Imaging of Charcot foot Clinics 08(1)

Clin Podiatr Med Surg

Imaging of the Charcot Foot

Lee C. Rogers, DPM*, Nicholas J. Bevilacqua, DPMAmputation Prevention Center at Broadlawns Medical Center, 1801 Hickman Road,

Des Moines, IA 50314, USA

Charcot’s foot is a serious problem that causes considerable morbidityand may lead to limb loss. Arriving at a definitive diagnosis can be challeng-ing. Because of the difficulty in diagnosis, one study showed the diagnosiscan be delayed on an average of 29 weeks [1]. Given the progressive, destruc-tive nature of Charcot’s arthropathy, this delay can result in advancingdeformity, ulceration, infection, and place the limb at risk for amputation.

Syphilis has been referred to as the ‘‘great imitator’’ [2]. Charcot’s foot isalso an ‘‘imitator.’’ Early on, with a hot, red, swollen foot it is commonlymisdiagnosed as cellulitis, deep venous thrombosis, or acute gout. Later,the radiographic bone destruction is often confused with osteomyelitis.Complicating the matter is the fact that infection and Charcot’s arthropathycan coexist in the same extremity. Although clinical signs and symptoms andhistorical information are crucial, this article focuses on the imaging modal-ities that can aid practitioners in arriving at an early diagnosis and how todifferentiate Charcot’s arthropathy from osteomyelitis of the feet. The arti-cle is divided into sections by imaging modality.

25 (2008) 263–274

Plain radiography

In 1966, American orthopedist Sidney Eichenholtz described a logical andpredictable sequence of changes in ‘‘Charcot joints’’ observed by means ofserial radiographs. For the purpose of classification, he divided these changesinto three stages (Table 1). Stage 1 (stage of development) shows debrisformation at the articular margins followed by fragmentation of the subchon-dral bone and capsular distention. Stage 2 (stage of coalescence) is character-ized by absorption of fine debris and fusion of large fragments to adjacentbones; the bone ends become sclerotic. Stage 3 (stage of reconstruction) is

* Corresponding author.

E-mail address: [email protected] (L.C. Rogers).

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Table 1

Eichenholtz classification

Stage 1 Stage of development Bone fragmentation

Stage 2 Stage of coalescence Absorption of bone fragments and coalescence

to adjacent bone

Stage 3 Stage of reconstruction Remodeling and rounding of bone ends

264 ROGERS & BEVILACQUA

characterized by rounding of the bone ends with decrease in sclerosis [3]. Thisstaging system has become widely accepted and is now known as the ‘‘Eichen-holtz classification’’ (Figs. 1–3).

In 1990, Shibata and coworkers [4] reviewed patients who had anarthrodesis of one or both ankles for leprotic neuroarthropathy and addedan additional, earlier stage to Eichenholtz’s classification. Shibata describeda stage 0, in which there are no radiographic changes noted, but there iswarmth, swelling, and instability. Yu and Hudson [5] described stage 0 asan acute sprain or fracture in the presence of neuropathy and reviewedthe evaluation and treatment of this stage in Charcot’s foot and ankle. Sellaand Barrette [6] developed another classification scheme, also based onradiographic findings, which includes an early phase consisting of localizedheat and swelling.

The Eichenholtz classification is based solely on radiographic findingsand its lack of clinical correlation is a weakness of the staging system.The diagnosis should be made on clinical presentation consisting of edema,redness, and elevated temperature. Plain radiographs are an important tool,however, in detecting, staging, and monitoring Charcot’s foot [7]. Addition-ally, radiographs are inexpensive and universally available and may be usedto describe the anatomic pattern of involvement. Sanders and Frykberg [8]described five different anatomic patterns: involvement in the forefoot (pat-tern 1); the tarsometatarsal joint (pattern 2); the naviculocunieform andmidtarsal joints (pattern 3); the ankle joint (pattern 4); and the posteriorcalcaneous (pattern 5).

Fig. 1. Eichenholtz stage 1 showing fragmentation of the navicular-cuneiform joint (arrow).

Fig. 2. Eichenholtz stage 2 in the same patient as Fig. 1. Note the absorption of the debris and

the sclerosis of the periarticular bone.

265IMAGING OF THE CHARCOT FOOT

The tarsometatarsal joint is the most commonly involved joint [9]. Anequinus deformity at the ankle is a key contributor to the collapse at thisanatomic level. This biomechanical factor, along with sensory neuropathyand the repetitive trauma of walking, create a condition conducive to mid-foot collapse [10]. A detailed radiographic analysis of the angular relation-ships of the bones is necessary and important for monitoring the progressionof deformity. Often, the calcaneal inclination decreases with equinus at theankle. Measurement of talar–first metatarsal angle may reveal dislocation ofthe midfoot (Fig. 4).

Fig. 3. Eichenholtz stage 3 characterized by rounding of the bone edges and consolidation.

Fig. 4. A lateral radiographic view of the foot showing (A) decrease in the calcaneal inclination

angle and (B) dislocation and breaking of the talar–first metatarsal angle.


Early stages are not as easily recognizable. Physicians need to havea heightened index of suspicion to detect all early Charcot’s feet. Failureto recognize early, stage 0 Charcot may result in progressive deformitywith deleterious effects. Radiographs should not be relied on to rule outCharcot’s foot.

An adjunctive finding to the radiographic bone destruction associatedwith Charcot’s foot is the presence of medial calcific sclerosis (vascular cal-cification) on radiographs, which occurs in up to 90% of cases (Fig. 5) [11].It is increasingly evident that receptor activator nuclear factor kappa-Bligand is up-regulated in Charcot’s foot causing osteolysis, and the samemolecule may be responsible for calcification of vascular smooth musclecells [12]. This process leads to a decrease in bone mineral density and depo-sition of minerals (calcium) into the intima media of the arterial wall.

CT

Although CT has not been advocated in the literature as the diagnosticmodality of choice for Charcot’s foot, it can be helpful. CT can detect early

Fig. 5. Medial calcific sclerosis of the posterior tibial and medial plantar arteries (arrows).


intra-articular fractures not visualized by plain radiography [13]. Pseudocystformation may be evident [14] but can be difficult to distinguish fromosteomyelitis. CT is most useful in cases where surgical reconstruction isplanned and not necessarily for the diagnosis of Charcot’s foot. The addi-tion of three-dimensional computer-generated images may also help in pre-operative planning (Fig. 6).

MRI

MRI is becoming increasingly popular for the investigation of osteomy-elitis in the feet because it has a high sensitivity (77%–100%) [15–17] andspecificity (80%–100%) [15,18,19] for the disease. Additionally, it producesan accurate anatomic picture of the extent of the infection. It is useful forboth the diagnosis of osteomyelitis and the preoperative planning of surgicalresection. The difficulty is distinguishing osteomyelitis from Charcot’sarthropathy, because both produce similar signal changes on MRI. Char-cot’s foot and osteomyelitis are characterized by a decrease in intensity inthe marrow on T1-weighted images and increased signal intensity on T2-weighted images (Fig. 7) [20]. This confusion has led some authors to con-clude that Charcot’s foot and osteomyelitis are indistinguishable by MRI[21]. Hans Peter Ledermann, who has published a great deal of work onMRI in the diabetic foot, is a proponent of the capability of MRI to differ-entiate osteomyelitis from Charcot’s foot. Ledermann advocates the use ofsecondary signs of osteomyelitis, which can improve specificity [22]. Becauseover 90% of cases of osteomyelitis are caused by contiguous spread ofinfection from skin ulcerations, he evaluates the images for adjacent softtissue defects and tracts with extensions to bone [23]. Other clues to considerare that (1) osteomyelitis predominately affects one bone, Charcot’s

Fig. 6. Three-dimensional CT of a foot with a previous transmetatarsal amputation and

a Charcot’s ankle fused in a plantarflexed position. Note the exuberant bone formation and

ossification of the interosseus membrane.

Fig. 7. (A) Dorsoplantar radiograph of a patient with fragmentation at the second metatarsal-

cuneiform joint (arrow), secondary to stress from previous partial first ray amputation. (B) Coro-

nalCTat the tarsometatarsal scan revealingmore fragmentation thanvisible byplain radiography.

(C) CoronalMRI of themidfoot (T2-weighted image) significant formarrow edema of the second

and thirdmetatarsal shafts (arrow). (D) Three-phase 99Tc bone scanuncovering activity across the

entire tarsometatarsal joint, more extensive than previous imaging.


arthropathy is more commonly diffuse; (2) deformity is common withCharcot’s foot, but uncommon with osteomyelitis; and (3) Charcot’s foottypically affects the midfoot, whereas osteomyelitis more commonly affectsthe toes and forefoot [20].

Chantelau and Poll [24] comparedMRIwith plain radiographs in 26 Char-cot’s feet of different stages. In stage 0, radiographs displayed normal bone.MRI, by contrast, showed advanced stress injuries and edema in the bone,and edema of adjacent soft tissue and joint effusion. In stages 1 and 2, MRIconfirmed radiographic findings and in addition showed bone and soft tissueedema, and joint effusion, which were not evident on radiographs. In stage 3,MRI again confirmed radiographic findings and additionally noted boneedema that was not visible on radiograph [24]. This study demonstrated thesuperiority of MRI over radiography for assessing early, stage 0 Charcot’sfoot, but merely confirmed the radiographic finding in later stages.


Bone scintigraphy

The term ‘‘bone scan’’ refers to any study where a radiolabel is used, whichlocalizes to osseous tissue to diagnose bone diseases. There are many types ofbone scans, including traditional 99technetium-labeled scans, 67galium citratescans, 111indium scan, Cipro-labeled scans, sulfur-colloid marrow scans, and99mtechnetium HMPAO ‘‘leukocyte labeled’’ scans. This section reviews themost common and accessible bone scans.

The traditional 99technetium bone scan is highly sensitive for osseouspathology but not specific (Fig. 8). Its sensitivity can be as high as 100%for osteomyelitis, but specificities range from 25% to 38% [25,26]. The threeimaging phases of the 99Tc bone scan are the blood flow, blood pool, anddelayed phases. The blood flow image is taken within seconds of infusionof the radiolabel and confirms the flow through the macrovasculature.The blood pool phase is taken several minutes later and can show increasedpooling in the soft tissue in the case of inflammation, including infection.The delayed image is obtained 3 to 4 hours later and can reveal uptake of

Fig. 8. (A) Photograph of a female diabetic patient with an erythematous, edematous ankle

and a rupture bulla at the lateral malleolus. (B) Normal ankle radiograph of the same patient.

(C) Increased signal in the lateral ankle/distal fibula noted with 99Tc three-phase bone scan.


the radiolabel in areas of increased bone turnover. Additionally, a fourthphase or 24-hour image can be used if there is too much background activityto discern the anatomic location of the increased uptake (Fig. 9) [27].

Leukocyte-labeled scans are more specific for osteomyelitis, but may havea lower sensitivity than 99Tc scans. 111Indium bone scans are sensitive andspecific for osteomyelitis. Sensitivities range from 89% to 100% and specific-ities from 69% to 80% [28,29]. Seabold and colleagues [21] used traditional99Tc and 111In scans to differentiate Charcot’s changes from osteomyelitisin 14 patients with clinically or radiographically diagnosed Charcot’s foot.The sensitivity for osteomyelitis was 80% and the specificity was 54% [30].

99mTc HMPAO (Ceretec) scans require the white blood cells to be labeledex vivo, then reinfused, which is more time consuming. The sensitivity andspecificity for osteomyelitis in the foot are very favorable. One study of 42patients with diabetic foot infections found a sensitivity of 88.4% and a spec-ificity of 96.6% [31]. Poirier and colleagues [32] reported similar results in 75patients, with the scan being 92.6% sensitive and 97.6% specific. They addedthat Charcot’s neuroarthropathy did not affect the performance of the scan.

Positron emission tomography

There has been an explosion of literature and uses for positron emissiontomography (PET) using radiolabeled glucose (18F-FDG). This makes thescan very useful as a physiologic and functional scan for cancer and otherdiseases that increase local cellular metabolism and glucose uptake. Its lim-itation has been the poor anatomic resolution, leading to the use of hybridPET-CT where a CT is performed at the same instance and image slices canbe compared side-by-side.

In the diabetic foot, there are limited data on the use of PET.What may bemost useful is the ability of 18F-FDG PET to differentiate osteomyelitis fromCharcot’s foot based on the intensity of the metabolism of 18F-FDG. Keidar

Fig. 9. (A) Delayed image of a diabetic patient with a plantar midfoot ulcer. Note the high

amount of background tracer. (B) A 24-hour image in the same patient, which sharpened the

image considerably.

Table 2

Sensitivity and specificity of diagnosing osteomyelitis in the feet by various imaging modalities

% Sensitivity % Specificity

MRI [15–19] 77–100 80–10099Tc 3-phase bone scan [25,26] 100 25–38111In bone scan [28,29] 89–100 69–8099mTc HMPAO [31,32] 88–93 97–98


and colleagues [33] evaluated 14 patients with suspected foot infection forosteomyelitis. Hybrid PET-CT correctly identified osteomyelitis in fourpatients, confirmed infection in soft tissue in five patients, and ruled outinfection in four patients. In the one remaining patient, PET-CT was ablecorrectly to differentiate the osseous destruction of Charcot’s arthropathyfrom osteomyelitis. Hopfner and colleagues [34,35] published two studies(there may be duplication of data in the later study) on the use of PET to

Fig. 10. Clinical flowchart to guide the choice of imaging modality to aid in the differentiation

of Charcot’s arthropathy or osteomyelitis of the feet. *It is controversial if MRI can accurately

differentiate Charcot’s foot from osteomyelitis of the feet. OM, osteomyelitis; 99Tc bone scan,99Technitium three-phase bone scan; 111In, 111Indium bone scan; 99mTc HMPAO, 99mTc

HMPAO leukocyte scan. (From Rogers LC, Bevilacqua NJ. The diagnosis of Charcot foot.

Clin Podiatr Med Surg 2008;25:43–51; with permission.)

Fig. 11. (A) Photograph of a male diabetic patient with a plantar cuboid ulcer serving as a por-

tal of entry increasing the likelihood for osteomyelitis. (B) Dorsoplantar radiograph in the same

patient showing osseous destruction at the midfoot consistent with Charcot’s foot, osteomyeli-

tis, or both. (C) A 99mTc HMPAO ‘‘leukocyte’’ scan, which is negative for osteomyelitis.


identify Charcot’s lesions. The authors confirmed the lesions surgically andfound that 37 (95%) of 39 lesions were identified successfully using PET.

The ability to differentiate osteomyelitis from Charcot’s foot lies in thestandardized uptake value, which may differ between the two conditions;and software can detect these variances. Hopfner and colleagues foundthat the standardized uptake value averaged 1.8 (0.5–4.1) [34] and 1.2(0.5–2.9) [35] for Charcot’s foot. Keidar and colleagues [33] reported anaverage standardized uptake value of 5.4 (1.4–11.1) in diabetic foot infec-tions. Keidar’s only patient with Charcot’s arthropathy had a standardizeduptake value of 1.4, the lowest in the study. By contrast, glucose metabolismis high in osteomyelitis [36], which may make PET a useful tool to differen-tiate infection from Charcot’s arthropathy.

Summary

Making the diagnosis of Charcot’s foot based on imaging is straightfor-ward, but can be complicated by concomitant osteomyelitis. Table 2 presentsall the modalities described previously and reports their usefulness in


diagnosis of Charcot’s foot, osteomyelitis, or both. Fig. 10 shows a flowcharton how to use imaging to diagnose Charcot’s foot and distinguish it from os-teomyelitis, if necessary. On the presentation of an erythematous, edematousfoot without an ulcer or radiographic changes, an MRI or 99Tc bone scanis useful to rule in (or rule out in the case of 99Tc scans) bony destruction.Feet that have no open wounds (or a history of one) and show radiographicevidence of bone destruction at the midfoot, can accurately be diagnosed asCharcot’s foot. In the presence of an open wound, however, especially onethat extends to bone, further diagnostic study is required. MRI may beperformed, but it is difficult to differentiate Charcot’s changes from osteomy-elitis. 99Tc bone scan are useless if there is already bone destruction con-firmed by plain radiographs, because they likely show increased uptakeand fail to narrow the differential diagnosis. In these cases, 111In or 99mTcHMPAO scans are sensitive and specific for osteomyelitis, even in the pres-ence of concomitant Charcot’s arthropathy (Fig. 11). CT scans and MRI canbe useful for presurgical planning. PET scans, although not widely availableat present, may be the future in imaging of Charcot’s foot because earlyevidence seems to show that this scan can reliably diagnose Charcot’s footand osteomyelitis, and most importantly differentiate between the two.

References

[1] Pakarinen TK, LaineHJ, Honkonen SE, et al. Charcot arthropathy of the diabetic foot: cur-

rent concepts and review of 36 cases. Scand J Surg 2002;91(2):195–201.

[2] Fitzgerald F. The great imitator, syphilis. West J Med 1981;134(5):424–32.

[3] Eichenholtz SN. Charcot joints. Springfield (IL): Charles C. Thomas Publisher; 1966. p. 7–8.

[4] Shibata T, Tada K, Hashizume C. The results of arthrodesis of the ankle for leprotic

neuroarthropathy. J Bone Joint Surg Am 1990;72A:749–56.

[5] YuGV,Hudson JR. Evaluation and treatment of stage 0 Charcot’s neuroarthropathy of the

foot and ankle. J Am Podiatr Med Assoc 2002;92(4):210–20.

[6] 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(1):34–40.

[7] ArmstrongDG, Peters EJ. Charcot’s arthropathy of the foot. J AmPodiatrMedAssoc 2002;

92(7):390–4.

[8] Sanders LJ, Frykberg RG. The Charcot foot. The high risk foot in diabetes mellitus. In:

Frykberg RG, editor. New York: Churchill Livingstone; 1991. p. 325–35.

[9] ArmstrongDG, ToddWF, Lavery LA, et al. The natural history of acute Charcot’s arthrop-

athy in a diabetic foot specialty clinic. Diabet Med 1997;14:357–63.

[10] Armstrong DG, Stacpoole-Shea S, Nguyen H, et al. Lengthening of the Achilles tendon in

diabetic patients who are at high risk for ulceration of the foot. J Bone Joint Surg Am

1999;81(4):535–8.

[11] Clouse ME, Gramm HF, Legg M, et al. Diabetic osteoarthropathy: clinical and roentgeno-

graphic observations in90cases.AmJRoentgenolRadiumTherNuclMed1974;121(1):22–34.

[12] Jeffcoate W. Vascular calcification and osteolysis in diabetic neuropathy: is RANK-L the

missing link? Diabetologia 2004;47(9):1488–92.

[13] Chantelau E. The perils of procrastination: effects of early vs. delayed detection and

treatment of incipient Charcot fracture. Diabet Med 2005;22(12):1707–12.

[14] AmitalH,ApplbaumYH, Bar-OnH, et al. Inside aCharcot joint. IsrMedAssoc J 2003;5(6):

458–9.


[15] Levine SE, Neagle CE, Esterhai JL, et al. Magnetic resonance imaging for the diagnosis of

osteomyelitis in the diabetic patient with a foot ulcer. Foot Ankle Int 1994;15(3):151–6.

[16] Weinstein D, Wang A, Chambers R, et al. Evaluation of magnetic resonance imaging in the

diagnosis of osteomyelitis in diabetic foot infections. Foot Ankle 1993;14(1):18–22.

[17] Yuh WT, Corson JD, Baraniewski HM, et al. Osteomyelitis of the foot in diabetic patients:

evaluation with plain film, 99mTc-MDP bone scintigraphy, and MR imaging. AJR Am J

Roentgenol 1989;152(4):795–800.

[18] MorrisonWB, SchweitzerME,WapnerKL, et al. Osteomyelitis in feet of diabetics: clinical ac-

curacy, surgical utility, and cost-effectiveness ofMR imaging. Radiology 1995;196(2):557–64.

[19] Croll SD, Nicholas GG, Osborne MA, et al. Role of magnetic resonance imaging in the di-

agnosis of osteomyelitis in diabetic foot infections. J Vasc Surg 1996;24(2):266–70.

[20] Ledermann HP, Morrison WB. Differential diagnosis of pedal osteomyelitis and diabetic

neuroarthropathy: MR Imaging. Semin Musculoskelet Radiol 2005;9(3):272–83.

[21] Seabold JE, Flickinger FW, Kao SC, et al. Indium-111-leukocyte/technetium-99m-MDP

bone and magnetic resonance imaging: difficulty of diagnosing osteomyelitis in patients

with neuropathic osteoarthropathy. J Nucl Med 1990;31(5):549–56.

[22] Morrison WB, Schweitzer ME, Batte WG, et al. Osteomyelitis of the foot: relative impor-

tance of primary and secondary MR imaging signs. Radiology 1998;207(3):625–32.

[23] Ledermann HP, Morrison WB, Schweitzer ME. MR image analysis of pedal osteomyelitis:

distribution, patterns of spread, and frequency of associated ulceration and septic arthritis.

Radiology 2002;223(3):747–55.

[24] 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(8):428–31.

[25] KeenanAM, Tindel NL, Alavi A. Diagnosis of pedal osteomyelitis in diabetic patients using

current scintigraphic techniques. Arch Intern Med 1989;149(10):2262–6.

[26] Caprioli R, Testa J, Cournoyer RW Jr, et al. Prompt diagnosis of suspected osteomyelitis by

utilizing percutaneous bone culture. J Foot Surg 1986;25(4):263–9.

[27] Gold RH, Tong DJ, Crim JR, et al. Imaging the diabetic foot. Skeletal Radiol 1995;24(8):

563–71.

[28] Newman LG. Imaging techniques in the diabetic foot. Clin Podiatr Med Surg 1995;12(1):

75–86.

[29] Schauwecker DS, Park HM,Mock BH, et al. Evaluation of complicating osteomyelitis with

Tc-99m MDP, In-111 granulocytes, and Ga-67 citrate. J Nucl Med 1984;25(8):849–53.

[30] Sella EJ, Grosser DM. Imaging modalities of the diabetic foot. Clin PodiatrMed Surg 2003;

20(4):729–40.

[31] Devillers A, Moisan A, Hennion F, et al. Contribution of technetium-99m hexamethylpro-

pylene amine oxime labelled leucocyte scintigraphy to the diagnosis of diabetic foot infec-

tion. Eur J Nucl Med 1998;25(2):132–8.

[32] Poirier JY, Garin E, Derrien C, et al. Diagnosis of osteomyelitis in the diabetic foot with

a 99mTc-HMPAO leucocyte scintigraphy combined with a 99mTc-MDP bone scintigraphy.

Diabete Metab 2002;28(6 Pt 1):485–90.

[33] Keidar Z,MilitianuD,Melamed E, et al. The diabetic foot: initial experience with 18F-FDG

PET/CT. J Nucl Med 2005;46(3):444–9.

[34] 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(12):890–5.

[35] Hopfner S, Krolak C, Kessler S, et al. [Preoperative imaging of Charcot neuroarthropathy:

does the additional application of (18)F-FDG-PET make sense?]. Nuklearmedizin 2006;

45(1):15–20 [in German].

[36] SugawaraY, BraunDK,Kison PV, et al. Rapid detection of human infections with fluorine-

18 fluorodeoxyglucose and positron emission tomography: preliminary results. Eur J Nucl

Med 1998;25(9):1238–43.

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Imaging of Charcot foot Clinics 08(1)