〈Review 〉 Imaging of the Diabetic Foot - CiteSeerX

Foot & Ankle Specialist 249

DOI: 10.1177/1938640010383154. From the Department of Radiology, The University of Texas Health Science Center at San Antonio, San Antonio, Texas. Address correspondence to Rebecca Loredo, MD, Professor, Department of Radiology, Chief of Musculoskeletal Imaging, The University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, TX 78229-3900; e-mail: [email protected].

For reprints and permissions queries, please visit SAGE’s Web site at http://www.sagepub.com/journalsPermissions.nav.

Copyright © 2010 The Author(s)

⟨ Review ⟩

Imaging of the Diabetic FootDiagnostic Dilemmas Rebecca Loredo, MD, Andres Rahal, MD,

Glenn Garcia, MD, and Darlene Metter, MD, FACR

vol. 3 / no. 5

There is no ‘one best test’ for sorting

out the diagnostic dilemmas commonly

encountered. . . . Each radiologic modality

plays a key role in diagnosis and early

treatment.”

“

Abstract: Multiple diagnostic imag-ing modalities are available and bene-ficial for the evaluation of the diabetic foot. There is not yet “one best test” for sorting out the diagnostic dilem-mas commonly encountered. The dif-ferentiation of cellulitis alone from underlying osteomyelitis and the early detection of abscesses remain impor-tant diagnostic goals. Equally impor-tant, differentiation of osteomyelitis and neuroarthropathy remains a dif-ficult job. This is often compounded by postoperative diabetic foot states status after reconstruction. Diagnostic evalua-tion often involves multiple studies that are complementary and that include conventional radiography, computed tomography, nuclear medicine scintig-raphy, magnetic resonance imaging, ultrasonography, and positron emission tomography.

Keywords: diabetic foot imaging; osteo-myelitis; neuroarthropathy; Charcot foot

Imaging of the diabetic foot entails multi-ple imaging modalities. There is no “one best test” for sorting out the diagnos-

tic dilemmas commonly encountered. The diagnostic evaluation often includes con-ventional radiography, computed tomog-raphy (CT), scintigraphy, and magnetic resonance (MR) imaging and, in some cases, ultrasonography and positron

emission tomography (PET). Angiography is also a diagnostic imaging modality fre-quently used to evaluate the diabetic foot; however, it is not covered in this article. Each radiologic modality plays a key role in diagnosis and early treatment.

Overview of Imaging ModalitiesConventional radiography or plain

X-rays have been the basis for evaluation of the dia-betic foot. This important modality remains a valu-able means of document-ing anatomical detail and major structural changes.

CT is associated with optimal spatial resolu-tion. In comparison with plain films, CT offers 3-dimensional imaging and improved tissue con-trast. In comparison with plain X-rays and magnetic resonance imaging, CT is more sensitive and specific for identification of cortical erosions, small sequestra, soft tis-sue gas, calcification, and foreign bodies.1 The more recent technical advancement of multidetector CT permits CT scan-ners to acquire multiple slices simulta-neously. This capability greatly increases the speed of CT image acquisition and provides thin-slice images (< 1 mm) with improved image resolution.

Nuclear medicine scintigraphy provides physiologic information and improved diagnostic sensitivity when compared with conventional radiography. The proce-dures that are often used in evaluation of the diabetic foot include technetium-99m methylene diphosphonate bone scans, indium-111-labeled leukocyte scans, and technetium-99m sulfur colloid studies.2-4 Comparatively, these studies vary in

sensitivity and specificity. Although the ideal scintigraphic method for localizing infection would entail one study alone, multiradionuclide studies have been found to be more accurate, owing to improved specificity.

In the diabetic foot, the technetium-- 99m methylene diphosphonate bone scan is clinically invaluable in detecting and localizing abnormal bone, with an accuracy of 90%, a sensitivity of 94%, and a specificity of 95%.5,6 This modal-ity is particularly remarkable for the

at PENNSYLVANIA STATE UNIV on September 17, 2016fas.sagepub.comDownloaded from

http://fas.sagepub.com/

October 2010Foot & Ankle Specialist250

diagnosis of osteomyelitis in nonvio-lated bone or in bone that has not been affected by other conditions. In com-plicated cases, in which there is bone remodeling (neuroarthropathy, trauma, surgery, or tumor), this specificity is markedly reduced to 33%, whereas the sensitivity remains high at 95%.6

Indium-111 leukocyte scintigraphy and technetium-99m leukocyte scintigraphy have proven to be especially useful in the diabetic foot for diagnosing infec-tions, particularly in patients who have bone or joint involvement.7 Within the foot, the clinical indications for the use of white blood cell scintigraphy include fever of unknown origin, the postopera-tive patient (> 2 weeks) with fever, bone and soft tissue infection, and vascular graft infection. False-positive results are described in the setting of recent frac-ture, recent surgery, acute arthritis, and neuropathic joints and in metastatic carcinoma.8 In the hope of increas-ing specificity, the use of radionuclide studies combined with single-photon emission CT and CT imaging has been investigated.9

Gallium-67 citrate scans in combina-tion with the bone scan have been inves-tigated in the literature10 for evaluation of the foot afflicted by diabetic problems. The addition of a gallium scan has been shown to increase specificity, although the diagnostic accuracy is low owing to false-positive results related to recent bone fractures or neuroarthropathy.10 Therefore, it is not typically used in the routine diabetic foot evaluation.

MR imaging has the ability to reveal numerous diabetic pedal abnormalities, including stage 0 Charcot neuroarthrop-athy, that are not detectable with other imaging techniques; it provides excellent anatomic detail, visualization of bone mar-row, superior soft tissue contrast, and mul-tiplanar imaging capability. Given that greater than 50% of limb-threatening infections do not manifest systemic signs or symptoms,11 MR imaging is an excel-lent modality because it offers exquisite detail of soft tissue and marrow anat-omy. MR imaging has been shown to have high sensitivity and specificity for diag-nostic imaging of the diabetic foot.12 This

statement has been supported in the liter-ature in which pooled retrospective and prospective study results, variably compar-ing MR imaging to radionuclide imaging, reported a high sensitivity for MR imag-ing, ranging from 88% to 100%, with a specificity of 78% to 100%. This is in com-parison to Tc-99m-MDP (50% to 69% sen-sitivity and 50% to 83% specificity) and Indium-111 white blood cell (WBC) scans (33% sensitivity and 69% specificity).13-16

Ultrasonography may provide structural and functional information in the diabetic foot for diagnostic and therapeutic pur-poses. Functional information is derived from the dynamic evaluation of structures during motion. Ultrasound is excellent at differentiating fluid or cystic lesions from solid structures. Therefore, it may be used for evaluating joint effusions and soft tis-sue fluid collections, such as cysts and abscesses, with the added capability of localizing foreign bodies and collections for removal or aspiration, respectively.

Fluorine 18-fluorodeoxyglucose (FDG) PET is a promising modality for evalua-tion of the diabetic foot because the F-18 FDG tracer of increased intracellular glu-cose metabolism accumulates at sites of infection and inflammation. The prelimi-nary results from a number of investiga-tive studies have demonstrated that PET scans are promising for use in diagnos-tic imaging of the diabetic foot,17-20 with a reported 91% to 100% sensitivity and a 85% to 86% specificity. With the com-bined use of CT, the hybrid PET-CT tech-nology provides precise registration of metabolic and structural imaging data, obtained in the same session, on a sin-gle device, and it may improve diagnosis and localization of infection. In a study by Höpfner et al, data demonstrated that PET provides results comparable to those of MR imaging in the preoperative eval-uation of patients with Charcot neuro-arthropathy.21 In addition, PET offers the advantages of being unaffected by metal implants, the ability to differentiate between inflammatory and infectious soft tissue lesions, and the ability to dif-ferentiate between the skeletal con-ditions of osteomyelitis and Charcot arthropathy.21

Bone and Joint ProblemsNeuropathic OsteoarthropathyDiabetic neuroarthropathy represents a

spectrum of pathology, ranging from pain-ful mild alterations resembling degener-ative arthritis to the extreme of complete articular disorganization (Figure 1A and 1B). The identification and documentation of neuropathic disease and the progres-sion of neuroarthropathy may be followed with conventional radiography as it rapidly evolves over days or weeks or slowly pro-gresses over months to years. The changes of acute or rapidly progressive neuroar-thropathy are often observed in the tar-sus and proximal metatarsus on plain films and with CT imaging. Frequently, the areas of involvement are some dis-tance from ulcers or other sites of infec-tion. As neuroarthropathy progresses, multiple fractures and dislocations result in complete collapse of the foot22 (Figure 2). Even in the absence of infection, there may be loss of the normal foot architec-ture and gross bone fragmentation.2 On CT scans, chronic neuroarthropathy may demonstrate nonunited fractures (Figure 3) and adjacent soft tissue swell-ing. However, the early subtle changes of neuroarthropathy, such as microfractures, may not be obvious.2

The nuclear medicine bone scan allows visualization and localization of osseous anatomy, where there is positive uptake in a neuropathic foot. The abnormal pat-tern of increased uptake on a positive 3-phase bone scan can then be used as a “road map” to assess the area (or areas) of clinical concern. If an indium-111 leu-kocyte scan is performed at this point, a neuropathic foot may not show abnor-mal osseous uptake, or it may show mild abnormal joint or bone uptake in the early stages of neuroarthropathy. It is in the early stages of neuroarthropathy that the interpretation of white blood cell scans can be confounded by the effect of leukocyte accumulation in an early phase Charcot joint.23 If the follow-up leuko-cyte study is negative, then there is no acute infectious process (Figure 4A-4C). The leukocytes, predominantly polymor-phonuclear cells, accumulate in these joints owing to an early, acute



Foot & Ankle Specialistvol. 3 / no. 5 251

Figure 1.

Neuropathic osteoarthropathy. (A) Anteroposterior and (B) oblique views of the foot demonstrating homolateral Lisfranc fracture-dislocation with midfoot and proximal metatarsus joint destruction.

Figure 2.

Neuropathic arthropathy. Lateral weightbearing view showing osseous and articular disorganization, midfoot collapse, and talar plantar flexion (arrow) with development of “rocker-bottom” deformity.

Figure 3.

Fracture nonunion. Coronal computed tomography image demonstrating fracture-nonunion of the medial and intermediate cuneiforms (arrows).

inflammatory response triggered by peri-articular microfractures. In a chronic Charcot joint, the effusion contains mainly

mononuclear cells. Thus, the uptake of labeled polymorphonuclear cells is low in these joints and more likely due to

hematopoietically active marrow involved in the repair process.23 Another point to be made regarding the diagnostic inter-pretation of diabetic foot nuclear med-icine scans is that there is a difference in sensitivity and specificity depending on the location of the foot pathology. Forefoot scans are more easily inter-preted owing to better spatial resolution because the bony anatomy is more delin-eated than in the midfoot where bones overlap. Where there is no clear anatomic definition, it is difficult to differentiate soft tissue from bone infection using leu-kocyte scans alone.23 Therefore, to dimin-ish the number of diagnostic errors, a 3-phase bone scan is the preferred initial nuclear medicine study in a diabetic foot with underlying neuropathic changes.

On MR images, small joint effusions are common in diabetic patients— perhaps a manifestation of peripheral neuropathy.12,24 The changes of acute or rapidly progressive neuroarthropathy are observed as osseous inhomogeneous low T1-weighted marrow signal intensity and

A B




high T2-weighted marrow signal intensity, often observed in the tarsus and proximal metatarsus (Figure 5A and 5B). Frequently, the areas of involvement are some dis-tance from ulcers or other sites of infec-tion, such as abscesses or sinus tracts. The appearance of the soft tissue about the osseous neuropathic region ranges from little or no abnormal T2-weighted MR image signal intensity to high T2-weighted signal intensity (Figure 5B). However, the degree of increased signal intensity is rela-tively less than what may be seen in cellu-litis and osteomyelitis.2

Chronic neuroarthropathy is often seen as nonunited fractures with low signal intensity fracture lines and adjacent nor-mal or mildly increased T2-weighted mar-row signal intensity.2 Even in the absence of infection, neuroarthropathy may be seen as scattered areas of abnormal bone marrow signal intensity, loss of the normal foot architecture, and gross bone frag- mentation2 (Figure 6A-6D). Nevertheless, the bone marrow signal intensity and amount of surrounding abnormal soft tissue signal intensity should be relatively less in the neuropathic foot than in the infected one (Figure 6C).

Figure 4.

Fifty-nine-year-old woman with neuropathic osteoarthropathy and clinical suspicion of osteomyelitis. (A) Anteroposterior view showing neuropathic changes in the midfoot and proximal metatarsus (box). (B) Positive bone scan demonstrating uptake in the symptomatic foot (box). (C) Indium scan showing no abnormal uptake (box), consistent with a diagnosis of Charcot joint.

Figure 5.

Acute neuroarthropathy. (A) Axial fat-suppressed MR image of the midfoot and proximal metatarsus demonstrating high T2-weighted signal intensity (arrows) marrow edema. (B) Corresponding T1-weighted image showing diminished marrow signal intensity (arrows), the combined findings consistent with reactive marrow of acute neuroarthropathy. Note the adjacent high T2-weighted signal intensity edema in the deep plantar foot and superficial dorsal soft tissues (A).

A B C

A B




OsteomyelitisUlcerations are the most frequent predis-

posing factor in the development of a dia-betic foot infection, and early infection tends to involve the compartments adja-cent to the ulcers.25 In the diabetic foot, radiographic signs of osteomyelitis most commonly involve the first, fifth, and sec-ond rays.22 Calcaneal involvement may also occur; however, the other tarsal bones of the foot are not commonly affected. Focal demineralization is a classic mani-festation of early osteomyelitis (Figure 7). Unfortunately, osteomyelitis may not pro-duce significant radiographic changes until the late stages of destruction, periosteal reaction, and sclerosis occur2,24 (Figure 8A and 8B).

CT image findings correlate well with the extent of osseous infection.8 At times, CT does not provide clear bone mar-row visualization in the small bones of the feet owing to beam-hardening artifact caused by the adjacent cortical bone.26 However, the advancement of CT tech-nology to multidetector capability has improved diagnostic image quality in the small bones of the feet.

The primary nuclear medicine method of detection of infection is indium-111 leukocyte scintigraphy. Both indium-111 leukocyte scans and technetium-99m leu-kocyte scans have proven to be clin-ically useful for diagnosing bone and joint infections,7 following a positive bone scan. In a setting of osteomyeli-tis, within 48 to 72 hours following the onset of symptoms, a 3-phase positive bone scan will demonstrate hyperemia in the first phase (angiographic), increased activity in the second phase (blood pool), and increased focal uptake in the third phase (delayed, 2-3 hours) (Figure 9A-9E). Four-phase bone scan imaging (24 hours) is an additional method that has been used to enhance the specific-ity of the radionuclide diagnosis of osteo-myelitis. In osteomyelitis, tracer uptake in infected bone should be greater at 24 hours (fourth phase) than at 2 to 3 hours (third phase), thereby increasing the target:background ratio and the con-spicuity of abnormal foci of increased activity. The extended fourth phase of

Figure 6.

Chronic neuropathic osteoarthropathy. Anteroposterior (A) and lateral (B) views of the foot and ankle illustrating chronic neuropathic changes affecting the midfoot and talus. (C) Fat-suppressed T2-weighted axial magnetic resonance image demonstrating high signal intensity marrow (arrows) within the calcaneus, talus, and navicular, without surrounding soft tissue edema. (D) Corresponding T1-weighted magnetic resonance image showing intermediate marrow signal intensity (arrows).

the examination has been shown to be of value in the assessment of osteomy-elitis in patients with peripheral vascular

disease.27 However, the utility of four-phase imaging in the diabetic foot is questioned. Investigators such as Tronco

B

A

C D




et al have shown that although 4-phase imaging is more specific than 3-phase imaging, the accuracy of a 4-phase study is well below the 85% to 90% reported for dual-tracer studies, such as combined labeled leukocyte scans and bone scans and combined labeled leukocyte scans and sulfur colloid marrow scans (sensitiv-ity, 92%; specificity, 100%).28 Tronco et al concluded that the 4-phase imaging pro-cedure had no role in the radionuclide evaluation of osteomyelitis.28

The most common clinical request for MR imaging of the diabetic foot is related to the detection of osteomyelitis. MR image evaluation may be requested as a search for undiagnosed disease or as documentation of healing or progres-sion of infection. MR imaging has been shown to have high sensitivity and spec-ificity in the detection of osteomyelitis in diabetic patients.29 The MR image tech-niques usually include T1-weighted and T2-weighted (fluid-sensitive) sequences in multiple planes with the addition of a gadolinium contrast–enhanced T1-weighted sequence. T1-weighted and T2-weighted MR images provide a combination of excellent anatomic

detail and demonstrate areas of abnor-mal signal intensity in bone marrow (Figure 10A-10D). STIR (short tau inver-sion recovery) images are sensitive in the detection of subtle water changes in the marrow caused by osteomyelitis. The role of intravenous contrast enhance-ment is unclear. Some authorities believe that contrast enhancement is “extremely useful”30 and improves the specificity of MR imaging, allowing for the iden-tification of osteomyelitis, intraosseous abscesses (Figure 11A-11C), and seques-tra. Unfortunately, contrast is contrain-dicated in diabetic patients with renal impairment owing to the risk of sys-temic fibrosis. In addition, tissue devi-talized by ischemia may show confusing patterns of contrast uptake, and neuroar-thropathy may closely mimic osteomyeli-tis.30 Furthermore, postsurgical changes, trauma, and adjacent septic arthritis can cause false-positive results.31,32 Morrison and colleagues33 evaluated the clini-cal accuracy, surgical utility, and cost-effectiveness of MR imaging of diabetic

feet in the evaluation of osteomyelitis. Comparisons were made among contrast-enhanced MR imaging, 3-phase techne-tium-99m bone scans, gallium-67 scans, and indium-111 leukocyte scans. With MR imaging, there was comparatively good sensitivity and specificity, with rates of 82% and 80%, respectively, in diabetic patients, and 89% and 94%, respectively, in nondiabetic patients. Using cost analy-sis techniques, the authors found that MR imaging was competitively priced when one takes into account the high costs associated with multistudy preoperative scintigraphy, costs related to the com-bined cost of multiple studies, and the additional days of preoperative hospital-ization required for the performance of the tests.33

Osteomyelitis Versus Neuropathic OsteoarthropathyThe location of foot disease is an

important factor in differentiating between infection and neuropathic

Figure 7.

Acute osteomyelitis. Anteroposterior view of the hallux demonstrating focal demineralization (arrow) and loss of the cortical white line along the medial aspect of the hallux with overlying soft tissue swelling.

Figure 8.

Subacute-chronic osteomyelitis of the fibula. Anteroposterior views of the ankle taken over a 2-month interval (A → B) demonstrating progressive osseous destruction, periostitis, and osteosclerosis of the fibula. There is an overlying skin ulcer.

A B




Figure 9.

Positive 3-phase bone scan in a 43-year-old male status after arthrodesis with clinical suspicion of osteomyelitis. (A) Anteroposterior and (B) lateral views of the ankle demonstrate chronic tibia and fibula fracture malunion and tibiotalar arthrodesis. (C) First phase (angiographic): bone scan demonstrating asymmetric blood flow with markedly increased tracer delivery to the region of the left distal tibia throughout the angiographic phase (arrows). (D) Second phase (blood pool): bone scan image illustrating marked left ankle increased blood pool tracer activity adjacent to the proximal extent of the tibia hardware (long arrow) and at the level of the ankle joint/arthrodesis (short arrow). (E) Third phase (delayed): image showing diffuse increased activity throughout the distal tibia, more focally intense at the level of the proximal hardware (long arrow) and region of the ankle arthrodesis (short arrow). Differential diagnostic considerations at this point include postoperative changes, ongoing repetitive injury, hardware loosening, and infection. An indium white blood cell scan is indicated to better specify.

osteoarthropathy. Osteomyelitis is usu-ally confined to a solitary site in the metatarsal heads, toes, or calcaneus.34 Approximately 20% of patients have infection at 2 or more sites. In contrast, neuropathic osteoarthropathy occurs most frequently in the intertarsal and tar-sometatarsal joints (60% of cases), fol-lowed by the metatarsophalangeal joints of the forefoot (30% of cases).34

Involvement of the interphalangeal joints is uncommon. Although the site of involvement is helpful, it is not consis-tently reliable. Neuropathic changes at the metatarsophalangeal and interpha-langeal joints are frequently associated with skin ulceration, whereas involve-ment of the tarsometatarsal and intertarsal

joints is rarely associated with ulceration until the midfoot is sufficiently collapsed to elicit new pressure points.34 Small joint effusions are common in diabetic patients and may be present with or without infec-tion, perhaps a manifestation of peripheral neuropathy.12,24

In a large number of cases, the early, often subtle, radiographic changes of osteomyelitis may be obscured by the chronic destructive process of neuroar-thropathy. In that case, nuclear medicine imaging plays a large role. In the set-ting of a negative bone scan in a neuro-pathic foot, the diagnosis of osteomyelitis is excluded. However, bone scan images that are complicated by osseous remodel-ing (neuroarthropathy, tumor, trauma, or

surgery) have a markedly reduced speci-ficity of 33% (Figure 9A-9E), whereas the sensitivity remains high at 95%.6 In cases complicated by neuroarthropathy or trauma, the bone scan alone can give sig-nificant false-positive results, and sup-plemental imaging with radiolabeled leukocyte studies can aid in improv-ing diagnostic specificity. Labeled leuko-cyte studies—despite false-positive results described in the setting of recent fracture, recent surgery, acute arthritis, neuro-pathic joints, and metastatic carcinoma8—are the imaging study of choice for investigation of infection at sites of bone remodeling, with an accuracy of approx-imately 80% in the case of diabetic pedal osteomyelitis.35 Despite some difficulty in

A B C

D E




separating bone and soft tissue infection, one study demonstrated high sensitivity and specificity of Indium-111 leukocytes in a small group of patients with neuropathic joint disease.3

A combined evaluation using bone scintigraphy, leukocyte scintigraphy, and sulfur colloid bone marrow imaging has been shown to be useful in diagnosing osteomyelitis in patients with underlying neuroarthropathy.4 On the nuclear med-icine images, increased uptake on the bone scan corresponding to increased bone uptake of labeled leukocytes, in the absence of a corresponding uptake of sulfur colloid, is consistent with infec-tion (Figure 12A-12D). Sites of infection stimulate uptake of labeled leukocytes and by the same mechanism will displace or infarct normal marrow elements, lead-ing to reduced accumulation of the sulfur colloid bone marrow scanning agent. It is important to document abnormal bone uptake on a bone scan before perform-ing combined WBC and sulfur colloid studies because the WBC study may be positive in a setting of soft tissue infec-tion and the sulfur colloid marrow scan will be negative owing to less peripheral active bone marrow, mimicking osteo-myelitis to the untrained eye. Combined indium and sulfur colloid bone marrow imaging improves the diagnostic accuracy in the diabetic foot with the sensitivity of this combination at 92% and the specific-ity at 100%.4

MR image findings of acute osteomy-elitis may be similar to those of acutely evolving neuropathic osteoarthropathy, biomechanical stress changes related to altered weightbearing, and bone marrow signal intensity changes after orthopedic surgery and trauma.29 Morphological fea-tures in conjunction with signal intensity alterations may assist in differentiation of osteomyelitis and neuroarthropathy. Osteomyelitis is said to be clinically pres-ent when there is confluent, decreased geographic T1-weighted signal inten-sity, concordant increased T2-weighted signal intensity, and T1-weighted con-trast enhancement (Figures 10A-10D and 13A-13C). This appearance is to be dis-tinguished from reactive marrow edema that is observed as nongeographic, hazy, or reticulated diminished subcorti-cal T1-weighted marrow signal intensity

Figure 10.

Osteomyelitis of the hallux, status after amputation. (A) T1-weighted and (B) fat-suppressed T2-weighted sagittal magnetic resonance image showing intermediate and high marrow signal intensity, respectively, throughout the metatarsal stump (arrows). (C) T1-weighted and (D) fat-suppressed T1-weighted contrast-enhanced axial image demonstrating hallux intermediate marrow signal intensity and contrast enhancement (asterisk), respectively.

Figure 11.

Intraosseous calcaneal abscess. (A) Sagittal T1-weighted magnetic resonance image of the heel illustrating inhomogeneous low calcaneal marrow signal intensity (box). (B) Corresponding fat-suppressed T2-weighted and (C) fat-suppressed T1-weighted contrast-enhanced images showing high signal intensity purulent material (arrow) and contrast rim enhancement of the abscess (arrow), respectively. Marked surrounding marrow edema and soft tissue enhancement is seen owing to the marked inflammation.

A

A B

C

C D

B




and increased T2-weighted signal inten-sity, regardless of contrast enhancement30 (Figure 13A-13C).

PET imaging can be used to differen-tiate infection from neuroarthropathy. Studies have shown that the precise ana-tomic localization of increased F-18 FDG uptake provided by PET-CT enables accurate differentiation between osteo-myelitis and neuroarthropathy observed as relative areas of increased FDG uptake.19,21,29,36,37 On the basis of pub-lished literature,19,21,29,36,37 orthopaedic/podiatric infections, including those occurring in the diabetic foot and partic-ularly those related to implanted hard-ware/prostheses and osteomyelitis, can be successfully detected with the use of FDG-PET. Because of this ability to pro-vide complementary imaging data, PET has been suggested as an adjunct to con-ventional radiography and MR imaging in the preoperative evaluation of patients with Charcot neuroarthropathy of the foot.21 Of note is that in patients who have metal implants/hardware, ferromag-netic artifact normally precludes adequate MR image evaluation. A study showed that PET can supply adequate informa-tion in such patients with metal implants, as confirmed by surgical findings.21

Soft Tissue ProblemsThe predominant types of soft tissue

infection that involve the diabetic foot are nonsuppurative cellulitis and deep soft tis-sue abscess. Radiographically, soft tis-sue infection is seen as diffuse or focal swelling with or without soft tissue gas. If foot infection is detected, radiographs of the ankle and the tibia and fibula are obtained to evaluate for possible proxi-mal infection searching for soft tissue gas (Figure 14A-14C) or foreign bodies. If soft tissue gas is detected, the radiographic evaluation should proceed to include the joint proximal to the level of the visu-alized gas. Unfortunately, the soft tissue problems, such as cellulitis, fasciitis, pyo-myositis, abscesses, and sinus tracts, are not as easily appreciated or distinguished on plain films.

Cellulitis and AbscessIn a patient who has cellulitis, the plain

films show nonspecific increased soft

Figure 12.

Diagnosis of osteomyelitis in postoperative patient, confirmed with indium white blood cell (WBC) and sulfur colloid marrow scans. (A) Positive left ankle osseous uptake on the bone scan; (B) 2 foci of increased activity in the left distal tibia on the WBC scan; (C) subsequent sulfur colloid marrow scan without areas of relatively similar increased activity in the same regions (arrows). (D) Findings of osteomyelitis confirmed on the sulfur colloid subtraction study (box).

Figure 13.

Reactive marrow edema in the bones of the midfoot adjacent to fifth metatarsal osteomyelitis. (A) T1-weighted, (B) fat-suppressed T2-weighted, and (C) fat-suppressed T1-weighted contrast-enhanced axial magnetic resonance images of the foot illustrating intermediate T1-weighted (arrow) and increased T2-weighted marrow signal intensity (arrow) with corresponding lack of contrast enhancement (arrow) in the bones of the midfoot compared with the more confluent signal intensity changes and enhancement in the fifth metatarsal (asterisks). Relatively less hyperintense T2-weighted marrow signal intensity and minimal enhancement of the reactive marrow compared with the adjacent infected fifth metatarsal are emphasized.

A B C

A B

DC




administration of intravenous contrast. Frequent sites of soft tissue abscess for-mation are the toes, web spaces, flexor sheaths, plantar spaces, and heel39 (Figure 17). On CT images, focal hypoattenuation is seen with rim or wall enhancement fol-lowing administration of contrast mate-rial. On MR images, an abscess may be distinguished from edema or focal cellu-litis because of its smooth margin, focal higher/brighter T2-weighted signal inten-sity (purulence) (Figure 17B) compared to the surrounding edema, and rim or wall enhancement following administra-tion of intravenous gadolinium contrast. MR imaging may be beneficial in the presurgical evaluation of patients with known or suspected multifocal abscesses because it provides information regard-ing the precise location and number of collections.12

Necrotizing Fasciitis and PyomyositisOwing to the emergent nature of soft

tissue conditions such as necrotizing fas-ciitis and pyomyositis, radiologic evalua-tion needs to be as accurate as possible. Plain radiography, CT, and MR imag-ing may suggest the diagnosis. The most common plain radiographic find-ings of necrotizing fasciitis are similar to those of cellulitis, with increased soft tis-sue thickness and opacity.40 The charac-teristic finding is gas in the soft tissues, although this is seen in only a minority of cases because plain radiographs are frequently normal until the infection and necrosis are advanced.41 The CT find-ings of necrotizing fasciitis are soft tis-sue air associated with fluid collections within the deep fascia42,43 and thicken-ing and enhancement of one or both of the superficial and deep fascial layers, with or without subcutaneous fat simi-larly affected.42,43 On MR images, the sub-cutaneous tissue and deep fascia show hyperintense T2-weighted signal inten-sity and contrast enhancement in patients with necrotizing fasciitis and those with pyomyositis.44 The subcutaneous tis-sues may have reticular increased sig-nal intensity, similar to that of cellulitis. Unlike cellulitis, however, the deep fas-cia is involved in necrotizing fasciitis.

Figure 14.

Radiologic evaluation of an infected extremity. (A) Anteroposterior view of the foot, (B) lateral view of the ankle, and (C) lateral tibia-fibula view showing soft tissue gas throughout the foot (arrows), extending into the ankle and leg (arrows).

tissue thickness and opacity. On CT images, the subcutaneous tissues may demonstrate stranding, reticular increased signal intensity, and skin thickening. The presence of soft tissue edema on MR images cannot be differentiated from cel-lulitis by MR imaging alone. MR images will demonstrate diffuse high T2-weighted (or STIR) signal intensity related to edema in the soft tissues as one of the most fre-quent positive findings when evaluating the diabetic foot.24 The edema most fre-quently involves the plantar foot and less frequently involves the dorsal subcutane-ous soft tissues.24 In the absence of clini-cal signs of infection and cellulitis, edema may be secondary to vascular insufficiency or peripheral neuropathy alone versus a combined effect of these common prob-lems. Cellulitis may be diagnosed when there is subcutaneous thickening/reticula-tion with fluid collections on T2-weighted images and when subcutaneous tissue or superficial fascia or both show contrast enhancement, most often in a diffuse

pattern38 At times, focal cellulitis may be seen as abnormal signal intensity tracking from an ulcer or a region of osteomyeli-tis. A sinus tract may appear as low sig-nal intensity on a T1-weighted MR image with high T2-weighted signal intensity in the tract (Figure 15A and 15B). Following administration of intravenous contrast, enhancement of the wall of the tract may be observed (Figure 15C).

A bone scan is often used to determine if there is cellulitis alone or concomitant osteomyelitis. In a setting of cellulitis, a bone scan demonstrates increased flow during the first phase (angiographic) and in the second phase (blood pool). On the third phase (delayed), the increased soft tissue activity (hyperemia) in a setting of cellulitis clears owing to renal excre-tion of the tracer, and the underlying bone is scintigraphically normal (Figure 16A-16C).

In the diagnosis of soft tissue abscess, CT or MR imaging may be used success-fully (Figure 14), particularly with the

A B

C




bubbles, if present, appear as focal sig-nal voids on both T1- and T2-weighted images. Gadolinium contrast material is not necessary for diagnosis, although it may be helpful in detecting abscesses and pyomyositis, bearing in mind that the degree of contrast enhancement may cause the extent of disease to be under-estimated owing to hypoperfusion and

tissue necrosis.45 Comparatively, patients with pyomyositis show a significantly greater prevalence of diffuse hyperin-tense fat-suppressed T2-weighted sig-nal intensity (edema and inflammation) in the affected muscle (or muscles), dif-fuse muscular contrast enhancement, and thick irregular enhancement of the deep fascia, with or without intramus-cular abscess formation observed as small areas of intramuscular contrast rim enhancement44 (Figure 19A-19C).

MyonecrosisA number of conditions can cause myo-

necrosis, to include severe ischemia, diabetic myonecrosis, compartment syn-drome, crush injury, rhabdomyolysis, sickle cell crisis, and intra-arterial chemo-therapy.46 Diabetic myonecrosis is a dis-tinctive myopathy associated with poorly controlled diabetes mellitus.47-50 Although the clinical features of severe pain, mild physical findings, and, at times, a low-grade fever are most frequently observed in the thigh muscles, the leg muscles may occasionally be involved down to the level of the ankle. A poorly controlled diabetic patient may present with lower extremity findings related to this entity and not infection. MR images demon-strate marked edema and enhancement around often irregular masslike regions of muscle necrosis (Figure 20A and 20B). Myonecrosis can simulate an abscess, clinically and with MR imaging. Clinical correlation for evidence of an underly-ing condition associated with myonecro-sis may allow an unnecessary aspiration to be avoided.

On a smaller scale, tenosynovitis is an additional localized soft tissue problem to briefly mention. A small quantity of fluid in a tendon sheath is frequently observed in diabetic foot studies and is nonspe-cific. However, infected tenosynovitis may be suspected if there is gross distention of the sheath or abnormal signal intensity within or about a tendon sheath (Figure 21A and 21B), particularly if located adja-cent to an ulceration or if other clinical signs of an infection exist (Figure 21B). In general, infected fluid within a sheath cannot be distinguished from uninfected

Figure 15.

Plantar forefoot sinus tract underlying third metatarsal osteomyelitis. (A) Axial T1-weighted magnetic resonance image showing low signal intensity in the superficial plantar soft tissues (arrow). (B) Corresponding fat-suppressed T2-weighted image illustrating increased signal intensity along the wall. (C) Fat-suppressed contrast-enhanced T1-weighted image showing enhancement of the wall of the sinus tract (arrow). The sinus tracks to the third metatarsal, which shows cortical disruption, high T2-weighted marrow signal intensity inflammation, and enhancement secondary to osteomyelitis (asterisks).

Liquefactive tissue necrosis and inflam-matory edema both create fascial fluid that is detected with MR imag-ing as peripheral band-like hyperintense T2-weighted signal intensity in muscles on fat-suppressed images, peripheral band-like contrast enhancement of mus-cles, and thin smooth enhancement of the deep fascia44 (Figure 18A-18C). Gas

A

B

C




fluid with MR imaging because both will appear as high T2-weighted signal inten-sity fluid.

If ultrasonography is used to evalu-ate fluid collections within the soft tis-sues, the appearance of simple fluid is characteristic and appears hypoechoic or black on ultrasound imaging with an absence of echoes. An abscess is charac-teristically seen as fluid containing mul-tiple internal echoes, seen to move and swirl on compression, and can be reli-ably diagnosed or suggested with ultra-sound. If there is clinical suspicion of tendon pathology, the ability to dynam-ically assess tendons by passive and active movements during imaging allows for a reliable assessment of tendon integrity. In complete tendon tears, the end of a retracted tendon can be located and marked before operative interven-tion, with the exception of the tibialis posterior and peroneus longus ten-dons, which are more difficult to visu-alize because they pass more distal to the navicular bone and the inferolateral cuboid margin, respectively.

PostreconstructionKnowledge of any previous surgical,

traumatic, or iatrogenic manipulation is essential when interpreting the radio-logic studies of a diabetic patient’s foot. Whether it be postsurgical debridement, vascular surgery, endovascular interven-tion, or soft tissue and skeletal recon-struction, a detailed history is paramount for accurate interpretation of all patient studies.

Radiologic evaluation of surgical repair of unstable diabetic neuropathic osteoar-thropathy of the foot and ankle remains a challenge, with little specific informa-tion available in the medical or radiologic literature. More frequent surgical inter-vention with the use of external fixation, with or without combined internal fixa-tion, is being observed in daily radiologic practices following difficult limb salvage procedures. For the evaluation of the postoperative foot, 3-dimensional CT car-ries an advantage over traditional axial and multiplanar reformatted imaging by

Figure 16.

Cellulitis, differentiation from osteomyelitis on bone scan. Increased flow (arrow) during (A) the first phase (angiographic) and (B) the second phase (blood pool). (C) In the third phase (delayed, 2-3 hours), the increased soft tissue activity (hyperemia) in a setting of cellulitis clears owing to renal excretion of the tracer. The underlying bone is scintigraphically normal.

Figure 17.

Abscess. (A) Soft tissue bone window computed tomography image of the foot demonstrating hindfoot osseous destruction and an abscess (arrow) with gas bubbles about the periphery of the collection. (B) T2-weighted magnetic resonance image showing smooth-margined focus of high signal intensity consistent with abscess formation.

A B C

A B




being used to achieve wound cover-age and closure. Complication rates can be high for pedicle flaps in patients with diabetes.53 Venous congestion with subse-quent flap necrosis is the most common complication associated with pedicle flaps around the foot and ankle.53 Wound reconstruction and amputation sites are prone to ulcer formation and infection. The differentiation between osteomy-elitis and cellulitis at an amputation site remains extremely difficult; however, gad-olinium enhancement of the bone mar-row in osteomyelitis assists in making the distinction (Figure 10A-10D). MR images can be useful to document the progres-sion of disease or healing of postoperative complications.

SummaryThis writing focuses on the utility of mul-

tiple diagnostic modalities that are avail-able and beneficial for imaging of the diabetic foot. There is not yet “one best test” for sorting out the diagnostic dilem-mas that are commonly encountered. Conventional radiography, although use-ful for defining anatomy, is neither sen-sitive nor specific in the diagnosis of osteomyelitis or soft tissue infections. Three-phase bone scintigraphy is sensi-tive; however, it is not specific. Indium-111-labeled leukocyte imaging and MR imaging are both useful and comple-mentary. On one hand, labeled leuko-cyte scans are valuable for diagnosis and subsequent evaluation of osteomyeli-tis following treatment. On the other, MR imaging offers exquisite anatomic detail, which is invaluable for guidance of surgi-cal management.

Infection of the neuropathic joint is infrequent yet is often a diagnostic dilemma. The extensive osseous changes that are often present severely dimin-ish the value of radiography and bone scintigraphy. It is not always possible to distinguish marrow edema of neuropa-thy from that of osteomyelitis. Although there is a role for MR imaging in this sit-uation, it is not always clear or consis-tent, and it depends on various clinical situations.

Figure 18.

Fasciitis. (A) T1-weighted axial magnetic resonance image just above the ankle in a diabetic patient correlating with (B) fat-suppressed T2-weighted image showing anterior compartment peripheral and deep fascial high signal intensity inflammation/edema (arrow) and (C) peripheral-subcutaneous contrast enhancement (asterisk) and deep fascial thin smooth contrast enhancement (arrow) on a postcontrast T1-weighted image.

markedly diminishing artifact associated with the presence of hardware. Three-dimensional CT is an effective means of examining postsurgical patients for the integrity of their hardware and the course of their healing. Potential postsurgical complications such as nonunion, osteol-ysis, new fracture, and heterotopic ossifi-cation are all well assessed by 3D CT.51

In cases complicated by surgery, the bone scan alone can give significant false-positive results, and supplemen-tal imaging with radiolabeled leukocyte studies can aid in improving diagnos-tic specificity. Berquist et al compared the use of several imaging modalities in 42 patients with suspected postsur-gical osteomyelitis52 (Figure 12A-12D).

Sixty-four percent of the patients had undergone surgery before their diagnos-tic imaging, and 36% were referred for the differentiation of acute osteomyelitis from other pathologic conditions. CT and MR imaging studies were directly com-pared in 12 cases. Given the results of their study, the authors concluded that MR imaging demonstrated the presence and extent of infection more definitively than did CT. Despite this, they found that it was difficult to differentiate postop-erative changes from infection and that indium-111 WBC scans were even more specific than MR imaging or CT in these patients.52

In many complex wounds, plastic and reconstructive surgical techniques are

A B

C




Uptake of indium-111 leukocytes in the absence of infection may occur and is owing, at least in part, to early inflam-mation of the bone and joint in neu-ropathic osteoarthropathy and, also in part, to hematopoietically active marrow. Combined 3-phase bone, indium-111 leukocyte, and sulfur colloid marrow imaging offers considerable diagnostic accuracy and can be useful to the clini-cian in assessment of the diabetic foot.

Necrotizing fasciitis is a rapidly progres-sive soft tissue infection with a high mortality rate if treatment is delayed. Rapid diagnosis and prompt debridement are necessary, and plain radiography and cross-sectional imaging techniques have been used to expedite the diagno-

sis. Whichever modality is employed, the goal of imaging is to hasten the diagnosis and treatment; however, treatment should not be delayed to facilitate imaging.54

MR imaging shows high sensitivity and specificity for diagnosing osteomyeli-tis of the foot and for identifying asso-ciated soft tissue abnormalities such as cellulitis, abscesses, sinus tracts, and ulcers. However, the downside of MR imaging of soft tissue problems is that MR images may show nonspecific high T2-weighted signal intensity in the soft tissues that may be secondary to inflam-mation, infection, neuropathy, or vascular insufficiency.

PET imaging has great promise for becoming the study of choice in the

Figure 19.

Pyomyositis. (A) T1-weighted axial magnetic resonance image of the foot in a diabetic patient, correlating with (B) fat-suppressed T2-weighted image showing plantar muscle diffuse high signal intensity (arrow) edema and inflammation. (C) Postcontrast T1-weighted image shows small areas of intramuscular contrast rim enhancement (arrow).

Figure 20.

Myonecrosis. (A) Fat-suppressed T2-weighted axial magnetic resonance image of the leg in a diabetic patient, showing anterior compartment diffuse muscular high signal intensity edema/inflammation (box) correlating with (B) fat-suppressed T1-weighted postcontrast image demonstrating muscular peripheral contrast enhancement (box).

often complex diabetic foot setting. One problem related to its underusage is that F18 FDG PET is expensive and not yet approved by Medicare as a reimburs-able diagnostic test for the evaluation of infection. Although it has been success-fully used for the detection of prosthetic infection, it is not yet reimbursable for this use. Nonetheless, the study may be approved for individual use in the detec-tion of infection on a case-by-case basis if a physician makes a special request for approval and can show that the con-dition is not adequately demonstrated by any other radiologic or nuclear medi-cine test.

A B

C

A

B




Figure 21.

Tenosynovitis. Axial magnetic resonance images of the ankle demonstrating (A) intermediate T1-weighted and (B) high fat-suppressed T2-weighted signal intensity fluid within the medial flexor tendon sheaths. High T2-weighted signal intensity inflammation is seen within the subcutaneous tissues, consistent with associated cellulitis. Note the peripheral reactive marrow edema (high signal intensity; arrows) within the tibia.

AcknowledgmentWe thank Mr. Patricio Hernandez for his literary excellence in composition of this article.

References1. Murphy WA, Totty WG, Destouet JM,

et al. Musculoskeletal system. In: Lee JKT, Sagel SS, Stanley RJ, eds. Computed Body Tomography With MRI Correlation. New York, NY: Raven Press; 1989:899-987.

2. Moore TE, Yuh WTC. Magnetic reso-nance imaging of the diabetic foot. In: Bloem JL, Sartoris DJ, eds. MRI and CT of the Musculoskeletal System: A Text-Atlas. Baltimore, MD: Williams & Wilkins; 1992:207-216.

3. Maurer AH, Millmond SH, Knight LC, et al. Infection in diabetic osteoarthropathy: use of indium-labeled leukocytes for diagnosis. Radiology. 1986;161:221-225.

4. Palestro CJ, Mehta HH, Patel M, et al. Marrow versus infection in the Charcot joint: indium-111 leukocyte and techne-tium-99m sulfur colloid scintigraphy. J Nucl Med. 1998;39:346-350.

5. Love C, Din AS, Tomas MB, et al. Radionuclide bone imaging: an illustrative review-1. Radiographics. 2003;23:341-358.

6. Schauwecker DS. The scintigraphic diagno-sis of osteomyelitis. AJR Am J Roentgenol. 1992;158:9-18.

7. Devillers A, Miosan A, Jean S, et al. Tecnetium-99m-HMPAO leukocyte scintig-raphy for the diagnosis of bone and joint infections: a retrospective study in 116 patients. Eur J Nucl Med. 1995;22:302-307.

8. Abreu SH. Skeletal uptake of indium-111 labeled white blood cells. Semin Nucl Med. 1989;19:152-155.

9. Filippi L, Schillaci O. Usefulness of hybrid SPECT/CT in Tc-99m HMPAO-labeled leukocyte scintigraphy for bone and joint infections. J Nucl Med. 2006;47(12):1908-1913.

10. Van der Wall H. Assessment of infec-tion. In: Murray IPC, Ell PJ, eds. Nuclear Medicine in Clinical Diagnosis and Treatment. New York, NY: Churchill Livingstone; 1994:963-981.

11. Lipsky BA, Berendt AR, Deery HG, et al. Diagnosis and treatment of dia-betic foot infections. Plast Reconstr Surg. 2006;117:212S-238S.

12. Yuh WTC, 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;152:795-800.

13. Wang A, Weinstein D, Greenfield L, et al. MRI and diabetic foot infections. Magn Reson Imaging. 1990;3:219-230.

14. Newman LG, Waller, Palestro CJ, et al. Leukocyte scanning with in-111 is superior to magnetic resonance imaging in diagno-sis of clinically unsuspected osteomyeli-tis in diabetic foot ulcers. Diabetes Care. 1992;15:1527-1530.

15. Croll SD, Nicholas GG, Osborn MA, Wasser TE, Jones S. Role of magnetic resonance imaging in the diagnosis of osteomyeli-tis in diabetic foot infections. J Vasc Surg. 1996;24(2):266-270.

16. Weinstein D, Wang A, Chambers R, et al. Evaluation of magnetic resonance imag-ing in the diagnosis of osteomyelitis in diabetic foot infections. Foot Ankle Int. 1993;14:18-22.

17. deWinters F, van de Wiele C, Vogelaers D, de Smet K, Verdonk R, Dierckx, RA. Fluorine-28 fluorodeoxyglucose-posi-tron emission tomography: a highly accu-rate imaging modality for the diagnosis of chronic musculoskeletal infections. J Bone Joint Surg Am. 2001;83(5):651-660.

18. Dumarey N, Egrise D, Blocklet D, et al. Imaging infections with 18F-FDG-labeled leukocyte PET/CT: initial experience in 21 patients. J Nucl Med. 2006;47(4):625-632.

19. Basu S, Chryssicos T, Houseni M, et al. Potential role of FDG PET in the setting of diabetic neuro-osteoarthropathy: can it dif-ferentiate uncomplicated Charcot’s neu-roarthropathy from osteomyelitis and soft tissue infection? Nucl Med Commun. 2007;28(6):465-472.

20. Schwegler B, Stumpe KD, Weishaupt D, et al. Unsuspected osteomyelitis is fre-quent in persistent diabetic foot ulcer and better diagnosed by MRI than by 18F-FDG PET or 99mTC-MOAB. J Intern Med. 2008;263(1):99-106.

21. Höpfner S, Krolak C, Kessler S, et al. Preoperative imaging of charcot neuroar-thropathy in diabetic patients: compari-son of ring PET, hybrid PET, and magnetic resonance imaging. Foot Ankle Int. 2004;25(12):890-895.

22. Zlatkin MB, Pathria M, Sartoris DJ, et al. The diabetic foot. Radiol Clin North Am. 1987;25:1095.

23. Sello EJ. Current concepts review: diagnos-tic imaging of the diabetic foot. Foot Ankle Int. 2009;30(6):568-576.

24. Moore TE, Yuh WTC, Kathol MH, et al. Abnormalities of the foot in patients with

A B




diabetes mellitus: findings on MR imaging. AJR Am J Roentgenol. 1991;157:813-816.

25. Lavery LA, Armstrong DG, Wunderlich RP, Mohler MJ, Wendel CS, Lipsky BA. Risk fac-tors for foot infections in individuals with diabetes. Diabetes Care. 2006;29:1288-1293.

26. Spaeth HJ, Dardani M. Magnetic resonance imaging of the diabetic foot. Magn Reson Imaging Clin N Am. 1994;2(1):123-130.

27. Alazraki N, Dries D, Datz F, Lawrence P, Greenberg E, Taylor A Jr. Value of a 24-hour (four-phase bone scan) in assessing osteomyelitis in patients with peripheral vascular disease. J Nucl Med. 1985;26:711-717.

28. Tronco G, Tomas MB, Palestro CJ. Four-phase bone scintigraphy and osteomy-elitis: a reevaluation. Clin Nucl Med. 1999;24(3):216.

29. Keidar Z, Militianu D, Melamed E, Bar-Shalom R, Israel O. The diabetic foot: ini-tial experience with F-18-FDG PET/CT. J Nucl Med. 2005;46(3):444-449.

30. Vartanians VM, Karchmer AW, Giurini JM, Rosenthal DI. Is there a role for imaging in the management of patients with diabetic foot? Skeletal Radiol. 2009;38(7):633-636.

31. Unger E, Moldofsky P, Gatenby R, Hartz W, Broder G. Diagnosis of osteomyeli-tis by MR imaging. AJR Am J Roentgenol. 1988;150(3):605-610.

32. Erdman WA, Tamburro F, Jayson HT, et al. Osteomyelitis: characteristics and pitfalls of diagnosis with MR imaging. Radiology. 1991;180(8):533-539.

33. Morrison WB, Schweitzer ME, Wapner KL, et al. Osteomyelitis in feet of diabetics: clinical accuracy, surgical utility, and cost-effectiveness of MR imaging. Radiology. 1995;196:557-564.

34. Tan PL, Teh J. MRI of the diabetic foot: dif-ferentiation of infection from neuropathic change. Br J Radiol. 2007;80(959):939-948.

35. Palestro CJ, Tomas MB. Scintigraphic eval-uation of the diabetic foot. In: Freeman LM, ed. Nuclear Medicine Annual 2000. Philadelphia, PA: Lippincott Williams & Wilkins; 2000:143-172.

36. Dumarey N, Egrise D, Blocklet D, et al. Imaging infection with F-18-FDG-labeled leukocyte PET/CT: initial experience in 21 patients. J Nucl Med. 2006;47:625-632.

37. Basu S, Chryssikos T, Moghadam-Kia S, Zhuang H, Torigian D, Alavi A. Positron emission tomography as a diagnostic tool in infection: present role and future possibilities. Semin Nucl Med. 2009;39(1):36-51.

38. Schmind MR, Kossman T, Duewell S. Differentiation of necrotizing fasciitis and cellulitis using MR imaging. AJR Am J Roentgenol. 1998;170(3):615-620.

39. Nguyen VD. The radiologic spec-trum of abnormalities of the foot in dia-betic patients. Can Assoc Radiol J. 1992;43(5):333-339.

40. Struk D, Munk P, Lee M, Ho S, Worsley D. Imaging of soft tissue infections. Radiol Clin North Am. 2001;39:277-301.

41. Walshaw C, Deans H. CT findings in necro-tizing fasciitis: a report of four cases. Clin Radiol. 1996;51:429-432.

42. Donnelly L, Frush D, O’Hara S, Bissett G. Necrotizing fasciitis: an atypical cause of acute abdomen in an immu-nocompromised child. Pediatr Radiol. 1998;28:109-111.

43. Becker M, Zbaren P, Hermans R, et al. Necrotizing fasciitis of the head and neck: role of CT in diagnosis and management. Radiology. 1997;202:471-476.

44. Seok JH, Jee WH, Chun KA. Necrotizing fasciitis versus pyomyositis: discrimination with using MR imaging. Korean J Radiol. 2009;10(2):121-128.

45. Miller T, Randolph D, Staron R, Feldman F, Cushin S. Fat-suppressed MRI of mus-culoskeletal infection: fast T2-weighted techniques versus gadolinium-enhanced T1-weighted images. Skeletal Radiol. 1997;26:654-658.

46. May DA, Disler DG, Jones EA, Balkissoon AA, Manaster BJ. Abnormal signal inten-sity in skeletal muscle at MR imaging: pat-terns, pearls, and pitfalls. Radiographics. 2000;20:295-315.

47. Nunez-Hoyo M, Gardner CL, Motta AO, Ashmead JW. Skeletal muscle infarction in diabetes: MR findings. J Comput Assist Tomogr. 1993;17:986-988.

48. Van Slyke MA, Ostrov BE. MRI evaluation of diabetic muscle infarction. Magn Reson Imaging. 1995;13:325-329.

49. Kiers L. Diabetic muscle infarction: mag-netic resonance imaging (MRI) avoids the need for biopsy [letter]. Muscle Nerve. 1995;18:129-130.

50. Chason DP, Fleckenstein JL, Burns DK, Rojas G. Diabetic muscle infarction: radiologic evaluation. Skeletal Radiol. 1996;25:127-132.

51. Fayad LM, Patra A, Fishman EK. Value of 3D CT in defining skeletal complica-tions of orthopedic hardware in the post-operative patient. AJR Am J Roentgenol. 2009;193:1155-1163.

52. Berquist TH, Brown ML, Fitzgerald R, et al. Magnetic resonance imaging: application in musculoskeletal infection. Magn Reson Imaging. 1985;3:219-230.

53. Zgonis T, Stapleton JJ, Roukis TS. A stepwise approach to the surgical management of severe diabetic foot infections. Foot Ankle Spec. 2008;1:46-53.

54. Fugitt B, Puckett ML, Quigley MM, Kerr SM. Necrotizing fasciitis. Radiographics. 2004;24:1472-1476.



〈Review 〉 Imaging of the Diabetic Foot - CiteSeerX

Documents

Transcript of 〈Review 〉 Imaging of the Diabetic Foot - CiteSeerX