Published online before print July 26, 2002, 10.1148/radiol.2243011259
(Radiology 2002;224:669-674.)
© RSNA, 2002
Posterior Distal Femoral and Proximal Tibial Metaphyseal Stripes at MR Imaging in Children and Young Adults1
Tal Laor, MD,
Galen F. H. Chun, MD,
Bernard J. Dardzinski, PhD,
Judy A. Bean, PhD and
David P. Witte, MD
1 From the Departments of Radiology (T.L., B.J.D., G.F.H.C.), Biostatistics (J.A.B.), and Pathology (D.P.W.), Children’s Hospital Medical Center, University of Cincinnati College of Medicine, 3333 Burnet Ave, Cincinnati, OH 45229. Received July 23, 2001; revision requested August 27; final revision received January 8, 2002; accepted January 29. Address correspondence to T.L. (e-mail: laor@chmcc.org).
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ABSTRACT
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PURPOSE: To determine the frequency and distribution of the hyperintense stripe seen along the posterior surface of distal femoral and proximal tibial metaphyses at magnetic resonance (MR) imaging.
MATERIALS AND METHODS: One hundred forty-two MR imaging studies obtained in 139 children and young adults were reviewed. The authors recorded the presence and distribution of posterior distal femoral and proximal tibial metaphyseal stripes. Presence of stripe was correlated with patient age and sex and with patency of the adjacent physis. Fifty-nine studies of adults were reviewed similarly. Two-way analysis of variance was performed to compare mean patient age for sex among four different categories that were based on stripe presence and physeal patency. Orthogonal contrasts were used to determine whether a linear trend across the categories existed. In one cadaveric femur, imaging and histologic analysis were performed.
RESULTS: A metaphyseal stripe was seen in all patients with a completely or partially open physis (110 femora, 102 tibiae) and in 56 femora and 60 tibiae in the patients with fused physes. Thirty-five femora and 35 tibiae showed no stripe; all patients were skeletally mature. Correlations between metaphyseal stripe visualization and physeal patency were significant (P < .001). Differences in mean patient age among the four categories were significant for both (femoral and tibial) locations (P < .001), and a linear trend with age (P < .001) was demonstrated. This linear trend was also observed in both sexes (P < .001). Histologic analysis revealed highly vascular loose fibrous tissue.
CONCLUSION: A posterior metaphyseal stripe is seen at MR imaging of the skeletally immature knee and likely reflects normal bone growth.
© RSNA, 2002
Index terms: Bones, growth and development • Femur, MR, 451.121411, 451.121412, 451.121413, 451.121416, 451.12143 • Fibrous cortical defect, 451.3131 • Knee, anatomy, 45.92 • Tibia, 454.121411, 454.121412, 454.121413, 454.121416, 454.12143
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INTRODUCTION
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The increasing use of magnetic resonance (MR) imaging to evaluate musculoskeletal disorders of the knee in children requires recognition of the normal developmental appearance. This knowledge can facilitate differentiation between the appearance of skeletal growth and that of disease. The MR imaging characteristics of normal cartilaginous epiphyses, physes, and metaphyseal marrow during growth have been studied (1–6). When interpreting MR images of the lower extremities of children for a variety of clinical indications, we consistently observe a high-signal-intensity stripe along the posterior surface of the distal femoral metaphysis on images obtained with all routine sequences except T1-weighted sequences (Fig 1). To our knowledge, this has not been described as a finding of MR imaging of the knee in pediatric patients. We hypothesize that this metaphyseal stripe is normal and related to the dynamic bone modeling that occurs during skeletal growth.
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Figure 1. Sagittal MR images of the knee obtained by using nonenhanced T1-weighted (300/14) (top left), fast spin-echo intermediate-weighted (repetition time msec/echo time msec, 3,500/17) (top middle), fast spin-echo T2-weighted (3,500/85) (top right), spoiled gradient-recalled-echo (60/5, 60° flip angle) (bottom left), fast spin-echo inversion-recovery (4,000/34, 155-msec inversion time) (bottom middle), and contrast-enhanced T1-weighted (300/14) sequences. On all MR images except the nonenhanced T1-weighted image (top left), a high-signal-intensity distal femoral metaphyseal stripe (arrow) is seen.
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Therefore, the purpose of this study was to determine the frequency and distribution of the high-signal-intensity stripe seen along the posterior surface of the distal femoral and proximal tibial metaphyses at MR imaging.
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MATERIALS AND METHODS
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MR Imaging
All consecutive MR imaging studies of the knee or lower extremity including the knee that were obtained at our hospital between March 2000 and November 2000 were reviewed. One hundred forty-two MR images obtained in 139 children and young adults (79 female patients, 60 male patients; age range, newborn to 25 years; mean age, 12.6 years) met our inclusion criteria and were analyzed retrospectively by two radiologists (T.L., G.F.H.C.). An additional 59 consecutive MR images of the knee that were obtained in 58 adults (21 women, 37 men; mean age, 28 years; age range, 18–40 years) at an affiliated hospital were reviewed. Approval for this retrospective study was not required by the institutional review board of one institution and was received from the institutional review board of the other institution. Neither institution required patient informed consent.
An MR image was included in the study if it was obtained with a sagittal intermediate-weighted, T2-weighted (fast or conventional spin-echo), or fast spin-echo inversion-recovery sequence and showed the distal femoral metaphysis. An MR image was excluded if a depicted abnormality obscured the posterior distal femoral metaphysis. However, no images were excluded on the basis of either the clinical indication for imaging or the type of abnormality. The examinations were performed for a variety of clinical indications, including pain, acute and chronic trauma, infection, arthritis and other inflammatory disorders, and benign and malignant neoplasms. Three of 145 studies from our pediatric hospital did not meet the inclusion criteria. The same inclusion criteria were used for the 59 MR images obtained in adults at the affiliated hospital, and all of these studies met the inclusion criteria.
All examinations were performed by using a 1.5-T MR imaging unit (Signa and Horizon; GE Medical Systems, Milwaukee, Wis). The extremities were imaged by using a transmit-receive extremity coil, torso phased-array coil, or quadrature head coil. The choice of coil was based on patient size, desired field of view, and need for unilateral or bilateral extremity imaging. When necessary, patients were sedated according to our radiology department guidelines (7).
The following sequences were used to obtain the 142 MR images in the children and young adults: conventional spin-echo intermediate weighted and T2 weighted (1,500–2000/20, 80), fast spin-echo intermediate weighted and T2 weighted (2,500–4,000/17–34, 68–102 [effective], echo train length of six to eight, with fat saturation), and fast spin-echo inversion recovery (3,000–5,000/34, 155-msec inversion time, echo train length of six to eight). The matrix size (256–512 x 128–224) and section thickness (3–5 mm) varied according to the size of the patient and the area of interest. All examinations also included transverse fast spin-echo intermediate- or T2-weighted imaging. Sixty-four patients received intravenous contrast material: 0.1 mmol of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) per kilogram of body weight.
Additional MR imaging sequences performed included conventional spin-echo T1-weighted sequences (300–600/17, with or without fat suppression) both before and after intravenous gadopentetate dimeglumine administration, three-dimensional spoiled gradient-recalled-echo sequences (60/5, 60° flip angle), and dynamic three-dimensional spoiled gradient-recalled-echo sequences (4.6/1.7, 60° flip angle). Image subtraction was performed by subtracting the signal intensity values, pixel by pixel, between two image sets (post- and precontrast dynamic three-dimensional spoiled gradient-recalled-echo) with use of the operator’s console. Ten patients who were imaged for clinical indications but also were part of a study of cartilage in pediatric patients underwent sagittal T2 relaxation time mapping (1,500/9–99, echo train length of 11). Institutional review board approval for T2 relaxation time mapping was obtained. Patient informed consent was not required.
The 59 MR imaging studies obtained in adult patients at an affiliated hospital included images obtained with sagittal fast spin-echo intermediate-weighted (1,800/ 12 [effective]) and T2-weighted (2,450–3,400/45 [effective]) sequences with fat saturation. Each of these patients also underwent transverse fast spin-echo intermediate-weighted imaging.
A cadaveric distal femur specimen from a 5-year-old boy who died owing to complications of metastatic neuroblastoma was available for in vitro MR imaging and histologic evaluation. Although the child had osseous metastases, none was seen at imaging or histologic analysis of the distal femoral specimen.
Image Analysis
Each MR image was reviewed retrospectively in consensus by two radiologists (T.L., G.F.H.C.), who were blinded to the patient’s identity, age, sex, and clinical indication for MR imaging. All sagittal images of the distal femur were evaluated for the presence or absence of a posterior high-signal-intensity metaphyseal stripe. The presence and distribution (ie, medial, lateral, or across the entire posterior surface) of high signal intensity on the corresponding transverse image also were recorded. Similar analyses of posterior metaphyseal stripes of the proximal tibiae were performed when this area was examined at MR imaging.
We recorded the patency of the distal femoral and proximal tibial physes. The physis was considered to be open, partially open, or completely fused, depending on the visualization of persistent high signal intensity from the physeal cartilage (8). We tabulated the direction of the frequency-encoding gradient to evaluate the contribution from chemical shift artifacts. We also recorded the presence and location of fibrous cortical defects in the knee. If these were present, we documented whether the longitudinal dimension of the defect was longer than, equal to, or shorter than the metaphyseal stripe in the sagittal plane.
If the patient received intravenous contrast material, we evaluated the degree of enhancement. We subjectively determined whether the signal intensity of the posterior metaphyseal stripe was higher than, equal to, or lower than that of the adjacent physis or physeal scar. If the patient underwent T2 relaxation time mapping (9) as part of the cartilage study in pediatric patients, the T2 relaxation times of the metaphyseal stripe were described as greater than, equal to, or less than those of the adjacent physis.
The same image analysis was performed with the 59 MR images of the knee obtained in adults at the affiliated hospital. These images were reviewed retrospectively by the same two radiologists in consensus.
Statistical Analyses
Correlations between distal femoral physeal closure (as an indication of relative skeletal maturity) and visualization of a posterior metaphyseal stripe were determined. Patients were grouped according to the appearance of the distal femoral physis: Group 1 consisted of patients with an open physis; group 2, of patients with a partially open physis; and group 3, of patients with a fused physis (Fig 2). The patients in groups 1 and 2 were considered to be skeletally immature. The group 3 patients were considered to be skeletally mature. To determine whether there was a difference in the frequency of visualization of a metaphyseal stripe with skeletal maturation, the Fisher exact test was performed. A P value of less than .05 indicated a significant difference. Similar analyses were performed with data from proximal tibiae.
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Figure 2. Three sagittal intermediate-weighted fast spin-echo MR images of the knee show the different groups of physeal patency in the distal femur. Left (3,500/17): Open physis (group 1). Middle (3,500/17): Partially open physis (group 2). Right (1,800/12): Fused physis (group 3). The arrow points to the physis or physeal area.
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Patients were then regrouped into four categories: Patients in category 1 had an open physis and a visible metaphyseal stripe; patients in category 2, a partially open physis and a visible metaphyseal stripe; patients in category 3, a fused physis and a visible metaphyseal stripe; and patients in category 4, a fused physis and an undetectable metaphyseal stripe. Two-way analysis of variance was applied to the data to determine whether any correlations between the factors of sex and category existed or only main effects were present. In addition, an orthogonal contrast for linear trend in age for all subjects across the categories was tested.
Because the numbers of male and female patients of each age and category were unequal, a linear trend in age for each sex separately could not be determined with two-way analysis of variance. However, because the correlation was not significant, we examined the male and female patients individually with analysis of variance to ascertain whether a linear trend was present for each sex.
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RESULTS
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Image Analysis
A posterior metaphyseal stripe was seen in 166 (83%) of 201 distal femora at MR imaging. In all of these studies, the stripe seen on the sagittal images was distributed across the posterior aspect of the metaphysis on the transverse images and formed a hemispheric "cuff" of increased signal intensity (Fig 3). A similar, less prominent posterior metaphyseal stripe was seen in 162 (82%) of 197 proximal tibiae. In four examinations, the proximal tibia was not completely seen. The two observers agreed on the interpretation of all of these MR studies.
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Figure 3. Transverse intermediate-weighted fast spin-echo MR image (3,500/17) obtained in a 12-year-old boy shows a high-signal-intensity cuff (arrow) along the posterior distal femur.
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The physis was patent at MR imaging in 75 distal femora (patient age range, 1–16 years; mean age, 9.7 years), partially open in 35 (patient age range, 8–18 years; mean age, 14.6 years), and fused in 91 (patient age range, 15–40 years; mean age, 24.3 years). The physis was patent at MR imaging in 71 proximal tibiae (patient age range, 1–16 years; mean age, 9.6 years), partially open in 31 (patient age range, 8–17 years; mean age, 14.3 years), and fused in 95 (patient age range, 14–40 years; mean age, 23.9 years). The two observers agreed on the interpretation of 196 studies and reached a consensus with regard to the interpretation of five.
In 47 cases, the sagittal image was obtained with the frequency-encoding gradient in a superoinferior direction, and in 154 cases, the sagittal image was obtained with the frequency-encoding gradient in an anteroposterior direction. Forty-one of the 47 femora imaged in the superoinferior frequency-encoding direction were skeletally immature, and 69 of the 154 femora imaged in the anteroposterior frequency-encoding direction were skeletally immature. All 110 (100%) of the skeletally immature femora showed a metaphyseal stripe at MR imaging, regardless of the frequency-encoding direction.
Other Imaging Observations
Twenty-one fibrous cortical defects were seen immediately adjacent to the distal femoral or proximal tibial posterior metaphyseal stripe (Fig 4). In all cases, the longitudinal dimension of the fibrous cortical defect was shorter than that of the adjacent metaphyseal stripe. In the transverse plane, all fibrous cortical defects were medially located, whereas the metaphyseal stripe was distributed across the entire posterior bone surface.
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Figure 4. Sagittal contrast-enhanced T1-weighted fat-suppressed MR image (400/17) obtained in a 6-year-old girl shows a high-signal-intensity posterior metaphyseal stripe (straight arrow) and a smaller distal femoral fibrous cortical defect (curved arrow).
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All 64 patients who received intravenous contrast material had a metaphyseal stripe at MR imaging prior to contrast material injection. Fifty-nine of these 64 patients were considered to be skeletally immature—that is, they were in groups 1 and 2. In these 59 patients, the posterior femoral and tibial stripes had a signal intensity that was similar to that in the adjacent physis (Fig 5). All five skeletally mature patients (aged 17–18 years) had a thin hyperintense metaphyseal stripe after intravenous contrast material administration. In all of the skeletally immature patients who underwent T2 relaxation time mapping (9), the T2 relaxation time of the posterior metaphyseal stripe was similar (50–80 msec) to that of the adjacent physis (Fig 6).
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Figure 5. Sagittal MR image of the distal femur in a 12-year-old boy, obtained by subtracting the signal intensity values of a nonenhanced image from those of a contrast-enhanced dynamic three-dimensional spoiled gradient-recalled-echo image (4.6/1.7, 60° flip angle) on a pixel-by-pixel basis. The enhancement of the distal posterior femoral metaphyseal stripe is similar to that of the distal femoral and proximal tibial physes. Note the enhancement along the proximal posterior tibial metaphysis (arrow).
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Figure 6. Sagittal T2 relaxation time map (1,500/9-99) of the knee of a 12-year-old boy. The T2 relaxation times (in milliseconds) of the posterior distal femoral metaphyseal stripe (top right arrow), distal femoral physis (top left arrow), and proximal tibial physis (bottom arrow) are similar.
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Statistical Analyses
Femora.—All 110 (100%) skeletally immature distal femora had a posterior metaphyseal stripe at MR imaging. Of the 91 skeletally mature distal femora, 56 (62%) did and 35 (38%) did not have a stripe at MR imaging. There was a statistically significant correlation between presence of a distal femoral metaphyseal stripe and skeletal immaturity (P < .001, Fisher exact test) (Table 1).
Tibiae.—All 102 (100%) skeletally immature proximal tibiae had a posterior metaphyseal stripe at MR imaging. Of the 95 skeletally mature proximal tibiae, 60 (63%) did and 35 (37%) did not have a stripe at MR imaging. There was a statistically significant correlation between presence of a proximal tibial metaphyseal stripe and skeletal immaturity (P < .001, Fisher exact test) (Table 2).
The differences in mean patient age among the four categories were significant for both the distal femoral and proximal tibial study groups (P < .001) (Table 3, Fig 7). The factors of age and sex did not correlate (P = .269 for the femur, P = .345 for the tibia). There was a significant linear trend (P < .001) in mean patient age across the categories. When the male and female patients were examined separately, the linear trend persisted for both sexes (P < .001). The mean age of patients with a persistent femoral stripe was older than the mean age of patients with a persistent tibial stripe.
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Figure 7. Category analysis. Patients in category 1 had an open physis and a visible metaphyseal stripe; patients in category 2, a partially open physis and a visible metaphyseal stripe; patients in category 3, a fused physis and a visible metaphyseal stripe; and patients in category 4, a fused physis and an undetectable metaphyseal stripe on the horizontal axis. Mean patient ages are represented on the vertical axis. Data on this graph show that there was a statistically significant linear correlation (P < .001) between mean patient age and category.
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Histologic Analysis
In vitro fast spin-echo T2-weighted MR imaging of the distal femoral specimen depicted a prominent hyperintense metaphyseal stripe (Fig 8a, 8b) just beneath the periosteum. The corresponding region on the histologic specimen was composed of highly vascular loose fibrous tissue in a subperiosteal location (Fig 8c).
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Figure 8a. (a) Gross specimen of the distal femur from a 5-year-old boy who died owing to complications of metastatic neuroblastoma. The nonossified epiphysis, physis, and bone cortex are white. No discrete distal metaphyseal stripe is seen. No metastases are present in the distal femur. (b) Corresponding in vitro fast spin-echo T2-weighted MR image of the specimen in a shows a high-signal-intensity stripe (open arrow) along the posterior distal femur. The periosteum has low signal intensity. The distal femoral physis (dotted arrow) is open. (c) Histologic section from the distal metaphysis of the same femoral specimen shows vascular channels (solid arrows) coursing through loose fibrous tissue in a subperiosteal location. Open arrow = periosteum, * = marrow. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 8b. (a) Gross specimen of the distal femur from a 5-year-old boy who died owing to complications of metastatic neuroblastoma. The nonossified epiphysis, physis, and bone cortex are white. No discrete distal metaphyseal stripe is seen. No metastases are present in the distal femur. (b) Corresponding in vitro fast spin-echo T2-weighted MR image of the specimen in a shows a high-signal-intensity stripe (open arrow) along the posterior distal femur. The periosteum has low signal intensity. The distal femoral physis (dotted arrow) is open. (c) Histologic section from the distal metaphysis of the same femoral specimen shows vascular channels (solid arrows) coursing through loose fibrous tissue in a subperiosteal location. Open arrow = periosteum, * = marrow. (Hematoxylin-eosin stain; original magnification, x100.)
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Figure 8c. (a) Gross specimen of the distal femur from a 5-year-old boy who died owing to complications of metastatic neuroblastoma. The nonossified epiphysis, physis, and bone cortex are white. No discrete distal metaphyseal stripe is seen. No metastases are present in the distal femur. (b) Corresponding in vitro fast spin-echo T2-weighted MR image of the specimen in a shows a high-signal-intensity stripe (open arrow) along the posterior distal femur. The periosteum has low signal intensity. The distal femoral physis (dotted arrow) is open. (c) Histologic section from the distal metaphysis of the same femoral specimen shows vascular channels (solid arrows) coursing through loose fibrous tissue in a subperiosteal location. Open arrow = periosteum, * = marrow. (Hematoxylin-eosin stain; original magnification, x100.)
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DISCUSSION
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Our study results show that a posterior metaphyseal stripe, or cuff in the transverse plane, in the distal femoral and proximal tibial metaphyses is seen universally at MR imaging in skeletally immature young patients. As children approach skeletal maturity, the probability of observing the stripe diminishes. Chemical shift artifact appears to have no role in the etiology of the stripe. In our study, all immature femora showed a metaphyseal stripe at MR imaging, regardless of the frequency-encoding direction.
Histologic correlation between the MR imaging and femoral specimen findings in the cadaver of a young boy revealed that the high-signal-intensity stripe was composed of highly vascular subperiosteal loose fibrous tissue. The vascularity of the tissue was reflected in the intensity of the signal after intravenous contrast material administration, which was similar to the signal intensity seen in the highly vascular physis (Fig 5) (4). The T2 relaxation times of the metaphyseal stripe and the adjacent vascular physis were similar (Fig 6).
We postulate that the metaphyseal stripe seen at MR imaging is a manifestation of normal skeletal growth. Growth is an intricate combination of periosteal resorption and endosteal bone deposition. Although the diaphysis of a long bone has a relatively uniform diameter, the metaphysis must progressively widen to accommodate the growing physis and epiphysis. This can be likened to bridging an egg (the expanding epiphysis) to a cylinder (the diaphysis).
The metaphyseal cortex is thinner and more porous than the diaphyseal cortex. Abundant trabecular fenestrations contain fibrovascular soft-tissue elements that connect the metaphyseal marrow spaces to the subperiosteum (10). This subperiosteal envelope increases in size with growth but becomes progressively less active with skeletal maturity (11). The diameter increase needed to connect the diaphysis to the growing physis occurs with appositional bone growth, which is also referred to as intramembranous bone formation in what has been termed the cutback zone along the margins of long bones (11). The cutback zone originally referred to the trailing edge of the metaphysis, the diameter of which was thought to decrease to that of the diaphysis. It appears, however, that the diameter of the diaphysis eventually increases to that of the metaphysis by means of subperiosteal membranous new bone deposition (11). There is relatively more growth posteriorly to accommodate the larger, more bulbous posterior femoral condyle. These processes cease as skeletal maturity is reached and the final flared bone contour is achieved. This slowing down of activity likely accounts for the diminishing probability of seeing the metaphyseal stripe as a child matures.
In a growing child, the femur accounts for 57% of longitudinal growth at the knee, and the tibia accounts for 43% (12). The relatively greater contribution of the distal femur to the entire leg length is probably why the femoral stripe is more evident than the tibial stripe (Fig 1). Tibial growth plateaus at an earlier age than femoral growth in both sexes (13). We also noted that the mean age of patients when the tibial stripe is no longer seen is younger than that of patients when the femoral stripe is no longer seen (Table 3, Fig 7).
Fibrous cortical defects are commonly seen in the knee of growing children, especially along the medial aspect of the distal femur (14,15). Although a fibrous cortical defect often overlaps a portion of the metaphyseal stripe, in all cases in the present study, the fibrous cortical defect that was seen at MR imaging was shorter than the metaphyseal stripe. The fibrous cortical defect was localized to the medial portion of the distal femur at transverse imaging, whereas the metaphyseal stripe was distributed along the entire posterior portion of the bone in a cuff configuration. Although these structures are in the same region of the bone, they probably are unrelated.
Our study was limited by its focus on the bones of the knee, but we would expect to observe a similar high-signal-intensity stripe or cuff of fibrous and vascular tissue in other growing long bones. In fact, we have observed a similar finding along the proximal humerus and distal fibula.
In summary, posterior distal femoral and proximal tibial metaphyseal stripes are seen on the MR images obtained in all skeletally immature patients. If a stripe is not seen, the patient is skeletally mature. This hyperintense stripe on intermediate-weighted, T2-weighted, and inversion-recovery MR images probably reflects rapid bone development and remodeling during growth and should not be considered abnormal.
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FOOTNOTES
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Author contributions: Guarantors of integrity of entire study, T.L., G.F.H.C., B.J.D.; study concepts and design, T.L., G.F.H.C., B.J.D.; literature research, T.L.; clinical studies, T.L., G.F.H.C., B.J.D.; data acquisition, T.L., G.F.H.C., D.P.W.; data analysis/interpretation, all authors; statistical analysis, T.L., B.J.D., J.A.B.; manuscript preparation, definition of intellectual content, and editing, T.L., G.F.H.C., B.J.D.; manuscript revision/review and final version approval, all authors.
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T. Laor and D. Jaramillo
MR Imaging Insights into Skeletal Maturation: What Is Normal?
Radiology,
January 1, 2009;
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28 - 38.
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ABSTRACT
INTRODUCTION
