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1 Department of Radiology, Children's Hospital, 300 Longwood Ave., Boston, MA
02115.
2 Departments of Orthopaedics and Biostatistics, Children's Hospital, Harvard
Medical School, Boston, MA 02115.
3 Rheumatology Program, Division of Immunology and the Department of Pediatrics,
Children's Hospital, Harvard Medical School, Boston, MA 02115.
Received June 30, 2004;
accepted after revision September 13, 2004.
Address correspondence to K. Ecklund
(kirsten.ecklund{at}childrens.harvard.edu).
Abstract
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MATERIALS AND METHODS. Knee MR images in 11 children with Lyme arthritis and 7 with septic arthritis, with a mean age 10.6 years old and 11.7 years old, respectively, were reviewed by a radiologist blinded to the final diagnosis. Joint effusion size, synovial thickness, adenopathy, subcutaneous, marrow, and muscle edema on MRI; and clinical parameters including age, sex, fever, WBC, erythrocyte sedimentation rate, C-reactive protein, and joint fluid WBC in the two patient groups were compared using univariate and multivariate analyses.
RESULTS. Subcutaneous edema was seen in all septic arthritis patients but in only one of 11 patients with Lyme arthritis (p < 0.01). Myositis and adenopathy were present in all Lyme arthritis patients and two of seven patients with septic arthritis (both p < 0.01). No significant difference was present in synovial thickness, marrow edema, or joint fluid size. There were no statistically significant differences in the clinical parameters assessed.
CONCLUSION. Our results identified three MRI features, specifically, myositis, adenopathy, and lack of subcutaneous edema, that strongly suggest the diagnosis of Lyme arthritis rather than septic arthritis in children with acute inflammation of the knee. Awareness of these characteristic MRI features may avoid unnecessary invasive procedures and cost.
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Lyme disease is divided into early and late phases, with early infection characterized by constitutional symptoms and the hallmark rash, erythema migrans. Fewer than half of patients present with early-phase symptoms, and even fewer recall a tick bite. In contrast to adults, who typically develop neurologic symptoms in the late phase of Lyme disease, children more often present with oligoarticular arthritis, especially involving the knee [3].
Timely diagnosis of Lyme arthritis is difficult. No rapid laboratory test reliably identifies serologic markers of borellial infection, and there is considerable overlap in the clinical, laboratory, and radiographic presentation of children with Lyme arthritis and those with other acute arthritides. In fact, Lyme arthritis is diagnosed on initial presentation in fewer than 20% of children [4]. Yet early differentiation from septic arthritis is particularly important because of the disparate therapeutic implications of each diagnosis. Treatment for septic arthritis involves hospitalization, joint aspiration, a lengthy course of IV antibiotics, and, often, surgical drainage. In contrast, initial therapy for Lyme arthritis is a 4-week course of oral doxycycline or amoxicillin [3].
Even when Lyme is suspected, the diagnosis can be delayed pending the results of serologic analysis. Formal diagnosis of Lyme disease is dependent on visualization of antibodies to the causative spirochete by serum enzyme immunoassay (EIA), followed by Western immunoblot confirmation, which can take up to a week [5]. The purpose of this study was to determine whether unique MRI characteristics of Lyme arthritis in children may differentiate the disease from septic arthritis. Awareness of such findings could avoid delay in diagnosis and unnecessary invasive interventions.
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MRI was performed on a 1.5-T MR scanner using a standard extremity coil with the following sequences: axial and sagittal fast spin-echo inversion recovery or T2-weighted spin-echo with fat suppression, sagittal intermediate-weighted spin-echo, and coronal T1-weighted spin-echo. All but two patients also had sagittal T1-weighted images with fat suppression obtained after the IV administration of gadopentetate dimeglumine (Magnevist, Berlex). Images were viewed on the radiology department's Fuji Synapse PAC system (Fujifilm Medical Systems). An experienced pediatric radiologist blinded to the final diagnosis reviewed the MRI examinations.
MR images were reviewed for size of joint effusion; presence of marrow, muscle, and subcutaneous edema; synovial thickness; synovial enhancement; and presence of popliteal lymph nodes. The amount of joint fluid was considered small if the suprapatellar bursa was mildly distended, moderate if extension into the posterior recesses of the joint was present, and large if maximal distention of the suprapatellar bursa was present (Fig. 1). Subcutaneous edema was considered present only if it was generalized rather than focal, which could be related to recent joint aspiration. Maximum synovial thickness was measured along the anterior aspect of the suprapatellar bursa on the sagittal postcontrast images using the standard PAC system measurement tool (Fig. 2).
The patients' clinical records were reviewed for the following data at the time of presentation and MRI: age, sex, presence of fever, serum WBC, serum erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), joint fluid WBC, and Lyme titer results. Institutional review board approval was obtained for review of the MR images and clinical and laboratory records of the 18 patients.
Statistical Analysis
Univariate and multivariate analyses were performed to identify differences
in clinical and MRI variables between patients with Lyme arthritis and those
with septic arthritis. All continuous variables were tested for normality to
determine the most appropriate statistical tests. CRP and joint fluid WBC were
evaluated as median values and ranges with groups compared using the
nonparametric Mann-Whitney U test. All other continuous variables,
including age, serum WBC, ESR, and synovial thickness, were presented in terms
of the mean ± SD and compared using the Student's t test.
Categoric data, including sex; fever; presence of marrow, muscle, and
subcutaneous edema; and hemarthrosis were compared using Fisher's exact test
for binomial proportions. Joint effusion size was assessed using the
chi-square test with Yates correction. Multiple logistic regression with the
backward stepwise procedure was applied to identify which variables were
independently associated with differentiation of Lyme disease and septic
arthritis using the likelihood ratio test to determine significance
[6]. Data analysis was
conducted using the Statistical Package for the Social Sciences (version 12.0,
SPSS). Two-tailed values of p < 0.05 were considered statistically
significant.
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The comparison of MRI findings between the patients with Lyme arthritis and those with septic arthritis is shown in Table 2. All of the children had joint effusions. All 16 patients who received IV contrast showed synovial enhancement. No difference was present in synovial thickness between the two groups of children. Two patients with Lyme arthritis did not have postcontrast imaging. A mild amount of marrow edema was present in two children with septic arthritis but none with Lyme arthritis. All 11 children with Lyme arthritis had edema within the adjacent muscles, especially within the popliteus (Fig. 3), while associated myositis was seen in only two of the seven children with septic arthritis. Similarly, popliteal adenopathy was seen in all patients with Lyme arthritis (Fig. 4), but in just two patients with septic arthritis. Subcutaneous edema was present in all patients with septic arthritis (Fig. 5). Only one child with Lyme arthritis showed subcutaneous edema at MRI, and that examination was obtained 24 hr after surgical drainage. There was no significant difference in the presence of subcutaneous edema between the children who underwent preimaging arthrocentesis and those who did not. Hemarthrosis was seen in two children with Lyme arthritis and none with septic arthritis. Popliteal cysts were present in three patients with Lyme arthritis and none with septic arthritis.
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Based on univariate analysis, three MRI variables were significantly different between patients with Lyme disease and those with septic arthritis. The findings of muscle edema, subcutaneous edema, and popliteal lymphadenopathy showed statistical significance (all p < 0.01). None of the other imaging variables were significantly different between the two study groups (all p > 0.05). Multiple logistic regression analysis confirmed that the best independent predictor of Lyme arthritis versus septic arthritis was the lack of subcutaneous edema on MRI with a likelihood ratio test of 10.89, p < 0.001. This implies that independently of all of the other variables evaluated in this study, patients who were found to have subcutaneous edema on MR images were significantly more likely to have septic arthritis compared with Lyme disease. The final logistic regression model indicated that irrespective of the other variables, when subcutaneous edema was absent in the patient groups evaluated, the estimated probability that a patient had Lyme disease was greater than 99% and the probability of septic arthritis was less than 1%.
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Articular involvement due to B. burgdorferi may develop from 2 weeks to 2 years after infection or onset of systemic symptoms, making attribution to Lyme disease difficult. Patients usually present with fever, limp, joint pain, and elevated acute phase reactants, all of which are also seen in children with acute septic arthritis. Radiographs reveal joint effusion in both groups. Our finding that clinical and laboratory parameters, including serum WBC, ESR, CRP, or joint fluid WBC, cannot distinguish between Lyme and septic arthritis are consistent with earlier reports [9]. MRI may be requested in children with acute infectious arthritis to assess severity or to exclude associated osteomyelitis. Our results identified three MRI features, specifically myositis, lymphadenopathy, and lack of subcutaneous edema, that help differentiate Lyme arthritis from septic arthritis of the knee in children (Figs. 6A, 6B, and 6C).
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In addition, the MR images of two patients with Lyme arthritis revealed hemarthrosis. This feature of Lyme arthritis has been described [11] and may be the result of subclinical trauma to the hyperemic synovium. Although not seen in our series, hemarthrosis has also been reported in septic arthritis and probably cannot be used as a distinguishing feature.
One recent study of Lyme arthritis in children stated that MRI was not useful in the diagnostic evaluation [9]. However, only two of 10 patients in that study underwent MRI and no control patients with bacterial septic arthritis were used for comparison. Differences between our conclusions and those of that study may be related to the small number of MR images that they evaluated.
The results of this study are limited by its retrospective nature and the small sample size. This is in part because patients thought to have septic arthritis are not routinely referred for MRI on acute presentation at our institution. MRI is most often requested when there is lack of clinical improvement after joint aspiration and antibiotic therapy. It is interesting to note that eight of the 18 total patients underwent MRI in the last year of the 6-year study period. This coincides with the time of our initial observation that associated soft-tissue findings might help differentiate Lyme from septic arthritis. It is likely that the increase in referrals for MRI relates to increased awareness of these findings on the part of referring physicians.
Our study was confined to a comparison of the MRI findings of Lyme arthritis with those of acute septic arthritis in children. We did not evaluate other common inflammatory monoarthridites, such as juvenile rheumatoid arthritis (JRA). JRA is somewhat less likely to be confused clinically with acute infectious arthritis. Some children with Lyme arthritis, however, come to medical attention in the chronic phase of their illness, when the disease is more likely to be confused with JRA. It will be important for future studies to compare the MRI features of Lyme arthritis with those of JRA.
Despite the small number of patients, we identified three MRI features in children with acute onset of arthritis of the knee—myositis, lymphadenopathy, and lack of subcutaneous edema—that are more suggestive of Lyme than septic arthritis. In geographic regions where Lyme disease is endemic, MRI may play an important role in the diagnosis and management of children with acute arthritis. This should not be interpreted as a recommendation for MRI in all children presenting with acute arthritis, but rather as a report that MRI can offer additional information in those cases where clinical and laboratory data are inconclusive for septic arthritis. If myositis, lymphadenopathy, and especially lack of subcutaneous edema are identified, Lyme disease should be suggested. However, caution should be used when MRI is performed after operative drainage procedures that may alter the findings, especially with respect to subcutaneous edema. Since our initial recognition of the soft-tissue features accompanying Lyme arthritis, we have found that the radiologist is often the first to suggest the diagnosis. Confirmation of our findings would allow educational efforts to be directed toward disseminating these MRI manifestations of Lyme arthritis among other caregivers responsible for the diagnosis and treatment of children with acute arthritis, including emergency department physicians, orthopedists, and rheumatologists.
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