Embryology, Anatomy, and Normal Findings
Embryology
Both striated muscle and bone are derived from the mesodermal germ layer. The limb buds form at the end of the fourth week of fetal life. Near the end of the second month of fetal life, the embryonal cartilaginous skeleton is already subdivided into its principal segments, which are the forerunners of bones of the limbs. Primary ossification centers are formed by deposition of calcium in the cartilaginous matrix after hypertrophy and vacuolization of local cartilage cells.1 In tubular bones, this process occurs at approximately the midpoint of the shaft and is followed by central resorption, which gives rise to the primary marrow cavity. Calcified disks proximal and distal to the primary cavity become preparatory zones of calcification after the development of the advancing, proliferating shaft during growth. Cartilage proximal and distal to the zones of calcification becomes the epiphyses. A layer of cells within the epiphyses near the shaft produces new cells that are interposed between the resting cartilage of the epiphysis and the older cells and calcified cartilage adjacent to the shaft. The matrix around the old cells calcifies and is invaded by capillaries and bone cells from the marrow. Bone is formed on the calcified cartilage, and new bone and cartilage undergo remodeling by osteoclasts and osteoblasts, so that the length of the bone is increased (Fig. 129-1). The girth of the bone and the thickness of the cortex are increased by subperiosteal accretion caused by activity of the subperiosteal osteoblasts. Peripheral resorption of bone at the advancing ends of the shaft maintains the gentle flaring that characterizes normal tubular bone and is the mechanism responsible for what is termed “modeling.” Disproportionate osteoclastic activity within the shaft of the bone reams out a marrow cavity. Continued, balanced activity of all these processes permits a small tubular bone to become a large tubular bone while functional shape and relations with adjacent structures are maintained.
Figure 129-1 Schema of progressive stages in the growth and maturation of the tibia.
A, The mass of embryonal cartilage that is the anlage of the tibia. B, Initial enlargement and multiplication of the central cartilage cells and an increase in cartilaginous matrix—the chondrification center that is the forerunner of the primary ossification center. C, The early primary ossification center shows the formation of a central belt of subperiosteal bone (early cortex) and penetration of the cartilaginous matrix by the periosteal elements; the channel of this penetration persists as the nutrient canal. D, Extension of ossification toward both ends of the shaft, with central resorption forming the medullary cavity. E, The tibia at birth, with a secondary ossification center in the proximal epiphyseal cartilage. F, At approximately the fourth postnatal month, ossification centers are seen in both of the epiphyseal cartilages. G, The juvenile tibia shows the growth of all components and enlargement of the epiphyseal secondary ossification centers. H, The adult tibia, with complete fusion of the shaft and both epiphyses. The narrow plates of articular cartilage that cap each end of the bone persist throughout life. 1, nutrient canal; 2, epiphyseal cartilage; 3, corticalis; 4, spongiosa; 5 and 6, provisional zones of calcification or epiphyseal plates; 7, articular cartilages; 8, secondary epiphyseal ossification centers. (Modified from an original drawing by W. M. Rogers, MD.)
Secondary ossification centers appear in the cartilaginous epiphyses and apophyses and enlarge by similar but much slower processes than those that enlarge the shaft. Irregularities in density and discontinuities in the structure of secondary ossification centers are frequent during normal mineralization and simulate the features of disease. The known ages at first appearance and upon fusion of these ossification centers can serve as indicators of physical maturation (Figs. 129-2 and 129-3; Table 129-1).
Table 129-1
Epiphyseal Ossification in the Fetus and Neonate: Fifth and Ninety-Fifth Percentiles
| Ossification Center | Fifth Percentile | Ninety-Fifth Percentile |
| Humeral head | 37th week | 16 postnatal weeks |
| Distal femur | 31st week | 39th week (female) |
| 40th week (male) | ||
| Proximal tibia | 34th week | 2 postnatal weeks (female) |
| 5 postnatal weeks (male) | ||
| Calcaneus | 22nd week | 25th week |
| Talus | 25th week | 31st week |
| Cuboid | 37th week | 8 postnatal weeks (female) |
| 16 postnatal weeks (male) |
Data from Kuhns LR, Finnstrom O. New standards of ossification of the newborn. Radiology. 1976;119:655-660.
Physiology
The bones provide rigid support for the body and sites of insertion for muscles, to which the bones respond as levers. The bones are active physiologically in infants and children, changing size and shape with growth and hormone activity (related to levels of vitamin D, parathyroid hormone, calcitonin, or serum calcium and phosphate levels) and in response to mechanical stresses.2
During growth, in addition to its constant increase in length and breadth, the shaft is continuously molded or reshaped to its final form. The mechanism responsible for these changes in shape has been called “modeling” or “tubulation.” One of the most conspicuous features of modeling is progressive concentric contraction of the shaft behind the wider, advancing terminal segment (Fig. 129-4); this process results in flared ends of bones.
Anatomy
Three types of bones are found in the limbs: (1) long and short tubular bones, (2) round bones in the wrists and ankles, and (3) sesamoids, which are small bones in the tendons and articular capsules. Functionally, a growing tubular bone is made up of the following segments: diaphysis, metaphysis, physis, and epiphysis (Fig. 129-5). “Long bones” have epiphyses at both ends. Short tubular bones (“short bones”) have epiphyses at one end—generally, where the greater joint motion of the individual bone occurs. In the hands and feet, secondary ossification centers appear in the bases of the phalanges and in the distal ends of the second through fifth metacarpals and metatarsals. Epiphyses for the first metacarpal and first metatarsal are found in the proximal ends of the bones. The location of the secondary centers appears to be related to the sites of maximal joint motion of individual bones. Apparent epiphyseal ossification centers observed at the ends of short bones, where their occurrence is not expected, are termed “pseudoepiphyses.”
Normal Findings
The gestational age of a newborn can be estimated radiographically through several methods. The proximal humeral ossification center appears shortly after birth, with a 95% confidence interval between 37 weeks’ gestation and 16 weeks’ postnatal life.3 Because ossification before 37 weeks is unusual, the presence of the proximal humeral ossification center is an indication that a newborn is at term or near term. Teeth appear at a characteristic time; the first deciduous molars form at 33 weeks, and the second deciduous molars form at 36 weeks. The range of values is great for the radiographic appearance of various appendicular bone epiphyseal ossification centers, even in premature infants (see Table 129-1).
Evaluation of bone age is used to estimate biologic maturation relative to chronologic age. Differences in familial, racial, and socioeconomic factors limit the applicability of the standards of Greulich and Pyle (which were developed in the 1940s) to today’s children.4 It is well accepted that maturation varies between races. For instance, African American children mature faster than do white children.5 The hand, with its numerous secondary centers in phalanges and metacarpals, and to a lesser degree the wrist, are used as an index of total skeletal maturation. Standard deviations, which are based on chronologic age, are somewhat broad. A bone age within the 5% to 95% confidence interval (or ±2 standard deviations) is considered normal.
In children younger than 2 years, use of the standards of Greulich and Pyle is limited because relatively little change is noted in the ossification centers of the hand and wrist during this period. More rapid changes may be observed in the knee or foot, however. Radiographs of the left knee or left foot—anteroposterior and lateral—therefore are obtained in children younger than 2 years of age and are compared with published standards (for the knee, standards of Pyle and Hoerr [1969]6; for the foot and ankle, standards of Hoerr, Pyle, and Francis [1962]7).
The Risser classification can be used to assess skeletal maturation through evaluation of the appearance and state of fusion of the iliac crest.8 Ossification of the iliac crest begins laterally and proceeds medially: stage 0—no ossification; stage I—up to 25% ossified; stage II—25% to 50% ossified; stage III—50% to 75% ossified; stage IV—75% to 100% ossified; and stage V—fully ossified and fused (e-Fig. 129-6).
Assessment of skeletal age by radiography is useful in many clinical scenarios. Boxes 129-1 and 129-2 list causes of advanced and delayed skeletal maturation, respectively. Menarche typically occurs after fusion of the physes of the distal phalanges. Bone age can be used with long bone measurements to predict adult height. Assessment of bone age is valuable in the planning of orthopedic treatments, including epiphysiodesis, leg-lengthening procedures, and scoliosis management.
Anatomic Variants
Experience and knowledge often are the best resources for successfully identifying normal variants. Compendiums of normal variants (e.g., An Atlas of Normal Roentgen Variants That May Simulate Disease by Keats and Anderson9 and Borderlands of Normal and Early Pathological Findings in Skeletal Radiography by Freyschmidt et al.10) are invaluable resources.
Many epiphyseal and apophyseal ossification centers are irregular and fragmented in their early development (Fig. 129-7). When evaluating the significance of irregular ossification in a single area, it is important to remember that normal irregularities of ossification usually are symmetric and accompanied by similar changes in other areas of the skeleton. Normal epiphyseal and apophyseal fragmentary ossification tends to have a smooth, round, and sclerotic appearance. Sometimes epiphyseal fragmentary ossification centers may have a jigsaw configuration. Normal epiphyseal fragmentary ossification should be differentiated from acute fractures that tend to have a linear contour with nonsclerotic margins with accompanying soft tissue swelling and joint effusions.
Figure 129-7 Common sites of normally irregular mineralization in the growing skeleton are marked by crosses.
A, The cranium. During the first weeks of life and continuing for several months, edges of the bones at the great sutures are commonly irregular, and in many infants deep fissures extend from the sutures into the bodies of the bones. Irregularities also are common on the edges of the temporal suture (not shown). B, The pelvis: 1, crest of ilium; 2, secondary center in crest of ilium; 3, secondary center of anterior superior spine; 4, os acetabuli marginalis; 5, body of ischium; 6, secondary center of ischium; 7, ischium and pubis at the ischiopubic synchondrosis; 8, body of pubis; 9, ilium at sacroiliac joint; 10, sacrum at sacroiliac joint; 11, iliac edge and roof of the acetabular cavity. C, The scapula: 1 and 2, secondary centers of acromion process; 3, secondary center of vertebral edge; 4, secondary center of inferior angle. D, The upper limb: 1, secondary center of trochlea, always irregular; 2 and 3, proximal and distal epiphyseal centers of ulna; 4, proximal epiphyseal center of radius; 5, greater and lesser multangulars; 6, inconstant center of second metacarpal (pseudoepiphysis); 7, pisiform. E, The lower limb; 1, proximal metaphysis of femur; 2 and 3, secondary center and edges of shaft at greater and lesser trochanters, respectively; 4 and 5, lateral and medial edges, respectively, of distal epiphyseal center of femur; 6, patella; 7 and 8, medial and lateral edges, respectively, of proximal epiphyseal center of tibia; 9, secondary center in anterior tibial process; 10, proximal epiphyseal center of fibula; 11 and 12, distal metaphysis and distal epiphyseal center of fibula, respectively; 13, internal malleolus of distal epiphyseal center of tibia; 14, apophysis of calcaneus; 15, primary center of calcaneus; 16, navicular; 17, cuboid; 18, cuneiform; 19, proximal epiphyseal center of first metatarsal; 20, epiphyseal centers of phalanges. F, The spine; 21, marginal centers (end plate apophyses).
Physiologic osteosclerosis of the newborn is a common finding. The long tubular bones of fetuses, premature infants, and term newborn infants often appear sclerotic compared with the bones of older children because of proportionately thicker cortical bone and more abundant spongiosa during fetal and neonatal life (e-Fig. 129-8). The sclerotic features disappear gradually during the first weeks of life and resolve by 2 to 3 months of age.
e-Figure 129-8 Normal osteosclerosis of the newborn.
All of the bones appear dense. The medullary cavities of the pubic bones and proximal femurs are obscured.
Physiologic periosteal reaction in the newborn also is a common finding that is seen in infants from 1 to 4 months of age and in both premature and term infants. Physiologic periosteal new bone is diaphyseal, smooth, regular, and 2 mm or less in thickness (Fig. 129-9).11 Physiologic periosteal new bone is most common in the tibia, femur, and humeral diaphysis and occasionally is seen in the radius and ulna. In most infants, physiologic periosteal new bone is symmetric; however, it may be asymmetric in one third to half of patients. Traumatic periosteal new bone tends to be asymmetric, metaphyseal, thicker, and irregular compared with physiologic periosteal new bone.
A variety of normal variants in the metaphyses of infants may simulate injury. It is important to distinguish these findings from the classic metaphyseal lesions of child abuse (see Chapter 145). The most common variant is the subperiosteal bone collar of the juxtaphyseal metaphysis, which has a normal step-off that may mimic a metaphyseal lesion of child abuse (Fig. 129-10).12
The following selected, important variants should not be confused with pathology.
Hands and Feet
Ivory Epiphyses: Sclerotic epiphyseal ossification centers of the phalanges are called “ivory epiphyses” (e-Fig. 129-11).13 They occur in approximately 1 in every 300 patients. Ivory epiphyses usually are found in the distal phalanges and in the middle phalanx of the fifth digit. Maturation may be retarded. Ivory epiphyses also may occur in association with cone-shaped epiphyses in dysplastic syndromes. Ivory epiphyses are more frequently found in the toes compared with the fingers.
Cone-Shaped Epiphyses: Cone-shaped epiphyses of the phalanges (e-Fig. 129-12) occur singly or in combination and most commonly affect the terminal phalanges. When they occur in isolation, they may be related to trauma with resultant central physeal growth disturbance. When they are multiple, they may be seen in association with dysplastic syndromes and metabolic bone disease. Cone-shaped epiphyses are found more frequently in the toes than in the fingers (Fig. 129-13).
Figure 129-13 Symmetric conical or bell-shaped epiphyseal ossification centers (arrows) in the proximal phalanges of the second, third, and fourth toes of an asymptomatic 5-year-old girl.
The contiguous distal end of each shaft is recessed to receive its elongated ossification center. The epiphyseal ossification centers in the proximal phalanges of the first and fifth toes are the normal, flat, shallow, transverse disks usually present in all of the phalanges.
Fifth Metatarsal Apophysis: During puberty, a longitudinally oriented, scalelike secondary ossification center appears within the proximal apophyseal cartilage of the fifth metatarsal (Fig. 129-14). Irregular ossification of the apophysis is common. The normal apophyseal ossification center may appear widely spaced from the underlying fifth metatarsal, simulating fracture.14 The fifth metatarsal apophysis also may be bifid (e-Fig. 129-15). This presentation should be differentiated from a fifth metatarsal avulsion fracture related to the peroneus brevis insertion, which has a horizontal orientation (e-Fig. 129-16) (see also Chapter 143).
Figure 129-14 Normal apophysis of the fifth metatarsal in a 10-year-old girl (arrow).
The apophyseal growth plate is longitudinal in orientation, and the apophysis appears “scalelike.”
Pseudoepiphyses: Pseudoepiphyseal ossification centers may appear in the proximal cartilaginous portion of the growing second through fifth metacarpals and metatarsals and in the distal cartilage of the first metacarpals and metatarsals (Fig. 129-17 and e-Fig. 129-18).15 They are formed from a thin rod of osteogenic tissue that invades the proximal cartilage from the shaft. The end of the rod enlarges to form a mushroom-shaped mass of bone that appears radiographically as the “pseudoepiphysis.” The site of fusion of the pseudoepiphysis with the shaft often is indicated by a notch. Pseudoepiphyses are well formed by 4 to 5 years of age and fuse with the underlying shaft at the time of skeletal maturation. Pseudoepiphyses are frequent in children with hypothyroidism and cleidocranial dysplasia.
Figure 129-17 Pseudoepiphyses (arrows) in the proximal second and fifth metacarpals of a 3-year-old boy.
Sesamoid Bones: Sesamoid bones are present in the foot and hand. Sesamoids of the great toe reside within the medial and lateral slips of the hallux brevis tendon overlying the head of the first metatarsal. The medial great toe sesamoid is bipartite in 4% to 33% of patients (e-Fig. 129-19). Sesamoids of the feet may develop a stress reaction or a complete fracture and may be difficult to distinguish from a bipartite sesamoid on radiographs; magnetic resonance imaging (MRI) may be useful in distinguishing a normal bipartite sesamoid and underlying stress injury. For the first metatarsal phalangeal, stress injury tends to affect the medial sesamoid more frequently than the lateral sesamoid.16 In addition to the sesamoids, numerous other supernumerary ossicles of the foot and ankle exist (Fig. 129-20).
Figure 129-20 Normal supernumerary ossicles of the feet in ventrodorsal (A) and lateral (B
