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Musculoskeletal Imaging |
1 From the Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, Pa. Received July 26, 2001; revision requested September 12; revision received October 30; accepted December 10. Address correspondence to H.P.L., Department of Radiology, University Hospital Basel, Petersgraben 4, 4031 Basel, Switzerland (e-mail: hans-peter.ledermann@gmx.ch).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Contrast material–enhanced magnetic resonance (MR) imaging findings were reviewed for 161 feet in 51 women and 107 men (82% of whom had diabetes mellitus) who were suspected of having osteomyelitis and who underwent tissue diagnosis. Location of skin ulceration and presence of osteomyelitis (indicated by means of low T1-weighted signal intensity, high T2-weighted signal intensity, and contrast enhancement) and septic arthritis (indicated by synovial enhancement and adjacent cellulitis) were evaluated by two musculoskeletal radiologists.
RESULTS: In the forefoot, osteomyelitis occurred most frequently at the fifth metatarsal (n = 24), first metatarsal (n = 21), and first distal phalanx (n = 15). In the hindfoot, the calcaneus (n = 21) was involved most frequently. Osteomyelitis was directly adjacent to skin ulcers or surgical defects in all cases but one. Spread of osteomyelitis to adjacent bones in the forefoot occurred in 26 (16%) bones. Evidence of septic arthritis on MR images was present in 53 (33%) feet and involved most frequently the fifth (n = 13) and first (n = 8) metatarsophalangeal joints.
CONCLUSION: Pedal osteomyelitis results almost exclusively from contiguous infections and occurs most frequently around the fifth and first metatarsophalangeal joints. One-third of patients with advanced pedal infection show evidence of septic arthritis on MR images.
© RSNA, 2002
Index terms: Arthritis, septic, 46.26, 46.79 • Bones, infection, 465.211, 466.211, 467.211 • Cellulitis, 468.241 • Foot, infection, 468.21, 468.241 • Foot, MR, 468.121411, 468.121412, 468.121413, 468.121415 • Soft tissues, infection, 468.241
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Recently, magnetic resonance (MR) imaging has been increasingly used to evaluate the extent of pedal infections and to diagnose underlying osteomyelitis. Furthermore, MR imaging allows assessment of the presence and location of pedal ulcers (7) and the presence of concomitant septic arthritis (8,9).
This study was undertaken to evaluate the anatomic distribution of pedal osteomyelitis and septic arthritis in a large patient group with advanced pedal infection and to compare ulcer location with the distribution of osteomyelitis and septic arthritis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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One or more surgical procedures were performed on 49 feet prior to MR imaging. These included débridement (n = 24), toe amputation (n = 13), ray amputation (n = 9), transmetatarsal amputation (n = 4), internal reduction of a fracture (n = 3), and Chopart amputation (n = 1). The interval between these surgical procedures and MR imaging ranged between 2 days and 6 years (mean, 235 days ± 440 [SD]).
Our study was conducted after approval was obtained from our institutional review board to review patient images and medical charts. The board determined that this retrospective study could be conducted without informed patient consent.
MR Imaging
MR imaging was performed with a 1.5-T superconducting magnet (Signa; GE Medical Systems, Milwaukee, Wis). An extremity coil was used to image a total of 155 feet (field of view, 14–20 cm), and a head coil was used with six patients who underwent imaging of both feet (field of view, 16–20 cm). In the patients who underwent simultaneous imaging of both feet, subsequent surgery or biopsy was performed in only one foot per patient, and only that foot was included in the study. Images of all feet were obtained by means of at least two orthogonal planes.
T1-weighted spin-echo (SE) images were obtained with one to two signals acquired, a repetition time of 400–750 msec and an echo time of 8–20 msec (400–750/8–20), and a matrix size of 256 x 192 or 256 x 256. T2-weighted images were obtained by using a fast SE technique with two signals acquired, 2,000–7,800/75–108 (effective), an echo train length of eight, and a matrix size of 256 x 128 or 256 x 192. Contrast material–enhanced T1-weighted images were obtained in 30 feet by using a T1-weighted SE sequence and in 131 feet by using a fast multiplanar spoiled gradient-echo technique with 200–305/1.8–2.2, a flip angle of 90°, and a matrix size of 256 x 128 or 256 x 192. Gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) at a dose of 0.1 mmol per kilogram of body weight was used as the intravenous contrast agent. T1-weighted fast multiplanar spoiled gradient-echo sequences were performed with fat suppression before and after contrast agent administration. For T2-weighted and gadolinium-enhanced T1-weighted SE sequences, fat suppression was accomplished by using selective presaturation of lipid-resonance frequency. Fast SE short inversion time inversion-recovery (STIR) images were obtained with an echo train length of eight, 2,000–3,000/20–78 (effective), an inversion time of 150–160 msec, and a matrix size of 256 x 128 or 256 x 192. Fast SE STIR images were available for a total of 137 feet. Section thickness was 4 mm, and there was a 1-mm gap for most sequences.
Image Analysis
Diagnosis of a skin ulcer relied on recognition of a soft-tissue defect or an interruption of the skin line on any imaging sequence or plane (7). Cellulitis was defined as soft-tissue contrast enhancement with fat signal loss on T1-weighted images and hyperintense signal intensity on T2-weighted images when compared with that of surrounding muscle, as described by prior authors (9,10).
MR imaging criteria for the diagnosis of osteomyelitis were based on those described in previous studies (8,11), including focally decreased marrow signal intensity on T1-weighted images, focally increased signal intensity on fat-suppressed T2-weighted and fast SE STIR images, and focal marrow enhancement on gadolinium-enhanced fat-suppressed T1-weighted images. Osteomyelitis was also diagnosed if focal decrease of marrow signal intensity was absent on T1-weighted images in the presence of signal intensity increase on T2-weighted images and contrast-enhanced images (ie, discordant marrow signal intensity), as previously reported (7,12). Osteomyelitis in contiguous bones without evidence of direct infection of both bones by an ulcer or surgical defect was defined as osseous spread of osteomyelitis. The bone that had direct contact with the ulcer was defined as the primary bone. Evidence of septic arthritis had to be present between bones on MR images to qualify as osseous spread.
MR imaging criteria for the presence of septic arthritis were contrast enhancement of the joint capsule (10) and adjacent soft-tissue infection (13,14). Increased joint fluid was not necessary for this diagnosis, since erosion of the joint capsule of digital joints can lead to decompression of joint effusion.
To facilitate data acquisition, a spreadsheet was designed that contained two schematic drawings of the bones of the foot and ankle with anteroposterior and lateral projections. The foot and ankle were divided into three anatomic regions: forefoot (from the toes to the Lisfranc joint), midfoot (from the Lisfranc joint to the Chopart joint), and hindfoot (from the Chopart joint to the ankle joint, including the malleoli).
Two musculoskeletal radiologists (W.B.M., M.E.S.) reviewed all images by means of consensus. The reviewers were blinded to patient history and the presence and location of an ulcer. They did, however, know that all images were obtained to evaluate the presence of osteomyelitis. First, the reviewers determined the location of the ulcer or surgical defect on the MR images and noted its position in the anatomic diagram on the spreadsheet. Skin ulcerations and soft-tissue defects at postoperative sites of amputations and débridements were analyzed separately. Since postoperative soft-tissue defects often extended over an area of several bones, we noted the presence of such defects for each underlying bone separately.
Next, the reviewers determined the presence and location of osteomyelitis and septic arthritis on the MR images and marked their positions on the spreadsheet. In cases of contiguous spread of osteomyelitis from one bone to another, all infected bones and the direction of spread (ie, proximal or distal) were noted.
Comparison with Reference Standards
After MR imaging, percutaneous or surgical biopsy was performed to evaluate the presence of osteomyelitis. The date and nature of surgical interventions performed on the feet prior to MR imaging were reviewed, and the date and type of surgical treatment performed after MR imaging were recorded. Charts and surgical reports were reviewed for all patients by the author (H.P.L.) who was not involved in image interpretation.
The following procedures were performed after MR imaging: toe amputation (n = 44), débridement (n = 37), ray amputation (n = 33), amputation below the knee (n = 16), transmetatarsal amputation (n = 16), Chopart amputation (n = 7), percutaneous bone biopsy (n = 5), amputation above the knee (n = 3), and foot amputation (n = 1). To avoid both contamination of the bone biopsy samples by adjacent soft-tissue infection and inoculation of potentially sterile bone, percutaneous bone biopsy was performed in only a minority (n = 5) of patients. Care was taken to pass the 12-gauge needles through intact, uninfected soft tissue into the bone. All other bone biopsies were performed by the surgeons themselves during surgical procedures. Pathologic findings of bone samples were available for all patients, and microbiologic findings were available for 112 patients.
If the location of an ulcer or surgical defect was adequately described on a patient chart, then this location was compared with the location observed on MR images as determined by the two reviewers. Diagnosis of osteomyelitis with the use of MR imaging was verified in all patients with review of microbiologic and pathologic reports. A positive diagnosis of osteomyelitis was established by means of culture growth or characteristic histologic findings of osteomyelitis. These histologic findings included aggregates of inflammatory cells (including neutrophils, lymphocytes, histiocytes, and plasma cells), erosions of trabecular bone, and marrow signal intensity changes that ranged from loss of normal marrow fat with acute osteomyelitis to fibrosis and reactive bone formation with chronic disease.
Diagnosis of septic arthritis was verified with review of surgical reports. The presence of associated conditions, such as diabetes mellitus, peripheral vascular disease, and postoperative or posttraumatic sequelae, were noted.
Data Analysis
We compared the histologic and culture findings of bone samples with MR imaging findings and calculated sensitivity and specificity values for the use of MR imaging in the diagnosis of osteomyelitis. After comparing the presence and location of skin ulcers as described in patient charts and surgical reports with that determined at MR image analysis, we calculated the sensitivity of MR imaging in the diagnosis of skin ulcerations.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Evidence of septic arthritis was seen in 53 (33%) feet and involved most frequently the fifth (n = 13) and first (n = 8) metatarsophalangeal joints in the forefoot (Fig 5), which was similar to the distribution of ulcers and osteomyelitis. The most frequently affected rays were the second (n = 16), first (n = 14), and fifth (n = 14).
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Twenty-four (75%) hindfoot infections had proven osteomyelitis that involved the calcaneus (n = 21) most frequently. Other infected bones were the lateral malleolus (n = 5), talus (n = 4), tibia (n = 2), and navicular bone (n = 1). One patient with a history of intravenous drug abuse and endocarditis had hematogenous osteomyelitis of the tibia and fibula (Fig 7). There was evidence of septic arthritis in five ankle joints and two subtalar joints.
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After MR imaging, all patients underwent either surgery or percutaneous bone biopsy, which included the following procedures: toe amputation (n = 44), débridement (n = 37), ray amputation (n = 33), amputation below the knee (n = 16), transmetatarsal amputation (n = 16), Chopart amputation (n = 7), percutaneous bone biopsy (n = 5), amputation above the knee (n = 3), and foot amputation (n = 1). The interval between MR imaging and surgery ranged between 1 and 66 days (mean, 9.3 days ± 12.3). Comparison of MR imaging interpretations of osteomyelitis with pathologic and histologic reports revealed that findings at 103 sites were true-positive, 37 were true-negative, 11 were false-negative, and 10 were false-positive. This resulted in a sensitivity of 90.4% and a specificity of 78.7% for the diagnosis of osteomyelitis with the use of MR imaging. Discordant marrow signal intensity in infected bones with normal signal intensity on T1-weighted images and hyperintense signal intensity on T2-weighted and contrast-enhanced images (7,12) was seen in four feet in which MR imaging was performed in our study.
Presence of septic arthritis was confirmed with review of surgical reports for 17 feet and included the interphalangeal joint (n = 1), the metatarsophalangeal joint (n = 14), and the ankle joint (n = 2). In most of the other feet with evidence of septic arthritis on MR images, amputation was performed proximally without dissection of the infected joint.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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All pedal infections but one in our patient population resulted from contiguous spread from an ulcer or skin defect. Most ulcers in our patient group that were clinically suggestive of osteomyelitis were seen around the fifth and first metatarsal heads and the distal phalanx of the great toe. Ulceration below the first metatarsophalangeal joint is commonly cited to be the most frequent location in the feet of diabetic patients (21) and often results from deformity (eg, hallux valgus) and limited mobility of the first metatarsophalangeal joint (22,23). Ulceration around the fifth metatarsophalangeal joint was reported in only a minority of ambulatory patients (16), however, or was equal in frequency to the occurrence of ulcers below the second to fourth metatarsal heads in another study (23). Interestingly, most reports (1,24–27) provide only the total number of toe or metatarsal ulcers without providing the number of ulcers for each toe or metatarsal head. If ulceration of one ray is provided separately, then only the frequency of ulceration of the first ray is described (24,27).
Predominant involvement of the fifth metatarsal head in our study cannot be explained with a normal plantar foot pressure pattern, since normal biomechanical forces lead to high plantar pressures at the first and second metatarsal heads and the plantar aspect of the first toe (28). It has been shown, however, that foot deformities such as forefoot varus and valgus (29) or the presence of a rigid, plantar, flexed first ray (30) result in excessive plantar pressure around the fifth metatarsal head with subsequent ulceration. Predominant ulceration below the fifth metatarsal head in our study may therefore have been due to the selection of patients with such foot deformities. Alternatively, increased mechanical friction at the lateral border of the foot may impede healing of ulcers, with progression to deep infection.
One-fifth of toe ulcerations were observed dorsally, reflecting the frequent occurrence of claw-toe deformity in the feet of diabetic patients, with resulting friction against footwear and excessive pressure over the dorsal aspect of the toes (31). Clawing of the toes is thought to arise from motor neuropathy of the intrinsic muscles and may also lead to ulceration below the metatarsal heads because of anterior displacement of the fat pad from under the metatarsal heads (31). Only one of our patients had a midfoot ulceration, and this was associated with a rocker-bottom deformity that resulted from Charcot arthropathy of the midfoot (29) (Fig 6).
We observed ulcerations at 10 amputation sites in the forefoot. It has been previously reported (32,33) that partial foot amputations interfere with normal biomechanics and may lead to focally increased plantar pressures with subsequent ulceration.
Bone infection was most frequently present in our study at the fifth and first metatarsal bones and at the distal phalanx of the first toe. Since almost all bone infections in our study represented contiguous infections from skin ulcerations or postoperative defects, a close association between the locations of ulceration and osteomyelitis was observed. To the best of our knowledge, only one study (34) has provided the distribution of pedal osteomyelitis. The authors describe a similar distribution pattern of pedal osteomyelitis in their 42 diabetic patients to that in our patients, with decrease of frequency of osteomyelitis in rays 2–5 toward the distal phalanges and predominant involvement of the distal phalanx in ray 1. Osteomyelitis of the midfoot was also rare in that study, and the calcaneus was the most frequently infected bone in the hindfoot (34), as observed in our study group.
Septic arthritis is a well-known complication of advanced diabetic foot infection that occurs around the metatarsophalangeal and interphalangeal joints, but to our knowledge, its incidence has not been analyzed or reported in the literature. In our patient group, one-third of all feet had evidence of septic arthritis on MR images. MR signal intensity characteristics indicative of septic arthritis, such as increased joint fluid and thickening of the synovium with contrast enhancement, are also seen in inflammatory arthropathies and are nonspecific (13,35). Graif et al (14) have reported that the combination of bone erosions and marrow edema is highly suggestive of a septic articulation. In pedal infections, the diagnosis of a septic joint with the use of MR imaging may be more specific, however, since ulceration and adjacent soft-tissue infection directly abut the joint. MR imaging often demonstrates sinus tracts that extend into the joint with obvious destruction of the joint capsule or the joint itself. Increased intraarticular fluid may not be evident in the small interphalangeal joints, especially if the joint capsule is eroded, and it is therefore not a valuable MR imaging criterion for septic arthritis. It has also been shown that even infections in larger joints, such as the knee or hip, may not show signs of joint effusion in up to 16% of cases (14).
Hindfoot infection was present in one-fifth of the feet in which MR imaging was performed in our study, and ulcerations were seen predominantly over the heel (15%). Reported frequencies of heel ulceration range from 6.3% to 26% in previous reports (24–26,36,37), which included mostly ambulatory patients. The relative frequency of heel ulceration in advanced infection is therefore comparable with the prevalence in ambulatory patients. The most frequently infected bone in the hindfoot in our study was the calcaneus, and evidence of septic arthritis was seen in five ankle joints and two subtalar joints.
Several findings in our study are of direct importance to the radiologist. Most ulcers that require evaluation with MR imaging occur either at the proximal or distal end of the foot (in the heel and at the tip of the great toe) or at the lateral or medial border of the foot (at the fifth and first metatarsal heads). It is therefore important to image the entire volume of the forefoot or hindfoot, unless a targeted examination is performed in the region of the ulceration. Fat suppression may be incomplete at the forefoot because of inhomogeneity of the magnetic field or because the toes may extend out of the extremity coil. This may lead to diagnostic difficulties. Homogenous fat suppression can be assisted with plantar flexion of the foot or with the use of a standoff pad under the calcaneus. One-fourth of toe ulcers that require evaluation with MR imaging are located predominantly dorsally or medially over the interphalangeal joints in claw-toe deformities and may be less recognizable as ulcers at the plantar aspect.
Diagnosis of osteomyelitis with the use of MR imaging is based on identification of altered bone marrow signal intensity. Infection of the marrow compartment results in loss of normal fatty marrow signal intensity on T1-weighted images, with edema on T2-weighted or fast SE STIR images and enhancement on postcontrast gadolinium-enhanced T1-weighted images (38). Other entities, including fracture, tumors, severe inflammatory arthritis or neuropathic disease, and recent postoperative change, can alter the bone marrow signal intensity in a similar fashion (8,39–42). However, these entities can generally be distinguished from osteomyelitis on the basis of the pattern and location of the signal intensity abnormality, as well as associated findings in the adjacent bone, joint, or soft tissue (7). Review of our false-positive results revealed that osteomyelitis was often diagnosed in the presence of clearly visible signal intensity abnormalities that did not absorb contrast material on T1- and T2-weighted images. These signal intensity alterations represented either reactive hyperemic changes or subacute neuropathic osteoarthropathy thought to represent osteomyelitis, with little or no enhancement because of underlying vascular disease (11). Most false-negative results in our study could be attributed to misinterpreting or overlooking subtle signal intensity changes, including small areas of enhancement. Another frequent cause of false-negative results was lack of enhancement due to severe vascular disease and established gangrene. No particular locations could be identified that led to erroneous diagnosis of osteomyelitis or lack thereof. No false-positive or false-negative results could be attributed to poor fat suppression, since we performed pre- and postcontrast fat-saturated fast multiplanar spoiled gradient-echo sequences in most patients. This technique allowed us to see contrast enhancement despite occasional heterogeneous fat suppression. In general, T2-weighted sequences, including fast SE STIR sequences, are more sensitive but less specific than T1-weighted and postcontrast sequences (7).
Definite diagnosis of osteomyelitis relies on culture of causative organisms from a biopsy sample (43). However, the accuracy of tissue evaluation in the diagnosis of osteomyelitis is, to our knowledge, unknown. Limitations of percutaneous and surgical bone biopsy include (44) sampling error, false-negative cultures in patients who receive antibiotics, difficulties in histopathologically distinguishing osteopathy from osteomyelitis, and risk of damaging the bone as a result of trauma or iatrogenic infection (34,45). Culture findings from percutaneous bone biopsy specimens obtained in patients with pedal infection may furthermore be unreliable because of contamination from underlying infected soft tissue (34,44,45). It has also been shown that bone biopsy cultures in patients with osteomyelitis may have false-negative results in up to 50% of cases (43), whereas accuracy of histopathologic diagnosis of osteomyelitis is high (46–49). White et al (43) therefore advocated both microbiologic and histologic evaluation of the bone samples to increase the sensitivity of the procedure.
Some limitations apply to our study. Our patient group was highly selected, since we wanted to study the distribution of pedal ulceration, osteomyelitis, and septic arthritis. It is probable that ulcerations were more obvious in this population than in a group selected at random, and, thus, may have led to a high sensitivity of diagnosis with the use of MR imaging. Sensitivity and specificity analysis of ulcer recognition on MR images would require a prospective study, since retrospective analysis of ulcer locations from patient reports does not provide reliable data to exclude ulceration. The selection of patients with advanced foot infection may have also led to an overestimation of the specificity of MR imaging in the diagnosis of osteomyelitis. The presence of septic arthritis was confirmed in only a minority of patients by means of surgical reports. However, the diagnosis of septic arthritis in pedal infection may be specific, as discussed above.
We conclude that advanced pedal infection that is suggestive of osteomyelitis almost always results from contiguous infection and occurs predominantly in diabetic patients. Most ulcerations are seen in the forefoot, one-fifth are seen in the hindfoot, and ulcerations in the midfoot are rare. Ulcerations in the forefoot were most frequently seen in this selected population below the fifth and first metatarsal heads and at the tip of the great toe. In the hindfoot, most ulcers occurred in the heel. Pedal osteomyelitis and septic arthritis represent almost exclusively contiguous infections, occur most frequently around the fifth and first metatarsophalangeal joints, and mirror the distribution of pedal ulcers. Osseous spread of osteomyelitis is seen most frequently at the fifth and first metatarsophalangeal joints and spreads distally to the proximal phalanges. Evidence of septic arthritis is seen on MR images in one-third of patients suspected of having osteomyelitis.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, H.P.L., M.E.S.; study concepts, W.B.M., M.E.S.; study design, H.P.L., W.B.M.; literature research, H.P.L.; clinical studies, H.P.L., W.B.M., M.E.S.; data acquisition, H.P.L.; data analysis/interpretation, H.P.L., W.B.M.; statistical analysis, H.P.L.; manuscript preparation and definition of intellectual content, H.P.L., W.B.M., M.E.S.; manuscript editing, H.P.L.; manuscript revision/review and final version approval, W.B.M., M.E.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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