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Age-Related Vascular Changes in the Epiphysis, Physis, and Metaphysis: Normal Findings on Gadolinium-Enhanced MRI of Piglets

¹ Department of Radiology, Harvard Medical School and Massachusetts General Hospital, 32 Fruit St., Boston, MA 02114.
² Department of Radiology, Harvard Medical School and Children's Hospital Boston, 300 Longwood Ave., Boston, MA 02115.
³ Department of Orthopaedic Surgery and Orthopaedic Research Laboratory, Harvard Medical School and Children's Hospital Boston, Boston MA 02115.

View larger version (126K): [in a new window]   Fig. 1A. —Epiphysis of 3-week-old piglet. Photomicrograph of coronal macroscopic section of proximal femur shows major vascular canal (lateral epiphyseal vessel, thin arrow) within white epiphyseal cartilage. Dark area in metaphysis (thick arrows) corresponds to metaphyseal spongiosa.

View larger version (93K): [in a new window]   Fig. 1B. —Epiphysis of 3-week-old piglet. Photomicrograph of coronal histologic section of proximal femur reveals numerous vascular canals (arrows) within epiphyseal cartilage surrounding secondary center of ossification (O). (Toluidine blue, x2)

View larger version (135K): [in a new window]   Fig. 1C. —Epiphysis of 3-week-old piglet. Coronal T1-weighted spin-echo image (TR/TE, 300/25) of entire femur obtained 3 min after IV administration of gadoteridol. In both proximal and distal femoral epiphyses, marked enhancement is observed in physis (white arrow) and in band (black arrow) in juxtaphyseal metaphysis corresponding anatomically to metaphyseal spongiosa. Enhancement of vascular canals (arrowhead) within epiphyseal cartilage is less marked.

View larger version (114K): [in a new window]   Fig. 2A. —Phases of gadoteridol enhancement in distal femur of 2-week-old piglet. Coronal T1-weighted spin-echo images (TR/TE, 300/25) of distal femur obtained at same level before and at various times during IV administration of gadoteridol. On unenhanced sagittal image of distal femur, cartilage is of homogenous intermediate signal intensity, and marrow is of low signal intensity in metaphysis and secondary ossification center (O).

View larger version (110K): [in a new window]   Fig. 2B. —Phases of gadoteridol enhancement in distal femur of 2-week-old piglet. Coronal T1-weighted spin-echo images (TR/TE, 300/25) of distal femur obtained at same level before and at various times during IV administration of gadoteridol. Vascular phase image obtained 1 min after gadoteridol injection shows thin areas of enhancement converging radially toward ossification center within vascular canals (straight arrows), along physis (curved arrow), in physis surrounding ossification center (O), and in juxtametaphyseal physis.

View larger version (113K): [in a new window]   Fig. 2C. —Phases of gadoteridol enhancement in distal femur of 2-week-old piglet. Coronal T1-weighted spin-echo images (TR/TE, 300/25) of distal femur obtained at same level before and at various times during IV administration of gadoteridol. On canalicular phase image obtained 5 min after gadoteridol injection, radial vascular canals (straight arrows) now appear thicker and have less distinct margins. Main physis (curved arrow), physis of secondary ossification center, and metaphyseal band are well visualized.

View larger version (99K): [in a new window]   Fig. 2D. —Phases of gadoteridol enhancement in distal femur of 2-week-old piglet. Coronal T1-weighted spin-echo images (TR/TE, 300/25) of distal femur obtained at same level before and at various times during IV administration of gadoteridol. On cartilaginous phase obtained 20 min after gadoteridol injection, cartilage is of homogenous, high-signal intensity; structures can no longer be differentiated.

View larger version (16K): [in a new window]   Fig. 3. —Graph shows physeal cartilage enhancement occurs rapidly and begins to peak 3 min after administration of gadoteridol. From that point on, enhancement gradually increases and ultimately plateaus. Similar enhancement is seen in proximal and distal femoral physes (error bars, not shown, indicated significant overlap), but enhancement is much greater in piglets younger than 3 weeks than in those 3 weeks and older. Enhancement in piglets younger than 3 weeks: = proximal femoral physis, = distal femoral physis. Enhancement in piglets 3 weeks and older: = proximal femoral physis, = distal femoral physis.

View larger version (14K): [in a new window]   Fig. 4. —Graph shows that epiphyseal cartilage enhancement is gradual and slowly increases to peak 20 min after injection. Enhancement is greater in distal femur than in proximal femur. Greater enhancement is seen in epiphysis of younger animals. Enhancement in piglets younger than 3 weeks: = proximal epiphyseal cartilage, = distal epiphyseal cartilage. Enhancement in piglets 3 weeks and older: = proximal epiphyseal cartilage, = distal epiphyseal cartilage.

View larger version (14K): [in a new window]   Fig. 5. —Graph shows brisk enhancement of epiphyseal marrow. Enhancement in older animals is slower. Enhancement in piglets younger than 3 weeks: = proximal epiphyseal marrow, = distal epiphyseal marrow. Enhancement in piglets 3 weeks and older: = proximal epiphyseal marrow, = distal epiphyseal marrow.

View larger version (14K): [in a new window]   Fig. 6. —Graph shows that in this population of animals with predominantly hematopoietic marrow, metaphyseal marrow enhancement is similar to that of epiphysis. In metaphysis, difference in enhancement between younger and older animals is less marked, which probably reflects greater marrow change of epiphysis compared with marrow change in metaphysis. Enhancement in piglets younger than 3 weeks: = proximal metaphyseal marrow, = distal metaphyseal marrow. Enhancement in piglets 3 weeks and older: = proximal metaphyseal marrow, = distal metaphyseal marrow.

View larger version (8K): [in a new window]   Fig. 7. —Graph of age and proximal femoral enhancement shows that enhancement in epiphyseal cartilage () declines gradually over time. In physeal cartilage (), however, enhancement initially decreases but gradually increases thereafter. Error bars = standard error of mean.

View larger version (8K): [in a new window]   Fig. 8. —Graph of changes seen in femoral length () as piglets matured shows that there is no resemblance between physeal enhancement and growth rate. If anything, fastest growth occurs during period of least enhancement. Error bars = standard error of mean. No measurements were taken in piglets older than 6 weeks, although skeletal growth is expected to continue for approximately 4 more months.

View larger version (111K): [in a new window]   Fig. 9A. —Marrow enhancement in 6-week-old piglet. A and B, Sagittal T1-weighted spinecho images (TR/TE, 300/25) of distal femur obtained after gadoteridol injection. At 3 min after injection, central lack of enhancement in epiphyseal marrow (arrow, A) is seen. At 10 min after injection, epiphyseal marrow shows homogeneous enhancement (arrow, B).

View larger version (112K): [in a new window]   Fig. 9B. —Marrow enhancement in 6-week-old piglet. A and B, Sagittal T1-weighted spinecho images (TR/TE, 300/25) of distal femur obtained after gadoteridol injection. At 3 min after injection, central lack of enhancement in epiphyseal marrow (arrow, A) is seen. At 10 min after injection, epiphyseal marrow shows homogeneous enhancement (arrow, B).

View larger version (131K): [in a new window]   Fig. 10A. —Histopathologic specimens of vascular canals of 1-week-old piglet. Photomicrograph of epiphyseal cartilage section shows chondrocytes in midst of pink-staining matrix. Longitudinal space (arrow) within cartilage contains several vascular structures surrounded by tissue with scanty cellularity that in turn is surrounded by cartilage matrix. (Toluidine blue, x40)

View larger version (111K): [in a new window]   Fig. 10B. —Histopathologic specimens of vascular canals of 1-week-old piglet. Photomicrograph of transverse section of vascular canal shows three compartments that determine phases of epiphyseal vascular enhancement: 1 = intravascular space, 2 = canalicular space; 3 = cartilaginous space. (Toluidine blue, x100)

View larger version (143K): [in a new window]   Fig. 11A. —Epiphysis and physis in 1-week-old piglet.Compare T2-weighted image with gadoteridol-enhanced T1-weighted image. Sagittal T2-weighted fast spin-echo image (TR/TE, 2500/98; echo-train length, 8) shows differentiation between epiphysis and physis, but no distinct vascular canals are visible.

View larger version (149K): [in a new window]   Fig. 11B. —Epiphysis and physis in 1-week-old piglet.Compare T2-weighted image with gadoteridol-enhanced T1-weighted image. Sagittal T1-weighted spin-echo image (300/25) shows clearest physeal–epiphyseal differentiation, physis of secondary ossification center, and epiphyseal vascular canals.

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