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Bardeen CR. XI. Development of the Skeleton and of the Connective Tissues in Keibel F. and Mall FP. Manual of Human Embryology I. (1910) J. B. Lippincott Company, Philadelphia.

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XI. Development of the Skeleton and of the Connective Tissues

By Charles R. Bardeen, Madison, Wis.

Skeleton and Connective Tissues: Connective Tissue Histogenesis | Skeletal Morphogenesis | Chorda Dorsalis | Vertebral Column and Thorax | Limb Skeleton | Skull Hyoid Bone Larynx

Part II. Morphogenesis of the Skeletal System

Charles Bardeen
Charles Russell Bardeen (1871 – 1935)

A. General Features

The definitive skeletal system is composed of bones and cartilages united to one another at joints by means of ligaments. In the lowest vertebrates a cellular rod, the chorda dorsalis or notochord, situated in the mid-axial line ventral to the central nervous system, constitutes the chief part of the axial skeleton. In the higher vertebrates a chorda dorsalis is also formed during early embryonic development, though in mammals and man it lends little or no skeletal support to the embryo and mere derivatives of it are to be found in the adult. The definitive skeleton of the higher vertebrates, including man, is differentiated from the mesenchyme of the head, trunk, and limbs. The process of differentiation is somewhat complex. As a rule, the first visible step in the process is marked by condensation in the sclerogenous mesenchyme or scleroblastema. Thus, in the development of the skeleton of the inferior extremity, condensation begins in the vicinity of the future hip-joint and from here extends distally and proximally, so that there is produced a continuous mass of condensed tissue in which pelvic, femoral, tibio-fibular, and tarsal regions and five metatarso-phalangeal rays may be distinguished. The hard parts of the skeleton are developed from centres which appear in the scleroblastema. The joints are developed in the scleroblastema which intervenes between the hard parts.

The Bones

It has been mentioned in the section on histogenesis that most of the bones of the body are first formed of cartilage and then, during subsequent development, bone is gi*adually substituted for cartilage, substitution or cartilaginous bones (Figs. 277 and 278). Other bones are formed directly in the membranous scleroblastema, membrane or investment bones. The bones of the extremities, with the partial exception of the clavicle, the bones of the spinal column and thorax, and the greater part of those of the base of the cranium, have a chondrogenous origin. The greater part of the bones of the cranial vault and of the face arise directly in the scleroblastema.

It is to be noted, however, that during the formation of many of the typical substitution bones ossification may extend into membranes attached to the cartilage, so that certain processes on these bones are membranous in origin, and that, on the other hand, certain parts of bones of membranous origin may secondarily give rise to cartilage (temporomandibular joint). Several of the definitive bones of the skull have an origin partly cartilaginous, partly membranous.

Substitution Bones

As a rule, a centre of chondrification appears in the midst of condensed scleroblastema. (See femur, tibia, and fibula, Fig. 275.) It may, however, appear in tissue but slightly condensed, as in case of the vertebral bodies. Fig. 273. The cartilaginous centres expand rapidly, both by apposition from the surrounding blastema and by interstitial growth. Neighboring centres are thus soon brought into close approximation. Some of the centres fuse with one another in the region of approximation. Between other centres joints are developed. The fate of the cartilaginous centres, therefore, differs considerably in different regions.

The conditions in the skeleton of the limbs are the simplest. Here for each of the bones, including the pubis, ischium, and ilium, there is a single centre of chondrification (see Fig. 226 and Figs. 275 and 276). The clavicle forms an exception to the other bones in that the tissue at the centre of chondrification is not converted into typical embryonic hyaline cartilage (see pp. 380 and 388). The centres of chondrification for the pubis, ischium, and ilium soon fuse with one another so as to produce a continuous cartilaginous hip-bone, which gradually assumes definitive form (Figs. 276, 277, and 278). With the exception of a few cartilages in the wrist, the fate of which is treated elsewhere (p. 383), each of the other embryonic limb cartilages undergoes an independent development. In the region of the knee-joint, however, and possibly in some other articular regions of the limbs, independent skeletal elements become at an early period temporarily fused together by a kind of precartilage (Fig. 283). Temporary joints of this kind resemble the permanent joints of the shark's fin.

A centre of ossification appears ia the main body of each of the cartilages of the skeleton of the limbs; in most of them early in fetal development, but not until after birth in those of the ankle and wrist, with the exception of the calcaneus, talus and cuboid and in the patella and other sessamoid bones. These chief centres of ossification establish bone in place of cartilage as growth proceeds. In case of all the limb bones except those of the ankle and wrist secondary epiphyseal centres of ossification appear early in childhood in those portions of the bone still cartilaginous, and as maturity is approached become fused with the main part of the bone. Growth in length of bone, as stated in the section on histogenesis (p. 311), is dependent upon the growth of the cartilaginous matrix and ceases when the epiphyses become fused with the main body of the bone. In the adult limb skeleton the only cartilage remaining is that upon the joint surfaces of the bones.

In the vertebral columyi there are two bilaterally placed centres of chondrification for the body of each vertebra and one for each half arch (Figs. 239 and 249). The arch cartilages join the body considerably before they unite dorsally so as to complete the arch about the spinal cord. The ribs develop from separate centres of chondrification and do not fuse with the bodies. In the cervical, lumbar, and sacral regions there are more or less distinct centres of chondrification of costal elements which quickly fuse with the cartilage of the body. In the sacral region the various cartilages fuse to form a cartilaginous sacrum. The cartilaginous vertebral bodies are at first separated by thick blastemal discs, but as development proceeds the discs near the centre become thin and partially converted into a precartilaginous tissue, so that for a brief period there is a continuous vertebral axis composed of tissue of a cartilaginous nature but in which segmentation is clearly marked.

The cartilage of the sternum arises mainly from the cartilage of the ribs, from which it is secondarily separated by the formation of costosternal joints. There are primary centres of ossification for the bodies of the vertebrae, each half arch, the ribs, and some of the costal elements of the sacrum. In addition, there are many epiphyseal centres. In the cranial blastema numerous centres of chondrification appear (Figs. 310 and 311). These, however, fuse to form a continuous chondrocranium, in which no blastemal sutures remain to separate one cartilaginous element from another (Figs. 312 and 313). The incus and stapes remain distinct cartilages. The malleus is long continuous with Meckel's cartilage, the cartilaginous skeleton of the mandibular arch. The cartilage of the hyoid arch becomes attached to the chondrocranium. While the chondrocranium is being formed, centres of ossification begin to appear in various parts of the cranial scleroblastema. From these centres of ossification, partly by expansion and partly by fusion of neighboring centres, there are produced the membranous bones of the skull (Fig. 321). Meanwhile, centres of ossification appear in the chondrocranium and by expansion and fusion give rise to the substitution bones of the skull. In the definitive skull some bones, like the parietal, frontal, and maxillary, are purely membranous in origin. Some, like the ethmoid, hyoid, incus, and stapes, are fairly typical substitution bones, while many of the bones, like the occipital, sphenoid, and temporal bones, arise partly from centres which appear in membranous tissue, partly from centres which appear in the chondrocranium. In the membranous tissue in which the centres for the investment bones appear the definitive form of the skeletal part is much less clearly marked than in the chondrocranium (compare Figs. 310, 311, 312, 313, 321).


Not all the cartilage of the embryonic skeleton becomes replaced by bones. Some of the embryonic cartilages become reduced to fibrous tissue, as in the case of the stylohyoid ligament; some give origin to the cartilages of the definitive skeleton, such as the costal cartilages and parts of the nasal capsule; some merely disappear.


When first diiferentiated the fixed parts of the skeleton are united to one another by dense blastemal tissue in which little definite form is to be observed. In ease of synarthroses this intervening blastemal tissue becomes directly or indirectly transformed into fibrous tissue (syndesmosis), into cartilage (synchondrosis), or into bone (sjTiostosis). While, as a rule, the fibrous tissue of a syndesmosis comes fairly directly from the primitive blastema of the embryonic joint, it may arise as the result of retrograde metamorphosis of cartilage (lig. stylohyoideum). A synchondrosis is usually preceded by an embryonic blastemal syndesmosis. A synostosis is usually preceded by a sjnidesmosis or a synchondrosis.® In a diarthrosis the joint cavity, synovial membrane, and the various ligaments characteristic of the joint are diiferentiated from the dense blastemal tissue which unites at first the two embryonic cartilages entering into the joint. Disci articulares and menisci articulares are also diiferentiated from this blastema. In case of the few diarthroses formed between membrane bones, as for instance between the mandible and the temporal bone, the blastemal tissue has the power of giving rise to cartilage which covers the joint surfaces of the bones.

The various steps in the diiferentiation of a simple diarthrosis are well illustrated in the digital articulations (Figs. 226-228). In Fig. 226 are shown the cartilaginous anlages (a) of the three phalanges and the distal part of the metacarpal of a finger of an embryo 2.7 cm. long. These cartilaginous anlages are embedded in a dense blastema which shows lighter areas in the vicinity of the future joints (c). The term intermediate zone has been applied to the dense tissue lying between the two cartilages entering into a joint (6). As the cartilages expand they come into close approximation, as shown in the finger of a fetus 7 cm. long (Fig. 227). At this stage the cartilage is undergoing changes preliminary to ossification. The perichondrium about the joint surfaces of the cartilage entering into the joint is very dense. The joint cavity first appears at the periphery of the joint (Fig. 227). Gradually it extends in between the two cartilages entering into the joint and a variable distance over the head toward the shaft (Fig. 228, A, B, C). The form of the joint surfaces of the bones entering into the joint is highly diiferentiated before the joint cavity appears (Fig. 227).

In the more complex joints in which menisci or intra-articular ligaments are diiferentiated, as in the knee-joint and hipjoint

  • The nucleus pulposus of the intervertebral fibrocartilage (disc) arises from the tissue of the chorda dorsalis (see p. 341).

Fig. 826-228.

(Figs. 281, 282, 285), the cartilages of the bones entering into the joint are less closely approximated at the time of the formation of the joint cavity than in simple joints, like those of the fingers. The external ligaments and the various intra-articular structures are differentiated directly from the intermediate zone of blastema, while the blastemal tissue next the joint surfaces of the cartilages entering into the joint becomes condensed into a dense perichondrium. The rest of the tissue becomes less dense in character and is converted into mucoid tissue with a few cells scattered through the matrix (Fig. 282). As in all diarthroses the formation of the joint cavity begins at the side and extends toward the centre of the joint. The definitive cavity may be formed by the fusion of several cavities which appear at various places in the periphery of the joint (knee-joint, p. 372). The mucoid tissue disappears as the joint cavity enlarges. The capsular ligament which is formed from the periphery of the intermediate blastemal zone is continuous on each side of the joint at first with the perichondrium and later with the periosteum. The synovial membrane is formed on the inner surface of the capsular ligament. Synovial villi arise in the latter part of fetal life

At the time of the appearance of the joint cavity the bones entering into the joint are composed of cartilage in the region of the articulation, although ossification may be well under way at some distance from the articulation (Figs. 227 and 228). After the appearance of the joint cavity the articulating parts undergo an elaboration in form (Fig. 228), which may be quite extensive (Figs. 286, 288). This elaboration of form is due not only to interstitial growth of cartilage, but also to the appositional growth of bone. As the result of the ossification, all the cartilage near the joint becomes entirely replaced by bone except on the joint surface, where, as a rule, a layer of hyaline cartilage remains throughout life. The thin, dense layer of blastemal perichondrium which for a short time covers the joint cartilage, as a rule disappears early, although it may give rise to a permanent film of tissue or the joint cartilage may become in part composed of fibrocartilage ( sternoclavicular, temperomandibular, costovertebral, sternoccstal articulations).

The relative positions of the articulating bones vary greatly in different regions at the time of the formation of the joints. The kneeand elbowjoints, for instance, are flexed at an angle of about 90"^ while the wrist-joint is nearly straight.

Sesamoid Bones

Tendons are closely fused to the joint capsule in many articulations of the extremities. In certain regions where this occours sesamoid bones are developed. The largest of the sesamoid bonesis the patella. Well-marked sesamoid bones are found regularly on the flexor side of the metacarpoand metatarsophalangeal joints, usually of the first and frequently of the other digits of the hand and foot. Dorsally placed sesamoid bones have also been seen in connection with the thumb. On the flexor surface of the thumb a sesamoid bone is frequently found at the inter phalangeal joint. Fibrous interphalangeal sesamoids have been found in connection with the fingers.

The sesamoid bones are better developed in some of the lower mammals than in man, and, according to Pfitzner, are more frequent in the human embryo than in the adult. They are developed at the periphery of the intermediate blastemal zone. The blastema becomes condensed, and then in the better marked sesamoid bones becomes gradually transformed into cartilage. Ossification takes place relatively late in childhood. On the intracapsular origin of the sesamoid bones see Bradley (1906). In some tendons not intimately connected with a joint capsule a sesamoid bone may be developed in a region where the tendon is subjected to stress against a bone about which it turns. An example is the sesamoid bone often found in the tendon of the peroneus longus where this plays over the tuberosity of the cuboid. according to Lunghetti (1906), the sesamoid bone in the tendon of the M. peroneus longus develops in fibrous connective tissue, not in cartilage. It is commonly stated that it passes through a fibrocartilaginous stage before becoming ossified.

Variations in the Development of the Skeleton

Variations in the bones of the adult human skeleton are frequent. Thus, for instance, skeletons with only eleven or with thirteen free ribs are not uncommon. Rosenberg, Pfitzner, Thilenius, and others would ascribe some of the variations found in the adult skeleton to the chance persistence of transitory conditions normally present in the embryonic or fetal skeleton and supposedly of phylogenetie importance.

The studies of Thilenius, Bardeen, Mall, and others have shown, however^ that the skeleton of the embryo is subject to fluctuating variations like those found in the adult. At present there are not sufficient data to determine definitely the relative frequency of skeletal variations in the adult compared with those in the embryo or fetus.

Abnormalities in the Development of the Skeleton

The form of the skeleton as a whole and of the individual bones which compose it depends partly upon heredity, partly upon the mechanical and chemical influences to which it is subject during growth. The variations which are a normal inheritance of the race, including such extreme forms as individuals with six toes or six fingers, are to be distinguished from the abnormalities of structure due to unfavorable environment either within or without the body. In the main the shapes of the bones and joints are inherited, but to some slight extent both bones and joints are moulded by the experience of the indiridual. Abnormal stress of muscular or other origin, and abnormal lack of stress, as in cases of muscle paralysis, both give rise to bones and joints abnormal in form.

During development the skeleton is markedly influenced by internal chemical conditions affecting the growth or general nutrition of the body. The skeleton in some cases seems to be the part primarily affected. The skeletal lesions vary all the way from a retardation in the time of appearance of centres of ossification to the failure of a part of the skeleton to develop or to hyperplasia and abnormal form-differentiation.

Agenesis, or failure of skeletal development, may be due either to primary lack of origin of a part or to an affection which destroys the skeletal anlage after it has begun to differentiate. It is most frequently found in the cranial vault and in the vertebral arches, less frequently in the vertebral bodies and the bones of the extremities. The osseous defect is usually, but not always, associated with other marked physical deformities.

Hypoplasia, underdevelopment of the skeleton, whether generalized or eonfined to a part, may be due either to prenatal or to postnatal conditions. The failure of the bones to develop normally may be due (1) to lack of active proliferation of cartilage (characteristic of cretins), (2) to inactivity in the process of ossification, membranous, subperiosteal or endochondral (see Michel, 1903, Lindemann, 1903), (3) to a premature union of epiphyses with the main part of a bone, (4) to growth of connective tissue between the growing cartilage •of a bone and the region where ossification usually extends into the cartilage (micromelia chondromalacia, fetal rickets), and (5) to inflammation and other abnormal conditions affecting the growing parts of the bone.

Various congenital forms of hypoplasia are recognized, — microsomia, micromelia, micromelia chondromalacia (fetal rickets), cretinism, etc. In most instances while there is a general underdevelopment of the skeleton the long bones are especially affected and appear short and relatively thick; the pelvis and thorax are also usually abnormally smaU, and the root of the nose is broad and not infrequently sunken in. The causative factors of these conditions are obscure. In cretinism growth of cartilage is retarded and there is a delay in the appearance of centres of ossification and also in the fusion of epiphyses with the main parts of the bones (Wyss, 1900). In this disease there is good evidence that the failure of development of the body, including the skeleton, is due to lack of normal secretion by the thyroid gland. It is not improbable that the secretions of other glands of similar type may affect the development of the skeleton. Some diseases involving both the skeleton and the hypophysis have led to the belief that there is a relation between this gland and skeleton development. This relation has, however, been disputed (Arnold, 1894). K. Bach (1906) has recently discussed the apparent influence of the thymus on the growth of bones.

Hyperplasia overgrowth of the bones, is due (1) to an excessive activity of membranous or subperiosteal ossification or (2) to a prolonged persistence of actively growing epiphyseal cartilages, union of epiphysis with the main part of the bone being delayed, while endochondral ossification continues beyond the usual time. Hyperplasia may be local or general and may give rise to a well-proportioned or to disproportionate enlargement of the skeleton. It is stated that removal of the testicles early in infancy or congenital absence of the testicles may lead to an excessive prolongation of the activity of the epiphyseal cartilages and hence to gigantism (P. Launois and P. Roy, 1903, Poncet, 1903). Phosphorus and arsenic in small doses are said to promote bone growth. Partial hyperplasia is found most frequently in the skull and in the bones of the hands and feet. An irritative stimulus, such as a blow, may excite excessive growth of bone. In young people a small centre of inflammation (tuberculosis, osteomyelitis) in the diaphysis may excite activity in the processes concerned in ossification and induce abnormal growth in size of bone. If the centre of inflammation is near the epiphyseal cartilage, ossification is apt to be very irregular.

In congenital syphilis there are frequently, although not always, present characteristic irregularities in the deposition of calcium salts and in the formation of narrow cavities in the ossifying cartilage. This sometimes gives rise to marked ahnormality of form.

In rickets the process of bone absorption is abnormally active, while the formation of new bone is characterized by lack of deposit of the normal amount of calcium salts. In endochondral ossification there is no well-marked zone of calcification. The bones are abnormally thick, clumsy, and heavy and may be much distorted. In teratomata of various forms the skeletal abnormalities correspond with those of the rest of the body.


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Skeleton and Connective Tissues: Connective Tissue Histogenesis | Skeletal Morphogenesis | Chorda Dorsalis | Vertebral Column and Thorax | Limb Skeleton | Skull Hyoid Bone Larynx

   Manual of Human Embryology I 1910: The Germ Cells | Fertilization | Segmentation | First Primitive Segment | Gastrulation | External Form | Placenta | Human Embryo and Fetus Age | Ovum Pathology | Integument | Skeleton and Connective Tissues | Muscular System | Coelom and Diaphragm | Figures | Manual of Human Embryology 1 | Manual of Human Embryology 2 | Franz Keibel | Franklin Mall | Embryology History

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