Musculoskeletal development: a review.

JM Walker, Phd, PT, is Professor and Director, School of Physiotherapy, Dalhousie University, 5869 University Ave, Halifax, Nova Scotia, Canada B3H 3j5.

Increasing survival rates of prematurely born infants and the frequency of pediatric orthopedic problems necessitate a sound understanding of prenatal and postnatal development of the musculoskeletal system. in this article, I will review early development of the limbs, the skeletal and muscular systems, and the joints, as well as early changes in joint mobility.

The stages, timing, and major events of prenatal development are well described in the literature and are outlined in Table 1. To precisely establish the sequence and timing of developmental events, the embryonic period is divided into 23 stages, which are based on external and internal morphological criteria elicited from studies on staged embryos at the Carnegie Institute. These stages will be referred to when reviewing the development of the musculoskeletal system. Development, encompassing differentiation, maturation, and growth, occurs at disparate rates throughout the body. Development in the premature infant is significantly different than that in a full-term infant.

During the embryonic period (2-8 weeks), major development of all systems occurs. This period is distinguished by a series of spatially controlled cellular events primarily dependent on the sequential switching on and off of specific gene activities that define the enzyme activity of a cell and hence its ultimate biological nature. From the initial stage, characterized by a homogeneous structure and variable potential for all cells, development proceeds toward a stage in which differentiation prescribes a precise biological role for each cell. Through cytodiferentiation, a process of change in the morphology or chemistry of embryonal cells that renders them more specialized than their antecedents, the predestination becomes visible in the heterogeneous structure of cells. Other important cellular activities of the embryonic period are pattern formation; cell-to-cell and cell- and tissue-contact interactions., morphogenetic movements, defined as the coordinated and directed migrations of individual cells or masses of cells; and mass cell necrosis.(3) are important in the modeling process.

The fetal period, commencing at the beginning of the eighth week, is characterized by continued, but less spectacular, differentiation and growth. Increasing complexity of structure and function is noted, with a marked increase in fetal weight in the third trimester secondary to development of adipose tissue. These processes continue to varying degrees in the different systems in the postnatal period. Normal dynamics of cell growth give an orderly increase in size in three phases: initial hyerplasia (increase in cell number), hyperplasia with hypertrophy, and hypertrophy alone.

Critical periods in development of limbs and the central nervous system are shown in Figure 1.4 Major morphological abnormalities occur only during the embryonic period, although minor morphological abnormalities of the limbs can occur in the early fetal period. Distinction must be made between malformation, which indicates a primary problem in morphogenesis of a tissue; disruption, or a breakdown of a previously normal tissue-, and deformation, or anomalies that represent normal response of a tissue to unusual mechanical force.(5,6) Disruption and deformation can arise at any time during the fetal period, with deformation more frequent in the third trimester when the fetus is subjected to greater constraint.

Limb Development

Most of the tissues differentiating in the newly formed limb bud arise from mesenchymal cells.(7,8) Neural elements invade the limb at a later stage. Mesenchymal cells destined to become myoblasts appear to be a distinct population, are derived from somites, and have a different lineage than other limb-bud cells. The ectodermal covering of the limb bud plays an important role and will form the skin. The lower limb bud lags behind that of the upper limb, appearing about the 28th day, 2 days later than that of the upper limb. The sequence of limb-bud development between 26 and 42 days is shown in Figure 2. (Most of our knowledge of limb-bud development evolves from studies in avian models.)

Under the influence of the underlying mesenchymal cells, the apical ectodermal ridge (AER) forms as a thickened specialization of ectoderm. By 33 days, mesenchymal cells commence differentiation into cartilage. Structures are laid down in a proximodistal sequence; thus, the humerus and femur appear before the digits. How the AER exerts its influence on spatial organization of the developing limb is not clearly established. Experiments in which portions of the AER in avians were removed, however, demonstrate the important role of the AER. Experiments with a chick embryo model have shown that removing the AER at an early stage results in loss of distal parts; removal of a small portion results in loss of one to two digits.(7) Influence of the AER is no longer thought to be a simple cell-to-cell interaction.

The subadjacent mesenchymal cells may produce an AER-maintenance factor, with the AER playing a more "permissive" than "instructive" role during pattern formulation on the proximodistal axis. The AER may have mitogenic properties that mediate its ability to stimulate limb-bud outgrowth. More is known of pattern formulation in the proximodistal and anteroposterior axes than in the ventrodorsal axis in which the dorsal ectoderm appears in avians to have more dominant effect.(9) Regions in which cell death will occur, such as between the digits, have thinner ectoderm. Cell death is a programmed and ontogenic mechanism, which, if poorly timed, reduced, or excessive, can lead to abnormal limb development.

Figure 3A demonstrates the basically parallel arrangement of the longitudinal axes of the limb buds. The preaxial borders, bearing the thumb and the great toe, face cranially, whereas the postaxial borders face caudally. By the end of the embryonic period, the upper limbs have altered such that the preaxial border has become medial rather than cranial; this position corresponds to pronation (Fig. 3B).(2) Postnatally, the limb can be rotated so that the palm of the hand faces forward because of the greater mobility of the upper limb.

At stage 23, the preaxial border of the lower limb, as indicated by the great toe, is still directed cranially with the soles directed medially, the so-called "praying feet." Translational movements, during the fetal and early postnatal periods, move the preaxial border medially so that the sole of the foot can be applied to the ground. These translational movements should not be referred to as medial rotation," h the implication of mature movement produced by muscle action. These alterations are completed after differentiation of the muscle mass, innervation of the muscles, and definition of the joint cavities have occurred. They are secondary to complex changes in all of the limb components, especially the skeletal and articular components.(2) According to Tickle and Wolpert, "The mechanisms involved are not understood but the pattern of growth may be a factor."(7)(p556) Blechschmidt and Gasser(10) related growth changes in the limb anlagen in part to the restraining function of vessels and nerves, which exhibit a slower growth rate than other limb tissues. Limb pattern formation may involve interplay between mesenchymal and vascular cells. Caplan" theorized that "the presence of particular vascular elements may, indeed, be 'positional information."'

From the earliest stage, blood vessels invade the limb as it grows, except where cartilage differentiates. Neural crest cells invade the limb bud at about the same time as the nerves (about the 33rd day, when the hand bud is visible) and give rise to sensory nerves and skin-pigment cells. All other limb structures develop in situ.

Skeletal Development

During the first month of fetal life, the matrix of the future skeleton is laid down. in the second month, bone formation commences. Except for the clavicle, mandible, and bones of the skull vault in which bone mineral is deposited directly in mesenchyme (membranous bone, endosteal or periosteal ossification), collagen is laid down to form the template on which bone mineral is deposited (endochondral ossification). Formation of matrix must precede deposition of bone mineral until growth ceases. Because the availability of oxygen in the cellular microenvironment is a factor in ossification, conditions that affect the oxygen supply may influence differentiation of precursor cells. Osteogenesis requires a good oxygen supply, whereas chondrogenesis occurs in the presence of a poor oxygen supply.(12)

Embryonic bone has an irregular arrangement of collagen fibers, is highly mineralized, and has a high number of osteocytes. Gradually, lamellar bone, which is less mineralized and has fewer and smaller osteocvtes, covers the connective tissue vascular spaces seen in embryonic bone. Fetal bone, in comparison with mature bone, has a very compact cortex; little remodeling occurs during prenatal life." The accumulation of calcium in bone parallels the increase in fetal weight. Thus, premature birth deprives the skeleton of an important component of calcium and phosphorus. Hormones (ie, somatotrophic hormone, sulphation factor, thyroxine, sex hormones, cortisol) and vitamins appear to play a larger role in development postnatally.(12) Anomalies of calcium metabolism, such as hypocalcemia or hypercalcemia in either the mother (osteomalacia, hypothyroidism or hyperthyroidism) or in the fetus, influence mineralization of the skeleton. For example, maternal osteomalacia causes rickets in the infant.(12) Human breast milk provides more calcium and inorganic phosphorus, which is vital to mineralization, than does cow's milk.

The infant exhibits a much higher rate of remodeling than does the adult, estimated at 50% per annum and 5% per annum, respectively. During the first 2 years, marked remodeling of the cortex of the long bones occurs, resorption increases, and secondary osteons are formed. it is thought that all primary bone has been remodeled by the age of 2 years.(11) Mechanical forces appear to have a negligible role during prenatal development of the skeleton, except for architectural details such as tendon attachments, but are important postnatally. Decreases in pressure parallel to the growth axis in long bones (as in weightlessness) favor growth in length, whereas increases inhibit and may even stop epiphyseal growth. (12,13) Carter et al,(13) using finite-element computer analysis, hypothesized that mechanical stress influences all features of skeletal morphogenesis, from development of primary ossification sites to the existence and thickness of articular cartilage.

The timing of ossification is clearly detailed in anatomical texts.(14,16) Whereas in long bones ossification begins in the periphery (perichondrial) and proceeds distally (enchondral), the vertebral bodies ossify from the center outward (endochondral). Each vertebra is the result of fusion of the caudal half of one somite and the cranial half of the adjacent somite. Both the notochord and the spinal cord appear to play a role in chondrogenesis of the vertebrae.(8,17,18) Ossification from three primary centers commences in the lower thoracic bodies about the eighth week, then proceeds in both cranial and caudal directions. Ossification of the arches commences in the upper cervical vertebra and proceeds caudally.(12) Union of ossified portions occurs postnatally. arches unite in the midline, starting in year 1 with the lumbar region. Fusion of the arches with the vertebral bodies starts in the third year in the cervical region and in the sixth year in the lumbar region.(19)

Skull sutures in the young child have relatively smooth edges, but progressively acquire the mature features of jagged, interlocking, and overlapping edges. Fusion follows a staggered schedule. Between years 1 and 2, the maxillary-premaxillary sutures normally fuse; the temporal sutures fuse between age 2 and 4 years, Closure of other sutures does not occur until adulthood 25-30 years of age); however, sutures bounding the temporal bone close about 5 years later and may only "be partially united even in the aged skull."(20)

Muscle Development

Primary myotubes (multinucleated muscle cells) appear at about the 5th week of human gestation. Early muscle fibers begin to appear in about the 11th week. Few myotubes remain after the 20th week when most muscle fibers are packed with myofibrils, have peripheral nuclei, and are similar to those of adult muscle.(21) "Fibroblastlike" cells associated with fetal muscle fibers are thought to remain as satellite cells, which are presumed to play a role in postnatal growth and regeneration following injury.(22) Whereas initial myogenesis can occur normally in the absence of a nerve supply, innervation (about 20-24 weeks) is shown to enhance muscle development and differentiation.

That functional demands influence muscle development is clearly demonstrated by the observation that diaphragmatic fibers are twice the size of intercostal and limb muscle fibers at birth, a reflection of the primacy of respiration in the neonate.(22) Clear distinction between the two main histochemical fiber types cannot be made until the 18th to 20th prenatal week. immature fibers all show physiological characteristics of slow-twitch fibers.(22) Type I (slow- itch, oxidative) fibers predominate in earlier development. Type 11 (fast-twitch, glycolvtic) fibers increase after the 26th week, and fiber types are about equal at term.2.(3) Given the extent of malnutrition in parts of the world, it is worthy of note that protein-calorie malnutrition in the rat is shown to lead to failure of normal postnatal growth of muscle fibers and is only partially reversible by normal diet.(24)

In the full-term infant, skeletal muscle contains less than 20% of the adult number of cells and accounts for about 25% of the weight of the average baby. Up to the 25th prenatal week, skeletal muscle shows a hyperplastic phase, with cells increasing in number but with little increase in size. After that time, cell size increases more rapidly and cell number more Slowly.(22) Although some investigators hypothesize that fiber number continues to increase into the 5th decade, others believe the full fiber number is attained soon after birth.(22) Once differentiation is complete, subsequent growth occurs through hypertrophy of existing fibers. Histological and biochemical analyses confirm that there is a 14-fold increase in sarcolemma nuclei throughout muscle growth, slightly smaller in girls than boys.(25) Widdowson stated that "in no respect has skeletal muscle reached its mature chemical composition at the time of a full-term birth."(26(p338))

Muscle Neural Elements

Primitive nerve branches ramify among muscle fibers by the loth week. Myoneural junctions form in the 11th week, and early motor end-plate formation has been observed by electron microscopy at 10 weeks. In the early stages, several motor axons innervate a single muscle fiber; eventually, however, only one axon will remain. In the rat, this changeover is related to "increase in speed of contractions and myosin light chain patterns of muscle fibres which occurs in early postnatal life."27(p25) By the 14th week, the muscle spindle has all the essential components; myelination of spindle fibers occurs after the second trimester. Golgi tendon organs (GTOs) commence innervation in the 12th week. Subsequently, the GTO structure becomes encapsulated, and myelination of its fibers occurs from 16 weeks.(22)

Tissue-tissue Attachments

Figure 4 demonstrates the differences between the myotendinous junction of human paravertebral muscle at term, in the adolescent, and in the adult. The neonatal myotendinous junction is less closely packed and interdigitated; the myofibrils at the end of the muscle cells vary in thickness and are less developed.(28)

The question of how soft tissues, such as muscles, maintain their appropriate attachments during long bone growth has long interested investigators. It is theorized that compensatory movement of soft structures must accompany the growth of long bones to ensure that muscles attached to the metaphysis are not "left behind" as length of the bones increases. Hurov(29) studied the attachment of several soft tissue structures about the medial side of the rabbit knee. His findings contradicted earlier theory that the periosteum/perichondrium directly slides along the tibial diaphysis. He demonstrated that collagen-fiber bundles link the periosteum to the subadjacent bone. Ligxnentous and muscular structures attach only to the periosteum at birth. At 60 days, however, only the popliteus was attached solely to the periosteum. With aging, the attachment of ligaments to the fibrous periosteum penetrates the fibrocartilage, which is gradually replaced by chondroid and lamellar bone and subsequently remodeled into compact lamellar bone.(29) These changes produce the strong ligament-bone attachment of maturity. Further research is needed to elucidate the roles of long bone growth and periosteal expansion in maintaining the relative positions of soft tissues during growth.

Joint Development

Embryonic Period

Most of the tissues differentiating in the newly forming limb rise from mesenchymal cells. These cells give rise to the various articular tissues, with the exception of neural elements and blood vessels. As the skeletal template begins to chondrify, joint formation commences. A region of flattened, undifferentiated cells forms between the two areas that are differentiating into cartilage. Experiments suggest that joint cells are prespecified and that the joint area is a specialized region.(30) The initial joint formation does not appear to be dependent on mechanical pressure that is generated by growth of the skeletal elements. At least in avians, however, movement is important. Paralysis may cause failure of joint cavitation (breakdown of interzonal mesenchyme to form precursor joint cavity).(31-33) Early limb movements by human embryos (about 54 days) may contribute to joint cavitation.

Figure 5 displays a diagrammatic representation of the events in synovial joint formation. Cellular activities in the homogeneous interzone between the skeletal elements transform the initially flattened area into a three-layered interzone that consists of two chondrogenous layers, which are continuous at the periphery of the future joint with the perichondrium, and a middle loose layer, which later forms the joint cavity (Fig. 5C). Synovial mesenchyme will give rise to the synovial membrane, the fibrous capsule, and such intra-articular structures as menisci, tendons, and ligaments. Vascularization of these structures then follows.

The next event is the formation of the joint cavity, which begins at about the same time as other joint tissues differentiate. The precise nature of cavitation is not well established. it is thought, however, to begin centrally. Cavities appear in the middle layer; these cavities coalesce and form a single cavity. Many bursae and synovial sheaths are formed and start cavitation by the end of the embryonic period.(8)

The differentiation of the limb joints, from the early template to structures similar to those in the adult, occurs over a relatively short period of time and in the human occurs between 4 1/2 to 7 weeks. The limbs are most susceptible to the action of teratogens during this embryonic period. Individual variability in the general sequence of the joint morphogenetic events described does occur. Some joints show considerable delay between differentiation and cavitation. The joints of the hand and foot may not develop a three-layered interzone until early in the fetal period.(9) The sacroiliac joint starts cavitation in the 10th week, but does not complete the process until the 7th month.(34,35) For most joints, however, cavitation is complete in the early fetal period. Other differences in developmental sequence are that the acromioclavicular joint does not show the usual homogeneous then three-layered interzone, the temporomandibular joint develops where a continuous blastema never existed, and the sternochondral joints show cartilaginous continuity in the early stages with subsequent cavitation uncertain.(8)

The sequence of events in joint formation thus may vary slightly within specific human joints. Figure 6 gives the timing for the main events of knee joint development. A number of investigators3-3 have provided detailed analyses of the development of individual joints. Ligaments tend to appear between stages 19 and 21, ossification commences in stages 21 to 23, and cavitation usually commences in the larger joints by stage 23 (end of the seventh week). The role of the developing vessels (and their location) and of the limb flexures (denoted by skin creases) in joint development is not known.

Fetal Period

Developmental changes in the fetal period consist of an increase in the size and maturation of formed structures; an increase in the amount of collagen, resulting in clearer definition of fibrous tissues such as ligaments; and extension of the joint cavity.(8) Even in early development, ligaments are thought to act as restraining structures.10 There is increased vascularization of epiphyseal cartilages from the third month, with the appearance, and then increase in number, of synovial villi. More bursae appear, and, in joints such as the knee, they extend the joint cavity by their communications with the cavity. Fat cells appear around the fourth to fifth months, marking the sites of future fat pads. Some elastic fibers appear in the fibrous capsule late in the fetal period when tendons and ligaments become increasingly avascular.(8)

Nerve fibers begin to enter the joint tissues in the fetal period, but specialized structures such as Ruffini and Pacini endings only occur late in the fetal period. Dee(44) observed that Hilton's law (ie, nerves, in which branches supply muscles moving a joint, give an articular contribution) is substantially true for all joints. Each joint has a dual nerve supply: Specific articular nerves, which are independent branches of adjacent peripheral nerves, reach the capsule, and nonspecific secondary articular branches arise from related muscle nerves.(44)

Role of Movement

The nature of cavitation and its dependence on movement for its initiation has been shown in avians but not in humans.(7,8) Although the role of movement for initiation and maintenance of cavitation is not clearly demonstrated for human joints, movement is very important in maintaining and in molding the articular form of human joints once the form is established.(7,8,31) This process continues in the postnatal period.

Movement, as a modeling force, may be more critical to joints such as the hip joint, characterized as a shallow concave socket for a spherical partner. When the hip joint is first formed, the acetabulum is a deep cavity that almost completely surrounds the femoral head.(38,45) As the fetus ages, the depth of the socket increases at a significantly slower rate than does the transverse diameter of the femoral head and the socket. Although acetabular and femoral head diameters increase more than fourfold from 12 weeks to term, depth increases less than threefold.(46,47 The net effect of these differential rates of growth is a change in the shape of the socket.(47) The hip joint at birth is the most unstable joint in the body.

In the immediate postnatal period, depth again increases in relation to diameter, creating a mature and secure ball-and-socket joint.(48) It is theorized that the shallowness of the socket at birth facilitates the passage of the fetus through the vaginal canal. initially, the femoral head forms as a spherical structure. Because of restrictions imposed on fetal movement, such as tightness of the uterine wall (Appendix),(5) the femoral head becomes increasingly less round.(49) postnatally, the cartilaginous femoral head again assumes a more spherical shape, presumably in response to the increased range of motion (ROM). The growth potential of the hip joint decreases steadily after birth. Significant acetabular growth may not occur after 18 months, and probably not after 3 years of age.(50,51) Thus, early diagnosis and management of congenital hip dysplasia is important.

The reported relationship between sleeping position and hip dysplasia suggests that the postnatal sleeping posture can influence acetabular development. When a preferred sidelying posture was demonstrated, hip dysplasia occurred in the upper hip of 19 of 41 children.(52) Presumably, the adducted and medially rotated position of the upper hip reduced the stimulus for growth in the acetabular cup. These changes demonstrate that movement plays an important role in modeling the joint surfaces in the early postnatal period and during infancy. The shallowness of the hip joint at term also means, however, that the neonatal hip joint is vulnerable and may subluxate or dislocate through forceful extension,(53) or simply because of the greater available mobility ex utero. Care should be exerted when moving the hip of premature babies and neonates toward extension, and extension should never be forced. It also is suggested that infants should not be consistently positioned on one side, but alternated between sides.

Skeletal Angles, Axes, and Curves

Stability of the mature hip joint is enhanced by the inclination of the acetabular socket and by the neck shaft and torsion angles of the proximal femur. The neck-shaft (anteversion or inclination) angle is apparently formed very early in the fetal period and changes little with age.(47) Mean birth values have been shown to differ little from the established adult values of 125 degrees.(47,54,55) Torsion (deinclination), the angle that the proximal femur makes with the distal femoral condyles, however, shows marked change during the fetal and postnatal periods.(47) Initially, this angle is negative or retroverted. Although torsion values at birth are about 35 degrees, they decrease to the adult value of about 11 degrees. This decrease is more marked in infancy, but continues gradually to puberty.(50,56-58)

The femoral-tibial axis is minimally greater in the neonate than in the adult (180[deg] versus 171[deg]) and changes spontaneously from the initial varus (bowing) to a valgus position (knockknee) at about age 2 to 3 years. After age 6 years, the valgus position almost completely straightens out in most children.(59) Variability in values reported is related to selection of anatomic axis. There is a valgus angle of between 4.2 and 5.8 degrees in the mature limb.(60) Persistence of physiologic infantile tibial varus or exaggeration of the subsequent valgus change requires observation and possibly clinical intervention. Substantially greater change is reported for tibial torsion, which is zero at birth and changes by puberty to a lateral tibial torsion value of 23 degrees.(61)

Differing cultural practices of baby carrying can influence changes in angles and axes and contribute to conditions such as bowleg and knock-knee. African mothers tend to carry their infants over one hip. Inuit and Chinese mothers carry their infants in a deep coat hood or sling on their backs. In contrast, mothers in several American Indian tribes (eg, CreeOjibwa, Navajo) carry their infants on a straight board with a leather harness, which positions the infants' limbs close to the standing position. This position has been considered detrimental to hip joint development because of association between cradling and congenital hip dysplasia (CHD).(53,62) Congenital hip dysplasia is almost unknown among the Inuit and Chinese and has a low incidence in Africans compared with Caucasians. Populations that cradle their infants have the highest reported incidences of CHD; however, other factors such as inbreeding may play a greater role in causation.

Fetal position also has been demonstrated to he an important contributor to the initial limb alignment and joint mobility of the neonate.(5,6.63) Fetal positions, particularly if abnormal (not vertex), or a size disparity between the fetus and the mother subject the growing fetus to unusual forces over a number of weeks and can result in unusual facies and limb postures and restrictions of neonatal joint mobility. Such presentations as face-brow (1 in 500 births) and transverse lie (1 in 300-600 births) maintain the cervical spine in hyperextension and are associated with abnormal facies.(5) The effect on the developing cervical spine and its musculature is unknown. Breech posture and presentation has an established correlation with congenital postural deformities (nonstructural, such as torticollis and hip dysplasia) and severe limitation of hip extension and knee flexion; genu recurvatum is often present.(5,6) Posture of the feet is especially affected by intrauterine space limitations. It has been shown that distraught infants can be more easily settled in their fetal position, or "position of comfort."(5)(p41) Therapists might recreate this position to detect potential developmental problems, such as weak deep cervical flexors in a transverse-lving infant.

Dunn(6) has described a "wind-swept" posture in which both limbs are twisted in the same direction, as well as a "locked" posture in which the femoral rotational element is opposite to that of the tibia. Such fetal postures can produce rotational malalignments such as medial rotation of the tibia associated with lateral femoral torsion (retroversion).(58) Especially in the premature infant, where medical attention often focuses on viability, the therapist should be attentive to the presence of deformities attributable to the fetal position.

Although many writers relate the development of cervical and lumbar curves to postnatal events such as head lifting, crawling, and upright stance, a forward cervical curvature has been observed in young fetuses. Bagnall et al,(64) in a study of fetuses between the ages of 8 and 23 weeks, found that 83% showed a secondary cervical curvature. It appears, therefore, that the forward convexity of the cervical curve may only be accentuated after birth. The early appearance of the secondary cervical curvature is thought to be related to the early ossification of the occipital bone, an event associated with neck extensor muscle activity in the gasp reflex that is present from 6 1/2 weeks of prenatal age.(65) Another factor in development of the secondary lumbar curve may be the relative tightness of the iliopsoas muscle.

Joint Mobility

At birth, the full-term neonate exhibits physiological limitation of hip and knee extension and ankle plantar flexion.(66-68) In contrast, the premature infant may show no limitation and hypermobility of most joints. The term "physiological limitation of motion" should not be confused with flexion contractures in mature joints. It is secondary to restriction of motion generally (ie, in utero), especially in the third trimester. Birth brings release from constraint and freedom of movement. Motion into extension evolves without need for intervention.

Tables 2 through 4 give reported values for joint ROM in neonates and infants.(67-72) differences in ROM values relate to variability in testing techniques, reporting of active versus passive ROM, measurement precision, and observer variability in end-range detection. Changes in joint mobility with age are paralleled by age-related changes in locomotor abilities. All investigators reported hip extension limitation at birth, which may still be present, though reduced, at 2 years of age, Except for Hoffer,(67) who reported ranges rather than mean values, the investigators demonstrated a clear trend for hip lateral rotation to exceed medial rotation in neonates and infants; both motions have similar values by 2 years of age.

Both the restriction of motion and the hypermobility seen in the neonate are criteria used in gestational assessment, such as the popliteal angle and the scarf and square-window signs.(73,74) Persistence of these characteristic motions may indicate pathology, such as arthrogryposis multiplex congenita and cutis laxa (cutaneous laxitv).(5,74)

Appendix. constraint Factors That May, Result in an Unitsual Fetal Position

Primigravida 

Tight uterus

Malformed uterus

Oligohydramnios

Fetal/maternal size disparity

Multiple fetuses

Malformed fetus

Unusual placental site

Derivation of estrogen intrinsically and extrinsically from the mother may account for the reported greater mobility of female infants compared with male infants. This at-birth difference is generally short-lived. No significant differences between sides of the body have been demonstrated, except where an abnormal fetal posture existed. As reported differences in ROM lie chiefly between neonates and children, or individuals under and over 18 years of age 75 average adult values are probably achieved by late childhood and well before completion of growth.

Conclusion

Major development of the musculoskeletal system occurs in the embryonic period. In the fetal period, development continues with increase in size and complexity of structure and function. The musculoskeletal system is vulnerable to failures of specific morphogenetic processes, resulting in limb fusions and ameli in the embryonic period. Congenital anomalies, however, may arise during the fetal period and are especially characterized by growth retardation. Late fetopathies, or congenital postural deformities, are probably produced by mechanical factors in utero, such as fetal position, amount of amniotic fluid, and tightness of the uterine wall. These deformities are essentially nonstructural and often resolve spontaneously. Awareness of prenatal and postnatal events and their timing will assist the therapist in management of pediatric patients.

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