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Clin Podiatr Med Surg

25 (2008) 263–274

Imaging of the Charcot Foot


Lee C. Rogers, DPM*, Nicholas J. Bevilacqua, DPM
Amputation Prevention Center at Broadlawns Medical Center, 1801 Hickman Road,
Des Moines, IA 50314, USA

Charcot’s foot is a serious problem that causes considerable morbidity


and may lead to limb loss. Arriving at a definitive diagnosis can be challeng-
ing. Because of the difficulty in diagnosis, one study showed the diagnosis
can be delayed on an average of 29 weeks [1]. Given the progressive, destruc-
tive nature of Charcot’s arthropathy, this delay can result in advancing
deformity, ulceration, infection, and place the limb at risk for amputation.
Syphilis has been referred to as the ‘‘great imitator’’ [2]. Charcot’s foot is
also an ‘‘imitator.’’ Early on, with a hot, red, swollen foot it is commonly
misdiagnosed 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 arthropathy
can coexist in the same extremity. Although clinical signs and symptoms and
historical information are crucial, this article focuses on the imaging modal-
ities that can aid practitioners in arriving at an early diagnosis and how to
differentiate Charcot’s arthropathy from osteomyelitis of the feet. The arti-
cle is divided into sections by imaging modality.

Plain radiography
In 1966, American orthopedist Sidney Eichenholtz described a logical and
predictable sequence of changes in ‘‘Charcot joints’’ observed by means of
serial radiographs. For the purpose of classification, he divided these changes
into three stages (Table 1). Stage 1 (stage of development) shows debris
formation 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 adjacent
bones; the bone ends become sclerotic. Stage 3 (stage of reconstruction) is

* Corresponding author.
E-mail address: lee.c.rogers@gmail.com (L.C. Rogers).

0891-8422/08/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved.
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264 ROGERS & BEVILACQUA

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

characterized by rounding of the bone ends with decrease in sclerosis [3]. This
staging 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 an
arthrodesis of one or both ankles for leprotic neuroarthropathy and added
an additional, earlier stage to Eichenholtz’s classification. Shibata described
a stage 0, in which there are no radiographic changes noted, but there is
warmth, swelling, and instability. Yu and Hudson [5] described stage 0 as
an acute sprain or fracture in the presence of neuropathy and reviewed
the evaluation and treatment of this stage in Charcot’s foot and ankle. Sella
and Barrette [6] developed another classification scheme, also based on
radiographic findings, which includes an early phase consisting of localized
heat and swelling.
The Eichenholtz classification is based solely on radiographic findings
and 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 used
to 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 and
midtarsal joints (pattern 3); the ankle joint (pattern 4); and the posterior
calcaneous (pattern 5).

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


IMAGING OF THE CHARCOT FOOT 265

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.

The tarsometatarsal joint is the most commonly involved joint [9]. An


equinus deformity at the ankle is a key contributor to the collapse at this
anatomic level. This biomechanical factor, along with sensory neuropathy
and 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 progression
of deformity. Often, the calcaneal inclination decreases with equinus at the
ankle. Measurement of talar–first metatarsal angle may reveal dislocation of
the midfoot (Fig. 4).

Fig. 3. Eichenholtz stage 3 characterized by rounding of the bone edges and consolidation.
266 ROGERS & BEVILACQUA

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 have


a heightened index of suspicion to detect all early Charcot’s feet. Failure
to recognize early, stage 0 Charcot may result in progressive deformity
with deleterious effects. Radiographs should not be relied on to rule out
Charcot’s foot.
An adjunctive finding to the radiographic bone destruction associated
with 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-B
ligand is up-regulated in Charcot’s foot causing osteolysis, and the same
molecule may be responsible for calcification of vascular smooth muscle
cells [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 diagnostic
modality 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).
IMAGING OF THE CHARCOT FOOT 267

intra-articular fractures not visualized by plain radiography [13]. Pseudocyst


formation may be evident [14] but can be difficult to distinguish from
osteomyelitis. CT is most useful in cases where surgical reconstruction is
planned 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] and
specificity (80%–100%) [15,18,19] for the disease. Additionally, it produces
an accurate anatomic picture of the extent of the infection. It is useful for
both the diagnosis of osteomyelitis and the preoperative planning of surgical
resection. The difficulty is distinguishing osteomyelitis from Charcot’s
arthropathy, because both produce similar signal changes on MRI. Char-
cot’s foot and osteomyelitis are characterized by a decrease in intensity in
the 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 on
MRI in the diabetic foot, is a proponent of the capability of MRI to differ-
entiate osteomyelitis from Charcot’s foot. Ledermann advocates the use of
secondary signs of osteomyelitis, which can improve specificity [22]. Because
over 90% of cases of osteomyelitis are caused by contiguous spread of
infection from skin ulcerations, he evaluates the images for adjacent soft
tissue defects and tracts with extensions to bone [23]. Other clues to consider
are 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.
268 ROGERS & BEVILACQUA

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-
nal CT at the tarsometatarsal scan revealing more fragmentation than visible by plain radiography.
(C) Coronal MRI of the midfoot (T2-weighted image) significant for marrow edema of the second
and third metatarsal shafts (arrow). (D) Three-phase 99Tc bone scan uncovering activity across the
entire tarsometatarsal joint, more extensive than previous imaging.

arthropathy is more commonly diffuse; (2) deformity is common with


Charcot’s foot, but uncommon with osteomyelitis; and (3) Charcot’s foot
typically affects the midfoot, whereas osteomyelitis more commonly affects
the toes and forefoot [20].
Chantelau and Poll [24] compared MRI with 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, MRI
confirmed radiographic findings and in addition showed bone and soft tissue
edema, and joint effusion, which were not evident on radiographs. In stage 3,
MRI again confirmed radiographic findings and additionally noted bone
edema that was not visible on radiograph [24]. This study demonstrated the
superiority of MRI over radiography for assessing early, stage 0 Charcot’s
foot, but merely confirmed the radiographic finding in later stages.
IMAGING OF THE CHARCOT FOOT 269

Bone scintigraphy
The term ‘‘bone scan’’ refers to any study where a radiolabel is used, which
localizes to osseous tissue to diagnose bone diseases. There are many types of
bone scans, including traditional 99technetium-labeled scans, 67galium citrate
scans, 111indium scan, Cipro-labeled scans, sulfur-colloid marrow scans, and
99m
technetium HMPAO ‘‘leukocyte labeled’’ scans. This section reviews the
most common and accessible bone scans.
The traditional 99technetium bone scan is highly sensitive for osseous
pathology 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 three
imaging phases of the 99Tc bone scan are the blood flow, blood pool, and
delayed phases. The blood flow image is taken within seconds of infusion
of the radiolabel and confirms the flow through the macrovasculature.
The blood pool phase is taken several minutes later and can show increased
pooling 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.
270 ROGERS & BEVILACQUA

the radiolabel in areas of increased bone turnover. Additionally, a fourth


phase or 24-hour image can be used if there is too much background activity
to discern the anatomic location of the increased uptake (Fig. 9) [27].
Leukocyte-labeled scans are more specific for osteomyelitis, but may have
a lower sensitivity than 99Tc scans. 111Indium bone scans are sensitive and
specific for osteomyelitis. Sensitivities range from 89% to 100% and specific-
ities from 69% to 80% [28,29]. Seabold and colleagues [21] used traditional
99
Tc and 111In scans to differentiate Charcot’s changes from osteomyelitis
in 14 patients with clinically or radiographically diagnosed Charcot’s foot.
The sensitivity for osteomyelitis was 80% and the specificity was 54% [30].
99m
Tc HMPAO (Ceretec) scans require the white blood cells to be labeled
ex vivo, then reinfused, which is more time consuming. The sensitivity and
specificity for osteomyelitis in the foot are very favorable. One study of 42
patients 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 75
patients, with the scan being 92.6% sensitive and 97.6% specific. They added
that 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 emission
tomography (PET) using radiolabeled glucose (18F-FDG). This makes the
scan very useful as a physiologic and functional scan for cancer and other
diseases that increase local cellular metabolism and glucose uptake. Its lim-
itation has been the poor anatomic resolution, leading to the use of hybrid
PET-CT where a CT is performed at the same instance and image slices can
be compared side-by-side.
In the diabetic foot, there are limited data on the use of PET. What may be
most useful is the ability of 18F-FDG PET to differentiate osteomyelitis from
Charcot’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.
IMAGING OF THE CHARCOT FOOT 271

Table 2
Sensitivity and specificity of diagnosing osteomyelitis in the feet by various imaging modalities
% Sensitivity % Specificity
MRI [15–19] 77–100 80–100
99
Tc 3-phase bone scan [25,26] 100 25–38
111
In bone scan [28,29] 89–100 69–80
99
mTc HMPAO [31,32] 88–93 97–98

and colleagues [33] evaluated 14 patients with suspected foot infection for
osteomyelitis. Hybrid PET-CT correctly identified osteomyelitis in four
patients, confirmed infection in soft tissue in five patients, and ruled out
infection in four patients. In the one remaining patient, PET-CT was able
correctly to differentiate the osseous destruction of Charcot’s arthropathy
from 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,
99
Technitium 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.)
272 ROGERS & BEVILACQUA

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 and
found that 37 (95%) of 39 lesions were identified successfully using PET.
The ability to differentiate osteomyelitis from Charcot’s foot lies in the
standardized uptake value, which may differ between the two conditions;
and software can detect these variances. Hopfner and colleagues found
that 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 an
average 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 standardized
uptake value of 1.4, the lowest in the study. By contrast, glucose metabolism
is 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 presents
all the modalities described previously and reports their usefulness in
IMAGING OF THE CHARCOT FOOT 273

diagnosis of Charcot’s foot, osteomyelitis, or both. Fig. 10 shows a flowchart


on how to use imaging to diagnose Charcot’s foot and distinguish it from os-
teomyelitis, if necessary. On the presentation of an erythematous, edematous
foot without an ulcer or radiographic changes, an MRI or 99Tc bone scan
is 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 radiographic
evidence of bone destruction at the midfoot, can accurately be diagnosed as
Charcot’s foot. In the presence of an open wound, however, especially one
that extends to bone, further diagnostic study is required. MRI may be
performed, 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 uptake
and fail to narrow the differential diagnosis. In these cases, 111In or 99mTc
HMPAO scans are sensitive and specific for osteomyelitis, even in the pres-
ence of concomitant Charcot’s arthropathy (Fig. 11). CT scans and MRI can
be useful for presurgical planning. PET scans, although not widely available
at present, may be the future in imaging of Charcot’s foot because early
evidence seems to show that this scan can reliably diagnose Charcot’s foot
and osteomyelitis, and most importantly differentiate between the two.

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