Femoral posture during embryonic and early fetal development: An analysis using landmarks on the cartilaginous skeletons of ex vivo human specimens

Abstract

The pre-axial border medially moves between the fetal and early postnatal periods, and the foot sole can be placed on the ground. Nonetheless, the precise timeline when this posture is achieved remains poorly understood. The hip joint is the most freely movable joint in the lower limbs and largely determines the lower-limb posture. The present study aimed to establish a timeline of lower-limb development using a precise measurement of femoral posture. Magnetic resonance images of 157 human embryonic samples (Carnegie stages [CS] 19-23) and 18 fetal samples (crown rump length: 37.2-225 mm) from the Kyoto Collection were obtained. Three-dimensional coordinates of eight selected landmarks in the lower limbs and pelvis were used to calculate the femoral posture. Hip flexion was approximately 14° at CS19 and gradually increased to approximately 65° at CS23; the flexion angle ranged from 90° to 120° during the fetal period. Hip joint abduction was approximately 78° at CS19 and gradually decreased to approximately 27° at CS23; the average angle was approximately 13° during the fetal period. Lateral rotation was greater than 90° at CS19 and CS21 and decreased to approximately 65° at CS23; the average angle was approximately 43° during the fetal period. During the embryonic period, three posture parameters (namely, flexion, abduction, and lateral rotation of the hip) were linearly correlated with each other, suggesting that the femoral posture at each stage was three-dimensionally constant and exhibited gradual and smooth change according to growth. During the fetal period, these parameters varied among individuals, with no obvious trend. Our study has merits in that lengths and angles were measured on anatomical landmarks of the skeletal system. Our obtained data may contribute to understanding development from anatomical aspects and provide valuable insights for clinical application.

Fig 1. Representative ventral image showing the lower-limb posture during the late embryonic period.

Note that the impressive “praying feet” posture (i.e., the hallux was located on the cranial side, and the foot sole oriented medially) was observed at CS23 or earlier stages. The hip joint showed <90° of lateral rotation, whereas the ankle showed adduction. Abbreviation: CS, Carnegie stage.

Fig 2. Definitions of the landmarks and coordinate system.

For embryonic specimens, the eight selected landmarks were as follows: center of bilateral femoral heads (H_r, H_l); bilateral knee (K_r, K_l) and ankle joints (A_r, A_l); and cranial region of the first and third sacral vertebrae (S1, S3). For fetal specimens, the medial and lateral femoral epicondyles (Me_r, Me_l, Le_r, Le_l) were selected instead of the bilateral ankle joints. S3 was defined as the origin and the z-axis (body axis) as the line through S1 and S3. The z–x plane (median plane) was defined using the midpoint between H_l and H_r (H_m); H_m was located in the median plane. The y-axis was defined as the normal vector of the median plane, and the x-axis was calculated as the outer product of the z- and y-axes.

Fig 3. Representative overall pictures and 3D reconstructions of skeletal structures: The hip joint (lateral view) during the embryonic period between CS19 and CS23 and during the early fetal period.

Note that the relative position of the hip joint and sacrum in the cranial–caudal direction changed between the embryonic and fetal periods. Legends: blue, femur (ossified); brown, femur (not ossified); green, pubis; light blue, coccyx; pink, sacrum; purple, ilium; yellow, ischium. “*” indicates the greater trochanter.

Fig 4. Flexion angle in the lower limbs.

Hip joint (A) and knee joint (B) flexion. (A) Hip joint flexion during the embryonic (left) and fetal (right) periods. (B) Knee joint flexion during the embryonic period. Legends: blue, right lower limb; red, left lower limb.

Fig 5. Representative 3D reconstructions of skeletal structures: The hip joint (ventral view).

Note that the pubic symphysis (black arrows) was first contacted at CS23. Legends: blue, femur (ossified); brown, femur (not ossified); green, pubis; light blue, coccyx; pink, sacrum; purple, ilium; yellow, ischium. “*” indicates the greater trochanter, and the red arrows point at the sacroiliac joint.

Fig 6. Abduction angle and lateral rotation angle of the hip.

(A) Abduction angle of the hip during the embryonic (left) and fetal (right) periods. (B) Lateral rotation angle of the hip during the embryonic (left) and fetal (right) periods.

Fig 7. Correlation between flexion, abduction, and lateral rotation of the hip.

Fig 8. Pelvic ring formation.

(A) Cranial view of the 3D reconstruction indicating pelvic ring formation during the embryonic period (CS19, CS21, and CS23). The red triangle indicates the hip–sacrum angle (i.e., the angle between the right femoral head, first sacrum, and left femoral head [∠H_r-S1 and S1-H_l]), which was projected onto the x–y plane (transverse plane). Legends: Blue, femur (ossified); brown, femur (not ossified); green, pubis; light blue, coccyx; pink, sacrum; purple, ilium; yellow, ischium. (B) Change in the hip–sacrum angle during the embryonic (left) and fetal (right) periods. (C) Height of the hip joint during the embryonic (left) and fetal (right) periods. The height of the hip joint along the z-axis (cranial–caudal direction) is shown, with the position of S3 indicated as a reference.

Fig 9. Length measurements of the lower limbs.

(A) Pelvic length measurements during the embryonic (left) and fetal (right) periods: lengths of the inter-hip joint (segment H_r-H_l) and sacrum (S1–S3). (B) Length measurements of the lower limbs during the embryonic (left) and fetal (right) periods: lengths of the bilateral femoral shafts (segment H-K) and lower limbs (segment K-A).