The Prenatal Development of the Human Locomotor System

Chapter 01 The Development of the Limb Buds / 1
Chapter 02 The Growth of Long Bones / 7
Chapter 03 The Development of the Joint / 17
Chapter 04 The Early Development of the Vertebrae / 27
Chapter 05 The Development of the Cervical Vertebrae / 35
Chapter 06 The Development of the Thoracic Vertebrae / 47
Chapter 07 The Development of the Lumbar Vertebrae / 61
Chapter 08 The Development of the Shoulder Joint / 75
Chapter 09 The Development of the Elbow Joint / 91
Chapter 10 The Development of the Wrist and Hand / 103
Chapter 11 The Development of the Pelvis and the Sacroiliac Joint / 119
Chapter 12 The Development of the Hip Joint / 129
Chapter 13 The Development of the Knee Joint / 145
Chapter 14 The Development of the Ankle and Foot / 165

Index / 185

Chapter 01 The Development of the Limb Buds

The first mesenchymatous condensations of the appendicular skeleton are in the region of the future girdles and those for the pectoral region appear a little before those of the pelvic region. In their basic plan of structure, the arm and leg are closely comparable. The upper limb buds develop opposite the lower cervical segments, and the lower limb buds appear at the level of the lower lumbar segments. Each limb bud consists of an outer ectodermal cap and an inner mesodermal core. At the apex of each limb bud, the ectoderm thickens to form an apical ectodermal ridge (AER).
By the start of the fifth week, the upper limb buds are paddle-shaped and lower limb buds are flipper-like. At the start of the sixth week, the upper limbs begin to show regional differentiation as the elbows and hand plates (Figs. 1-1 and 1-2). The primordia of the fingers begin to develop in the hand plates, which indicate the formation of digits. At the tip of each digital ray, a part of the apical ectodermal ridge induces development of the mesenchyme into the mesenchymal primordia of the bones in the digits. The AER of the upper and lower limbs are first seen in the fifth week (Figs. 1-3 and 1-7) and disappear after the sixth week. Development of the lower limbs occurs somewhat later than that of the upper limbs (Fig. 1-7). During the fifth week, the peripheral nerves grow from the developing brachial and lumbosacral plexuses into the mesenchyme of the limb buds.
The mesenchyme in the limb bud gives rise to bones, ligaments, and blood vessels. By the start of the sixth week, the mesenchymal precursor of the distal limb skeleton is distinct in the upper and lower limbs, and chondrification commences in the humerus, ulna, and radius (Fig. 1-4). By the end of the sixth week, the carpal and metacarpal bones also begin to chondrify (Fig. 1-5). Nerves also advance and the radial, median, and ulna nerves reach the hand plate (Fig. 1-6). In the lower limb, the femur, tibia, and fibula begin to chondrify by the middle of the sixth week (Fig. 1-7), and tarsal and metatarsals begin to chondrify by the end of the sixth week (Fig. 1-8).
During the fifth week, the somitic mesoderm invades the limb bud and forms two large condensations, one ventral to the axial mesenchymal column and the other dorsal to it. The cell of the condensations forms the anlagen of the limb muscles and differentiates into myoblasts. As the long bones form, myoblasts fuse together to form a large muscle mass in each limb bud. In general, this muscle mass separates into dorsal and ventral components.
The primary ossification centers of the limb bones appear in the eighth week. By 12th week, primary ossification centers have appeared in nearly all bones in the limbs.

References

O'Rahilly R, Gardner E: The timing and sequences of events in the development of the limbs in human embryo. Anat Embryol 148: 1-23, 1975.
Rutherford NC: A contribution to the embryology of the forelimb skeleton. J Anat 48: 355-377, 1914.
Streeter GI: Developmental horizons in the human embryos. A review of the histogenesis of cartilage and bone. Contrib Embryol 33: 151-168, 1949.

Chapter 02 The Growth of Long Bones

Most of the long bones of the body are developed by periosteal, endochondral and epiphyseal ossification.

Periosteal and endochondral ossification

The general shape of the femur is quite similar to that of the adult in a 20 mm embryo. Ossification begins at the middle of the cartilaginous model of the femur. A thin layer of the calcified bone matrix is laid down between the perichondrium and the portion of the shaft containing hypertrophied cartilage cells and by extending around the shaft forming a bony collar in the 25 mm embryo (Fig. 2-1), and in the 30 mm fetus it extends nearly one-fourth of the length of the femur (Fig. 2-2). This periosteal bone is in direct contact with cartilage. Simultaneously with the appearance of the bony collar, changes take place in the center of the diaphysis hypertrophy and become vacuolated. The hypertrophied chondrocytes result in the enlargement of their lacunae and reduction in the intervening cartilage matrix septa, which become calcified. Erosion of the bony collar is evident in the 40 mm fetus and destruction of the calcified cartilage occurs by the 45 mm fetus. Holes etched in the bony collar by osteoclasts permit a periosteal bud, composed of osteoprogenitor cells, and blood vessels, to enter the concavities within the cartilage model. These periosteal capillaries grow into the cartilage model and initiate the development of a primary center of ossification in the 50 mm fetus. This formation of bone constitutes endochondral ossification (Fig. 2-3). As endochondral ossification proceeds proximally and distally and growth zones become established, periosteal bone formation also proceeds longitudinally until the 260 mm fetus, and extends about 1-2 mm beyond the zone of cartilage destruction in the growth zones. After the 260 mm fetus, the extents of endochondral and periosteal ossification are the same and at term occupy 70% of the length of the femur. Trabeculation of the bony collar is first noted in the 50 mm fetus (Fig. 2-4). Fusion of endochondral trabeculae with the inner aspect of the periosteal shell begins by the 70 mm fetus (Figs. 2-5 and 2-6). Evidence of reconstruction appears in both the proximal and distal ends by the 105 mm fetus (Fig. 2-7) and is always present in both ends after the 120 mm fetus (Figs. 2-8. 2-9, and 2-10). The trabeculated compacta of the peristeal bone is thick and the marrow cavity is relatively narrow by the 150 mm fetus (Figs. 2-10 and 2-11).

Epiphseal ossification

Until skeletal growth is completed, a long bone continues to lengthen as a result of interstitial growth of the cartilage that is retained as its epiphyseal growth plates. Because the epiphyseal plates grow on one side and become replaced by bone on the other, they are gradually shifted apart, lengthening the bony diaphysis that lies between them (Fig. 2-12). The formation of long bones is slightly more complex because these bones develop the secondary center of ossification. The majority of secondary centers are formed postnatally, but those in the distal and proximal tibia begin to appear just prior to birth. The first morphological evidence of the developing secondary center of the ossification center in the distal femoral chondroepiphysis is found in the 300 mm fetus (Fig. 2-13). The ossification center is in the form of multiple foci of calcification. Initial calcification occurs immediately adjacent to the end of a cartilage canal and not an avascular matrix. Once the bony center appears, ossification along the articular side of the secondary center is different from that along the metaphyseal side. The hypertrophied chondrocytes of the articular side are not distinctly parallel and the intercellular matrix is mineralized in all directions. As the secondary center expands toward the metaphyseal side, many chondrocytes do not degenerate (Fig. 2-15). With the progressive development of the secondary ossification center, the epiphyseal growth plate becomes well differentiated and shows a typical zonal differentiation (Figs. 2-14 and 3-15). In the youngest child, the perichondral ring (membrane) extends well beyond the advancing trabeculae of the metaphysis and in the seven-year-old it extends only slightly beyond the adjacent trabeculae (Fig. 2-15). Throughout the period of active bone growth, the dense layer of the perichondral ring is demonstrated. These findings support the previous suggestion that the transverse diameter of the epiphyseal plate increases by appositional growth from the overlying perichondrium, and that the same source is responsible for the lateral extension of the articular cartilage during growth.

References

Bardeen C: Studies of the development of the human skeleton. Am J Anat. 4: 265-302, 1905.
Gardner E, O'Rahilly R: The early development of the knee joint in staged human embryos. J Anat 102: 289-299, 1968.
Gray DJ, Gardner E: Prenatal development of the human knee and superior tibiofibular joint. Am J Anat 86: 235-287, 1950.
Kuhlman RE: A microchemical study of the developing epiphyseal plate. J Bone Joint Surg 42A: 457-466, 1960.
Noback CR, Robertson GG: Sequences of appearance of ossification centers in the human skeleton during the first five prenatal months. Am J Anat 89: 1-28, 1951.
Park SL: The prenatal development of femur in Korean fetuses. Chonnam Medical J 10: 1075-1090, 1973.
Pratt CWM: Observations on osteogenesis in the femur of the foetal rat. J Anat 91: 533-544, 1957.