Caputo, Giovanni Ghirlanda and Alfredo Pontecorvi

Volume 16, Issue 1, 2020

Page: [62 - 72] Pages: 11

DOI: 10.2174/1573399815666190502121945

Price: $65

Abstract

Background: The diabetic Charcot foot syndrome is a serious and potentially limbthreatening lower-extremity complication of diabetes.

Introduction: The present review provides a concise account of the advances made over the last twentyfive years in understanding the pathogenesis and management of Charcot neuroarthropathy (CN).

Methods: In this study, the widely known pathogenetic mechanisms underpinning CN are brought into focus, particularly the role of RANKL/RANK/OPG system and advanced glycation end production in the pathogenesis of CN. Furthermore, other potential triggering factors, namely nitric oxide, endothelial dysfunction, macro calcifications and body weight that influence CN have also been discussed.

Results: The wide range of diagnostic tools available to clinicians for accurate staging of this pathology has been examined, particularly radiological and nuclear medicine imaging. Additionally, the difficult differential diagnosis between osteomyelitis and CN is also elucidated.

Conclusion: The review concludes with the comprehensive summary of the major promising therapeutic strategies, including conservative treatment involving orthopedic devices, pharmacological approach, and the most common surgical techniques currently employed in the diagnosis and treatment of this acute disease.

Keywords: Diabetes, charcot foot, neuropathy, osteoarthropathy, classification, inflammation.

[1]
Charcot J. Sur quelquesarthropathies qui paraissentdependred’une lesion du cerveauou de la moelleepiniere. Arch Des Phys Norm Pathol 1868; 1: 161.
[2]
Gouveri E, Papanas N. Charcot osteoarthropathy in diabetes: a brief review with an emphasis on clinical practice. World J Diabetes 2011; 2: 59-65.
[3]
Malhotra S, Bello E, Kominsky S. Diabetic foot ulcerations: biomechanics, charcot foot, and total contact cast. Semin Vasc Surg 2012; 25: 66-9.
[4]
Mumoli N, Camaiti A. Charcot foot. CMAJ 2012; 184: 1392.
[5]
Rogers LC, Frykberg RG, Armstrong DG, et al. The Charcot foot in diabetes. Diabetes Care 2011; 34: 2123-9.
[6]
Sanders LF. Charcot neuroathropathy of the foot. In: The diabetic foot. 6th edition. Bowker J, Pfeifer M. Mosby, St. Louis, MO 2001; pp. 439-66.
[7]
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.
[8]
Jordan WR. Neuritic Manifestation in Diabetes Mellitus. Arc. Int Med 1936; 57: 307-66.
[9]
Suder NC, Wukich DK. Prevalence of diabetic neuropathy in patients undergoing foot and ankle surgery. Foot Ankle Spec 2012; 5: 97-101.
[10]
Rajbhandari SJ, Jenkins RC, Davies C, Tesfaye S. Charcot neuroarthropathy in diabetes mellitus. Diabetologia 2002; 45: 1085-96.
[11]
Frykberg RG, Mendeszoon E. Management of the diabetic Charcot foot. Diabetes Metab Res Rev 2000; 16: S59-66.
[12]
Cofield RH, Motrisin M, Beabout JW. Diabetic neuroarthropathy in the foot: patient characteristics and patterns of radiographic changes. Foot Ankle Int 1983; 4: 15-22.
[13]
Fabrin J, Larsen K, Holstein P. Long-term follow-up in diabetic Charcot feet with spontaneous onset. Diabetes Care 2000; 23: 796-800.
[14]
Hartemann-Heurtier A, Ha Van G, Grimaldi A. The Charcot foot. Lancet 2002; 360: 1776-9.
[15]
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.
[16]
Sinha S, Munichoodappa C, Kozak G. Neuro-arthropathy (Charcot joints) in diabetes mellitus. Medicine 1971; 51: 191-210.
[17]
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.
[18]
Clohisy DR, Thompson RC Jr. Fractures associated with neuropathic arthropathy in adults who have juvenile-onset diabetes. J Bone Joint Surg Am 1988; 70: 1192-200.
[19]
Bayne O, Lu EJ. Diabetic Charcot’s arthropathy of the wrist. Case report and literature review. Clin Orthop Relat Res 1998; (357): 122-6.
[20]
Lambert AP, Close CF. Charcot neuroarthropathy of the knee in type 1 diabetes: treatment with total knee arthroplasty. Diabet Med 2002; 19: 338-41.
[21]
Petrova NL, Moniz C, Elias DA, Buxton-Thomas M, Bates M, Edmonds ME. Is there a systemic inflammatory response in the acute charcot foot? Diabetes Care 2007; 30: 997-8.
[22]
Trepman E, Nihal A, Pinzur MS. Current Topics Review: Charcot Neuroarthropathy of the Foot and Ankle. Foot Ankle Int 2005; 26: 46-63.
[23]
Saltzman CL, Hagy ML, Zimmerman B, et al. How effective is intensive nonoperative initial treatment of patients with diabetes and Charcot arthropathy of the feet? Clin Orthop Relat Res 2005; (435): 185-90.
[24]
Musa HG, Ahmed ME. Associated risk factors and management of chronic diabetic foot ulcers exceeding 6 months’ duration. Diabet Foot Ankle 2012; 3.
[25]
Sohn MW, Todd AL, Rodney MS. Mortality risk of charcot arthropathy compared with that of diabetic foot ulcer and diabetes alone. Diabetes Care 2009; 32: 816-21.
[26]
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.
[27]
Rudrappa S, Game F, Jeffcoate WJ. Recurrence of the acute Charcot foot in diabetes. Diabet Med 2012; 29: 819-21.
[28]
Jeffcoate WJ. Charcot foot syndrome. Diabet Med 2015; 32: 760-70.
[29]
Petrova NL, Edmonds ME. Charcot neuro‐osteoarthropathy-current standards. Diabetes Metab Res and Rev 2008; 24: S58-61.
[30]
Sanders LJ, Frykberg RG. Diabetic neuropathic osteoarthropathy: the Charcot foot. In: The high risk foot in diabetes mellitus. Frykberg R. Churchill Livingstone, New York 1998; pp. 297-338.
[31]
Rogers LC, Frykberg RG, Armstrong DG, et al. The charcot foot in diabetes. Diabetes Care 2011; 34: 2123-9.
[32]
Eichenholtz SN. Charcot joints With a foreword by PD Wilson Springfield [III]. Charles C. Thomas 1966.
[33]
Shibata T, Tada K, Hashizume C. The results of arthrodesis of the ankle for leprotic neuro-arthropathy. J Bone Joint Surg Am 1990; 72: 749-56.
[34]
Morrison WB, Ledermann HP. Work-up of the diabetic foot. Radiol Clin North Am 2002; 40: 1171-92.
[35]
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.
[36]
Ramanujam CL, Facaros Z. An overview of conservative treatment options for diabetic Charcot foot neuroarthropathy. Diabet Foot Ankle 2011; 2: 6418.
[37]
Pinzur MS, Lio T, Posner M. Treatment of Eichenholtz stage I Charcot foot arthropathy with a weightbearing total contact cast. Foot Ankle Int 2006; 27: 324-9.
[38]
Chantelau D, 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.
[39]
Saunders LJ, Mrdjenovich D. Anatomical patterns of bone and joint destruction in neuropathic diabetics. Diabetes 1991; 40: 529A.
[40]
Rajbhandari SM, Jenkins RC, Davies C, Tesfaye S. Charcot neuroarthropathy in diabetes mellitus. Diabetologia 2002; 45: 1085-96.
[41]
Brodsky JW. The diabetic foot. In: Surgery of the foot and ankle. 8th ed. Coughlin MJ, Mann RA, and Saltzman CL. Mosby, St. Louis, MO 2002; pp. 1281-368.
[42]
Brodsky JW, Rouse AM. Exostectomy for symptomatic bony prominences in diabetic Charcot feet. Clin Orthop Relat Res 1993; (296): 21-6.
[43]
La Fontaine J, Harkless LB, Sylvia VL, Carnes D, Heim-Hall J, Jude E. Levels of endothelial nitric oxide synthase and calcitonin gene-related peptide in the Charcot foot: a pilot study. J Foot Ankle Surg 2008; 47: 424-9.
[44]
Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet 2005; 10(366): 2058-61.
[45]
Mabilleau G, Petrova N, Edmonds ME, Sabokar A. Increased osteoclastic activity in acute Charcot’s osteoarthropathy: the role of receptor activator of nuclear factor-kappaB ligand. Diabetologia 2008; 51: 1035-40.
[46]
Jeffcoate W. Vascular calcification and osteolysis in diabetic neuropathy-is RANK-L the missing link? Diabetologia 2004; 47: 1488-92.
[47]
Gough A, Abraha GH, Li F, et al. Measurement of Markers of Osteoclast and Osteoblast Activity in Patients with Acute and Chronic Diabetic Charcot Neuroarthropathy. Diabet Med 1997; 14: 527-31.
[48]
Jones DH, Kong YY, Penninger JM. Role of RANKL and RANK in bone loss and arthritis. Ann Rheum Dis 2002; 61(Suppl. 2): ii32-9.
[49]
Mabilleau G, Petrova N, Edmonds ME, Sabokbar A. Number of Circulating CD14-Positive Cells and the Serum Levels of TNF-a Are Raised in Acute Charcot Foot. Diabetes Care 2011; 34(3) e33
[50]
Yasuda H, Shima N, Nakagawa N, et al. Identity of osteoclastogenesisinhibitory factor (OCIF) and osteoprotegerin (OPG): a mechanism by which OPG/OCIF inhibits osteoclastogenesis in vitro. Endocrinology 1998; 139: 1329-37.
[51]
Chipoy C, Berreur M, Couillaud S, et al. Downregulation of osteoblast markers and induction of the glial fibrillary acidic protein by oncostatin M in osteosarcoma cells require PKCdelta and STAT3. J Bone Miner Res 2004; 19: 1850-61.
[52]
Goshen I, Yirmiya R. Interleukin-1 [IL-1]: A central regulator of stress responses. Front Neuroendocrinol 2009; 30: 30-45.
[53]
Ndip A, Williams A, Jude EB, et al. The RANKL/RANK/OPG signaling pathway mediates medial arterial calcification in diabetic charcot neuroarthropathy. Diabetes 2011; 60: 2187-96.
[54]
Pitocco D, Zelano G, Gioffré G, et al. Association between osteoprotegerin G1181C and T245G polymorphisms and diabetic charcot neuroarthropathy. a case-control study. Diabetes Care 2009; 32: 1694-7.
[55]
Frykberg RG, Belczyk R. Epidemiology of the Charcot foot. Clin Podiatr Med Surg 2008; 25: 17-28.
[56]
Katayama Y, Akatsu T, Yamamoto M, Kugai N, Nagata N. Role of nonenzymatic glycosylation of type I collagen in diabetic osteopenia. J Bone Miner Res 1996; 11: 931-7.
[57]
Katayama Y, Celic S, Nagata N, Martin TJ, Findlay DM. Nonenzymatic glycation of type I collagen modifies interaction with UMR 201-10B preosteoblastic cells. Bone 1997; 21: 237-42.
[58]
McCarthy AD, Etcheverry SB, Bruzzone L, Lettieri G, Barrio DA, Cortizo AM. Non-enzymatic glycosylation of a type I collagen matrix: effects on osteoblastic development and oxidative stress. BMC Cell Biol 2001; 2: 16.
[59]
McCarthy AD, Etcheverry SB, Cortizo AM. Effect of advanced glycation endproducts on the secretion of insulin-like growth factor-I and its binding proteins: role in osteoblast development. Acta Diabetol 2001; 38: 113-22.
[60]
McCarthy AD, Uemura T, Etcheverry SB, Cortizo AM. Advanced glycation endproducts interfere with integrin-mediated osteoblastic attachment to a type-I collagen matrix. Int J Biochem Cell Biol 2004; 36: 840-8.
[61]
Alikhani M, Alikhani Z, Boyd ZC, et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 2007; 40: 345-53.
[62]
Mercer N, Ahmed H, Etcheverry SB, Vasta GR, Cortizo AM. Regulation of advanced glycation end product [AGE] receptors and apoptosis by AGEs in osteoblast-like cells. Mol Cell Biochem 2007; 306: 87-94.
[63]
Dong XN, Qin A, Xu J, Wang X. In situ accumulation of advanced glycation endproducts [AGEs] in bone matrix and its correlation with osteoclastic bone resorption. Bone 2011; 49: 174-83.
[64]
Rizzo P, Pitocco D, Zaccardi F, et al. Autoantibodies to post‐translationally modified type I and II collagen in Charcot neuroarthropathy in subjects with type 2 diabetes mellitus. Diabetes Metab Res Rev 2017; 33e2839
[65]
Tamaru M, Tomura K, Sakamoto S, Tezuka K, Tamatani T, Narumi S. Interleukin-1 beta induces tissue- and cell-specific expression of adhesion molecules in vivo. Arterioscler Thromb Vasc Biol 1998; 18: 1292-303.
[66]
Ikeda U, Ikeda M, Oohara T, Kano S, Yaginuma T. Mitogenic action of interleukin-1 alpha on vascular smooth muscle cells mediated by PDGF. Atherosclerosis 1990; 84: 183-8.
[67]
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.
[68]
Sattler AM, Schoppet M, Schaefer JR, Hofbauer LC. Novel aspects on RANK ligand and osteoprotegerin in osteoporosis and vascular disease. Calcif Tissue Int 2004; 74: 103-6.
[69]
Schoppet M, Preissner KT, Hofbauer LC. RANK ligand and osteoprotegerin: paracrine regulators of bone metabolism and vascular function. Arterioscler Thromb Vasc Biol 2002; 22: 549-53.
[70]
Walsh MC, Choi YW. Biology of the TRANCE axis. Cytokine Growth Factor Rev 2003; 14: 251-63.
[71]
Kaden JJ, Bickelhaupt S, Grobholz R, et al. Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulate aortic valve calcification. J Mol Cell Cardiol 2004; 36: 57-66.
[72]
Breuil V, Schmid-Antomarchi H, Schmid-Alliana A, Rezzonico R, Euller-Ziegler L, Rossi B. The receptor activator of nuclear factor [NF]-kappaB ligand [RANKL] is a new chemotactic factor for human monocytes. FASEB J 2003; 17: 1751-3.
[73]
Lehto S, Niskanen L, Suhonen M, Rönnemaa T, Laakso M. Medial artery calcification. A neglected harbinger of cardiovascular complications in non-insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 1996; 16: 978-83.
[74]
Nelson RG, Gohdes DM, Everhart JE, et al. Lower-extremity amputations in NIDDM. 12-yr follow-up study in Pima Indians. Diabetes Care 1988; 11: 8-16.
[75]
Young MJ, Adams JE, Anderson GF, Boulton AJM, Cavanagh PR. Medial arterial calcification in the feet of diabetic patients and matched nondiabetic control subjects. Diabetologia 1993; 36: 615-21.
[76]
Chen NX, Moe SM. Arterial calcification in diabetes. Curr Diab Rep 2003; 3: 28-32.
[77]
Costacou T, Huskey ND, Edmundowicz D, Stolk R, Orchard TJ. Lower extremity arterial calcification as a correlate of coronary artery calcification. Metabolism 2006; 55: 1689-96.
[78]
Khanolkar MP, Bain SC, Stephens JW. The diabetic foot 2008; 101: 685-95.
[79]
Pitocco D, Marano R, Di Stasio E, et al. Atherosclerotic coronary plaque in subjects with diabetic neuropathy: the prognostic cardiovascular role of Charcot neuroarthropathy—a case-control study. Acta Diabetol 2014; 51: 587-93.
[80]
Bierhaus A, Humpert PM, Morcos M, et al. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 2005; 83: 876-86.
[81]
Pinzur M. Benchmark analysis of diabetic patients with neuropathic [Charcot] foot deformity. Foot Ankle Int 1999; 20: 564-7.
[82]
Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444: 860-7.
[83]
Nijhuis J, Rensen SS, Slaats Y, van Dielen FM, Buurman WA, Greve JW. Neutrophil activation in morbid obesity, chronic activation of acute inflammation. Obesity 2009; 17: 2014-8.
[84]
Ghigliotti G, Barisione C, Garibaldi S, et al. Adipose tissue immune response: noveltriggers and consequences for chronicinflammatoryconditions. Inflammation 2014; 37: 1337-53.
[85]
La Fontaine J, Bhavan K, Talal TK, Lavery LA. Current concepts in the surgical management of acute diabetic foot infections. Foot 2014; 24: 123-7.
[86]
Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-30.
[87]
Pakarinen TK, Laine HJ, Mäenpää H, Mattila P, Lahtela J. The effect of zoledronic acid on the clinical resolution of charcotneuroarthropathy: a pilot randomized controlled trial. Diabetes Care 2011; 34: 1514-6.
[88]
Stuck RM, Sohn MW, Budiman-Mak E, Lee TA, Weiss KB. Charcot arthropathy risk elevation in the obese diabetic population. Am J Med 2008; 121: 1008-14.
[89]
Ross AJ, Mendicino RW, Catanzariti AR. Role of body mass index in acute charcotneuroarthropathy. J Foot Ankle Surg 2013; 52: 6-8.
[90]
Armstrong DG, Lavery LA, Liswood PJ, Todd WF, Tredwell JA. Infrared dermal thermometry for the high-risk diabetic foot. Phys Ther 1997; 77: 169-75.
[91]
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.
[92]
Jude EB, Boulton AJ. Medical treatment of Charcot’s arthropathy. J Am Podiatr Med Assoc 2002; 92: 381-3.
[93]
Najafi B, Wrobel JS, Grewal G, et al. Temperature response to walking in diabetes with and without acute Charcot: the Charcot Activity Response test. J Aging Res 2012. 140968
[94]
Yu GV, Hudson JR. Evaluation and Treatment of Stage 0 Charcot’s Neuroarthropathy of the Foot and Ankle. J Am Podiatr Med Assoc 2002; 92: 210-20.
[95]
Rogers LC, Bevilacqua NJ. Imaging of the Charcot foot. Clin Podiatr Med Surg 2008; 25: 263-74.
[96]
Tan PL, Teh J. MRI of the diabetic foot: differentiation of infection from neuropathic change. Br J Radiol 2007; 80: 939-48.
[97]
Ergen FB, Sanverdi SE, Oznur A. Charcot foot in diabetes and an update on imaging. Diabet Foot Ankle 2013; 20: 4.
[98]
Ertugrul BM, Lipsky BA, Savk O. Osteomyelitis or Charcot neuro-osteoarthropathy? Differentiating these disorders in diabetic patients with a foot problem. Diabet Foot Ankle 2013; 410.3402
[99]
Johnson JE, Kennedy EJ, Shereff MJ, Patel NC, Collier BD. Prospective study of bone, indium-111-labeled white blood cell, and gallium-67 scanning for the evaluation of osteomyelitis in the diabetic foot. Foot Ankle Int 1996; 17: 10-6.
[100]
Palestro CJ, Mehta HH, Patel M, et al. Marrow versus infection in the Charcot joint: indium-111 leukocyte and technetium-99m sulfur colloid scintigraphy. J Nucl Med 1998; 39: 346-50.
[101]
Höpfner S, Krolak C, Kessler S, Tiling R. Preoperative imaging of Charcot neuroarthropathy: does the additional application of [18]F-FDG-PET make sense? Nuklearmedizin 2006; 45: 15-20.
[102]
Basu S, Chryssikos T, Houseni M, et al. Potential role of FDG PET in the setting of diabetic neuro-osteoarthropathy: can it differentiate uncomplicated Charcot’s neuroarthropathy from osteomyelitis and soft-tissue infection? Nucl Med Commun 2007; 28: 465-72.
[103]
Ranachowska C, Lass P, Korzon-Burakowska A, Dobosz M. Diagnostic imaging of the diabetic foot. Nucl Med Rev Cent East Eur 2010; 13: 18-22.
[104]
van der Bruggen W, Bleeker-Rovers CP, Boerman OC, Gotthardt M, Oyen WJ. PET and SPECT in osteomyelitis and prosthetic bone and joint infections: a systematic review. Semin Nucl Med 2010; 40: 3-15.
[105]
Keidar Z, Militianu D, Melamed E, Bar-Shalom R, Israel O. The diabetic foot: initial experience with 18F-FDG PET/CT. J Nucl Med 2005; 46: 444-9.
[106]
Zhuang H, Duarte PS, Pourdehand M, Shnier D, Alavi A. Exclusion of chronic osteomyelitis with F-18 fluorodeoxyglucose positron emission tomographic imaging. Clin Nucl Med 2000; 25: 281-4.
[107]
Höpfner S, Krolak C, Kessler S, Tiling R. Preoperative imaging of Charcot neuroarthropathy: does the additional application of [18]F-FDG-PET make sense? Nuklearmedizin 2006; 45: 15-20.
[108]
Idusuyi OB. Surgical management of Charcot Neuroarthropathy. Prosthet and Orthot Int 2015; 39: 61-72.
[109]
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.
[110]
Sinha S, Munichoodappa CS, and Kozak GP. Neuroarthropathy (Charcot joints) in diabetes mellitus (clinical study of 101 cases). Medicine 1972; 51: 191-210.
[111]
Trieb K, Ramadani F, Hofstaetter SG. Full contact plaster cast for conservative treatment of Charcot foot. Orthopade 2015; 44: 39-44.
[112]
Verity S, Sochocki M, Embil JM, Trepman E. Treatment of Charcot foot and ankle with a prefabricated removable walker brace and custom insole. Foot and Ankle Surg 2008; 14: 26-31.
[113]
Pinzur MS, Lio T, Matthew Posner M. Treatment of eichenholtz stage I charcot foot arthropathy with a weight bearing total contact cast. Foot Ankle Int 2006; 27: 324-9.
[114]
Jude EB, Selby PL, Burgess J, Lilleystone P, Mawer EB, Page SR. Bisphosphonates in the treatment of Charcot neuroarthropathy: double blinded randomised controlled trial. Diabetologia 2001; 44: 2032-7.
[115]
Pitocco D, Ruotolo V, Caputo S, Mancini L, Collina CM, Manto A. Six month treatment with alendronate in acute Charcot neuroarthropathy: a randomized controlled trial. Diabetes Care 2005; 28: 1214-5.
[116]
Pakarinen T-K, Laine H-J, Mäenpää H, Kähönen M, Mattila P, Lahtela J. Effect of immobilization, off-loading and zoledronic acid on bone mineral density in patients with acute Charcot neuroarthropathy: A prospective randomized trial. Foot and Ankle Surg 2013; 19: 121-4.
[117]
Bern R, Jirkovska A, Fejfarova V, Skibova J, Jude EB. Intranasal calcitonin in the treatment of acute Charcot neurosteoarthropathy: a randomized controlled trial. Diabetes Care 2006; 29: 1392-5.
[118]
Molines L, Darmon P, Raccah D. Charcot’s foot: Newest findings on its pathophysiology, diagnosis and treatment. Diabetes Metab 2010; 36: 251-5.
[119]
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.
[120]
Pakarinen TK, Laine HJ, Honkonen SE, Peltonen J, Oksana H, Lahtela J. Charcot arthropathy of the diabetic foot: current concepts and review of 36 cases. Scand J Surg 2002; 91: 195-201.
[121]
Kalani M, Brismar K, Fagrell B, Ostergren J, Jörneskog G. Transcutaneous oxygen tension and toe blood pressure as predictors for outcome of diabetic foot ulcers. Diabetes Care 1999; 22: 147-51.
[122]
Schon LC, Easley ME, Weinfeld SB. Charcot neuroarthropathy of the foot and ankle. Clin Orthop Relat Res 1998; (349): 116-31.
[123]
Catanzariti AR, Mendicino R, Haverstock B. Ostectomy for diabetic neuroarthropathy involving the midfoot. J Foot Ankle Surg 2000; 39: 291-300.
[124]
Cooper PS. Application of external fixators for management of Charcot deformities of the foot and ankle. Foot Ankle Clin N Am 2002; 7: 207-54.
[125]
Grant WP, Garcia-Lavin S, Sabo R. Beaming the Columns for Charcot Diabetic Foot Reconstruction: A Retrospective Analysis. J Foot Ankle Surg 2011; 50: 182-9.
[126]
Zgonis T, Roukis TS, Stapleton JJ, Cromack DT. Combined lateral column arthrodesis, medial plantar artery flap, and circular external fixation for Charcot midfoot collapse with chronic plantar ulceration. Adv Skin Wound Care 2008; 21: 521-5.
[127]
Sayner RL, Rosenblum BI. External fixation for charcot foot reconstruction. Curr Surg 2005; 62: 618-23.
[128]
Roukis TS, Zgonis T. The management of acute Charcot fracture-dislocations with the Taylor’s spatial external fixation system. Clin Podiatr Med Surg 2006; 23: 467-83.
[129]
Pinzur MS. The role of ring external fixation in Charcot foot arthropathy. Foot Ankle Clin 2006; 11: 837-47.
[130]
Altindas M, Kilic A, Ceber M. A new limb-salvaging technique for the treatment of late stage complicated Charcot foot deformity: two-staged Boyd’s operation. Foot Ankle Surg 2012; 18: 190-4.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy