MRI of the diabetic foot: differentiation of infection from neuropathic ...

The British Journal of Radiology, 80 (2007), 939–948

PICTORIAL REVIEW

MRI of the diabetic foot: differentiation of infection from neuropathic change P L TAN,

MRCP, FRCR

and J TEH,

BSc, MRCP, FRCR

Nuffield Orthopaedic Centre NHS Trust, Windmill Road, Headington, Oxford OX3 7LD, UK

ABSTRACT. The aim of this review is to illustrate the magnetic resonance imaging features that can help differentiate osteomyelitis from neuropathic osteoarthropathy in the foot.

Received 31 October 2005 Revised 14 February 2006 Accepted 7 March 2006 DOI: 10.1259/bjr/30036666 ’ 2007 The British Institute of Radiology

Soft tissue and bone infection involving the foot is particularly common in patients with diabetes mellitus. In these patients, neuropathic osteoarthropathy often coexists. Differentiating between these two entities is often difficult but crucial as the management may differ significantly. Early and accurate diagnosis of foot infection is imperative as it allows prompt initiation of appropriate therapy such as antibiotics and surgical debridement, thereby avoiding future complications. Almost all foot infections result from contiguous spread [1]. Skin ulceration, secondary to diabetes, peripheral vascular disease, peripheral neuropathy, altered biomechanics, or trauma are particular risk factors. Direct implantation of infectious material into the bone, following surgery or penetrating injuries, represents another important route for infection. Haematogenous spread is not commonly seen in the foot but may be encountered in children and adolescents, or with unusual organisms such as Mycobacterium tuberculosis [2, 3]. In these cases there is usually no confusion over the clinical diagnosis. Neuropathic osteoarthropathy occurs as a result of chronic, repetitive trauma to the joints and supporting ligaments of the foot. The typical patient is a long-standing diabetic with a dense peripheral neuropathy and peripheral vascular disease. Peripheral neuropathy causes reduced perception to trauma and the peripheral vascular disease produces ischaemia, resulting in poor healing, joint instability, deformity and increased new bone formation. Cartilage damage is also a feature, resulting in a progressive arthropathy with erosions and subchondral cysts. Typically in neuropathic osteoarthropathy, the midfoot or tarso-metatarsal (Lisfranc) joints are affected. This leads to a collapse of the longitudinal arch and increased load bearing on the cuboid, resulting in a ‘‘rocker-bottom’’

Address correspondence to: Dr James Teh, Department of Radiology, Nuffield Orthopaedic Centre, Windmill Road, Headington, Oxford OX3 7LD, UK. E-mail: [email protected]

The British Journal of Radiology, November 2007

deformity (Figure 1). Both acute and chronic forms of neuropathic arthropathy are recognized [4]. The aim of this review is to illustrate the MRI features that can help differentiate osteomyelitis from neuropathic osteoarthropathy in the foot.

MRI: applications and techniques MRI is a powerful, non-invasive tool for determining the presence or absence of osteomyelitis in the diabetic patient. Although the use of bone scintigraphy and white cell scans have been advocated for the differentiation of osteomyelitis from neuropathic osteoarthropathy [5–7], there is now clear evidence that MRI [8–12] (combined with plain radiographs) offers the highest diagnostic accuracy. MRI protocols of the foot vary widely. When attempting to differentiate between suspected infection and neuropathic osteoarthropathy, high resolution, small field of view studies must be used. Examinations may be limited to the forefoot, midfoot or hindfoot and may even be restricted to an individual phalanx for optimal detail. The images are usually obtained with a small field of view (8–10 cm), with thin sections (3–4 mm) to optimize spatial resolution. Studies of the entire foot should be performed if there is concern of the extent of spread. The routine examination is performed with the patient lying supine with the foot positioned in an extremity coil. Alternatively the forefoot may be imaged in the prone position with the toes in an extremity coil. The foot is normally placed in the neutral position but may be plantar flexed if there is concern regarding the tendons. The scan planes should be tailored for each individual examination. For example, axial images allow good depiction of the tendons and delineate the compartments well, whereas coronal and sagittal images are better suited to ulcer and sinus tract evaluation. A minimum of two planes should be obtained. In the authors’ department the typical examination includes sagittal T1 939

P L Tan and J Teh

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Figure 1. (a) Chronic neuroarthropathy. Sagittal T1 weighted image demonstrating a ‘‘Rocker-bottom’’ appearance of the foot in a patient with diabetic neuroarthropathy. There is induration of the subcutaneous tissues at the site of a chronic healing ulcer (arrowheads). There is midfoot joint disruption and disorganization (arrow). (b) Sagittal short tau inversion recovery (STIR) image demonstrating preservation of the marrow signal despite the joint disorganization indicating a chronic neuroarthopathy.

weighted conventional spin echo (SE) and short tau inversion recovery (STIR) sequence along with coronal T1 SE and T2 fat-saturated sequences. The T1 weighted sequences allow excellent depiction of both normal and abnormal anatomy, whereas the T2 fatsaturated and STIR sequence are better at demonstrating oedema and inflammatory change in the soft tissues and bone. Although some studies recommend the routine use of gadolinium [10, 13], others suggest that it is unnecessary [14–16]. There is no convincing evidence that contrast improves the diagnostic accuracy for osteomyelitis, but it is clear that its use improves the evaluation of soft tissue pathology as it helps to demonstrate abscesses and sinus tracts more easily (Figure 2). The use of contrast may also allow differentiation of viable from non-viable bone or soft tissue (Figure 3).

Differentiating osteomyelitis from neuropathic osteoarthropathy MRI, with its high soft tissue contrast resolution and multiplanar capabilities, has been increasingly used over the last decade to evaluate the extent of the foot infection

[17, 18]. The presence of osteomyelitis [19, 20] and soft tissue infection [21] can be accurately determined by MRI. MRI for foot infection may reveal evidence of ulceration, oedema and localized fluid collections in the soft tissues, joints and tendon sheaths, and may demonstrate osteomyelitis, septic arthritis and necrosis. In diabetic patients, osteomyelitis and neuropathic osteoarthropathy of the foot often coexist, although one or other may be predominant. Differentiating these conditions can be a clinical and radiological challenge. Both entities may demonstrate bone marrow oedema and enhancement, joint effusion and surrounding soft tissue oedema [15]. To make a diagnosis the appearances and distribution of the abnormalities, and their correlation with the clinical features is required. There are several MRI features that are useful in helping to differentiate these entities (Table 1) which are discussed below.

Bone marrow signal change On MRI, osteomyelitis is characterized by altered bone marrow signal, with low signal on T1 weighted images,

Table 1. Features that help differentiate osteomyelitis from neuropathic osteoarthropathy Osteomyelitis

Neuroarthropathy

Bone marrow signal change

High signal on T2 and STIR. Low on T1. Demonstrates enhancement

Bone marrow oedema pattern

Tends to affect single bone with diffuse bone marrow involvement Focal involvement Weight bearing regions; toes, metatarsal heads, calcaneus Usually no deformity unless there is an underlying neuropathic joint High association with overlying ulcer, abscess or sinus tract

Acute: mimics osteomyelitis. Chronic: normal marrow signal or low on T1 and T2 Tends to be periarticular and subchondral

Distribution Typical location Deformity Soft tissue changes

Several joints/bones involved Predominant midfoot involvement Deformity is common along with bony debris Overlying skin is usually intact but may be oedematous

STIR, short tau inversion recovery.

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Pictorial review: MRI of the diabetic foot

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Figure 2. (a) Abscess and osteomyelitis. Axial T1 weighted image demonstrating low signal in the first metatarsal head (arrow) indicating osteomyelitis. (b) Axial T1 weighted image following intravenous gadolinium. There is rim enhancement of a collection adjacent to the first metatarsal head (arrows).

high signal on T2 weighted or STIR images, and enhancement post contrast [10]. Caution must be taken when viewing in the STIR sequence as the true extent of the infection may be overestimated, particularly if there is concomitant neuropathic disease or adjacent septic arthritis. Other MR findings that may be seen include cortical disruption and periostitis. Periostitis appears as a thin, linear pattern of oedema with enhancement surrounding the outer cortical margin. The latter may be thickened if the periostitis is chronic. It is noteworthy that periosteal

reaction other than at a metatarsal bone should alert one to the presence of an infection. Abnormal bone marrow signal in the appropriate clinical setting has a very high sensitivity for diagnosis of osteomyelitis. Other conditions such as fracture, tumour, inflammatory arthritis, neuropathic disease, infarction or recent post-operative surgery may also mimic this altered bone marrow signal [10, 22–25]. The presence of an intraosseous fluid collection is highly indicative of an intraosseous abscess. The ‘‘penumbra sign’’ is a characteristic MRI feature of subacute

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Figure 3. (a) Haematogenously acquired tuberculous osteomyelitis and arthritis with devitalized bony fragment. Sagittal short tau inversion recovery (STIR) sequence demonstrating diffuse midfoot joint infection with bone marrow oedema and synovitis. (b) Sagittal T1 weighted image following intravenous gadolinium demonstrates a non-enhancing bony fragment (arrow) indicating devitalization. There is diffuse marrow and synovial enhancement in the midfoot.


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Figure 4. (a) The ‘‘penumbra sign’’ in subacute osteomyelitis. Coronal T1 weighted image of the hindoot demonstrating an intermediate signal rim (arrow) around a central area of lower signal intensity indicating an intra-osseous abscess in the talus. (b) Coronal short tau inversion recovery (STIR) image demonstrating a fluid signal collection in the talus consistent with an abscess.

osteomyelitis. It describes a discrete peripheral zone of higher signal intensity than the central abscess cavity and the surrounding lower signal intensity of marrow oedema on unenhanced T1 weighted images (Figure 4). Neuropathic osteoarthropathy may present with one of two distinct patterns on MRI, depending on the chronicity of the articular process. MRI is an effective technique for distinguishing between osteomyelitis and chronic neuropathic osteoarthropathy [26]. The characteristic findings of chronic neuropathic osteoarthropathy are cortical fragmentation, joint deformity or subluxation, accompanied by altered bone marrow signal manifested by low signal intensity in the subchondral bone on both T1 and T2 weighted images, a finding that correlates with osteosclerosis radiographically [15, 26] (Figure 1). Periosteal new bone is observed exclusively in the metatarsal bones and phalanges [27]. In the acute form, alterations in bone marrow signal may be similar to osteomyelitis (i.e. low signal on T1 and high signal on T2 and STIR, with associated contrast enhancement). However, the distribution and pattern of oedema can be helpful in differentiating these two conditions. Neuropathic osteoarthropathy is primarily an articular disease, thus the oedema tends to be juxta-articular, centred on subchondral bone, whereas the oedema in osteomyelitis tends to be more diffuse and is generally greater on one side of the joint. It should be noted that the bone marrow oedema associated with infective or 942

inflammatory arthropathies is also usually subchondral in distribution (Figure 5). Joint effusions and periarticular erosions may occur in inflammatory, neuropathic and infective conditions.

Distribution The location of the disease is an important factor in differentiating between infection and neuropathic osteoarthropathy. Osteomyelitis is usually confined to a solitary site either in the metatarsal heads, toes or calcaneus [28]. Approximately 20% of patients have infection at two or more sites [29]. In contrast, neuropathic osteoarthropathy occurs most frequently in the intertarsal and tarsometatarsal joints (60% of cases), followed by the metatarsophalangeal joints of the forefoot (30% of cases) [27]. Involvement of the interphalangeal joints is uncommon. Although the site of involvement is helpful it is not consistently reliable. Neuropathic changes at the metatarsophalangeal and interphalangeal joints are frequently associated with skin ulceration, whereas involvement of the tarsometatarsal and intertarsal joints is rarely associated with ulceration until the midfoot is sufficiently collapsed to elicit new pressure points (Figure 1). The calcaneal insufficiency avulsion fracture is an extraarticular fracture of the posterior third of the calcaneus that is seen almost exclusively in diabetic patients. The British Journal of Radiology, November 2007


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Figure 5. (a) Neuropathic arthropathy with proven infection. Sagittal T1 weighted image demonstrating midfoot disorganization with talonavicular dislocation. There is loss of the normal fatty marrow signal, with very low signal foci (arrows) seen, indicating devitalized bony fragments. (b) Sagittal short tau inversion recovery (STIR) image demonstrating extensive bone marrow oedema and adjacent cellulitis.

Osteoporosis combined with neuropathic change is thought to be the underlying cause. The process usually begins at the calcaneal tuberosity and extends superiorly. The avulsed fragment is eventually displaced superiorly due to the pull of the Achilles tendon, a finding that is not encountered in typical stress fractures [30] (Figure 6).

Ulceration

In over 90% of cases, osteomyelitis of the foot results from contiguous spread through the skin [28] with apparent soft tissue disease, including skin ulceration, cellulitis, soft tissue abscess or sinus tracts [14]. These features can be considered as secondary signs of osteomyelitis, and their presence can improve overall diagnostic accuracy [20]. Bone marrow signal abnormalities without adjacent soft tissue change are unlikely to represent infection.

Skin ulceration occurs most frequently on points of highest pressure [31]: the plantar aspect of the first and fifth metatarsophalangeal joints, the first toe and the heel [32]. Skin ulceration appears on MR images as an interruption of the cutaneous signal line, typically with an enhanced margin (Figure 7). Ulceration can be very subtle if only superficial skin erosion is present. In diabetic patients, ulcers are usually surrounded by a thick mound of soft tissue or callus with low signal on T1 and intermediate signal on T2 weighted images. Chronic ulceration may be associated with fibrous healing and thus appears as intermediate/low signal subcutaneous induration on STIR or T2 fat-saturated sequences. Any form of cutaneous interruption may act as a portal for soft tissue infection. Ulcers greater than 2 cm in depth are particularly susceptible to osteomyelitis [28, 33]. Osteomyelitis should be suspected when there is a

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Secondary signs of infection

Figure 6. (a) Diabetic insufficiency fracture of the calcaneus. Sagittal T1 weighted image demonstrating an insufficiency fracture of the calcaneus in a diabetic patient. (b) Sagittal short tau inversion recovery (STIR) image demonstrating high signal in the calcaneus indicating stress change.


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seen if the tract has not been actively draining. On unenhanced MRI, these tracts can be difficult to detect, as they may blend with adjacent soft tissue oedema. The most sensitive sequence for detecting sinus tracts is a post contrast fat-suppressed T1 weighted image, where the tract is seen as parallel lines of enhancement with a ‘‘tram-track’’ pattern [10] (Figure 9).

Cellulitis

Figure 7. Open heel ulcer. Sagittal T1 weighted image demonstrating a typical heel ulcer with a defect extending into the subcutaneous tissues with a slightly raised mound of tissue adjacent to the defect (arrows). There is evidence of cortical involvement in the calcaneus indicating osteomyelitis.

suspicious marrow signal abnormality in the adjacent bone on MRI in the presence of cutaneous defect (Figure 8).

Cellulitis is an acute inflammatory process of the subcutaneous tissue and fat, often in close proximity to areas of skin ulceration. On MRI, this is seen as replacement of the normal fat signal in the subcutaneous tissues on T1 weighted images, with high signal on T2 weighted or STIR images, and diffuse enhancement with intravenous gadolinium [11, 33] (Figure 10). The margins are generally poorly defined. Characterization of cellulitis can be difficult, as diffuse soft tissue oedema in the foot is frequently encountered in diabetic neuroarthropathy (Figure 11).

Tenosynovitis

Sinus tracts are common in osteomyelitis with adjacent skin ulceration [20]. On MRI, a sinus tract is characterized by a thin, discrete line of fluid signal extending through the soft tissues [10]. This fluid signal may not be

Septic tenosynovitis of the foot typically occurs as a result of contiguous spread of infection. MR evidence of tendon infection is present in approximately half the patients who require surgery for pedal infection [34]. MRI reveals disproportionate fluid within the sheath, which is often complex. Post contrast images may show a thick rim of enhancement around the tendon representing the proliferative, inflamed synovium (Figure 12).

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Sinus tract formation

Figure 8. (a) Chronic heel ulcer with osteomyelitis. Sagittal T1 weighted image demonstrating induration and flattening of the subcutaneous tissues down to the calcaneus. There is cortical disruption with marrow signal change. (b) Sagittal short tau inversion recovery (STIR) sequence demonstrating relative low signal at the ulcer site indicating chronic fibrosis. There is marrow oedema indicating osteomyelitis.

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with thick rim enhancement on post-contrast images [13, 35]. However, the rim enhancement is not seen in areas of tissue devitalization or severe ischaemia [36]. In this situation, fluid signal is often seen on T2 weighted images in a broader region demonstrating lack of enhancement compared with the surrounding tissue. This represents liquefied necrotic tissue. Identification of this process and abscesses in general can be of great help to surgeons as to the extent of debridement required.

Differentiating infected from non-infected neuropathic osteoarthropathy

Figure 9. Sinus tract with ‘‘tram track’’ pattern. Coronal T1 fat-saturated image following intravenous gadolinium demonstrating an enhancing deep sinus tract (arrow) extending down to the second metatarsal head. There is abnormal signal in the underlying bone marrow indicating osteomyelitis.

Abscess Long-standing infection is commonly associated with abscess formation, but it can also be seen in early aggressive cases. The reported incidence of soft tissue abscesses in patients with foot infection ranges from 10% [11] to 50% [26] on MRI. Abscesses usually occur in close vicinity to the area of skin breakdown or along adjacent fascial planes. However, as infection spreads along the compartments of the foot, abscesses may be seen remote to the area of skin ulceration. Abscesses often communicate with sinus tracts that extend to bones, joints, tendon sheaths or skin ulceration (Figure 13). Skin ulceration can itself result in spontaneous drainage of the abscess and produce a flattened appearance of a fluid collection on MRI. On MRI, an abscess is seen as a focal collection of signal that approximates fluid on T2 or STIR,

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The differentiation of infected from non-infected neuropathic arthropathy remains extremely challenging as the clinical and radiological findings may overlap. In many cases the only way to exclude infection is to perform biopsy. A recent retrospective study has shown that in patients with known neuropathic osteoarthropathy, sinus tract formation, replacement of soft tissue fat, fluid collections and extensive marrow abnormality are MRI features likely to indicate superimposed infection [37]. The following changes were found to be suggestive of osteomyelitis on follow-up MRI of neuropathic osteoarthropathy: progression of bone erosions, loss of subchondral cysts, increased marrow hyperintensity and enhancement of the articular surface.

Factors influencing decision to biopsy Bone biopsy remains the only diagnostic method for definitive discrimination between osteomyelitis and neuropathic osteoarthropathy. This is not, however, always practical and can potentially lead to seeding of infection or damage to the area biopsied. If biopsy is performed, bone specimens can be obtained either percutaneously, under image guidance or by open surgery. The gold standard for diagnosing osteomyelitis

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Figure 10. (a) Cellulitis and midfoot haematogenous osteomyelitis. Sagittal T1 weighted image demonstrating extensive cellulitis of the mid and forefoot with loss of the normal subcutaneous fat signal (arrowheads). (b) Sagittal short tau inversion recovery (STIR) image demonstrating extensive cellulitis (arrowheads) in a patient with osteomyelitis affecting the mid and hindfoot (arrows).


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Figure 11. (a) Acute neuroarthropathy with soft tissue oedema. Sagittal T1 weighted image demonstrating loss of the normal fatty marrow signal in the midfoot and loss of the normal signal from the subcutaneous tissues indicating oedema. (b) Sagittal short tau inversion recovery (STIR) image demonstrating bone marrow oedema and soft tissue oedema in the midfoot. The appearances may mimic infection both clinically and on imaging.

is isolation of bacteria from a reliably obtained sample of bone concomitant with histological findings of inflammatory cells and osteonecrosis. Bone biopsy may, however, yield false negative results either because of patchy infectious involvement or previous antibiotic therapy. With these limitations in mind, bone biopsy is recommended if the diagnosis remains in doubt after imaging, or if osteomyelitis is likely [38, 39].

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Conclusion With its increased general availability, MRI is being adapted more frequently as the primary imaging modality for the investigation of foot conditions. This is of particular use in the assessment of diabetic foot where the diagnostic picture is often complicated by changes related to infection, trauma, neuropathy and ischaemia.

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Figure 12. (a) Septic tenosynovitis. Sagittal short tau inversion recovery (STIR) image demonstrating a rim of high signal (arrows) enveloping the extensor hallucis longus (EHL) tendon indicating septic tenosynovitis. The tendon itself returns normal low signal. Note the presence of septic arthritis of the first metatarso-phalangeal joint. (b) Coronal T2 fat-saturated image demonstrating septic tenosynovitis of the EHL tendon.

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Figure 13. (a) Abscess arising from joint. Sagittal T1 weighted image demonstrating a rounded low signal mass (arrows) which appears to communicate with the first metatarso-phalangeal joint. (b) Sagittal short tau inversion recovery (STIR) image demonstrating a round fluid signal collection overlying the first metatarsophalangeal joint. There is periarticular oedema in the first metatarsal head indicating septic arthritis.

Osteomyelitis and neuropathic osteoarthropathy are processes that frequently overlap. It is therefore important to have a strategy when interpreting the MRI findings. Familiarity with the advantages and disadvantages of this imaging technique will enable radiologists to make important contributions to the care of the patients with these conditions.

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