The border of the metaphysis became sharp with high signal intensity band phase 5 ; the phase 5 region as well as the vague region with low signal intensity phase 4 might become the epiphyseal cartilage plate. In comparison, the diaphysis showed a mixture of high and low signal intensity in fetuses with a CRL of mm. All borders of the femur were recognized as regions with high signal intensity, and the periosteal color was not discernible from the border of the epiphysis on MRI.
No characteristic external change was detected at the diaphysis, whereas internal differentiation—namely, femoral ossification—was identified at the center of the diaphysis in fetuses with a CRL of A Gross view, B proximal epiphysis posterior view , C distal epiphysis. Numbers represent the crown—rump length mm. Ossified region is indicated as purple. See also S7 , S8 and S9 Movies. As previously mentioned, the femoral neck was constricted and the femoral head and greater trochanter were discernable by the end of the embryonic period CS23 [CRL of The lesser trochanter was detected in embryos with a CRL of The greater trochanter and trochanteric fossa became evident in fetuses with CRL between The femoral head fovea was identified in fetuses with a CRL of The condyles were round and spherical in fetuses with a CRL of The lateral condyle appeared round in fetuses with a CRL of The upper portions of the condyles also became angular in the lateral view in fetuses with a CRL of Incipient cartilage canal invasion at the proximal epiphysis was first observed on the surface of the femoral neck in fetuses with a CRL of 62 mm OSL, 5.
In contrast, cartilage canals at the femoral head fovea were observed in much larger fetuses and were detected for the first time in fetuses with a CRL of Cartilage canals at the distal epiphysis were detected simultaneously at the epicondyle and intercondylar fossa in fetuses with a CRL of 75 mm OSL, The data of the present study indicated that cartilage canal invasion occurred earlier at the proximal epiphysis than at the distal epiphysis.
Fetal samples were grouped into eight according to OSL with 5-mm intervals. The angle increased, reaching a median of Variation was prominent among fetuses before ossification range: The angle decreased to a median of 3. In the box plots, the bars represent the sample range, the boxes represent the second and third quartiles, and the middle line represents the median. The Procrustes shape coordinates for the proximal epiphysis indicated that each landmark on the greater and lesser trochanters and femoral head fovea was located in the same position irrespective of OSL groups of fetuses Fig 8.
In comparison, semi-landmarks FH13 , which lined the femoral head, moved in accordance with the increase in OSL. FH-f: center of the femoral head fovea; GT-l: most lateral point of the greater trochanter; GT-t: top of the greater trochanter; LT-b: bottom end of the lesser trochanter; LT-t: top of the lesser trochanter; LT-u: upper end of the lesser trochanter; FH 13 semi-landmarks from the upper end to the lower end of the femoral head along the plane passing through the midpoint of the femoral head, femoral neck, and greater trochanter.
The Procrustes shape coordinates for the distal epiphysis indicated that each landmark was located in the same position irrespective of OSL groups of fetuses S5 Fig. Semi-landmarks were located in different positions according to OSL groups, although no obvious regularity was noted. Bardeen described that the chief features of the femur achieve the characteristics of the adult bone structure in the cartilaginous stage [ 10 ]. Images of the lower leg including the femur were provided in this previous study; unfortunately, the precise features could not be confirmed in these images.
Our study clearly showed the femur before ossification in gross 3-D view and revealed the timeline for the development of the chief features of the femur. In particular, the greater and lesser trochanters and femoral head at the proximal epiphysis and the lateral and medial condyles at the distal epiphysis were detected by the end of the embryonic period CS The fovea and trochanteric fossa were prominent during the early fetal period.
The timeline for the embryonic landmarks seems to be genetically determined. However, the subsequent differentiation of anatomic landmarks likely involves the contributions of synchronized development of the surrounding joints, tendons, and muscles, as these landmarks are components for the attachment of muscle tendons and ligaments and are susceptible to movement-related changes on the joint surface. The gross view of the cartilaginous femur in fetuses may be already similar to—but not identical to—that in adults.
The structure of the cartilaginous femur may require modification. Angle measurements reflect the torsion and flexion of the femur but are unrelated to longitudinal growth. The opportunity for modification may persist during the fetal period and even after birth. Semi-landmarks corresponding to the torsion of the femoral neck were moved and located in different positions during the fetal period.
The angles were various, particularly in samples at the time of ossification. Furthermore, negative anteversion was even observed.
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Torsion of the lower leg including the femur anteversion was continuously observed during the fetal period and after birth [ 12 , 23 , 24 ]. Torsion of the femur may be prone to be affected by repetitive and persistent mechanical forces and intrauterine position [ 3 ]. Severe intrauterine compressive forces may result in congenital rotational limb deformities [ 25 ]. Further studies should investigate the detailed mechanism concerning torsion of the femur.
Procrustes analysis showed that all anatomical landmarks were located in the same position. Remodeling at the metaphysis and epiphysis during the growth of a long bone such as the femur is well known as the mechanism that maintains the shape [ 2 ]. For remodeling, osseous tissues have to be added and removed at the metaphysis and epiphysis of the developing long bone. Anatomical landmarks remained in the same relative position during subsequent endochondral ossification in the present study, indicating that the remodeling system during femur shaft growth in the longitudinal direction is elaborate.
In the present study, internal femoral changes in the chondrogenic stage and subsequent endochondral ossification were successfully detected by changing the signal intensity at the diaphysis and metaphysis. We could evaluate the correlation with histological and MRI findings using embryonic rat samples S1 Supplementary Experiments.
Considering that fluids such as blood and extracellular fluid collections exhibit high signal intensity on MRI, the difference in signal intensity between phases 4 and 5 might have resulted from the influx of blood flow and degeneration of cartilage cells at phase 5. The change in phase 4 and 5 regions could have followed; that is, phase 4 and 5 regions were first detected at the center of the diaphysis in fetuses with a CRL of Phase 4 and 5 regions became narrow, which might become the epiphyseal cartilage plate in larger fetuses. Evaluation of fetal development using sonography is clinically performed mainly after the second trimester.
OSL measurement in the femur for fetal growth assessment and pregnancy dating is accepted worldwide because femur length and OSL show a strong positive correlation with CRL [ 4 , 12 ]. Such strong correlation was also confirmed in the present study. In contrast, findings for morphological features in the femur have not yet been applied to the diagnosis of skeletal dysplasia.
Currently, limited studies have reported the reference values for fetal limb bones at 9—16 weeks of gestation using transvaginal sonography [ 26 , 27 ]. Recent studies have indicated the possibility to detect various structural anomalies at 9—12 weeks of gestation by transvaginal sonography [ 28 ]. The results of the present study might aid in the application of morphological findings for the accurate clinical diagnosis of abnormal structure. The present study has some limitations. First, we could not directly compare the histological findings for the femur and 7-T MR images acquired in the present condition using human fetal specimens because we are not allowed to destroy the human fetal specimens.
Instead, the correlation with histological and MRI findings could be evaluated using embryonic rat samples. Second, our samples were stored in a medium containing formaldehyde for a long period. We speculate that the differentiation and maturation of the diaphysis may affect the change in signal intensity in that region. However, it cannot be excluded that conditions such as long-term fixation in each sample may alter the differences in signal intensity. The possibility that morphology and several morphometric data were affected as a result of fixation or the process of termination cannot be excluded.
Third, our samples, which were obtained by artificial abortion, were recognized as externally normal; nonetheless, it is not guaranteed that all samples show normal and standard development. Fourth, we employed several kinds of image acquisition methods based on specimen resolution and volume.
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Finally, the synchronized development of the surrounding muscles and joint formations was not analyzed together with femur formation, because the image resolution in the present study was not so high to precisely detect the attachments of the muscle tendons and joint ligaments.
In conclusion, the present study provided a useful standard for the morphogenesis of the femur, which could serve as a basis to better understand femur development and could aid in differentiating normal and abnormal development. Red arrow: phase 4; yellow arrow: phase 5; asterisk: phase OS. B High magnification showing endochondral ossification. Histology belongs to phases 3—5 and phase OS. Red arrow: phase 4; yellow arrow: phase 5. A Centroid size of the proximal epiphysis according to ossified shaft length OSL.
B Centroid size of the distal epiphysis according to OSL. IF: center of the intercondylar fossa; LC-B: bottom point of the lateral condyle; LC-p: most posterior point of the lateral condyle; LE: most lateral point of the lateral epicondyle; MC-p: most posterior point of the medial condyle; MC-b: bottom point of the medial condyle; ME: most lateral point of the medial epicondyle; LC 13 semi-landmarks along the roundness of the lateral condyle from the upper end to the opposite side; MC 13 semi-landmarks along the roundness of the medial condyle from the upper end to the opposite side.
The authors thank Ms.
Chigako Uwabe and Dr. Haruyuki Makishima at the Congenital Anomaly Research Center for their technical assistance in handling the human embryos. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract The present study aimed to better characterize the morphogenesis of the femur from the embryonic to the early fetal periods. Introduction The femur is a long bone that develops via endochondral ossification. Download: PPT. Fig 2. Morphometry of the femur and evaluation of cartilage canals at the epiphysis.
Procrustes analysis Thirteen landmarks and three semi-landmarks were defined, as shown in Table 1. Table 1. Landmarks and semi-landmarks for Procrustes analysis. Statistical analysis Wilcoxon signed-rank test was used to examine the laterality of all three angles i. Fig 3. Femur development between CS18 and CS23 before ossification.
Morphogenesis of the femur during the fetal period CRL of Fig 4. Representative cross-sectional view of the right femur during the early fetal period on 7-T MR image. Fig 5. Representative 3-D reconstruction of the right femur from the embryonic period to the early fetal period. Femur length and OSL. Fig 6. Growth and endochondral ossification of the femur according to crown—rump length CRL. Cartilage canal formation at the epiphysis. Femur modeling during the fetal period Angle measurements.
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Procrustes analysis. Fig 8. Reconstructed Procrustes shape coordinates for the proximal epiphysis. Discussion Bardeen described that the chief features of the femur achieve the characteristics of the adult bone structure in the cartilaginous stage [ 10 ]. Supporting information. S1 Supplementary Experiments. Comparison of histological findings and MR images using rat femurs.
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