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Mascio A, Comisi C, Cinelli V, Pitocco D, Greco T, Maccauro G, Perisano C. Radiological Assessment of Charcot Neuro-Osteoarthropathy in Diabetic Foot: A Narrative Review. Diagnostics (Basel) 2025; 15:767. [PMID: 40150109 PMCID: PMC11940856 DOI: 10.3390/diagnostics15060767] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/03/2025] [Revised: 03/05/2025] [Accepted: 03/16/2025] [Indexed: 03/29/2025] Open
Abstract
Charcot Neuro-Osteoarthropathy (CNO) is a debilitating complication predominantly affecting individuals with diabetes and peripheral neuropathy. Radiological assessment plays a central role in the diagnosis, staging, and management of CNO. While plain radiographs remain the cornerstone of initial imaging, advanced modalities such as Magnetic Resonance Imaging (MRI) and Computed Tomography (CT) have significantly enhanced diagnostic accuracy. Nuclear imaging, including bone scintigraphy, radiolabeled leukocyte scans, and FDG-PET/CT, offers additional diagnostic precision in complex cases, especially when differentiating CNO from infections or evaluating patients with metal implants. This review underscores the importance of a multimodal imaging approach suited to the clinical stage and specific diagnostic challenges of CNO. It highlights the critical need for standardized imaging protocols and integrated diagnostic algorithms that combine radiological, clinical, and laboratory findings. Advances in imaging biomarkers and novel techniques such as diffusion-weighted MRI hold promise for improving early detection and monitoring treatment efficacy. In conclusion, the effective management of CNO in diabetic foot patients requires a multidisciplinary approach that integrates advanced imaging technologies with clinical expertise. Timely and accurate diagnosis not only prevents debilitating complications but also facilitates the development of personalized therapeutic strategies, ultimately improving patient outcomes.
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Affiliation(s)
- Antonio Mascio
- Department of Orthopedics and Geriatric Sciences, Catholic University of the Sacred Heart, 00136 Rome, Italy; (A.M.); (V.C.); (T.G.); (G.M.); (C.P.)
- Department of Orthopedics and Rheumatological Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, 00136 Rome, Italy
| | - Chiara Comisi
- Department of Orthopedics and Geriatric Sciences, Catholic University of the Sacred Heart, 00136 Rome, Italy; (A.M.); (V.C.); (T.G.); (G.M.); (C.P.)
- Department of Orthopedics and Rheumatological Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, 00136 Rome, Italy
| | - Virginia Cinelli
- Department of Orthopedics and Geriatric Sciences, Catholic University of the Sacred Heart, 00136 Rome, Italy; (A.M.); (V.C.); (T.G.); (G.M.); (C.P.)
- Department of Orthopedics and Rheumatological Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, 00136 Rome, Italy
| | - Dario Pitocco
- Diabetes Care Unit, Endocrinology, University Hospital “A. Gemelli”, Catholic University of the Sacred Heart, 00136 Rome, Italy;
| | - Tommaso Greco
- Department of Orthopedics and Geriatric Sciences, Catholic University of the Sacred Heart, 00136 Rome, Italy; (A.M.); (V.C.); (T.G.); (G.M.); (C.P.)
- Department of Life Sciences, Health, and Healthcare Professions, Link Campus University, 00165 Rome, Italy
| | - Giulio Maccauro
- Department of Orthopedics and Geriatric Sciences, Catholic University of the Sacred Heart, 00136 Rome, Italy; (A.M.); (V.C.); (T.G.); (G.M.); (C.P.)
- Department of Orthopedics and Rheumatological Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, 00136 Rome, Italy
| | - Carlo Perisano
- Department of Orthopedics and Geriatric Sciences, Catholic University of the Sacred Heart, 00136 Rome, Italy; (A.M.); (V.C.); (T.G.); (G.M.); (C.P.)
- Department of Orthopedics and Rheumatological Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, 00136 Rome, Italy
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Bouman CMB, Mens MA, Wellenberg RHH, Streekstra GJ, Bus SA, Busch-Westbroek TE, Nieuwdorp M, Maas M. Assessment of bone marrow edema on dual-energy CT scans in people with diabetes mellitus and suspected Charcot neuro-osteoarthropathy. Skeletal Radiol 2025; 54:105-112. [PMID: 38833168 PMCID: PMC11573814 DOI: 10.1007/s00256-024-04714-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/27/2024] [Revised: 05/20/2024] [Accepted: 05/20/2024] [Indexed: 06/06/2024]
Abstract
OBJECTIVE This study aimed to quantitatively assess the diagnostic value of bone marrow edema (BME) detection on virtual non-calcium (VNCa) images calculated from dual-energy CT (DECT) in people with diabetes mellitus and suspected Charcot neuro-osteoarthropathy (CN). MATERIALS AND METHODS People with diabetes mellitus and suspected CN who underwent DECT of the feet (80kVp/Sn150kVp) were included retrospectively. Two blinded observers independently measured CT values on VNCa images using circular regions of interest in five locations in the midfoot (cuneiforms, cuboid and navicular) and the calcaneus of the contralateral or (if one foot was available) the ipsilateral foot. Two clinical groups were formed, one with active CN and one without active CN (no-CN), based on the clinical diagnosis. RESULTS Thirty-two people with diabetes mellitus and suspected CN were included. Eleven had clinically active CN. The mean CT value in the midfoot was significantly higher in the CN group (-55.6 ± 18.7 HU) compared to the no-CN group (-94.4 ± 23.5 HU; p < 0.001). In the CN group, the difference in CT value between the midfoot and calcaneus was statistically significant (p = 0.003); this was not the case in the no-CN group (p = 0.357). The overall observer agreement was good for the midfoot (ICC = 0.804) and moderate for the calcaneus (ICC = 0.712). Sensitivity was 100.0% and specificity was 71.4% using a cutoff value of -87.6 HU. CONCLUSION The detection of BME on VNCa images has a potential value in people with diabetes mellitus and suspected active CN.
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Affiliation(s)
- Carlijn M B Bouman
- Amsterdam UMC, Radiology and Nuclear Medicine, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands
| | - Marieke A Mens
- Amsterdam UMC, Radiology and Nuclear Medicine, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands.
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands.
| | - Ruud H H Wellenberg
- Amsterdam UMC, Radiology and Nuclear Medicine, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands
| | - Geert J Streekstra
- Amsterdam UMC, Radiology and Nuclear Medicine, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam UMC, Biomedical Engineering and Physics, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands
| | - Sicco A Bus
- Amsterdam UMC, Location University of Amsterdam, Rehabilitation Medicine, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands
| | - Tessa E Busch-Westbroek
- Amsterdam UMC, Location University of Amsterdam, Rehabilitation Medicine, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands
| | - Max Nieuwdorp
- Amsterdam UMC, Internal and Vascular Medicine, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands
| | - Mario Maas
- Amsterdam UMC, Radiology and Nuclear Medicine, Location University of Amsterdam, Meibergdreef 9, Amsterdam, The Netherlands
- Amsterdam Movement Sciences, Rehabilitation and Development, Amsterdam, The Netherlands
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Abstract
There are many similarities between nondiabetic and diabetic Charcot neuroarthropathy (CN) but many of the underlying causes causing nondiabetic neuropathy and CN are associated with poor bone quality. Patient workup for nondiabetic CN should include the underlying cause of the neuropathy and optimization of bony healing, such as vitamin D supplementation and bisphosphonate or calcitonin administration. Surgical reconstruction should include the most robust fixation possible, as nondiabetic patients with CN are more prone to delayed union.
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Management of Ankle Charcot Neuroarthropathy: A Systematic Review. J Clin Med 2021; 10:jcm10245923. [PMID: 34945220 PMCID: PMC8707751 DOI: 10.3390/jcm10245923] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/27/2021] [Revised: 12/12/2021] [Accepted: 12/13/2021] [Indexed: 11/17/2022] Open
Abstract
Background: Charcot neuroarthropathy is a non-infective, destructive process occurring in patients rendered insensate by peripheral neuropathy, which is caused mainly by diabetes. Repetitive trauma from standing and walking provides a neuro-traumatic stimulus that leads to dislocation, or peri-articular fracture, or both, within the ankle. This review concentrates on the management protocols regarding the ankle only. Methods: A Pubmed search for clinical trials performed to manage ankle Charcot neuroarthropathy and a systematic review of these articles were undertaken. Results: Twenty papers met the inclusion criteria: four of them describe non-surgical management, while the rest show different surgical management options of ankle Charcot neuroarthropathy. Conclusions: Surgical algorithms for the treatment of CN of the ankle are based almost entirely on level four. There is inconclusive evidence concerning the timing of treatment and the use of different fixation methods. Instability and ulceration are the main precursors for surgical interventions. Prospective series and randomized studies, albeit difficult to perform, are necessary to support and strengthen current practice.
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Davis BL, Tiell SM, McMillan GR, Goss LP, Crafton JW. Simple model of arch support: Relevance to Charcot Neuroarthropathy. Clin Biomech (Bristol, Avon) 2021; 87:105403. [PMID: 34091194 PMCID: PMC8316300 DOI: 10.1016/j.clinbiomech.2021.105403] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/01/2020] [Revised: 05/22/2021] [Accepted: 05/27/2021] [Indexed: 02/07/2023]
Abstract
BACKGROUND Charcot neuropathy is a common complication resulting from poorly controlled diabetes and peripheral neuropathy leading to the collapse, and ultimately the breakdown, of the midfoot. Mechanically, it is likely that a compromised arch support in this, or any other patient group that experiences foot flattening, would be associated with slippage at the distal and proximal interface regions of the plantar surface of the foot and the adjacent support surface. This slippage, although difficult to quantify with standard motion capture systems used in a gait laboratory, could potentially be assessed with systems for monitoring interface shear stresses. However, before investing in such systems, a correlation between arch flattening and interface shear stresses needs to be verified. METHODS For this purpose, a sagittal plane model of a foot was developed using a multi-body dynamics package (MSC Adams). This model mimicked a subject swaying back and forth, and was constructed to show the dependence of interface stresses on altered arch support. FINDINGS The model's predictions matched typical FootSTEPS data: lengthening of the arch of 1-2 mm, sway oscillations of 0.22-0.33 s and frictional force differences (calcaneus relative to forefoot) of 60 N. Of clinical relevance, when the stiffness of the plantar spring (representing aponeurosis and intrinsic muscles) was reduced by 10%, the frictional force difference increased by about 6.5%. INTERPRETATION The clinical implications of this study are that, while arch lengthening of less than 2 mm might be difficult to measure reliably in a gait lab, using shear sensors under the forefoot and hindfoot should allow arch support to be assessed in a repeatable manner.
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Affiliation(s)
- B L Davis
- Cleveland State University, WH 305 I, Washkewicz Hall, 2121 Euclid Avenue, Cleveland, OH 44115, USA.
| | - S M Tiell
- The University of Akron, 302 East Buchtel Avenue, Akron, OH 44325, USA
| | - G R McMillan
- Innovative Scientific Solutions Inc., 7610 McEwen Road, Dayton, OH 45459, USA
| | - L P Goss
- Innovative Scientific Solutions Inc., 7610 McEwen Road, Dayton, OH 45459, USA
| | - J W Crafton
- Innovative Scientific Solutions Inc., 7610 McEwen Road, Dayton, OH 45459, USA
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Chantelau EA, Antoniou S, Zweck B, Haage P. Follow up of MRI bone marrow edema in the treated diabetic Charcot foot - a review of patient charts. Diabet Foot Ankle 2018; 9:1466611. [PMID: 29713425 PMCID: PMC5918386 DOI: 10.1080/2000625x.2018.1466611] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/24/2018] [Accepted: 04/12/2018] [Indexed: 05/15/2023]
Abstract
Background: Ill-defined areas of water-like signal on bone magnetic resonance imaging (MRI), characterized as bone marrow edema or edema-equivalent signal-changes (EESC), is a hallmark of active-stage pedal neuro-osteoarthropathy (Charcot foot) in painless diabetic neuropathy, and is accompanied by local soft-tissue edema and hyperthermia. The longitudinal effects on EESC of treating the foot in a walking cast were elucidated by reviewing consecutive cases of a diabetic foot clinic. Study design: Retrospective observational study, chart review Material and methods: Cases with active-stage Charcot foot were considered, in whom written reports on baseline and follow-up MRI studies were available for assessment. Only cases without concomitant infection or skin ulcer were chosen, in whom both was documented, onset of symptomatic foot swelling and patient compliance with cast treatment. Results: From 1994 to 2017, 45 consecutive cases in 37 patients were retrieved, with 95 MRI follow-up studies (1-6 per case, average interval between studies 13 weeks). Decreasing EESC was documented in 66/95 (69%) follow-up studies. However, 29/95 (31%) studies revealed temporarily increasing, migrating or stagnating EESC. Conclusion: EESC on MRI disappear in response to prolonged offloading and immobilizing treatment; however, physiologic as well as pathologic fluctuations of posttraumatic EESC have to be considered when interpreting the MR images. Conventional MRI is useful for surveillance of active-stage Charcot foot recovery.
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Affiliation(s)
- Ernst-A. Chantelau
- Department of Endocrinology and Diabetology, Diabetic Foot Clinic, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
| | - Sofia Antoniou
- Department of Endocrinology and Diabetology, Diabetic Foot Clinic, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
| | - Brigitte Zweck
- Department of Endocrinology and Diabetology, Diabetic Foot Clinic, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
| | - Patrick Haage
- Department of Diagnostic and Interventional Radiology, HELIOS University Hospital Wuppertal, University Witten/Herdecke, Wuppertal, Germany
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Mautone M, Naidoo P, Zhou K. Imaging of the spectrum of bony injuries in the diabetic foot: a case series with emphasis on non-Charcot fractures. BJR Case Rep 2017; 3:20170026. [PMID: 30363235 PMCID: PMC6159173 DOI: 10.1259/bjrcr.20170026] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/14/2017] [Revised: 06/25/2017] [Accepted: 06/27/2017] [Indexed: 11/23/2022] Open
Abstract
Diabetes mellitus is associated with an increased risk of lower limb injuries. Peripheral neuropathy, often associated with diabetes, has been demonstrated to increase the risk of fracture almost two-fold and is associated with complications related to fracture healing. Detection of neuropathy-related foot injury is frequently delayed owing to the paucity of symptoms and low degree of suspicion by the clinician. Early recognition of fracture or bone injury and appropriate treatment are critical in preventing debilitating foot deformity and disability. Therefore, the astute radiologist cognizant of these potential injuries plays an essential role in early diagnosis of bony injuries in the diabetic foot. We present a series of radiological images that depict a range of osseous injuries in the diabetic foot and emphasize the role of the radiologist in early recognition of these abnormalities.
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Affiliation(s)
- Marcela Mautone
- Diagnostic Imaging Department, Monash Health, Melbourne, Australia
| | - Parm Naidoo
- Diagnostic Imaging Department, Monash Health, Melbourne, Australia
- Monash University, Melbourne, Australia
- University of Melbourne, Melbourne, Australia
| | - Kevin Zhou
- Diagnostic Imaging Department, Monash Health, Melbourne, Australia
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8
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Meacock L, Petrova NL, Donaldson A, Isaac A, Briody A, Ramnarine R, Edmonds ME, Elias DA. Novel Semiquantitative Bone Marrow Oedema Score and Fracture Score for the Magnetic Resonance Imaging Assessment of the Active Charcot Foot in Diabetes. J Diabetes Res 2017; 2017:8504137. [PMID: 29230422 PMCID: PMC5694565 DOI: 10.1155/2017/8504137] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/07/2017] [Revised: 08/04/2017] [Accepted: 08/13/2017] [Indexed: 11/17/2022] Open
Abstract
There are no accepted methods to grade bone marrow oedema (BMO) and fracture on magnetic resonance imaging (MRI) scans in Charcot osteoarthropathy. The aim was to devise semiquantitative BMO and fracture scores on foot and ankle MRI scans in diabetic patients with active osteoarthropathy and to assess the agreement in using these scores. Three radiologists assessed 45 scans (Siemens Avanto 1.5T, dedicated foot and ankle coil) and scored independently twenty-two bones (proximal phalanges, medial and lateral sesamoids, metatarsals, tarsals, distal tibial plafond, and medial and lateral malleoli) for BMO (0-no oedema, 1-oedema < 50% of bone volume, and 2-oedema > 50% of bone volume) and fracture (0-no fracture, 1-fracture, and 2-collapse/fragmentation). Interobserver agreement and intraobserver agreement were measured using multilevel modelling and intraclass correlation (ICC). The interobserver agreement for the total BMO and fracture scores was very good (ICC = 0.83, 95% confidence intervals (CI) 0.76, 0.91) and good (ICC = 0.62; 95% CI 0.48, 0.76), respectively. The intraobserver agreement for the total BMO and fracture scores was good (ICC = 0.78, 95% CI 0.6, 0.95) and fair to moderate (ICC = 0.44; 95% CI 0.14, 0.74), respectively. The proposed BMO and fracture scores are reliable and can be used to grade the extent of bone damage in the active Charcot foot.
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Affiliation(s)
- L. Meacock
- Department of Radiology, King's College Hospital NHS Foundation Trust, London, UK
| | - N. L. Petrova
- Diabetic Foot Clinic, King's College Hospital NHS Foundation Trust, London, UK
- Division of Diabetes and Nutritional Sciences, King's College London, London, UK
| | - Ana Donaldson
- Diabetic Foot Clinic, King's College Hospital NHS Foundation Trust, London, UK
| | - A. Isaac
- Department of Radiology, King's College Hospital NHS Foundation Trust, London, UK
| | - A. Briody
- Department of Radiology, King's College Hospital NHS Foundation Trust, London, UK
| | - R. Ramnarine
- Department of Radiology, King's College Hospital NHS Foundation Trust, London, UK
| | - M. E. Edmonds
- Diabetic Foot Clinic, King's College Hospital NHS Foundation Trust, London, UK
- Division of Diabetes and Nutritional Sciences, King's College London, London, UK
| | - D. A. Elias
- Department of Radiology, King's College Hospital NHS Foundation Trust, London, UK
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Abstract
This review describes the normal healing process for bone, ligaments, and tendons, including primary and secondary healing as well as bone-to-bone fusion. It depicts the important mediators and cell types involved in the inflammatory, reparative, and remodeling stages of each healing process. It also describes the main challenges for clinicians when trying to repair bone, ligaments, and tendons with a specific emphasis on Charcot neuropathy, fifth metatarsal fractures, arthrodesis, and tendon sheath and adhesions. Current treatment options and research areas are also reviewed.
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Affiliation(s)
- Jessica A Cottrell
- Department of Biological Sciences, Seton Hall University, 400 South Orange Avenue, South Orange, NJ 07101, USA.
| | - Jessica Cardenas Turner
- Department of Biomedical Engineering, New Jersey Institute of Technology, 323 Martin Luther King Boulevard, Newark, NJ 07102, USA
| | - Treena Livingston Arinzeh
- Department of Biomedical Engineering, New Jersey Institute of Technology, 323 Martin Luther King Boulevard, Newark, NJ 07102, USA
| | - J Patrick O'Connor
- Department of Orthopaedics, Rutgers-New Jersey Medical School, Medical Sciences Building, Room E-659, 185 South Orange Avenue, Newark, NJ 07103, USA
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10
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Evran M, Sert M, Tetiker T, Akkuş G, Biçer OS. Spontaneous calcaneal fracture in patients with diabetic foot ulcer: Four cases report and review of literature. World J Clin Cases 2016; 4:181-186. [PMID: 27458594 PMCID: PMC4945589 DOI: 10.12998/wjcc.v4.i7.181] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/17/2016] [Revised: 04/05/2016] [Accepted: 06/03/2016] [Indexed: 02/05/2023] Open
Abstract
Spontaneous calcaneal fractures in diabetic patients without obvious trauma may occur, sometimes accompanying diabetic foot ulcers. In the current study we report four cases who were hospitalized for diabetic foot ulcer with concomitant calcaneal fractures. There were four diabetic patients (one type 1 and three type 2) who registered with diabetic foot ulcers with coexisting calcaneal fractures, all of which were classified as Type A according to Essex Lopresti Calcaneal Fracture Classification. Two of the patients with renal failure were in a routine dialysis program, as well as vascular compromise and osteomyelitis in all of the patients. The diabetic foot ulcer of the 61 years old osteoporotic female patient healed with local debridement, vacuum assisted closure and then epidermal growth factor while the calcaneal fracture was then followed by elastic bandage. In two patients could not prevent progression of diabetic foot ulcers and calcaneal fractures to consequent below-knee amputation. The only patient with type 1 diabetes mellitus improved with antibiotic therapy and split thickness skin grafting, while the calcaneal fracture did not heal. In the current study we aimed to emphasize the spontaneous calcaneal fractures as possible co-existing pathologies in patients with diabetic foot ulcers. After all the medical treatment, amputation below knee had to be performed in 2 patients. It should be noted that other accompanying conditions such as impaired peripheral circulation, osteomyelitis, chronic renal failure, and maybe osteoporosis is a challenge of the recovery of calcaneal fractures and accelerate the progress to amputation in diabetic patients.
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Abstract
Diabetes is associated with a number of lower extremity orthopedic conditions and complications including fractures, Charcot neuroarthropathy, plantar ulcers, and infection. These complications are of significant clinical concern in terms of morbidity, mortality, and socioeconomic costs. A review of each condition is discussed, with particular emphasis on the clinical importance, diagnostic considerations, and orthopedic treatment recommendations. The goal of the article is to provide a clinical picture of the challenges that orthopedic surgeons confront, and highlight the need for specific clinical guidelines in diabetic patients.
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Affiliation(s)
- Daniel J Gehling
- Department of Orthopaedic Surgery, University of Toledo College of Medicine, 3000 Arlington Avenue, Toledo, OH 43614, United States.
| | - Beata Lecka-Czernik
- Department of Orthopaedic Surgery, University of Toledo College of Medicine, 3000 Arlington Avenue, Toledo, OH 43614, United States; Department of Physiology and Pharmacology, University of Toledo College of Medicine, 3000 Arlington Avenue, Toledo, OH 43614, United States; Center for Diabetes and Endocrine Research, University of Toledo College of Medicine, 3000 Arlington Avenue, Toledo, OH 43614, United States
| | - Nabil A Ebraheim
- Department of Orthopaedic Surgery, University of Toledo College of Medicine, 3000 Arlington Avenue, Toledo, OH 43614, United States
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12
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Schade VL, Andersen CA. A literature-based guide to the conservative and surgical management of the acute Charcot foot and ankle. Diabet Foot Ankle 2015; 6:26627. [PMID: 25795102 PMCID: PMC4368713 DOI: 10.3402/dfa.v6.26627] [Citation(s) in RCA: 25] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/17/2014] [Revised: 01/30/2015] [Accepted: 02/01/2015] [Indexed: 02/06/2023]
Abstract
Acute Charcot neuroarthropathy of the foot and ankle presents with the insidious onset of a unilateral acutely edematous, erythematous, and warm lower extremity. The acute stages are typically defined as Eichenholtz Stage 1, or Stage 0, which was first described by Shibata et al. in 1990. The ultimate goal of treatment is maintenance of a stable, plantigrade foot which can be easily shod, minimizing the risk of callus, ulceration, infection, and amputation. The gold standard of treatment is non-weight-bearing immobilization in a total contact cast. Surgical intervention remains controversial. A review of the literature was performed to provide an evidenced-based approach to the conservative and surgical management of acute Charcot neuroarthropathy of the foot and ankle.
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Affiliation(s)
- Valerie L Schade
- Vascular/Endovascular Surgery, Madigan Army Medical Center, Tacoma, WA, USA
| | - Charles A Andersen
- Vascular/Endovascular Surgery, Madigan Army Medical Center, Tacoma, WA, USA;
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13
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Blume PA, Sumpio B, Schmidt B, Donegan R. Charcot neuroarthropathy of the foot and ankle: diagnosis and management strategies. Clin Podiatr Med Surg 2014; 31:151-72. [PMID: 24296023 DOI: 10.1016/j.cpm.2013.09.007] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/18/2023]
Abstract
This article reviews current literature discussing the etiology, pathophysiology, diagnosis and imaging, and conservative and surgical treatment of Charcot osteoarthropathy. The treatment of Charcot osteoarthropathy with concurrent osteomyelitis is also discussed.
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Affiliation(s)
- Peter A Blume
- Orthopedics and Rehabilitation, and Anesthesia, Yale School of Medicine, 20 York Street, New Haven, CT 06510, USA.
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Kaynak G, Birsel O, Güven MF, Oğüt T. An overview of the Charcot foot pathophysiology. Diabet Foot Ankle 2013; 4:21117. [PMID: 23919113 PMCID: PMC3733015 DOI: 10.3402/dfa.v4i0.21117] [Citation(s) in RCA: 50] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/12/2013] [Revised: 06/09/2013] [Accepted: 07/01/2013] [Indexed: 01/15/2023]
Abstract
Charcot arthropathy of the foot is a rare but devastating complication of diabetes that remains to be a challenging issue for the foot and ankle surgeons. Charcot foot fails to be an obvious diagnostic option that comes to mind, even in a pathognomonic clinical appearance. The rarity of the disorder, more common pathologies that mimic the condition, and the self-limiting prognosis deviate the clinician from the right diagnosis. The clinical challenges in the diagnosis of Charcot foot require in-depth investigations of its enigmatic nature to establish useful guidelines. Yet, this goal seems to be beyond reach, without a holistic view of the immense literature concerning the pathophysiology of the disorder. The primary objective of this article is to put together and review the recent advancements about the etiology and intrinsic mechanisms of diabetic Charcot foot.
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Affiliation(s)
- Gökhan Kaynak
- Cerrahpasa Faculty of Medicine, Department of Orthopedics and Traumatology, Istanbul University, Istanbul, Turkey
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16
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Papanas N, Maltezos E. Etiology, pathophysiology and classifications of the diabetic Charcot foot. Diabet Foot Ankle 2013; 4:20872. [PMID: 23705058 PMCID: PMC3661901 DOI: 10.3402/dfa.v4i0.20872] [Citation(s) in RCA: 44] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2013] [Revised: 04/18/2013] [Accepted: 04/25/2013] [Indexed: 12/20/2022]
Abstract
In people with diabetes mellitus, the Charcot foot is a specific manifestation of peripheral neuropathy that may involve autonomic neuropathy with high blood flow to the foot, leading to increased bone resorption. It may also involve peripheral somatic polyneuropathy with loss of protective sensation and high risk of unrecognized acute or chronic minor trauma. In both cases, there is excess local inflammatory response to foot injury, resulting in local osteoporosis. In the Charcot foot, the acute and chronic phases have been described. The former is characterized by local erythema, edema, and marked temperature elevation, while pain is not a prominent symptom. In the latter, signs of inflammation gradually recede and deformities may develop, increasing the risk of foot ulceration. The most common anatomical classification describes five patterns, according to the localization of bone and joint pathology. This review article aims to provide a brief overview of the diabetic Charcot foot in terms of etiology, pathophysiology, and classification.
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Affiliation(s)
- Nikolaos Papanas
- Outpatient Clinic of the Diabetic Foot, Second Department of Internal Medicine, Democritus University of Thrace, Alexandroupolis, Greece
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MRI of the cuboid bone: analysis of changes in diabetic versus non-diabetic patients and their clinical significance. Eur J Radiol 2011; 81:2771-5. [PMID: 22078792 DOI: 10.1016/j.ejrad.2011.10.001] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/18/2011] [Revised: 10/05/2011] [Accepted: 10/08/2011] [Indexed: 11/20/2022]
Abstract
OBJECTIVES (1) To investigate the association between diabetes and marrow changes in the cuboid; and (2) to evaluate the influence of age, gender, body mass index (BMI) and use of insulin in the occurrence of marrow changes in the cuboid. RESEARCH DESIGN AND METHODS MR and X-ray foot examinations of 237 patients [94 males, 143 females; mean age, 47.1 years (range 16-93 years)], five of whom underwent bilateral examinations, were reviewed. MR and radiographic studies were analyzed for the presence of marrow edema and fractures in the cuboid. Findings were correlated with demographic data (age, gender) and clinical information (BMI and use of insulin). RESULTS Two hundred and forty two feet - 69 diabetic and 173 non-diabetic - were retrospectively evaluated. There was a higher prevalence of marrow edema and fractures in the diabetic cuboid (n=31, 45%) compared to non-diabetic cuboid (n=25, 14%, p=0.02). A fracture line was seen in fourteen (20%) diabetic cuboid bones compared to 4 (2%) in non-diabetic cuboid bones (p<0.0001). Eleven (79%) cases of cuboid fractures in the diabetic population were radiographically occult. Multivariate data analysis revealed an adjusted odds ratio of 4.416 (95% CI; 2.307, 8.454) for the relationship between marrow changes (edema and fractures) in the cuboid and diabetes. For each year of age, the odds of changes in the cuboid increased by 2.2% (95% CI; 1.001, 1.044). CONCLUSION Despite not bearing weight, the cuboid bone is more vulnerable to marrow edema and fractures in diabetic patients compared to non-diabetic patients. Age seems to be an influential factor.
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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. [PMID: 21274711 DOI: 10.1007/s00256-010-1092-0] [Citation(s) in RCA: 35] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/01/2010] [Revised: 12/21/2010] [Accepted: 12/27/2010] [Indexed: 02/02/2023]
Abstract
PURPOSE To evaluate the usefulness of magnetic resonance imaging (MRI) in assessing the level of activity of acute Charcot foot, monitoring treatment response and predicting healing time. MATERIALS AND METHODS Forty diabetic patients with acute Charcot foot were prospectively enrolled. Patients underwent limb immobilization and were followed every 3 months by clinical examination (skin temperature and circumferences) and MRI. MR protocol included T1-weighted and fast spin echo inversion recovery (FSE-IR) sequences, and a dynamic study (fast spoiled gradient echo), after gadolinium administration (0.1 ml/kg). The contrast medium uptake rate at D-MRI and the signal intensity (SI) ratio on the FSE-IR sequence were measured. RESULTS At baseline, mean contrast medium uptake rate was 136 ± 49.7% and the mean SI ratio was 5 ± 3. A high intra- and inter-observer agreement was found for the contrast medium uptake rate, whereas a low agreement was observed for the SI ratio. At 3 months' follow-up, reduction of the contrast medium uptake rate was observed in all patients with improved clinical findings (n = 34), whereas the SI ratio was reduced in 15/34 (44.1%) patients. Mean healing time was significantly related to the baseline contrast medium uptake rate (P=0.005); it was 5.3 ± 2.7 months in patients with contrast medium uptake rate ≤ 100%, compared with 9.1 ± 2.5 months in the remaining patients (P=0.0003). CONCLUSIONS Contrast medium uptake rate obtained at D-MRI represents a reproducible parameter that is reliable for predicting and monitoring treatment outcome in acute Charcot foot.
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Affiliation(s)
- Virna Zampa
- Department of Diagnostic and Interventional Radiology, University of Pisa, Via Paradisa 2, 56127, Pisa, Italy.
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Gouveri E, Papanas N. Charcot osteoarthropathy in diabetes: A brief review with an emphasis on clinical practice. World J Diabetes 2011; 2:59-65. [PMID: 21691556 PMCID: PMC3116009 DOI: 10.4239/wjd.v2.i5.59] [Citation(s) in RCA: 75] [Impact Index Per Article: 5.4] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/11/2010] [Revised: 03/26/2011] [Accepted: 04/01/2011] [Indexed: 02/05/2023] Open
Abstract
Charcot osteoarthropathy (COA) is a potentially limbthreatening condition that mainly affects diabetic patients with neuropathy. In everyday practice, it presents as a red, hot, swollen foot, usually painless, and is frequently triggered by trivial injury. Its etiology is traditionally attributed to impairment of either the autonomic nervous system, leading to increased blood flow and bone resorption, or of the peripheral nervous system, whereby loss of pain and protective sensation render the foot susceptible to repeated injury. More recently, excessive local inflammation is thought to play a decisive role. Diagnosis is based on clinical manifestation and imaging studies (plain X-rays, bone scan, Magnetic Resonance Imaging). The mainstay of management is immediate off-loading, while surgery is usually reserved for chronic cases with irreversible deformities and/or joint instability. The aim of this review is to provide an overview of COA in terms of pathogenesis, classification and clinical presentation, diagnosis and treatment, with an emphasis on the high suspicion required by clinicians for timely recognition to avoid further complications.
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Affiliation(s)
- Evanthia Gouveri
- Evanthia Gouveri, Nikolaos Papanas, Outpatient Clinic of the Diabetic Foot, Second Department of Internal Medicine, Democritus University of Thrace, Alexandroupolis 68100, Greece
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Poll LW, Weber P, Böhm HJ, Ghassem-Zadeh N, Chantelau EA. Sudeck's disease stage 1, or diabetic Charcot's foot stage 0? Case report and assessment of the diagnostic value of MRI. Diabetol Metab Syndr 2010; 2:60. [PMID: 20923545 PMCID: PMC2958966 DOI: 10.1186/1758-5996-2-60] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/19/2010] [Accepted: 10/05/2010] [Indexed: 11/10/2022] Open
Abstract
BACKGROUND The diagnosis of Sudeck's syndrome stage 1 (nowadays termed complex regional pain syndrome I, abbreviated CRPS I) is based on clinical features, namely swelling and pain in a limb. Plain X-ray may be normal. In the absence of pain sensitivity, e.g. in diabetic neuropathy, CRPS I of the foot can be mistaken for Charcot's foot stage 0 (so-called neuro-osteoarthropathy). CASE PRESENTATION The case of a type-1 diabetic woman is reported, in whom CRPS I following a calcaneal fracture was mistaken for Charcot's osteoarthropathy (because of bone marrow edema displayed by conventional MR imaging). In addition, a review is presented on 6 consecutive cases with CRPS I of the foot, and on 20 cases with Charcot's foot stage 0, with particular emphasis on MR imaging findings. The number of bones per foot affected with marrow edema was similar in either condition, with a tendency towards a more patchy, diffuse distribution of bone marrow edema in CRPS I. Bone marrow edema apparently regressed more promptly in response to treatment in Charcot's foot stage 0. CONCLUSION Differentiation of CRPS I from Charcot's foot stage 0 remains a diagnostic dilemma in patients with pain insensitivity. Conventional MRI may be helpful, when repeated for monitoring the treatment response.
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Affiliation(s)
- Ludger W Poll
- Department of Radiology, Berufsgenossenschaftliche Unfallklinik Duisburg GmbH, Grossenbaumer Allee 250, D-47249 Duisburg, Germany
| | - Philipp Weber
- Department of Traumatology, Orthopedic and Reconstructive Surgery, Berufsgenossenschaftliche Unfallklinik Duisburg GmbH, Grossenbaumer Allee 250, D-47249 Duisburg, Germany
| | - Hermann-Josef Böhm
- Department of Traumatology, Orthopedic and Reconstructive Surgery, Berufsgenossenschaftliche Unfallklinik Duisburg GmbH, Grossenbaumer Allee 250, D-47249 Duisburg, Germany
| | - Nahid Ghassem-Zadeh
- Diabetes Foot Clinic, Heinrich-Heine-University Düsseldorf, MNR-Klinik, P.O. Box 10 10 07, D-40001 Düsseldorf, Germany
- Praxis Dr. Fleischer, Herderstr 71B, D-40237 Düsseldorf, Germany
| | - Ernst A Chantelau
- Diabetes Foot Clinic, Heinrich-Heine-University Düsseldorf, MNR-Klinik, P.O. Box 10 10 07, D-40001 Düsseldorf, Germany
- Holthorster Weg 16, D-28717 Bremen, Germany
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Wukich DK, Sung W. Charcot arthropathy of the foot and ankle: modern concepts and management review. J Diabetes Complications 2009; 23:409-26. [PMID: 18930414 DOI: 10.1016/j.jdiacomp.2008.09.004] [Citation(s) in RCA: 142] [Impact Index Per Article: 8.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/04/2008] [Revised: 08/14/2008] [Accepted: 09/13/2008] [Indexed: 01/19/2023]
Abstract
Charcot arthropathy (Charcot neuroarthropathy, diabetic neuropathic osteoarthropathy, or neuropathic arthropathy) remains a poorly understood disease, although recent research has improved our level of knowledge regarding its etiology and treatment. The effects of Charcot arthropathy are almost exclusively seen in the foot and ankle, and the diagnosis is commonly missed upon initial presentation. It has been well established that this complication of diabetes mellitus severely reduces the overall quality of life and dramatically increases the morbidity and mortality of patients. However, there are few high-level evidence studies to support management and treatment options at this point in time. The goal of this study is to evaluate the modern concepts of Charcot arthropathy through a review of the available literature and to integrate a perspective of management from the authors' extensive experience.
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Affiliation(s)
- Dane K Wukich
- UPMC Comprehensive Foot and Ankle Center, University of Pittsburgh School of Medicine, Pittsburgh, PA 15203, USA.
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Type 1 diabetes in young rats leads to progressive trabecular bone loss, cessation of cortical bone growth, and diminished whole bone strength and fatigue life. J Bone Miner Res 2009; 24:1618-27. [PMID: 19338453 PMCID: PMC2730931 DOI: 10.1359/jbmr.090316] [Citation(s) in RCA: 114] [Impact Index Per Article: 7.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
People with diabetes have increased risk of fracture disproportionate to BMD, suggesting reduced material strength (quality). We quantified the skeletal effects of type 1 diabetes in the rat. Fischer 344 and Sprague-Dawley rats (12 wk of age) were injected with either vehicle (Control) or streptozotocin (Diabetic). Forelimbs were scanned at 0, 4, 8, and 12 wk using pQCT. Rats were killed after 12 wk. We observed progressive osteopenia in diabetic rats. Trabecular osteopenia was caused by bone loss: volumetric BMD decreased progressively with time in diabetic rats but was constant in controls. Cortical osteopenia was caused by premature arrest of cortical expansion: cortical area did not increase after 4-8 wk in diabetic rats but continued to increase in controls. Postmortem muCT showed a 60% reduction in proximal tibial trabecular BV/TV in diabetic versus control rats, whereas moments of inertia of the ulnar and femoral diaphysis were reduced approximately 30%. Monotonic bending tests indicated that ulna and femora from diabetic animals were approximately 25% less stiff and strong versus controls. Estimates of material properties indicated no changes in elastic modulus or ultimate stress but modest ( approximately 10%) declines in yield stress for diabetic bone. These changes were associated with a approximately 50% increase in the nonenzymatic collagen cross-link pentosidine. Last, cyclic testing showed diminished fatigue life in diabetic bones at the structural (force) level but not at the material (stress) level. In summary, type 1 diabetes, left untreated, causes trabecular bone loss and a reduction in diaphyseal growth. Diabetic bone has greatly increased nonenzymatic collagen cross-links but only modestly reduced material properties. The loss of whole bone strength under both monotonic and fatigue loading is attributed mainly to reduced bone size.
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Abstract
Patients with diabetes mellitus have higher complication rates following both open and closed management of ankle fractures. Diabetic patients with neuropathy or vasculopathy have higher complication rates than both diabetic patients without these comorbidities and nondiabetic patients. Unstable ankle fractures in diabetic patients without neuropathy or vasculopathy are best treated with open reduction and internal fixation with use of standard techniques. Patients with neuropathy or vasculopathy are at increased risk for both soft-tissue and osseous complications, including delayed union and nonunion. Careful soft-tissue management as well as stable, rigid internal fixation are crucial to obtaining a good outcome. Prolonged non-weight-bearing and subsequently protected weight-bearing are recommended following both operative and nonoperative management of ankle fractures in patients with diabetes.
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Affiliation(s)
- Dane K Wukich
- University of Pittsburgh Medical Center Comprehensive Foot and Ankle Center, Roesch-Taylor Building, Suite 7300, 2100 Jane Street, Pittsburgh, PA 15203, USA.
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Chantelau E, Kimmerle R, Poll LW. Nonoperative treatment of neuro-osteoarthropathy of the foot: do we need new criteria? Clin Podiatr Med Surg 2007; 24:483-503, ix. [PMID: 17613387 DOI: 10.1016/j.cpm.2007.03.006] [Citation(s) in RCA: 16] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/26/2022]
Abstract
The worst manifestation of neuro-osteoarthropathy of the pain-insensitive foot is the Charcot foot with its devastating osteoarticular destructions and irreversible deformities. New diagnostic tools such as MRI have revealed that mechanical injury and overuse is the origin of the condition. Traditionally, only feet with bone and joint damage apparent on plain radiographs (fracture and dislocation injuries) have undergone nonoperative treatment with off-loading and immobilization; however, treating painless, seemingly asymptomatic nonfracture injuries (bone bruise or bone marrow edema) with off-loading and immobilization has proven highly effective in preventing the Charcot foot. Whether pharmaceutical treatment has a role in terms of prevention or healing of osteoarticular destructions remains to be demonstrated.
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Affiliation(s)
- Ernst Chantelau
- Diabetes Foot Clinic, Department of Endocrinology, Diabetes and Rheumatology, Heinrich-Heine-University Düsseldorf, PO Box 10 10 07, D-40001 Düsseldorf, Germany.
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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. [PMID: 17216478 DOI: 10.1007/s00402-006-0271-x] [Citation(s) in RCA: 44] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/31/2006] [Indexed: 12/19/2022]
Abstract
BACKGROUND Bone stress injuries are rarely being diagnosed in patients with sensory neuropathy, most likely because they may be silent in terms of pain. Load-related pain is considered a key feature of any bone stress injury, a symptom, which may be partially or completely absent in subjects with sensory neuropathy (loss of protective sensation). We evaluated the clinical course of bone stress injuries in insensitive feet in diabetic patients with polyneuropathy. METHODS We investigated 12 consecutive diabetic patients with bone stress injuries of the foot (bone marrow edema, bone bruise and microtrabecular fractures, on magnetic resonance imaging MRI), which were undetectable on plain X-ray. All patients suffered from diabetic polyneuropathy, none of them had an active foot ulcer. RESULTS The patients presented with a swollen foot, which was only mildly painful and did not prevent them from walking. Complaints were related to the swelling, which increased during load-bearing. In seven cases, a traumatic event preceding the onset of symptoms could be ascertained. MRI disclosed stress injuries in 2.5 (1-8) [median (range)] bones per foot. In 11 patients, treatment was started immediately by off-loading with total contact cast for 17 (8-52) weeks, followed by gradual increase in weight bearing. One patient unfortunately received off-loading treatment only after deforming fractures had developed. All bone injuries healed uneventuelly in eight patients, and with residual mild osteoarthrosis in three patients without gross deformities. However, the untreated patient developed severe Charcot foot deformity. CONCLUSIONS In diabetic patients with polyneuropathy, symptoms of bone stress injuries of the foot are atypical, in that there is load-related swelling rather than load-related pain. Immediate diagnosis, and treatment with off-loading, leads to a restitutio ad integrum like in non-neuropathic patients. Delayed cessation of overuse, however, may cause irreversible joint and bone damage (Charcot foot).
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Affiliation(s)
- E Chantelau
- Diabetes Foot Clinic, Department of Endocrinology, Diabetes and Rheumatology, Heinrich-Heine-University of Düssseldorf, Düsseldorf, Germany.
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