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Gerhard W. Bock, M.D., FRCPC1,
John M. Embil, M.D., FRCPC2

1. Department of Radiology, University of Manitoba, Winnipeg, MB
2. Department of Medicine, Section of Infectious Diseases, University of Manitoba, Winnipeg, MB

Introduction
Osteomyelitis is a common complication in the foot of persons with diabetes, affecting approximately 15% of patients. Acute contiguous focus osteomyelitis is the most commonly observed form of osteomyelitis in the diabetic foot. This review will consider the pathophysiology of the diabetic foot as it relates to radiologic imaging, present the various radiologic imaging techniques available, and suggest an algorithmic approach to the radiographic imaging evaluation of the diabetic foot.

 

 


Pathophysiology
Peripheral neuropathy is the major factor in skin breakdown with subsequent ulcer formation possibly leading to osteomyelitis. Repetitive trauma without protective reflexes leads to a skin or soft tissue injury that may become primarily or secondarily infected.1,2 The motor neuropathy causes pes cavus and equinus deformities leading to abnormal pressure points with subsequent skin breakdown. The autonomic neuropathy leads to thick, dry skin that can fissure and crack leading to ulcers and sinus tracts. A neutrophilic vasculitis develops secondary to soft tissue infection.3 This leads to a breakdown of the soft tissue envelope surrounding the bone. The vascular insufficiency seen in persons with diabetes complicates this process resulting in worsening ulceration. Once this local process begins, it may progress and persist to become chronic as it often goes unnoticed due to lack of local sensation. This process results in a chronic osteomyelitis where infected non-viable bone is contained within a compromised soft tissue envelope.4 Early diagnosis is important to decrease morbidity and avoid amputation of digits or entire lower extremity.

In the absence of an ulcer, osteomyelitis is rare.5, 6 .Systemic findings are often absent. The presence of fever, chills or elevated white cell count are unreliable in establishing a diagnosis of osteomyelitis. Studies have shown that exposed bone either viewed directly or detected by gentle probing at the base of the wound correlates well with the diagnosis of osteomyelitis.5,6

Diagnostic Imaging
Imaging techniques for the diagnosis of osteomyelitis have a wide range of sensitivity, specificity and positive predictive value. The plain radiograph will only demonstrate bony abnormalities related to osteomyelitis 10-20 days after the bone infection has occurred and 40-70% of the bone has been resorbed.7,8 Despite this, the initial diagnostic imaging evaluation should begin with high quality detail plain radiographs. These studies can detect the presence of foreign bodies, soft tissue gas and evaluate for accessory ossicles, pre-existing foot deformities, prior surgery and fractures which can complicate and confuse further advanced imaging techniques.

The plain radiographs should be evaluated for the presence of soft tissue swelling, cortical destruction, and periosteal new bone formation indicating the presence of active osteomyelitis. Previous radiographs if available should be reviewed, particularly if interval surgery has been performed. The reported sensitivity and specificity of plain film radiography varies widely. Combining multiple studies from the literature results in a mean specificity and sensitivity of 72% and 61% respectively 6,9-17 and a positive predictive value of 80%.

Nuclear Medicine
Nuclear Medicine techniques include three or four-phase bone scans, gallium scintigraphy and labeled white cell studies. A three phase bone scan consists of an initial blood flow or angiographic phase obtained immediately after injection of the radiopharmaceutical (technetium 99m-MDP), a blood pool phase obtained several minutes after injection and a final or delayed phase, 4-6 hours post injection. In soft tissue infections, the first two phases demonstrate increased uptake but the third phase is normal or slightly increased. In osteomyelitis, all three phases demonstrate increased activity with the third phase showing focal uptake in the area of osteomyelitis. In cases of neuropathic arthropathy, similar findings may be observed. To improve the specificity for osteomyelitis in these cases, a delayed 24-hour fourth phase may be performed. In osteomyelitis, there is continued increased uptake versus the neuropathic foot. As this technique requires an intact and patent blood supply, false negative scans may result in patients with vascular insufficiency. Reported sensitivities range from 75-100 % in the literature with a mean of 88%. Specificity is lower as a result of vascular insufficiency and complicating neuroarthropathy ranging from 0-75% with a mean of 36%.6,9-16,18,19

Gallium scintigraphy is based on the localization of radiotracer (gallium 67 citrate) in areas of osteomyelitis by granulocytes. This is a result of binding to lactoferrin in bacteria and granulocytes. Gallium is also taken up by bone at site of remodeling decreasing specificity. Gallium scans are usually combined with bone scanning. Differential uptake of gallium indicates osteomyelitis. The low specificity of this technique and the availability of white cells scans with improved specificity have limited the use of gallium.

White cell scans are based on labeled leukocytes (indium 111) which accumulate in infected areas. Leukocytes may also be labeled with technetium 99 HMPAO. The advantage of technetium 99m HMPAO is that the radionuclide is more readily available and larger doses can be administered improving image quality. Specificity is limited by adjacent soft tissue infection and to improve sensitivity, the technique is usually combined with bone scans. Reported sensitivities range from 75-100% with a mean of 93% and specificities ranging from 69-100% with a mean of 80%.6,8,12,14,18-20 As stated earlier, all of these nuclear medicine techniques are limited in the presence of ischemia in the lower extremity.

Computed Axial Tomography
Computed tomographic (CT) scanning can be used to evaluate the more advanced stages of osteomyelitis. This technique allows for the evaluation of the soft tissues as well as assessing bone destruction and the presence of sequestra and gas. It can be used to assist in surgical planning, however, the advent of magnetic resonance (MR) imaging has made this a less useful modality.

Magnetic Resonance Imaging
Magnetic resonance imaging has been shown to be more sensitive and more specific than the previously described nuclear medicine techniques.13,15,17,21,22 Additionally, MR allows anatomic definition and lesion characterization.23. It can distinguish between cellulitis, soft tissue abscess, septic arthritis and osteomyelitis.23, 24. By allowing precise anatomic definition and lesion characterization, it aids in biopsy and surgical planning.25. This technique has also been shown to be cost-effective in the management of complicated osteomyelitis.25.

To achieve the high sensitivity and specificity of MR in the evaluation of osteomyelitis, close attention to technique is required. A small field of view and higher resolution matrix need to be employed. The imaging planes must be optimized and the use of fat suppression and gadolinium administration furthers this technique. In osteomyelitis, the signal intensity of the marrow demonstrates a decreased signal intensity similar to muscle on T1 weighted images and demonstrates a markedly increasing intensity on T2 weighted sequences. The presence of cortical destruction confirms the diagnosis of osteomyelitis. Differentiation from neuropathic osteoarthropathy remains a challenge.24 The location of the signal abnormalities and polyarticular involvement in neuropathic osteoarthropathy can be helpful to distinguish this entity from osteomyelitis. The most significant limitation to the use of MR imaging is the availability of the technique.

Diagnostic Approach
Given the multiple techniques and variable sensitivity and specificity for the diagnosis of osteomyelitis, it is useful to develop a rational approach which combines clinical evaluation and imaging investigations. (Chart 1). The first stage of the evaluation should be the physical examination. Specifically it should be established whether an ulcer or draining sinus is present. If present, using a probe, determine whether bone can be palpated at the base of the lesion. If bone can be palpated, a diagnosis of osteomyelitis can be presumed and treatment may be initiated accordingly.5 If, however, bone cannot be palpated but clinical suspicion persists, obtain a baseline plain radiograph and repeat in 10-21 days. In the intervening period, osteomyelitic changes should be visible radiographically. If clinical suspicion of osteomyelitis is present, therapy may be initiated pending a follow-up plain radiograph. If suspicion persists but the evaluation has been unhelpful, further evaluation with MR imaging, if available, may be warranted. In the setting of ischemia or neuroarthropathy, MR imaging may be more sensitive and specific than nuclear medicine techniques. If MR imaging is not available, technicium bone scanning combined with white cell scans may be a consideration.

Conclusions
Extensive non-invasive investigations may generate significant expense without significant improvement in health outcomes for those persons with diabetes whom foot osteomyelitis is suspected.26 Careful clinical evaluation combined with an algorithmic approach to imaging as discussed above will lead to the most cost-effective and efficient care.



Chart 1: Simplified approach for the evaluation of a diabetic foot with suspected osteomyelitis (modified from Lipsky, 1997)

References
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