Book - Manual of Human Embryology 11D

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

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D. Skeleton of the Limbs

One of the most studied subjects in morphology has been the development of the vertebrate limbs. Since, fortunately, critical summaries of its literature have recently been given by several noted investigators, among whom may be mentioned Wiedersheim (1892), Mollier (1893, 1895, 1897), Gegenbaur (1898), Rabl (1901), Fiirbringer (1902), Ruge(1902), and Braus (1904), no attempt will be made here to review this work except so far as it deals directly with the development of the human limb.

During the third week of embryonic life the limb buds become filled with a vascular mesenchyme. The source of this tissue is uncertain. In part it may come from the primitive body-segments, but it seems probable that in the main it comes from the parietal layer of the unsegmented mesoblast. Toward the end of the fourth week a slight condensation of the mesenchyme can be seen at the centre of the arm bud, and early in the fifth week a similar condensation may be noted in the leg bud. This condensation represents the first rudiment of the skeleton of the limb. The tissue composing it may therefore be called * * scleroblastema. " From the scleroblastema there is developed a membranous skeleton. In this a cartilaginous skeleton is differentiated, and this in turn is replaced by the permanent osseous skeleton. We may thus distinguish three overlapping periods, a blastemal, a chondrogenous, and an osseogenous. We shall first consider in some detail the development of the skeleton of the inferior extremity and then more briefly that of the superior extremity.

Inferior Extremity

Blastemal Period.

At the time when the condensation takes place in the leg bud the latter has the general form shown in outline in Fig. 274. The bud projects considerably from the body, but shows no definite resemblance to the limb to which it is to give rise. The condensed tissue, scleroblastema, is not sharply outlined. It represents the region of the acetabulum and the proximal end of the femur.

Once begun, skeleton differentiation proceeds rapidly. In an embryo 11 mm. long (Fig. 275) it may be seen that from the original centre of skeletal formation the condensation of tissue has extended both distally and proximally, but much more freely in the distal direction. Distally the scleroblastema shows femur, tibia, fibula, and a foot-plate; proximally, an iliac, a pubic, and an ischial process. A series of sections through the skeletal mass shows that in the femur, tibia, and fibula chondrification has begun. At centres in the blastema of the ilium, ischium, and pubis a still earlier stage of chondrification has made its appearance. The leg of this embryo, therefore, represents a stage of transition from the blastemal to the chondrogenous stage of development.

Chondbogenous Period.

The further development of the skeleton of the limb during the second and third months of intra-uterine life may be followed in Figs. 276, 277, and 278. For the sake of convenience the development of the several parts of the skeleton will be taken up as follows: (a) the os coxae; (6) femur, hip-joint, tibia and fibula, and knee-joint; (c) ankle and foot. (a) The Os Coxm. — The pelvic scleroblastema of embryos of the stage illustrated in Fig. 275 undergoes a rapid development. Its iliac portion extends in a dorsal direction toward the vertebrae which are to give it support. The costal processes of the latter at the same time become fused into a dense mass of tissue which enters into close association with the iliac blastema (Fig. 276), although for some time separated from this by a narrow band of tissue staining less densely than the blastema. Cranialwards the iliac blastema extends toward the abdominal musculature, to which it finally gives attachment.

Fig. 274-278.— (After Bardeen, Amer. Journ, of Anat.. 1905.) Lateral view of modda to illugtn the development of the dialnl pBrt of the spinal column and of the inferior extremity of embryos Bmm. loDK, In Firs. 27*. 275, and 276 the sderoblaatems i! «honn, and in this in KiEs. 275 and 276 I centres of chondrification. In FigP. 277 and 278 the Partilaginous afceleton ia shown, and in this in F 27Brentr«9 0fo99iliCBtion.

Fig. 274. — Length of embryo, mm. Fig. 275. I-ength of embryo. 11 mm. Fin. 270. Length of e bryo. 14 mm. Fig. 277. Length of emhryo. 20 mm. Fig. 278. Length of fetus. SO mm. Chd,. ehoi dorsalis; Co", first eoeeygeai vertebia; Cnifa /*, iwcHih rib: Fi, fibular F.o., foramen obturatum; . ilium; L.i., ligBmentum inguinale: M.id., membnns interdorsalin: P.. pubis; Pr.a.o.. proee.wus artii pmcessus tmnaverBUs ; Ti, tibia.

While the blastemal ilium is thus becoming differentiated the pubic and ischial processes of the pelvic blastema extend rapidly forward. Ventral to the obturator nerve they become united by condensed tissue, which completes the boundary of the obturator foramen. Betwen the crest of the ilium and the ventral extremity of the pubis dense tissue is formed to give attachment to the oblique abdominal musculature. This represents the embryonic inguinal ligament and completes a femoral canal (Fig. 276).

While the blastemal pelvis is being completed the three centres of chondrification, barely visible in the 11 mm. embryo, give rise respectively to iliac, pubic, and ischial cartilages in which the adult form becomes gradually more distinct. (Compare Figs. 276, 277, and 278.) In embryos between 15 and 20 mm. long each of the three cartilages gives rise to a plate-like process over the head of the femur. These processes fuse with one another and give rise to a shallow acetabulum (Fig. 277), which during the third month gradually becomes deeper (Fig. 278). The iliac and ischial cartilages furnish a greater part of the floor of the acetabulum than the pubic cartilage and unite with one another before being joined by the pubic cartilage. Toward the end of the second month and the beginning of the third month of development the symphysis pubis is formed. This is at first composed of dense blastemal tissue. In this tissue first hyaline and then fibrocartilage become differentiated. At the centre of the joint a slight fissure may appear in adult life (Farabeuf, 1895).

(6) Femur and Hipjoint. Tibia, Fibula, and Knee-joint. — The rapid development of the blastemal skeleton of the lower limb has been briefly described above. Soon after the anlage of the femur makes its appearance condensation of tissue marks out the anlages of the tibia and fibula and the skeleton of the foot. This last seems to be at first a somewhat irregular continuous sheet of tissue. It is not clear whether or not the anlages of the tibia and fibula also begin as a continuous sheet which becomes divided, by ingrowth of blood-vessels, into tibial and fibular portions. The incomplete development of the interosseous fissure in an 11 mm. embryo suggests this (Fig. 275). The blastemal anlages of the tibia and fibula are here very incompletely separated.

Within the blastema of the femur, tibia, and fibula chondrification begins as soon as the outlines of the blastemal skeleton are fairly complete (Fig. 275). The embryonic cartilage appears slightly kneewards from the centre of the shaft of each bone and then eKtends toward the ends. The cartilage of the femur consists of a bar largest at the knee, whence it tapers off toward the hip. The cartilages of the lower leg lie nearly in a common plane. That of the tibia is larger than that of the fibula and toward the knee it broadens out considerably. At this stage the joints consist of a solid mass of mesenchyme (Figs. 279 and 280). The tissue uniting the femur and tibia has temporarily somewhat the appearance of precartilage (Fig. 283). From this period onwards the development of the individual bones and joints is rapid.

The cartilaginous femur expands at the expense of the surrounding blastemal perichondrium and at the same time acquires adult characteristics (Figs. 276, 277, and 278). the hip-joint is at first completely filled with a dense blastemal tissue (Fig. 280). While the embryo is growing from 20 to 30 mm. in length, cavity formation begins in the tissue lying between the cartilaginous floor of the acetabulum and the head of the femur. The first stage in the process is marked by a condensation of the capsular tissue immediately bordering upon the joint and of the perichondral tissue which at this stage covers the cartilages on tiieir articular surfaces as well as elsewhere. In the region of the ligamentum teres a fibrous band is likewise differentiated from the blastema of the joint. The rest of the tissue becomes looser in texture and ultimately is absorbed (Fig. 284). Henke and Eeyher (1874) gave a good account of the development of the hijKJoint. Moser (1893) has described that of the ligamentum teres. Schulin (1879) has given a good account of the later development of the joint cavity in its relations to the head and neck of the femur (see Figs. 286-288). It is to be noted that in the fetus 25 cm. long (Fig. 286) the joint cavity extends about the neck of the femur in a pocket lined on one side by perichondrium, on the other by the capsule of the joint, and that later the peridiondral lining becomes periosteum (Fig. 288).

Fig. .384.

Fig. 2S7. Fig. 288. Flos. 285 Ui 2B8.~(AfCaSchulin, Arohiv {. Asatoici*. 1879.) Fig. 285. Mcdiui SMtlon tlirouih th« knw-joiDt of a letut 13 on. lon(. a. p«MUb; b. a 286-288. Hip-joiat of s msle fetus '25 cm.'lonK, of it fenale cjiild six yean old, and of a male ndult. a. (wnfication ; d, epiphyseal aaxeoiis nudeiu : (, ligamentum teres.

The tibia and fibula at first lie nearly in the same plane (Fig. 275). As the head of the tibia enlarges toward the knee-joint it comes to lie ventral to the proximal extremity of the fibnla. This may be seen in Figs. 276 and 277.

The development of the knee-joint in man has been studied by a number of competent observers. Bernays (1878) gave a good review of the previous work of von Baer, Bruch, Henke, and Reyher, and an accurate description of the processes which take place. Of the more recent articles those of Schulin (1879), Kazzander (1894), and Lucien (1904) deserve mention. Until the embryo reaches a length of about 17 mm. the kneejoint is marked by a dense mass of tissue (Fig. 279). The medullary tissue at the knee, like that at the hip and other joints, is less dense than the surrounding cortical substance, so that when the cartilages of the femur, tibia, and fibula are first differentiated they seem to be connected by a tissue which, in some respects, resembles the cartilage of which they are composed (Fig. 283) ; but as the cartilages become more definite the apparent continuity disappears. As the musculature becomes differentiated a dense tendon for the quadriceps is formed in front of the knee-joint. At this period the joint is flexed at nearly a right angle.

In embryos of about 20 mm. the tissue immediately surrounding the cartilages becomes greatly condensed into a definite perichondrium. The peripheral blastemal tissue at the joint becomes transformed into a capsular ligament, strengthened in front by the tendon of the quadriceps. Within the joint most of the tissue begins to show signs of becoming less dense, but the menisci and the crucial ligaments, like the ligaments of the capsule, are differentiated directly from the blastema (Figs. 281 and 282). In the differentiation of the articular blastema the menisci first become distinct, then the capsule, then the crucial ligaments, the patella, and the lig. mucosum.

A knee-joint cavity first appears, in embryos about 30 mm. long, between the patella and the femur. according to Lucien, two other cavities somewhat later appear between the condyles of the femur and the menisci. These cavities secondarily communicate with the retropatellar cavity and with cavities formed between the menisci and the tibia. The cavity of the knee-joint is primitively partly divided into two parts by a median septum (lig. mucosum), which becomes greatly reduced in fetuses 10-12 cm. long (Fig. 285, C) and in the adult is replaced by a fat pad.

The shafts of the tibia and fibula are incompletely separated in the blastemal stage. The cartilages which arise in the scleroblastema are, on the other hand, separated by a distinct interval (Fig. 279). At first short and thick, the shafts become gradually more slender in proportion to their length. The fibula, at all times smaller, becomes increasingly more slender in comparison with the tibia. In fetases 50 mm. long (Fig. 278) both bones, and especially the fibula, are still relatively thick compared with the adult bones.

During a period of rapid development, in embryos of 15 to 20 mm., the tibia and fibala, like the femur, may extend so rapidly in length as to become temporarily distorted by resistance at the

Fig. 288. — (After R. Quoin. Qutin'a Anatomy, lOth «d„ vol. ii. Ft. I. Fign. 1S7 ud 158.) Osafi A. Bone st birth. B. Child under ax yean of ave. C. Child two to thres yean older thu B. D. PenoD of about twroty years. E. Acetabular resion of hip-bone at tourtaen yean of afe. 1. ililiro; 2, ixchium: 3, pubis; 4. oa aoeUbuli; S. bony nodules between ilium and ischiuni: 6 and 7, epiphyBeal lamins on ilium and ischiuni; S, 9, 10. 11, epiphyseg of aolerior inferior iliac spine, iliac crest isohial tuberosity, and gympbysia putni. ends. This is often especially marked in hardened specimens. Holl (1891), Sohomburg (1900), and others have called attention to this distortion.

(c) Ankle and Foot. — Of the papers dealing with the early development of the skeleton of the human foot the more important are those of Henke and Reyher (1874), Leboucq (1882), v. Bardeleben (188.3, 1885), Lazarus (1896), and Schomburg (1900). During the fifth week of embryonic development the free extremity of the limb bud becomes flattened and differentiated into a foot-plate (Fig. 275). Toward the end of the fifth week the anlages of the individual bones of the ankle and foot begin to become marked by specific condensation of the blastemal tissue. Within these anlages precartilage soon appears. The digital rays are marked at first by condensed bars of tissue, in which segmentation into metatarsals and phalanges appears during the period of chondrification (Fig. 276). The metatarsal cartilages become differentiated before the tarsal cartilages. The phalangeal cartilages appear relatively late.

Fig. 290. — (After R. Quain, Quain's Anatomy, 10th ed., vol. u, Pt. I, Fig. 169.) OssificaUon of the femur. A. Before the eighth month. B. At birth. C. About a year old. D. At about the fifth year. £. Near the age of puberty. 1, diaphysis; 2, distal epiphysis; 3, head; 4, great trochanter; 5, small trochanter.

Fig. 291. — (After R. Quain, Quain's Anatomy, 10th ed., vol. ii, Pt. I. Fig. 160.) Ossification of the tibia. A. Some weeks before birth. B. At birth. C. At the third year. D. Betweoi the eighteenth and twentieth years. E. Example of separate centre for tuberosity. 1, diaphysis ; 2, proximal epiphy> sis ; 2*, epiphysis of tuberosity; 3, distal epiphysis. The earliest appearance of the tarsal cartilages is found in an embryo about 14 mm. long (Fig. 276). Toward the end of the second month these cartilages become much more distinct (Fig. 277). By the middle of the third month the cartilages of the foot have a form distinctly corresponding to the adult. The similarity is still better marked at the end of the third month (Fig. 278).

The joint cavities begin to develop while the embryo is growing from 25 to 30 nun. in length. As in other cases, so here the blastemal tissue in which the cartilages are developed becomes condensed at their articulating ends and about the joint, while in the region of the joint the tissue becomes less dense and finally disappears, leaving a joint cavity. In embryos of about 30 mm. the joint cavities of the foot are filled with a loose fibrous tissue ; in fetuses of 50 nun. definite cavities are to be made out. During the progress of form differentiation above described, the shape of the foot is markedly altered. At the beginning of the development of the foot the tarsal and metatarsal bones lie nearly, though not quite, in the same plane as the bones of the leg. They are so arranged, however, that the foot is convex on its dorsal surface and concave on the plantar, and the projections of the calcaneus and talus serve to deepen the plantar fossa. The metacarpals spread widely apart. As differentiation proceeds, the metatarsals come to lie more nearly parallel to one another, and the tarsal elements become compacted in such a way as to give rise to the tarsal arch. The foot at the same time is dorsally flexed at the ankle and slightly everted. The toes are flexed. In the further development of the skeleton of the foot the various constituent structures are elaborated, and the foot gradually becomes more flexed dorsally and turned toward the fibular side.

Fig. 292. — (After R. Quain, Quain's Anatomy, 10th ed., vol. ii, Pt. I, Fig. 161.) Oaflification of the fibula. A. At birth. B. At about two yean. C. At about four years. D. At about twenty years. 1, diaphysis; 2, distal epiphysis; 3 proximal epiphysis.

Period of Ossification

The hip-bone is ossified from three primary centres, one for each of its constituent parts, the ilium, ischium, and pubis, and from several epiphyses. There is one primary centre of ossification for each of the other bones of the inferior extremity, and in addition most of the bones have one or more epiphyses. In the tarsus the calcaneus alone regularly has an epiphysis. The patella has no epiphysis. With the exception of those of the tarsal bones and of the various sesamoid bones the primary centres of ossification appear relatively early in intra-uterine life. At birth there are usually centres of ossification present in the calcaneus, talus, and cuboid, but not in the other tarsal bones. Ossification in these latter tarsal bones and in the sesamoid bones and the various epiphyses appears after birth. In the talus, according to Sewell (1906), dark-staining regions in the hyaline cartilage of which it is composed in the sixth fetal month indicate structural

Fig. 203.— (AfMr R. Quain, Quain's the bona of (he foot. A. Right foot or a digital phHJsnge< an owHlied. The Uraus i caneus. B. Fetus o( 7-8 monthe. Nurleit y«r. Nucleus in third cuDeiform. E. Ii G. About the age ol puijerty, calcaueua. Epiphyees of meta caneusi 1', in G, the epiphyMs of the caleaneu

nueloua o( the talun; 3, of the euboid : . . . . uLar; 7. of thosecond ouneiform; S, metAlanal bones; 8'. distal epiphysis of llie senmd metatarsal bone; S" p^o^i^lBl etiiphysis of the first metBtanal bone ; 9, first phalanx of Ihe second toe; 9', proximal epiphysifi of this phalanx; 9*, (hat of the first phalanx of th« ereiit U>9 ; 10. second phalanx; 10'. the ^pbysis of tliie phalanx; 10*, epiphysia of the terminal phalanx of the great toe : 11. terroiDal phalanx; 11 ', iu epiphysis. features characteristic of the adult bone. The following tables and the accompanying figures illustrate the process of ossification in the inferior extremity. Authors differ in the data which they give concerning the time of ossification of the various bones. When not otherwise indicated the tenth edition of Quain 's Anatomy is followed in the tables.

Table of Ossification of the Bones of the Inferior Extremity

(Days and weeks refer to the prenatal, years to the postnatal period.)

Bone.

Centres.

Time of appearance of centre.

Os COX2B Os ilium 56th day (Mall)

Femur

Os ischii

Os pubis

Os acetabuli.

Epiphyses: Those of the acetabulum

Crest of ilium Tuberosity of ischium

Patella Tibia . .

Ischial spine Ant. inf. spine of ilium Symphysis end of OS pubis (1 or 2 centres) Diaphysis Epiphyses: Distal end Head Great trochanter . . .

Small trochanter . .

FibuU.

Calcaneus

Diaphysis Epiphyses: Proximal end Distal end Tubercle (occas.)

Diaphysis Epiphyses: Distal end — Proximal end. Chief centre —

Epiphysis (distal end)

105th day (Mall)

4th to 5th fetal month

9th to 12th year

Soon after puberty

Soon after puberty. . . Soon after puberty. . . Soon after puberty. . . Soon after puberty. . .

18th to 20th year. (Sappey)

Time of fusion: general remarks.

The rami of the ischium and the pubis are united by bone in the 7th or 8th year (Ouain) ( 12-14 year^ Sappey). In the acetabulum the three hip bones are separated by a Y-shaped cartilage until after puberty. In this cartilage between the ilium and pubis the ' 'os acetabuli "appears betwe^i the ninth and twelfth years. This bone, variable in siae, forms a greater or less part of the pubic portion of the articular cavity. Leche (1884). Krause (1885), and many others consider it primarily an independent bone. About puberty between the ilium and ischium and over the acetabular surfaces of these bones small irregular epiphyseal centres appear. The OS acetabuli becomes imited to the pubic bone about puberty and soon afterwards the acetabular portions of the ilium and ischium and the ischium and pubis begin to become united by bone. The acetabular portions of the pubis and ilium are unit^ a little later. Osseous union takes place earlier on the pelvic than on the articular surface of the acetabulum. The imion of the several orimary centres and the epiphyses is usuaJly completed about the tw^itieth year. Fuses with main bone 20th to 25th year. Fusion begins in the 17th jrear and is completed between the 20th and 24th years (Sappey). 18th to 20th year (Poirier). 18th to 20th year (Poirier).

After the 20th year.

43d day (Mall)

Shortlybefore birth.»« , 20th to 24th year. Ist year 18th to 19th year. 3d to 4th year. (Osse18th year, ous granules soon afterbirth, Poirier) i 13th to 14th year ' 17th year (Quain). 8th year (Sappey) Proximal epiphysis 18th to 22d year I (Poirier). 3d to 5th year The osseous patella reaches its definitive form soon before puberty. 44th day (Mall). About birth | 19th to 24th year (Sappey). 2d year 16th to 19th year.

13th year 65th day (Mall). 2d year

Fuses with epiphysis of the proximal end and then with this to the diaphysis.

20th to 22d year.

3d to 5th year 22d to 24th year.

6th fetal month

10th year (Quain) 7th-8th year ( Sappey)

The chief nucleus is endochondral. A periosteal nucleus appears frequently in the 4-5 fetal month (Hassel wander). 15th-16th year (Quain). 16th-18th year (Poirier). (^ 17-21, average 20 years. 9 13-17, average 16 years (Hasselwander)

• • Poirier, Traite d'Anatomie, vol. 1. page 227, gives a summary of the literature on the time of the appearance of this epiphysis. The epiphysis has some medico-legal importance, since its presence or absence has been utilized to determine whether a child is bom at term. Schwegel found it to appear between birth and the third year; Casper in the ninth fetal month. Hartmann found it lacking in 12 per cent, of cases at birth and in 7 per cent, of cases present as early as the eighth fetal month.

Bone.

TaluB.

Cuboid Cuneiform III. Cuneiform I... Cuneiform II.. Navicular

Metatarsals .

Phalanges: Terminal row

Middle row.

Proximal row

Centres.

Diaphjrsee Epiphyses

Sesamoid bones of the great toe

Time of appearance of coitre.

6th fetal month (Hassel wander).

About birth 1st year. 2d-3d year. 3d-4th year. 4th-5th year.

8th-10th week 3d-8th year....

Diaphyses Epiphyses (distal) Diaphyses Epiphyses Diaphyses Epiphyses

58th day (Mall). 4th year 4th-10th fetal month 3d year , 3d fetal month 3d year

cf 14th year 9 12th-13th year

Time of fusion: general remarks.

In the 7th-8th year the posterior part of the talus, the os trigonum, is frequently ossified from a special c«itre (v. Bardeleben). It fuses about the 18th year.

according to v. Bardeleben a second centre of ossincation appears much later than the primary in the navicular, and finally about the time of puberty a medial epiphyseal centre arises. The centre for the 2d metatarsal usually appears first, then come the 3rd, 4th, Ist and 5th. The epiphysis of the 1st metatarsal appears at the proximal end of the bone: the other epiphyses arise at the distal exida of the metatarsals. There may be a distal epiphysis in the first metatarsal also.17 In some instances a proximal epiphysis is formed cm the tuberosity of the fifth metatarsal (Gruber). The epiphyses unite with the shafts in the 17-21 year in males and in the 14-19 year in females. (Hassd wander) .

cf 13-23, average 16-21 year. 9 13-17, average 14-17 year (Hasselwander). (5^ 15-19 year. 9 13-16 year (Hassel wander). cf 15-17 year. 9 14-15 year (Hassel wander). The centres for the shafts of the phalanges often appear double, one for the dorsal and one for the plantar surface. The centres for the medial phalanges in each row usually appear before the more laterally placed centres. The ooEitre for the 5th terminal phalanx appears much later than the other centres in this row (Mall). according to Rambaud and Renault the epiphyses arise each from two centres which fuse together. In the terminal phalanx of the ^reat toe the ossification centre of the epiphysis often appears as early as the secona or even the first year. (Hassel wander) . Ossification may begin in the 8th year in females, in the 11th in males (Hasselwander).

>^ Mayet has described two centres of ossification for the proximal epiphysis of the first metatarsal, one of which represents the real metatarsal of the first digit.

Infantile Characteristics of the Skeleton of the Inferior Extremity. — In the infant the pelvis is small in proportion to the size of the body and contains a smaller proportion of the abdomino-pelvic viscera than in the adult. The cavity of the infantile pelvis is cone-shaped and diminishes in diameter from the entrance to the outlet (Fehling, 1876, Hennig, 1880). The blades of the ilium are relatively slightly developed. In the first half of fetal life the sacropelvic angle is similar to that of quadrupeds, but during the latter half and after birth the angle becomes greater, expanding from 55** to 90-110" in the adult (Le Damany)."

The acetabulum is relatively shallow in the new-bom as compared with the adult. The shafts of the long bones are relatively shorter and thicker. The neck of the femur is but slightly developed at birth. The infantile foot has certain ape-like characteristics and is strongly flexed and inverted. The head of the talus is directed more medialwards than in the adult, the first metatarsal is relatively short and inclined medialwards by the oblique articular surface of the first cuneiform (Leboucq, 1882).

Superior Extremity

Blastemal and Chondrogenous Periods.

In general the development of the superior extremity resembles that of the inferior extremity. The various stages of differentiation begin in the former a little earlier than in the latter. W. H. Lewis (1902) has described the earlier stages in the development of the arm. His description is closely followed here.

In an embryo at the end of the fourth week the scleroblastema of the limb bud is marked by a slight condensation of the tissue near the future head of the humerus. Early in the fifth week this condensation has extended to the distal part of the limb bud and the anlages of the scapula, humerus, radius, and ulna are distinguishable (see Fig. 294). The skeleton of the wrist and hand is marked by a plate of condensed tissue. There are no distinct centres of chondrification at this stage.

In an 11 mm. embryo marked alterations have taken place in the skeleton of the superior extremity (Fig. 295). Centres of chondrification appear.

The scapula is composed of precartilage surrounded by a dense blastema. It lies opposite the lower four cervical and the first one or two thoracic vertebrae. From the superior border there springs a large curved acromion process. On the medial (costal) surface, at the junction of the humerus with the scapula, arises a large hooked coraccid process. A slight ridge on the medial surface marks the future anterior border. The perichondrium is well marked onlv on the medial surface.

The clavicle is an ill-defined mass of condensed tissue which extends from the acromion about a third of the distance to the tip of the first rib. The coraccclavicular ligament is partially differentiated.

For recent accounts of the development of the pelvis, see Merkel (1902) and Falk (1908). Fehling recognized sexual differences in the pelvis early in fetal life.

The humerus is short and thick. The shaft is composed of embryonic cartilage surrounded by a dense layer of perichondrium. Towards each end of the shaft the central tissue is precartilaginous in character. The surrounding perichondrium is continued directly into the dense tissue of the neighboring skeletal parts.

There is more flexion at the elbow than during the preceding stage. The forearm is midway between supination and pronation. The core of the shaft of each bone is composed of hyaline cartilage. The hand-plate is composed of condensed mesenchyme. There are several centres of increased condensation which probably correspond to the carpal bones. The digits are marked by condensed tissue in which no segmentation into metacarpals and phalanges is visible.

In an embryo of 14 mm. the skeleton of the superior extremity is well advanced in development (Fig. 296). The form of the scapula is shown in this figure. It is composed mainly of cartilage, covered by a thick layer of perichondrium. It has migrated caudalwards so that less than one-half of it lies anterior to the level of the first rib. The clavicle is a rod composed of dense tissue. It extends from the acromion to the tip of the first rib, where it is continued into the sternal anlage. It contains a small core of a peculiar precartilaginous tissue. The acromioclavicular ligament is distinct. The humerus is larger and more slender than at the preceding stage and has expanded at each end. It is composed chiefly of cartilage surrounded by a thick perichondrium which is continuous with that of the lateral angle of the scapula. There are no signs of a joint cavity at the shoulder.

The ulna and radius are likewise composed of cartilage surrounded by a thick perichondrium continuous at one end with that of the humerus and at the other with that of the wrist. There are no joint cavities at the elbow.

The carpus is composed of a dense tissue in which are embedded cartilages which represent the bones of the wrist with the exception of the lunar and the pisiform. These are still composed of condensed tissue.

The metacarpals are represented by five slender cartilages surrounded by a dense perichondrium. The first metacarpal is only about half the length of the others. The phalanges of the first row, with the exception of that of the thumb, have cartilaginous cores. The basal phalanx of the thumb is composed of condensed tissue. At the tip of each digit is a mass of condensed tissue. There are no joint cavities present in the hand.

In an embryo 20 mm. long the cartilaginons anlages of various bones of the superior extremity are all well marked, except those of the distal row of the phalanges of the fingers. The clavicle extends from the acromion to the sternum. It is composed of a peculiar kind of precartitaginous tissue. The general shape of the other cartilages may be seen from Fig. 297. The spine of the scapula is not yet distinct. There are distinct coraccclavicular, costoclavicular, and interclavicular ligaments. There is no joint cavity at the shoulder, but a capsular and a coraeo-humeral ligament may be distinguished. The humerus has well-marked tuberosities and condyles. The ulna and radius are larger and longer than at the preceding stage. The olecranon, coraccid, and styloid processes are composed of cartilage and condensed tissue. The perichondrium about the ulna and radius is quite thick. The capsular and annular ligaments are present, but there are no joint cavities.

Magn. R : 1. Flu. 2Bn.— (AfU im. emiir.vo. Magn. about 13 :

All the bones of the carpus have cartilaginous centres. There are no joint cavities in the hand.

During the third month of development the cartilages of the superior extremity assume more and more the form characteristic of the adult bones ; in several ossification begins ; the joint cavities appear at this time.

The early development of the bones of the forearm and hand, and especially those of the wrist, has engaged the attention of several investigators. The following details are based upon the recent paper of Graefenberg (1906).

Forearm

The form and relations of the cartilaginous radius and ulna in the fifth, sixth, and the seventh weeks of embryonic life are shown in Figs. 298, 299, 300. The two cartilages are at first some distance from one another. The proc. styloideus of the ulna begins to develop during the latter part of the second month. It extends at first to the dorsal side of the triquetrum and becomes relatively large. Later the process becomes smaller, and is carried proximally and volarwards.

The discus articularis arises from a mass of tissue which lies between the radius and the styloid process of the ulna. This mass of tissue gives rise to a special centre of chondrification, which by some is supposed to represent the os intermedium antebrachii of the lower vertebrates.

The Carpus

Os Centrale. — Most of those who have studied the development of the human carpus have described a cartilage which is homologous with the os centrale of the carpus of lower vertebrates. The position of this element is shown in Figs. 298, 299, and 300. It later disappears. In the process of retrograde metamorphosis it may become divided into several parts. according to Graefenberg it does not fuse with any of the other carpal.

The Proximal Row or Bones. — The navicular arises from two centres of chondrification. It is homologous with the radiale of lower forms. The lunar is the last of the carpalia to be differentiated. according to Gegengaur and some other investigators, it is homologous with the os intermedium of the lower vertebrates. In man, however, there are no indications of its wandering from the forearm into the wrist. The triquetrum is relatively small when first differentiated, but grows rapidly in size (Figs. 298, 299 and 300). Perna has found it arising from two centres of chondrification. The pisiform is relatively large in embryonic stages. It is a canonic carpal element and not a sesamoid bone. It arises later than the triquetrum. During its development it wanders from the ulnar margin to the volar surface of the triquetrum.

The Distal Row. — The cartilages of the distal row are at first relatively large compared with those of the proximal row

J. AnBlomiMhe Hefte, IBOO, Fi«. 1.) Dorml view of ■ model of th» le forearm and hand of * Gve-weeks human onbryo. Magn. TO : I. jf ibe skeleton of the forcann and hand of a

liniu; the cmtmla betwe

atum; »un.. humerus; M.mo)'., multaii(ulun ., pare radialit, ubt., i»r« ulnaris : P., pisiforme ; The oafwtatum Um betweeo tha bunatum and the muKanpi

Fig. 300.— A. (After Gr^fenberc, 1906. Pig. G.) ekelelOD of the right hand of a ten-weeks human fetua.

(Figs. 298 and 300). The capitatum is the largest, next comes the hamatum. The multangalar carpalia are small; the M. majus is for a time considerably smaller than the M. minus. The capitatum and hamatum are the first elements of the carpus to undergo chondrification. The hamulus ossis hamati is differentiated from a special centre of chondrification.

urn tuid hsmBtum. B. Elbow-joint of a fetui c. centnl udLdq: d, perichoadr*! put of Juia anoa. D, £, F. Should er-joiat o[ a fetua 13 m of mpiiulei t. intracepsuUr eonnwtive tiMi

Anat. Abt., 1879.) Fir diocarpflj ioiut in thrc« 

Metocarpalia. — These are at first relatively large. The first metacarpal, according to some investigators, represents a basal phalanx. Galen was the first to express the view that the metacarpal of the thumb is not present. Others have thought that a phalanx is missing from the thumb, but Graefenberg accepts the view of Galen. The other four cartilaginous metacarpals arise at some distance from one another (Fig. 298). They spread apart distally. The bases are first brought into contact with one another, and later the distal ends. The fifth metacarpal articulates at first with the triquetrum (Fig. 298) and later with the hamatum (Fig. 299).

The phalanges are differentiated in serial order, the basal row appearing first, the terminal row last. according to Graefenberg, the terminal phalanges show evidence of being composed of two elements, a proximal and a^ distal. The latter is composed of cartilage, the cells of which rapidly enlarge. It may represent a fourth phalanx. Primitively the digits were probably composed of many phalanges. The terminal phalanges are at first smaller than those of the middle row, but then develop faster so as to exceed them in length. After a time retrograde metamorphosis overtakes the distal ends of the terminal phalanges, so that the middle row once more exceeds the terminal in length. The tuberositas unguicularis is composed of fibrous tissue which becomes transformed directly into bone. The sesamoid bones, according to Thilenius, are more numerous in the fetus than in the adult. The following table, after Pfitzner and cited by Dwight (1907) illustrates this. This table is based on a study by Thilenius of 30 hands of fetuses of the fourth month, and of 1440 hands by Pfitzner of individuals from fourteen to eighty-nine years of age. The Roman numerals indicate the metacarpophalangeal joints opposite which sesamoid bones were found, and the Arabic numerals represent the percentage of frequency with which the bones were found.

Fig. 302. (After R. Qiiain, Qtiain's Anatomy, 10th ed., vol. ii, Pt. 1, Fig. 1 15.) Ossification of the clavicle. A. Clavicle at birth. B. At about the twenty-third year. 1, shaft; 2, epiphyma.

Joints

Schulin (1879) has given some account of the development of the joints of the upper extremity. At the shoulderjoint (Fig. 301, D, E, F) a joint fissure arises in the periphery of the intermediate zone and thence extends inwards between the head of the humerus and the glenoid fossa (Fig. 301, D). The joint cavity extends into the perichondrium for some distance on each side of the head of the humerus, so that there is from a very early period a well-developed layer of intracapsular connective tissue (6). The labrum glenoidale is differentiated at an early period. After the joint cavity appears the head of the humerus undergoes considerable development. (Compare D, E, F, Fig. 301.) During fetal development the tendon of the long head of the biceps sinks in through the capsule of the joint. For a time it is covered by a layer of synovial membrane which attaches it to the capsule, but in the third or fourth month it becomes free in the joint cavity (Welcker, 1878). The elbowjoint (Fig. 301, B and C) develops in a position of flexion at about 90°. The perichondral part of the joint cavity (Fig. 301, B, d) develops before the intercartilaginous part. The distal end of the humerus undergoes marked alterations in form during the development of the joint (Fig. 301, C). In the wris1>joiiit cavities appear during the third month (Fig. 301, A). At the radiocarpal joint the joint cavity arises from three separate fissures (&).

Fig. 303.—

Fig. 306. Fia8. 305 and 306. — (After R. Quain, Quain's Anatomy, 10th ed., vol. ii, Pt. I, Figs. 119 and 120.) Ossification of the radius and uhia. Fig. 305. Radius. A. At term. B. At 2 years. C. At 5 years. D. At 18 years. Fig. 306. Ulna. A. At birth. B. At the end of the fourth year. C. At 12 years. D. At 19 to 20 years. Ep., epiphysis.

Fig, 307.— <Aftar R. Quiin, Quwn'n Anatomy. 10th ed., vol, ii. Pt. I. Tie. 121.) OniGcatioD of the bODB at Ihe liMid. A. At birth. The carpus is cBrti1««inous. The thiLla of the metacarpals and phalanflee are oeaified. B. At the ead of the first /ear. C. About the third year, D. At the iifth year. E. At the ninth year. 1, csapitaCum; 2, hamatum; 3, triquetrum; 4, lunatuin; 5. multangulum loajus; 6, navicular; 7. multanAulum minus; 8, metacarpal shafts; 8*. four maCacarpalepiphyBce; 8', tHatof the thumbs 0. boasl phalanges; 9*, tbeii epiphyses; 9'. that of the thumb; 10. [Diddle pholaosea; 10', epiphysisof (erminal phalaUTt of thumb; It, terminal phalanflee of the fingers; 11*, their epiphysca. The development of the digital joints has been previously described (Figs. 226-228).

Period of Ossification.

With the exception of the clavicle the bones of the superior extremity pass through a stage of embryonic hyaline cartilage before becoming ossified. The shaft of the clavicle, which is the first bone in the body to exhibit a centre of ossification, is ossified in a peculiar kind of cartilage (Mall). The ends of tbis bone exhibit the more usual type of ossific cartilage. The following table gives the approximate periods when the various centres of ossification appear and the time of fusion of the various centres which unite to form the individual bones. Authors differ considerably concerning these data. When not otherwise indicated, the data included in this table are based upon those given in Quain's Anatomy, 10th edition, vol. 2, p. 106. according to Pry or (1906), the epiphyses of the hand appear earlier and unite to the shaft earlier in females than in males a|>d in the first-bom children earlier than in those bom later. **The fully developed hand of the female is at least two years in advance of the male.^^ Similar conditions have been found by Hasselwander in the skeleton of the foot.

Table of Ossification of the Bones of the Superior Extremity

(DtLYB and we^s refer to the prenatal, years to the postnatal period.)

Bone.

Clavicle

Scapula

Centres.

Diaphysis Sternal epiphysis.

Time of appearance of centre.

Primary centres: 1. That of the body, the spine, and the base of the glenoid cavity. 2. Goraooid process 3. Subcoraooid

Himierus .

Epiphyses: Acromial epiphyses Epiphysis of the inferior angle. Epiphyses of the vertebral border. Epiphjrses of upper surface of coraccid. Epiphysis of surface of glenoid fossa.

Diaphysis Epiphyses: Head Tuberculum majus . . . Tuberculum minus Capitulum Epioondylus med Lateral margin of trochlea. E|Hcondylus lat

6th week 18th to 20th year.

Union of primary and secondary centres; remarks.

8th week (Mall).>* 1st year. 10th to 12th year. 15th to 18th year. 16 to 18th year. 18th to 20th year. 16th to 18th year. 16th to 18th year.

6th to 7th week (Mall) 1st to 2d year. 2d to 3d year. 3d to 5th year. 2d to 3d year. 5th to 8th year. 11th to 12th year. 12th to 14th year.

There are two centres in the shaft, a medial and a lateral. These blend on the 45th day (Mall). Shaft and epiohysis unite between the 20tn and 25th years. The chief centre appears near the lateral angle. The subcoraccid centre appears at the base of the coraccid process and also gives rise to a part of the superior mar|^ of the glenoid fossa. The coraccid process joins the body about the age of puberty. The acromial epiphjrsMtl centres (two or three in number) fuse with one another so(m after their u>pearance and with the spine between the 22d and 25th years ((jjuain); 20th 3rear (Wilms). The subcoraccid and the epiphjrses of the coraccid process, the i^enoid fossa, the inferior anjB^e, and the vertebral margin join between the 18th and 24th years in the order mentioned (Sappey).

The epiphyses of the head, the tuberculum majus Bnd the tuberculum minus (the last is inconstant) imite with one another in 4th-6th srear and with the shaft in 20th-25th year. The epiphyses of the capitulum, lateral epicondyle, and trochlea unite with one another snd then in the 16th~ 17th year join the shaft. The epiphysis of the medial epicondyfe joins the shaft in the 18th year.

1* according to Poirier, Traitd d'Anatomie, p. 138, two centres appear in the eighth week, and unite in the third month to form a centre of ossification for the body of the scapula.

Bone.

Radius

Ulna

Carpus

Metacarpals ,

Centres.

Phalanges First row —

Middle row..

Diapbysis , Epiphyses: Carpal end Humeral end Diaphysis Epiphyses: Carpal end Humeral end Os capitatum Os hamatum Os triquetrum Oslunatum Os naviculare Os mult, maj Osmult. min Os pisiforme Diaphsrses Proximal epiphysis of the first metacarpal Distal epiphyses of the metacarpals.

Time of appearance of centre.

7th week (Mall)

9 8th month, cT 1 6th month (Pryor), 6th-7th year.

7th week.

9 6th-7th year. (^ 7th-«th year ( Pryor loth year.

Diaphyses Proximal epiphyses . .

93d-6th month (^ 4th-10th month. V5th-10th month. ^ 6th-12th month. 9 2d-3d year. cT about 3 yean, 93rd-4thyear. (^ about 4 years. Vat 4 years, or early in 5th year. d about 5 years. 94th-5thyear. (5'6th-6thyear. 94th-5thyear (f 6tn-6th year. 99th-10thyear. cT 12th-l3th year. 9th week (Mall)

3d year. 2d year.

9th week (Mall) l8t-3d year (Pryor).

Terminal row

Diaphyses Proximal epiphyses . . Diaphyses Proximal epiphyses .

Sesamoid bones

llth-12thweek(Mall) 2d-3d year.

7th-8th week. 2d-3d year.

Union of primary and secondary centres; remarks.

The superior epiphysis and shaft unite between the 17th and 20th years. The inferior epiphysis and shaft about the 21st year (Pryor); 921st year, cf2l8t-25th year (Sappey). Sometimes an epiphysis IS found m the tuberosity (R. and K.) and in the styloid process (Sappey). The centre for the shaft of the ulna arises a few days later than that for the radius. The proximal epiphysis is united to the shaft about the 17th year; the inferior epiphysis between the 18th and 20th years; 9 20th 7 21st years, cf 21st -24th years (Sappey) . There is sometimes an epiphysis in the styloid process (Sohwegel) and in the tip of the olecranon process (Sappey). The navicular sometimes has two centres of o.osification (Serres. Rambaud and Renault). Serres uid Pryor have described two centres of ossification in the lunatum. Debierre has described two centres in the pisiform, one in a girl of eleven, the other in a boy of twelve. The OS hamatum may have a special centre for the hamular process. Pryor has found two centres in the triquetrum. Pryor (1908), describes the centres of ossification of the carpal bones as assuming shapes characteristic of each bcme at an early period.

The centres for the shafts of the seComd and third metacarpals are the first to appear. There may be a distal epiphysis for the first metacarpal and a proximal epiphysis for the second. Pryor (1906). found the distal epiphysis of the first metacarpal in about 6 per cent, of cases. It is a family characteristic. It arises before the 4th year and unites later. Pryor found the proximal epiphysis of the second metacarpal in six out of two hundred families. It unites with the shaft between the 4th and 6th-7th year; sometimes, however, not until the 14th year. In the seal and some other animals all the metacarpals have proximal and distal epiphyses (Quain). The epiphyses join the shafts between the 15th and 20th years. There may bean independentepiphysis for the styloid process of the 5th metacarpcd. The epiphysis of the metacarpal of the index finger appears first. This is followed by those of the 3d, 4th, 5th, and 1st digits. The shafts of the phalanges of the second and third fingers are the first to show centres of ossification. The phalanges of the little finf^er are the last, ^he epiphysis in the middle finger is the first to appear. This is followed by those of the 4th, 2d, 5th, and 1st digits. The centres in the shafts of this row are the last to appear. The epiphysis of the phalanx of the middle finger is the first to appear. This is followed by thof«e of the ring, index, and little finger (Pryor). The terminal phalanx of the thumb is the first to show a centre of ossification in the shaft. This is the first centre of ossification in the hand. It is developed in connecti ve tissue while the centres of the other phalanges are developed in cartilage (Mall). The epiphysis of the ungual phalanx of the thumb is followed by those of the middle, ring, index, uid littlenngers. The fusion of the epiphyses of the phalanges with the diaphyses takes place in the 18th-20th year. Ossification begins generally in the 13th14th years, and may not take place until after middle life (Thilenius). For table of relative frequency in the embryo and adult see p. 385.

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