Effects of normal and abnormal loading conditions on morphogenesis of the prenatal hip joint: application to hip dysplasia

Abstract

Joint morphogenesis is an important phase of prenatal joint development during which the opposing cartilaginous rudiments acquire their reciprocal and interlocking shapes. At an early stage of development, the prenatal hip joint is formed of a deep acetabular cavity that almost totally encloses the head. By the time of birth, the acetabulum has become shallower and the femoral head has lost substantial sphericity, reducing joint coverage and stability. In this study, we use a dynamic mechanobiological simulation to explore the effects of normal (symmetric), reduced and abnormal (asymmetric) prenatal movements on hip joint shape, to understand their importance for postnatal skeletal malformations such as developmental dysplasia of the hip (DDH). We successfully predict the physiological trends of decreasing sphericity and acetabular coverage of the femoral head during fetal development. We show that a full range of symmetric movements helps to maintain some of the acetabular depth and femoral head sphericity, while reduced or absent movements can lead to decreased sphericity and acetabular coverage of the femoral head. When an abnormal movement pattern was applied, a deformed joint shape was predicted, with an opened asymmetric acetabulum and the onset of a malformed femoral head. This study provides evidence for the importance of fetal movements in the prevention and manifestation of congenital musculoskeletal disorders such as DDH.

Keywords: Computational model; DDH; Developmental dysplasia of the hip; Joint biomechanics; Joint development; Joint shape.

Fig. 1

(A) Dimensions of initial model of concave pelvis and spherical femoral head region. (B) Changes in shape were assessed by the measurements proposed by Ralis and McKibbin (1973), where the acetabular shape was assessed by the ratio between the deepest height (a₂) to the greatest width (a₁) of the acetabular cavity, and the femoral head shape was assessed as the ratio between the greatest height (h₂) as measured perpendicularly to the greatest diameter, and the greatest diameter (h₁) of the femoral head. (C) Changes in fetal weight on a logarithmic scale (extracted from data from (Doubilet et al., 1997) taken as a measure of the rate of fetal growth. Three stages of fetal growth were identified by fitting lines to regions of the growth curve; the movements applied for each stage are superimposed. (D) Initial configuration used for the abnormal (asymmetric) movement; the femoral head is rotated 20° to the right of the vertical axis of the acetabulum. (E) Method used to calculate the acetabular and femoral head skew factors; the former measured as the ratio of the distances between a reference point, calculated as the center of the initial acetabular cavity, and the left (x₁) and right (x₂) extremities of the acetabular space, the latter as the ratio of the distances between a reference point, calculated as the centre of the initial femoral head, and the left (y₁) and right (y₂) extremities which lie on the horizontal line passing through the reference point of the femoral head.

Fig. 2

(A) Two timeframes from a fetal cine-MRI at 22 gestational weeks showing a hip flexion-extension range of 88°. (B) Timeframes from a fetal cine-MRI at 34 gestational weeks showing a hip flexion-extension of 11°. These data were used to estimate the range of motion at the hip over gestation. Fetal cine-MR images courtesy of Professors Hajnal and Rutherford, King's College London, UK.

Fig. 3

(A) Biological contribution to growth; for the femoral head the chondrocyte density was greatest at the proximal end of the epiphysis, while for the pelvis the density was highest at the centre of the acetabulum. (B) Resulting hydrostatic stresses, averaged over the first full cycle of physiological motion. Stresses were higher along the acetabular rim and at the regions of curvature of the distal femoral head. (C) The stresses generated by the combination of biological and hydrostatic stresses lead to higher values of growth at the proximal end of the femoral head and at the center of the acetabulum.

Fig. 4

(A) Predicted hip joint morphogenesis under physiological symmetric movements; a progressive opening of the acetabulum and a gradual decrease in roundness of the femoral head were predicted. (B) Quantification of the changes in shape based on the acetabular shape and femoral head roundness parameters. (C) Changes in human hip joint shape over development measured experimentally by Ráliš and McKibbin (1973).

Fig. 5

(A) The effects on acetabular and femoral head shape of reduced movements at each stage of development (early, middle and late) and of a complete absence of movements. When movements were reduced at the early stage, the acetabulum became shallower and the femoral head roundness decreased compared to the predictions for physiological movements. Reduced movements in the middle and late stages of development resulted in minimal joint shape changes. When absent movements were simulated, the shape changes were similar to those of the early reduction simulation, with the predicted joint shape for absent movement having a slightly shallower acetabulum than that of the early reduction. (B) Predicted shapes under physiological movements (blue) and early reduction of movements (red). When movements were reduced in the early stage, a less rounded femoral head and a shallower acetabulum were predicted. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 6

(A) Predicted joint morphogenesis under asymmetric movements; a progressive opening of the acetabulum in the direction of the applied loads was predicted, while the femoral head showed a loss of head sphericity and malformation on the medial side. (B) The predicted hip joint shape at birth when asymmetric loading occurs is similar to the hip joint of a 30 month old infant affected by DDH. Image adapted with permission from Dr Frank Gaillard from website www.radiopaedia.org.

Fig. 7

(A) The effects of reduced asymmetric movements on acetabular shape and (B) skew factor at each stage of development (early, middle and late) and under a complete absence of movements. With a full range of asymmetric movement, or reduced movement at the middle or late stages, the predicted acetabular shape was shallower than for simulations with no movement or with reduced movement in the early stage.