(Radiology. 2000;215:504-511.)
© RSNA, 2000
Cartilaginous Path of Physeal Fracture-Separations: Evaluation with MR Imaging-An Experimental Study with Histologic Correlation in Rabbits1
Diego Jaramillo, MD,
Bamidele F. Kammen, MD 2 and
Frederic Shapiro, MD
1 From the Departments of Radiology (D.J., B.F.K.) and Orthopaedic Surgery (F.S.), Children's Hospital and Harvard Medical School, 300 Longwood Ave, Boston, MA 02115. Received June 1, 1998; revision requested July 22; final revision received August 30, 1999; accepted September 14. Supported in part by RSNA Research and Education Foundation and by National Institutes of Health grant AR42396-05. Address correspondence to D.J.
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Abstract
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PURPOSE: To define the transverse levels of intracartilaginous fractures by using magnetic resonance (MR) imaging and histologic analysis in experimental physeal fracture-separations.
MATERIALS AND METHODS: Physeal fracture-separations were evaluated with MR imaging in 28 distal femurs and 28 proximal tibias of 22 immature rabbits. The intraphyseal transverse level of injury was graded as juxtaepiphyseal (germinal or proliferative zones) or juxtametaphyseal (hypertrophic zone or zone of provisional calcification). Histologic sections from 23 specimens were studied to assess correlations. We assessed nonenhanced and gadolinium-enhanced T1-weighted, intermediate-weighted, T2-weighted, and spoiled gradient-recalled-echo T1-weighted images.
RESULTS: In all MR studies, the injury was visible as a cleft of signal intensity lower than the signal intensity of the physeal cartilage. Juxtaepiphyseal extension, seen in 18 (64%) of 28 fractures, was more frequent in the undulating central part of the distal femoral physis than in the flatter proximal tibial physis (P = .008). In 20 of 23 specimens, MR imaging and histologic findings had excellent correlation for the detection of fracture level and morphology.
CONCLUSION: The course and level of injury within the cartilage in physeal fracture-separations can be defined with MR imaging. Extension into the juxtaepiphyseal physis, a potential risk factor for growth arrest, is detectable with MR imaging; MR imaging and histologic findings correlate well.
Index terms: Animals • Bones, epiphyses, 451.414, 454.414 • Bones, growth and development, 451.433 • Bones, injuries, 451.414, 454.414 • Cartilage • Cartilage, MR, 451.12141, 451.485, 454.12141, 454.485 • Experimental study • Fractures, MR, 451.12141, 451.414, 454.12141, 454.414 • Knee, MR, 451.121411, 451.121412, 451.121415, 451.12143, 454.121411, 451.121412, 451.121415, 451.12143
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Introduction
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Most physeal injuries course transversely through the cartilage of the growth plate that separates the epiphysis from the metaphysis. Transverse fracture-separations are widely considered to involve the zone of provisional calcification of the physis, which is immediately adjacent to the metaphysis (1,2). Injuries at this juxtametaphyseal level do not compromise the stem cells of the germinal zone (or zone of resting cartilage, adjacent to the epiphysis), the columns of chondrocytes of the proliferative zone, or the epiphyseal vessels, which provide most of the physeal vascular supply. Findings of experimental studies in animals (1–6) and human specimens (7,8), however, have shown that transverse fracture-separations often extend to the juxtaepiphyseal region of the physis and in these instances are more likely to disturb growth (9).
Detection of the level of an injury through the physis in transverse fracture-separations could have great prognostic and even therapeutic importance. Radiographs cannot be used to distinguish the level of intraphyseal fracture (9). Negative growth sequelae currently are generally documented only after shortening, angular deformity, and bone bridge formation are seen clinically or radiologically (9).
Magnetic resonance (MR) imaging has been useful in demonstrating injuries to the physeal cartilage and in depicting early formation of transphyseal bone bridges (10–12). We hypothesized that transverse physeal fractures often extend into the juxtaepiphyseal portion of the physis and that MR imaging can reveal this pathway, which has more serious implications. In this study, we used MR imaging and histologic correlation to evaluate the course of experimental transverse fractures within the physeal cartilage.
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MATERIALS AND METHODS
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Experimental Design
MR images of 28 distal femurs and 28 proximal tibias in 22 skeletally immature 6-week-old New Zealand White rabbits and histologic sections from 25 of the specimens were studied following experimental creation of transverse physeal fracture-separations. The hospital's animal care and use committee approved the study. The research was divided into three parts: (a) MR imaging and histologic assessment of the level of epiphyseal fracture-separations produced immediately after death; (b) MR imaging evaluation of the level of physeal fractures in live rabbits; and (c) evaluation of various pulse sequences for the detection of intraphyseal injury.
Anesthetic Technique
The rabbits were anesthetized for surgery and imaging with intravenous injections of 40 mg of ketamine hydrochloride (Ketalar; Parke-Davis, Morris Plains, NJ) per kilogram of body weight, 5 mg/kg xylazine hydrochloride (Rompun; Mobay, Shawnee, Kan), and 0.25 mg/kg acepromazine maleate (Acepromazine; Fermenta Animal Health, Kansas City, Mo). The animals were sacrificed by using an intracardiac injection of pentobarbital sodium (Nembutal; Abbott Laboratories, North Chicago, Ill).
Creation of the Physeal Fracture-Separation
In group 1, we induced 14 distal femoral and 14 proximal tibial physeal fracture-separations in eight rabbits immediately after sacrifice. A lateral incision was made over the distal third of the thigh and the knee joint to approach the distal femur. The quadriceps muscle was elevated, and the periosteum was identified. A rectangular periosteal sleeve 1 cm wide and 2 cm long was elevated from the metaphysis, physis, and epiphysis, which thus removed perichondrial support from the lateral physis. With the knee held in full extension, a varus force was applied manually to create a distal femoral physeal fracture-separation. Using a similar medial surgical approach, we exposed the proximal tibial physis and created a physeal fracture with a valgus force. With this experimental model, we examined epiphyseal fracture-separations on MR images and histologic sections.
In group 2, we studied 10 distal femoral and 10 proximal tibial injuries in 10 live rabbits to assess whether findings of the initial study could be reproduced in vivo. With the periosteum intact, it was more difficult to create the physeal fractures, but slight knee hyperextension and rotation with application of varus and valgus forces accomplished this.
In group 3, we studied eight additional fractures (four distal femoral and four proximal tibial) in four rabbits injured immediately after death to compare different pulse sequences. We used the same technique outlined for the first group.
MR Imaging
The specimens and the live rabbits were imaged by using 1.5-T Signa and Horizon systems (GE Medical Systems, Milwaukee, Wis) and a 7.5-cm receive-only surface coil. The knees were fully extended and were positioned in an immobilizer with a constant distance between the surface coil and the femurs and tibias.
In groups 1 and 2, imaging was performed with the following parameters: 3-mm-thick contiguous sections with an 8 x 8-cm field of view (voxel dimensions, 0.32 x 0.32 x 3.00 mm), and one to two signals acquired. Transverse spin-echo (SE) T1-weighted imaging (300/25 [repetition time msec/echo time msec]) was followed by coronal and sagittal SE T1-weighted (300/25) imaging, SE intermediate-weighted and T2-weighted imaging (2,000/15, 80), and gradient-recalled-echo imaging (300/13, 30° flip angle). In the live animals (group 2), we added coronal and sagittal SE T1-weighted imaging (400/25) immediately after the intravenous administration into an ear vein of 0.1 mmol/kg gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) or gadoteridol (Prohance; Squibb, Princeton, NJ).
In group 3, we visualized the injury by using newer pulse sequences (three-dimensional spoiled gradient-recalled-echo and fast SE imaging) and gradient technology (which allowed for greater spatial resolution), which substantially improve the detection of cartilage abnormalities (13–15). We studied eight fractures with the following: coronal, fast spoiled gradient-recalled-echo, fat-suppressed, T1-weighted images (20.3/2.7, 40° flip angle, 256 x 160 matrix, 0.9-mm section thickness, 6 x 6-cm field of view) and fast SE T2-weighted images (2,000/100, echo train length of eight, 512 x 256 matrix, 2-mm section thickness, 5 x 5-cm field of view, 98 x 196 x 2,000-µm voxel size). These images were compared with coronal conventional SE intermediate-weighted and T2-weighted images by using the parameters outlined at the beginning of this section.
Analysis of Fracture Pathway
In studying group 1, the first 28 physes injured after sacrifice, we divided the physis into six longitudinal segments, from medial (segment 1) to lateral (segment 6) (Fig 1). Within each segment, the pathway of the fracture on MR images was graded as coursing through the juxtametaphyseal side of the physis (grade 1), the juxtaepiphyseal side of the physis (grade 3), or the middle of the physis (grade 2). Grade 0 was assigned whenever the segment was not affected by the fracture. The grading was performed by a pediatric radiologist (D.J.) prior to viewing the histologic sections.
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Figure 1. The drawing on the left depicts the quantitative evaluation of the path of injury. The plane of the physeal fracture-separation was graded from 1 (juxtametaphyseal) to 3 (juxtaepiphyseal) in six segments of the distal femoral and proximal tibial physes. The graphs on the right show grades (vertical axis) of physeal fracture-separation in the distal femur and proximal tibia in the six segments (horizontal axis) of the physis. • = mean grade in each physeal segment. Error bars = SEM. The metaphyses and epiphyses have the same orientation as the anatomic drawing on the left. These grades summarize the path of physeal fracture-separation in each anatomic area. In the distal femur, the fracture plane extends into the epiphysis in the central undulated portion of the physis. In the proximal tibia, the fracture plane is mostly juxtametaphyseal, and it remains relatively constant throughout the physis.
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Histologic Examination
Following sacrifice, the distal femurs and proximal tibias were carefully dissected, were fixed in 10% neutral buffered formalin for 2 weeks, and then were transferred to 25% formic acid for decalcification. Once the bones were soft, they were cut in the coronal plane as described later, trimmed to decrease the size, infiltrated with JB4 solution (Polysciences, Warrington, Pa) for 2 weeks, embedded in JB4 plastic, sectioned at 5-µm thickness, and stained with 1% toluidine blue. Efforts were made to cut histologic specimen sections at the same levels at which MR images were obtained in the coronal plane in all rabbits in which correlation was done (groups 1 and 2). The level of sectioning was measured from the posterior condylar margins toward the anterior part of the condyle. The first, or posterior, section was 3 mm from the posterior surface, the middle section was at 6 mm, and the most anterior section was at 9 mm.
In 25 specimens (12 femurs and 13 tibias), the entire physis could be evaluated to assess the predominant level of the intracartilaginous injury.
Correlation between MR Imaging and Histologic Findings
We made specific efforts to section the histologic specimen in the same location and in the same orientation as the MR image. The injuries sometimes resulted in loss of alignment between the fragments, or, less often, in excessive splitting or comminution. In those instances where the fracture plane was relatively uniform across the physis, excellent correlation was possible. Even when the level of a physeal fracture changed, it usually happened gradually over several millimeters, so appropriate correlations could be made. In some cases, the level of the histologic sections was slightly different from that of the MR sections. We initially examined the specimens to select the cases in which the orientation and level of sectioning were comparable. Twenty-three of 25 specimens (11 femurs and 12 tibias) fit these criteria; in all 23 specimens, we compared the MR images with the histologic sections.
One radiologist (D.J.) and one orthopedic surgeon (F.S.) examined the MR images and histologic sections simultaneously. The correlation was graded as follows: Grade 3 correlation indicated agreement in the level of the fracture, with close resemblance between the MR and histologic images of the abnormality. Figures 2 and 3 illustrate cases not only where MR imaging and histologic findings indicated the same level of the extension of the injury, but also where the sectioning was so similar that the MR images and histologic sections have an almost identical appearance. Grade 2 correlation indicated agreement in the level of extension of the fracture; however, because of differences in the obliquity of the plane of sectioning, the contour of the injury on MR images differed from that shown histologically. Grade 1 correlation indicated disagreement with respect to the level of the injury; for example, juxtaepiphyseal extension shown on the histologic section but not on the MR image.
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Figure 2a. Juxtaepiphyseal extension of a physeal fracture-separation in a distal femoral specimen. (a) Coronal intermediate-weighted MR image (2,000/15) of the distal femur shows what would correspond radiographically to a Salter-Harris type 2 injury, with a metaphyseal fragment (M) remaining attached to the epiphysis (E). The high signal intensity of the physis is interrupted (open arrow) in the area of central undulation of the distal femoral physis. Notice that the high signal intensity from the physis resumes laterally (solid arrow). (b) Low-power photomicrograph shows a metaphyseal fragment (M) superiorly and epiphyseal bone (E) inferiorly. Physeal cartilage is black. Note the central area of cartilage loss that corresponds to the central area of loss of physeal signal intensity in a. The open arrow shows fractured physeal cartilage adjacent to the epiphyseal fragment (all missing physeal cartilage would be on a metaphyseal fragment not shown). The curved arrow shows a region where the epiphyseal fragment is almost entirely denuded of cartilage. (Toluidine blue stain; original magnification, x4.)
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Figure 2b. Juxtaepiphyseal extension of a physeal fracture-separation in a distal femoral specimen. (a) Coronal intermediate-weighted MR image (2,000/15) of the distal femur shows what would correspond radiographically to a Salter-Harris type 2 injury, with a metaphyseal fragment (M) remaining attached to the epiphysis (E). The high signal intensity of the physis is interrupted (open arrow) in the area of central undulation of the distal femoral physis. Notice that the high signal intensity from the physis resumes laterally (solid arrow). (b) Low-power photomicrograph shows a metaphyseal fragment (M) superiorly and epiphyseal bone (E) inferiorly. Physeal cartilage is black. Note the central area of cartilage loss that corresponds to the central area of loss of physeal signal intensity in a. The open arrow shows fractured physeal cartilage adjacent to the epiphyseal fragment (all missing physeal cartilage would be on a metaphyseal fragment not shown). The curved arrow shows a region where the epiphyseal fragment is almost entirely denuded of cartilage. (Toluidine blue stain; original magnification, x4.)
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Figure 3a. Distal femoral growth plate fracture-separation that extends into the proximal epiphyseal bone. (a) Coronal T2-weighted MR image (2,000/80) shows that the fracture-separation (curved arrow) in the periphery courses between the layers of the physis (grade 2). In the central portion, the physeal high signal intensity is interrupted. The fracture then extends along the epiphyseal bone (straight arrows) and finally returns back to the physis. (b) Low-power photomicrograph shows line of fracture within the physeal cartilage on the right that passes through the epiphyseal bone centrally (arrows) and through physeal cartilage again on the left. The left extension was not seen in a. (Toluidine blue stain; original magnification, x5.) (c) Higher power photomicrograph shows central, intact physeal cartilage (P) above and a fracture line path through epiphyseal bone (E) below. This corresponds closely with the weaving fracture line through cartilage and adjacent bone in a. (Toluidine blue stain; original magnification, x30.)
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Figure 3b. Distal femoral growth plate fracture-separation that extends into the proximal epiphyseal bone. (a) Coronal T2-weighted MR image (2,000/80) shows that the fracture-separation (curved arrow) in the periphery courses between the layers of the physis (grade 2). In the central portion, the physeal high signal intensity is interrupted. The fracture then extends along the epiphyseal bone (straight arrows) and finally returns back to the physis. (b) Low-power photomicrograph shows line of fracture within the physeal cartilage on the right that passes through the epiphyseal bone centrally (arrows) and through physeal cartilage again on the left. The left extension was not seen in a. (Toluidine blue stain; original magnification, x5.) (c) Higher power photomicrograph shows central, intact physeal cartilage (P) above and a fracture line path through epiphyseal bone (E) below. This corresponds closely with the weaving fracture line through cartilage and adjacent bone in a. (Toluidine blue stain; original magnification, x30.)
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Figure 3c. Distal femoral growth plate fracture-separation that extends into the proximal epiphyseal bone. (a) Coronal T2-weighted MR image (2,000/80) shows that the fracture-separation (curved arrow) in the periphery courses between the layers of the physis (grade 2). In the central portion, the physeal high signal intensity is interrupted. The fracture then extends along the epiphyseal bone (straight arrows) and finally returns back to the physis. (b) Low-power photomicrograph shows line of fracture within the physeal cartilage on the right that passes through the epiphyseal bone centrally (arrows) and through physeal cartilage again on the left. The left extension was not seen in a. (Toluidine blue stain; original magnification, x5.) (c) Higher power photomicrograph shows central, intact physeal cartilage (P) above and a fracture line path through epiphyseal bone (E) below. This corresponds closely with the weaving fracture line through cartilage and adjacent bone in a. (Toluidine blue stain; original magnification, x30.)
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Pulse Sequence Comparison
In the eight physeal injuries studied for pulse sequence comparison, one radiologist (D.J.) analyzed the fractures according to the same grading system used for the correlation between MR imaging and histologic analysis: Grade 3 correlation indicated agreement in the level of extension of the fracture and close resemblance between the images obtained with each sequence. Grade 2 indicated agreement in the level of the extension of the fracture without a similar contour of the fragments on images obtained with each MR sequence. Grade 1 indicated disagreement with respect to the level of extension of the injury. We did not attempt blinding the observer to the parameters, as the images were easily recognizable.
Data Analysis
In group 1, we sought to evaluate whether there were differences in the plane of the fractures between corresponding segments of the distal femoral and proximal tibial physis. To do this, the grades for MR images of each section of the tibial and femoral physes were compared, and the significance of the differences was determined by using the Wilcoxon signed rank test.
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RESULTS
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MR Imaging Appearance of the Injured Physis
The normal physeal cartilage, as has been described previously (10–12), was of high signal intensity on intermediate-weighted images, T2-weighted images, gadolinium-enhanced T1-weighted images, and spoiled gradient-recalled-echo images (13) (Figs 2 –7). On intermediate-weighted images (Figs 2, 5), T2-weighted images (Figs 3, 7), and spoiled gradient-recalled-echo images (Fig 7), the fracture-separation within the physis was seen as a low-signal-intensity gap of air within the high-signal-intensity physeal cartilage. On gadolinium-enhanced images in the live animals, the plane of the fracture appeared as a nonenhancing line between the layers of enhancing cartilage (Figs 4, 6). When the fracture extended into the juxtaepiphyseal region, the signal intensity of the physis was interrupted entirely (Fig 2).
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Figure 4a. Juxtametaphyseal injury in the proximal tibial physis in a live rabbit with an injury from a valgus force. (a) Coronal gadolinium-enhanced T1-weighted image (400/25) obtained in vivo shows a low-signal-intensity juxtametaphyseal fracture (arrow). The high signal intensity from the physis is uninterrupted. (b) Low-power photomicrograph of corresponding proximal tibia obtained after sacrifice shows plane of juxtametaphyseal fracture-separation (arrow). Note a focal area of greater physeal thickness just superior to the arrow in both a and b. (Toluidine blue stain; original magnification, x5.)
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Figure 4b. Juxtametaphyseal injury in the proximal tibial physis in a live rabbit with an injury from a valgus force. (a) Coronal gadolinium-enhanced T1-weighted image (400/25) obtained in vivo shows a low-signal-intensity juxtametaphyseal fracture (arrow). The high signal intensity from the physis is uninterrupted. (b) Low-power photomicrograph of corresponding proximal tibia obtained after sacrifice shows plane of juxtametaphyseal fracture-separation (arrow). Note a focal area of greater physeal thickness just superior to the arrow in both a and b. (Toluidine blue stain; original magnification, x5.)
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Figure 5a. Injury extending along the layers of physeal cartilage in a proximal tibial specimen. (a) Coronal intermediate-weighted MR image (2,000/15) shows that most of the high-signal-intensity proximal tibial physeal cartilage (solid arrow) is spared despite an extensive fracture-separation. Open arrow corresponds to the small amount of physeal cartilage adherent to the metaphyseal fragment demonstrated in c. (b) Higher power photomicrograph of the epiphyseal fragment shows columns of physeal cartilage (arrow) adherent to epiphyseal bone at the top of the image. The fracture gap is at the bottom. (Toluidine blue stain; original magnification, x40.) (c) Higher power photomicrograph of the metaphyseal fragment shows a small amount of physeal cartilage (arrow) adherent to the metaphysis below it. The fracture gap is at the top. (Toluidine blue stain; original magnification, x40.) Note the high level of correlation between a and both b and c.
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Figure 5b. Injury extending along the layers of physeal cartilage in a proximal tibial specimen. (a) Coronal intermediate-weighted MR image (2,000/15) shows that most of the high-signal-intensity proximal tibial physeal cartilage (solid arrow) is spared despite an extensive fracture-separation. Open arrow corresponds to the small amount of physeal cartilage adherent to the metaphyseal fragment demonstrated in c. (b) Higher power photomicrograph of the epiphyseal fragment shows columns of physeal cartilage (arrow) adherent to epiphyseal bone at the top of the image. The fracture gap is at the bottom. (Toluidine blue stain; original magnification, x40.) (c) Higher power photomicrograph of the metaphyseal fragment shows a small amount of physeal cartilage (arrow) adherent to the metaphysis below it. The fracture gap is at the top. (Toluidine blue stain; original magnification, x40.) Note the high level of correlation between a and both b and c.
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Figure 5c. Injury extending along the layers of physeal cartilage in a proximal tibial specimen. (a) Coronal intermediate-weighted MR image (2,000/15) shows that most of the high-signal-intensity proximal tibial physeal cartilage (solid arrow) is spared despite an extensive fracture-separation. Open arrow corresponds to the small amount of physeal cartilage adherent to the metaphyseal fragment demonstrated in c. (b) Higher power photomicrograph of the epiphyseal fragment shows columns of physeal cartilage (arrow) adherent to epiphyseal bone at the top of the image. The fracture gap is at the bottom. (Toluidine blue stain; original magnification, x40.) (c) Higher power photomicrograph of the metaphyseal fragment shows a small amount of physeal cartilage (arrow) adherent to the metaphysis below it. The fracture gap is at the top. (Toluidine blue stain; original magnification, x40.) Note the high level of correlation between a and both b and c.
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Figure 6a. Juxtametaphyseal injury extending into the metaphysis in the proximal tibia of a live rabbit. (a) Coronal gadolinium-enhanced T1-weighted MR image (400/25) shows what would radiographically be a Salter-Harris type 2 injury. The high signal intensity from the physis is uninterrupted just above the fracture plane (long arrow). The short arrow indicates the extension into the metaphyseal bone. (b) Low-power photomicrograph shows the physis at the top of the image and a juxtametaphyseal fracture line (white arrow) and oblique metaphyseal fracture (black arrow). (Toluidine blue stain; original magnification, x4.)
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Figure 6b. Juxtametaphyseal injury extending into the metaphysis in the proximal tibia of a live rabbit. (a) Coronal gadolinium-enhanced T1-weighted MR image (400/25) shows what would radiographically be a Salter-Harris type 2 injury. The high signal intensity from the physis is uninterrupted just above the fracture plane (long arrow). The short arrow indicates the extension into the metaphyseal bone. (b) Low-power photomicrograph shows the physis at the top of the image and a juxtametaphyseal fracture line (white arrow) and oblique metaphyseal fracture (black arrow). (Toluidine blue stain; original magnification, x4.)
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Figure 7a. Juxtametaphyseal injury in a specimen of the proximal tibia depicted with various pulse sequences. (a) Coronal SE T2-weighted MR image (2,000/80) obtained with a field of view of 8 cm, a 256 x 256 matrix, and a 3-mm section thickness shows a juxtametaphyseal fracture (arrow) of the proximal tibia. (b) Coronal fast SE T2-weighted MR image (2,000/100; echo train length, eight) obtained with a field of view of 5 cm, a 512 x 256 matrix, and a 2-mm section thickness has better spatial resolution but shows the same configuration of the fracture (arrow). (c) Coronal, three-dimensional, spoiled gradient-recalled-echo, fat-suppressed, T1-weighted MR image (20.3/2.7, 40° flip angle) obtained with a field of view of 6 cm, a 256 x 160 matrix, and a 0.9-mm section thickness shows that the fracture (straight arrow) is juxtametaphyseal. It also demonstrates, however, that the transverse extension (curved arrow) is greater than that depicted with the other sequences.
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Figure 7b. Juxtametaphyseal injury in a specimen of the proximal tibia depicted with various pulse sequences. (a) Coronal SE T2-weighted MR image (2,000/80) obtained with a field of view of 8 cm, a 256 x 256 matrix, and a 3-mm section thickness shows a juxtametaphyseal fracture (arrow) of the proximal tibia. (b) Coronal fast SE T2-weighted MR image (2,000/100; echo train length, eight) obtained with a field of view of 5 cm, a 512 x 256 matrix, and a 2-mm section thickness has better spatial resolution but shows the same configuration of the fracture (arrow). (c) Coronal, three-dimensional, spoiled gradient-recalled-echo, fat-suppressed, T1-weighted MR image (20.3/2.7, 40° flip angle) obtained with a field of view of 6 cm, a 256 x 160 matrix, and a 0.9-mm section thickness shows that the fracture (straight arrow) is juxtametaphyseal. It also demonstrates, however, that the transverse extension (curved arrow) is greater than that depicted with the other sequences.
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Figure 7c. Juxtametaphyseal injury in a specimen of the proximal tibia depicted with various pulse sequences. (a) Coronal SE T2-weighted MR image (2,000/80) obtained with a field of view of 8 cm, a 256 x 256 matrix, and a 3-mm section thickness shows a juxtametaphyseal fracture (arrow) of the proximal tibia. (b) Coronal fast SE T2-weighted MR image (2,000/100; echo train length, eight) obtained with a field of view of 5 cm, a 512 x 256 matrix, and a 2-mm section thickness has better spatial resolution but shows the same configuration of the fracture (arrow). (c) Coronal, three-dimensional, spoiled gradient-recalled-echo, fat-suppressed, T1-weighted MR image (20.3/2.7, 40° flip angle) obtained with a field of view of 6 cm, a 256 x 160 matrix, and a 0.9-mm section thickness shows that the fracture (straight arrow) is juxtametaphyseal. It also demonstrates, however, that the transverse extension (curved arrow) is greater than that depicted with the other sequences.
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The fracture plane was detectable on all MR studies. The path of cartilaginous injury was easier to detect when the fracture was somewhat displaced. In these cases, fracture detection was facilitated by a gap of air between fragments, whereas in less displaced injuries the gap was more difficult to distinguish from posttraumatic changes (Fig 7). When there was fluid within the fracture, the fluid and the adjacent cartilage were of similar signal intensity on the intermediate-weighted and T2-weighted images. On spoiled gradient-recalled-echo images (Fig 7) and on gadolinium-enhanced images (Fig 4), the fluid within the fracture was of lower signal intensity than the cartilage. Therefore, differentiation between fluid and cartilage along the fracture was easier on the spoiled gradient-recalled-echo and gadolinium-enhanced T1-weighted images.
Analysis of Fracture Pathway
In group 1, on the MR images of the distal femoral physes fractured after sacrifice, 11 of 14 fractures extended into the juxtaepiphyseal cartilage. The majority of these extensions occurred in the central undulated portion of the femoral physis (Figs 2, 3). In specimens with injuries of the proximal tibial physis, the fractures had a straighter path along the juxtametaphyseal physis (Figs 4–7). In half of the fractures (seven of 14), however, there were extensions of the fracture into the juxtaepiphyseal region. These transphyseal extensions were smaller than those in the distal femoral physis and were relatively evenly distributed along the physis. Juxtaepiphyseal extension was more frequent in the central area of the distal femoral physis, where the mean fracture level grade was 2.1 ± 0.3 (SD), than in the flatter central proximal tibial physis, where the mean fracture level grade was 1.2 ± 0.2 (P = .008) (Fig 1).
Histologic Examination
In the 12 distal femurs with complete histologic sections, there were six Salter-Harris type 2 fractures and six type 1 fractures. None of the other fracture patterns were produced. The fracture pathway was infrequently through the hypertrophic zone throughout the entire width of the plate. There was frequent fracturing into the resting or germinal zone of the physis at the central undulation. At times, isolated full-thickness segments of physis adhered to either the epiphyseal or the metaphyseal bone. The fracture line sometimes cut across epiphyseal bone at the central undulation, which resulted in isolation of a segment of physis and even a small amount of epiphyseal bone with the metaphysis (Fig 3).
In the 13 proximal tibias with complete histologic sections, fracture pathways were Salter-Harris type 1 (n = 10) or type 2 (n = 3). Most often, the transverse plane of fracture was through the hypertrophic cell layer, but occasionally more juxtaepiphyseal transverse levels were also seen.
Correlation between MR Imaging and Histologic Findings
Twenty of 23 specimens (87%) showed a high degree of MR-histologic correlation in the level and morphology of the lesion (Figs 2 –6). In two cases (9%), the path of the fracture plane was visually different, but in both cases the MR images and the histologic sections suggested extension of the fracture into the juxtaepiphyseal cartilage. In one case, MR imaging did not demonstrate the juxtaepiphyseal extension seen histologically.
Pulse Sequence Comparison
The comparison between conventional intermediate-weighted images, T2-weighted images, spoiled gradient-recalled-echo images, and fast SE T2-weighted images with a 98 x 196-µm resolution (Fig 7) showed that in seven of eight cases there was good correlation with regard to the level and course of the fracture (grade 3). In the remaining case, the spoiled gradient-recalled-echo sequence showed that a Salter-Harris type 1 injury involved a slightly larger portion of the physis (Fig 7); there was no difference in the plane of the fracture (grade 2).
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DISCUSSION
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These study findings show that in physeal fractures, the plane of injury through the cartilage can be determined by using MR imaging. The path of physeal separation as depicted by MR imaging closely parallels the path of intracartilaginous fracture seen on histologic sections. The transverse intraphyseal fracture often courses into the juxtaepiphyseal side of the physis (germinal and upper proliferative zones). Juxtaepiphyseal extension is more frequent and severe in the distal femur than in the proximal tibia, which is probably related to the greater undulation of the physis. Although the plane of separation is well seen on intermediate-weighted and T2-weighted images, gadolinium-enhanced images and spoiled gradient-recalled-echo images facilitate differentiation between low-signal-intensity fluid in the fracture and high-signal-intensity cartilage.
An intracartilaginous intraphyseal injury that extends beyond the hypertrophic level can crush and devitalize the germinal and proliferating regions, which are more integral to growth, and may even pass into epiphyseal bone. This injury, the cartilaginous component of which is unrecognizable on radiographs, can allow for the development of transphyseal vascular communications between the normally separate epiphyseal and metaphyseal vascular beds. Osteoprogenitor cells follow the vessels and form a bridge of bone that acts as a tethering point against growth (16). Extension of the fracture into the epiphysis can also injure the epiphyseal vascular supply, which is the only source of oxygen and nutrients for the growth function of the physeal cartilage. Juxtaphyseal injuries thus result in ischemic damage to the physis and disorganization or bone bridging of the growth plate (12).
In our study, the distal femoral fractures had more complex intracartilaginous pathways and involved the juxtaepiphyseal physis more often than the proximal tibial fractures. Our data help confirm the relationship between the shape of the distal femoral physis and the high incidence of posttraumatic central physeal damage (17). In experimental distal femoral fractures in rats (3), there was almost invariably central physeal damage at the apex of the inverted "v." Various studies have noted that in humans the distal femoral physis is most susceptible to growth arrest regardless of the Salter-Harris type. The occurrence of leg length discrepancy following distal femoral physeal fractures has been reported to be 56% (37 of 66 cases) (18), 41% (seven of 17 cases) (19), 36% (12 of 33 cases) (20), and 25% (16 of 65 cases) (21). The fractured distal femoral physis is more than twice as likely to develop growth arrest as the proximal tibial physis (9).
The path of the fractures seen on MR images closely resembled the path seen histologically. Our study findings show that it is easiest to determine the plane of cartilaginous injury when the fracture is partially displaced, or not perfectly reduced, because visualization is facilitated by a gap of air between fragments. The air within the fracture was most likely introduced during the surgical creation of the injury, although we have seen a similar hypointense gap after closed injuries in some children. Fluid within the fracture may obscure the fracture gap, particularly on intermediate-weighted and T2-weighted images in which fluid and adjacent injured cartilage are of similar signal intensity (Fig 7). With gadolinium-based contrast material enhancement, the cartilage enhances but the fracture space does not, which maximizes the contrast between the physis and the injury gap. A three-dimensional spoiled gradient-recalled-echo image has a similar effect, with the fracture site being a hypointense gap between layers of high-signal-intensity cartilage. The resemblance of the lesions depicted by the two modalities of study is evident in the figures.
The correlation between MR imaging and histologic findings had some inherent problems. The fracture fragments sometimes changed in alignment between MR imaging and the completion of histologic processing. In addition, the level of sectioning of the decalcified bone during histologic preparation was determined with ruler measurement, since serial sections through the entire specimen were not feasible. Accurate correlation was impossible whenever the level of histologic sectioning varied by a few millimeters from that used for MR imaging. On the other hand, transitions in the transverse level of physeal fracture usually occur gradually over several millimeters so that absolute correlation is not essential to allow for clinically relevant comparisons. More important, the signal intensity characteristics of structures seen on MR images are an average of the signal intensities of tissues contained in a 2–3-mm section, compared with the 5-µm thickness of the individual histologic sections. We correlated only specimens where the level and orientation of the sections were comparable; however, once correlated, all data were used.
At the outset of this exploratory study, we did not know what would be the appearance of fracture-separations on MR images. We thought that only a careful side-by-side correlation between MR images and histologic sections would reveal the imaging correlates of the injuries. We decided, therefore, not to perform blinded comparisons between MR images and histologic sections.
We were able to create fractures in a more controlled fashion than those that occur in patients. The degree of displacement achieved following this relatively controlled method of injury was deliberately slight so as to produce complete but uncomplicated fracture patterns. When the displacement was minimal or the reduction was nearly perfect, the fracture plane was more difficult to follow but was nonetheless always detectable on MR images. However, those experimental fractures with displacement comparable to that seen after clinical reductions were readily demonstrated on the MR studies.
We believe that the results of our study are applicable to children with physeal fracture-separations. The New Zealand White rabbit is widely used as a model for physeal injury, and its distal femoral and proximal tibial epiphyses are comparable structurally to those of a child. In a patient with radiographs that show a transverse physeal fracture-separation, it would be useful to know whether the injury spares the juxtaepiphyseal physis. This is of particular prognostic importance in injuries that involve the main physes of the lower extremity, all of which have a high incidence of posttraumatic growth disturbance even with Salter-Harris type 1 or 2 injuries. Physeal injuries in the distal femur, proximal tibia, and distal tibia account for 1.4% (13 of 951), 0.8% (eight of 951), and 10.9% (104 of 951) of all fractures involving the cartilage (22), yet these areas account for 34% (61 of 178), 16% (29 of 178), and 29% (52 of 178) of all physeal bar resections, respectively (23). These are also the areas where growth arrest is clinically most important, as these physes at the knee contribute disproportionately to growth, with 70% of total femoral growth occurring at the distal physis and 55% of total tibial growth occurring proximally (16). Their dysfunction at a time when substantial growth remains results in clinically important shortening or angular deformity or both. There is, therefore, a subset of patients with physeal injury in whom the high risk of subsequent growth arrest may justify MR imaging.
The maneuver used to generate the injuries, varus or valgus force at the extended knee, is identical to that used by some to generate stress radiographs for the diagnosis of occult physeal injuries. We strongly recommend against proving the presence of a fracture by stressing the physis, as nondisplaced physeal injuries could be considerably worsened either by causing displacement or further crushing physeal cartilage in juxtaepiphyseal injuries. It is also likely that in physeal injuries that spontaneously reduce, the degree of physeal damage can be worse than appreciated.
In summary, the course of physeal fracture-separations is complex and often involves the juxtaepiphyseal cartilage. MR imaging can depict the course and level of the cartilaginous damage in these injuries and should be useful in identifying a select group of patients at high risk of growth disturbance.
Practical application: In physeal fracture-separations, MR imaging can depict the plane of injury within the physeal cartilage; our study findings help confirm that the course of physeal fracture-separations is complex and often involves the germinal and upper proliferating layers of the physis. Detection of juxtaepiphyseal extension on MR images may have prognostic implications in physeal injuries with a high risk of resultant growth arrest, such as fracture-separations of the distal femur, proximal tibia, and distal tibia.
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Acknowledgments
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We thank David Zurakowski, PhD, for his help with the analysis of the data.
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Footnotes
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2 Current address: Department of Radiology, University of California, San Francisco. 
Abbreviation: SE = spin echo
Author contributions: Guarantors of integrity of entire study, D.J., B.F.K., F.S.; study concepts and design, D.J., B.F.K., F.S.; definition of intellectual content, D.J., B.F.K., F.S.; literature research, D.J., F.S.; experimental studies, D.J., B.F.K., F.S.; data acquisition, D.J., B.F.K., F.S.; data analysis, D.J., F.S.; statistical analysis, D.J.; manuscript preparation and editing, D.J., F.S., B.F.K.; manuscript review, D.J., F.S.
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K. Ecklund and D. Jaramillo
Patterns of Premature Physeal Arrest: MR Imaging of 111 Children
Am. J. Roentgenol.,
April 1, 2002;
178(4):
967 - 972.
[Abstract]
[Full Text]
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Abstract
Introduction
