morphology of the sternochondral joints of mammals

MORPHOLOGY O F THE STERNOCHONDRAL JOINTS O F MAMMALS

MARIAN WILLIAMS Department of Anatomy, Stanford University, Stanford, California

THIRTY-TWO FIGURES

In the case of most human synovial joints it is possible to predict with reasonable certainty the stage of development at any developmental interval and the structure of the normal adult joint. This has not been found to be true of the sternochondral joints. According to detailed studies of these articulations in man by Gray and Gardner ( '43), a number of cavities has been found to exist at an early stage in the fetus, at birth a full set of joint cavities has been observed, or none at all may be in evidence at this time. Furthermore, a comparison of the occurrence of synovial cavities in the fetus and in the adult raises the question of whether or not certain of the sternochondral joints may ever develop cavities at all. This variability in human sternochondral joints suggested a study to determine the character of these joints in other mammals.

Many questions remain unanswered regarding the nature of fibrocartilage and the predisposing factors in its formation. In the human adult sternochondral joints, articular surfaces of joint cavities consist entirely of fibrocartilage, while in the fetus and newborn the articular surfaces are of hyaline cartilage. I t is not fully understood how this change takes place. In the absence of sufficient human laboratory material in the years between infancy and young adulthood, observations of joints of other mammals in various stages of development might be of value in approaching this problem providing species with suitable joint structure could be found, The present study was a step toward determining what material might be available for purposes of investigation.

275

276 MARIAN WILLIAMS

Data in the present report have been grouped according to Simpson’s classification of mammalian forms as adapted by Young (’50). The basic arrangement of the attachment of the costal cartilages to the sternum showed little variation among the species studied. The rib elements, ranging from 6 to 9 pairs, joined the lateral borders of the sternum at the levels of the intersternebral junctures. The first rib pair joined the manubrium, which was often broadened. In the case of the human and gibbon sterna, the entire structure was much broader than in the other species studied and lacked the typical segmentation (figs. 1, 7, and 10).

MATERIALS AND METHODS

The sterna with adjacent portions of the costal cartilages were removed in most instances from freshly killed animals. Several animals were preserved by previous freezing and the sternal portions then fixed either in Bouin’s solution or in 10% formalin (cow, pig, sheep, gibbon). Some animals had been preserved in alcohol (bats), and one (mountain beaver) in a solution of formalin before the sterna were removed and fixed. Two of the three human newborn specimens had been embalmed for laboratory use.

Serial sections of from 8 to 6 0 p were cut in the frontal plane of the sternum. The number of sections mounted and stained varied according to the size of the sternum. In the case of the bats and smaller mice, all sections were mounted. In slightly larger specimens, alternate sections were mounted, or one in three or four sections. I n the largest animals, sections were selected primarily from the center of the joint. The stain used was a modification of Mallory’s triple stain for connective tissue.

OBSERVATIONS

Sixty-three specimens representing 9 orders of mammals were prepared and examined. Examples of both eutheria (placentalia) and metatheria (didelphia) were included (table

MORPHOLOGY OF STERNOCHONDRAL JOINTS 277

1). Whenever possible, two or more specimens of a given species were obtained for study. Descriptions are based on selected sections of the specimen. Variations in the plane of the sections probably account for some structural character- istics such as instances in which rows of lacunae appeared to slant obliquely away from the articular surface. Occasion- ally a well-formed synovial cavity was present in several sections of a series while in adjoining sections the joint had the appearance of a synchondrosis.

In the following discussion, “diarthrodial” indicates a joint with a smooth-walled cavity and a synovial lining. The term “interzone,” which usually refers to the union at an early embryonic stage, has also been used in the description of the articulations of the human newborn, as well as in relation to adult joints which were found to have no cavity or only a partial cavity.

Human. newborn Three specimens were studied, with crown-rump lengths

of 353, 359, and 390 mm respectively. In two cases the manubrium was divided from the body of the sternum by a transverse zone of fibrocartilage (fig. 4) ; in the third instance the hyaline cartilage of these two sternal parts was continuous

Well-formed cavities were found in the second sternochondral joints of all specimens. In one case cavities were also found in all but two of the joints distal to the second; some of these had irregular margins and were crossed by strands. I n one instance the union of the first ribs with the manubrium was indicated by a narrow interzone (fig. 2) while in the remaining first joints such a zone was absent or faintly evident only in the lower half of the area.

The second sternochondral joints resembled those of the adult in having flattened sternal facets, a pointed costal cartilage extremity, and fibrous tissue extending between the costal cartilage and sternal notch near the middle of the joint (figs. 3 and 4). Cavities with hyaline walls were present

(fig. 3).

TABLE 1

Classification and number of specimens

QENUS AND SPECIES NUMBER OF SPECIMENS

Class MAMMALIA Subclass THERIA

Infra class METATHERIA Order MARSUPIALIA

Fam. Didelphidae Superfam. Didelphoidea

Infraclass EUTHERIA Cohort UNQUICULATA

Order INSECTIVORA Superf am. Soricoidea

Fam. Talpidae

Order CHIROPTERA Suborder Microchiroptera

Fam. Vespertilionidae Superf am. Vespertilionoidea

Subf am. Vespertilioniiiae Subf am. Nyctophilinae

Order PRIMATES Suborder ANTHROPOIDEA

Superfam. Cercopithecoidea Fam. Cereopithecidae

Subfam. Cercopithecinae Superf am. Hominoidea

Fam. Pongidae Subfam. Hglobatinae

Fam. Hominidae

Cohort GLIRES Order LAGOMORPHA

Fam. Leporidae Subfam. Leporinae

Order RODENTIA Suborder SCIUROMORPHA

Superfam. Aplodontoidea Fam. Aplodontidae

Superfam. Soiuroidea Fam. Seiuridae

Subfam. Seiurinae Tribe Sciurini

Didelphis virginianus (Virginia opossum)

Talpa scapanus lati- manus (California mole)

Myotis velif er (bat) Antrozous pallidus

pacifieus (bat)

Cynomolgus (monkey)

Hylobates sp. (gib-

Homo sapiens (human bon)

newborn)

Oryctolagus sp. (rabbit)

Aplodontia rufa (mountain ‘ ‘beaver ’ ’)

Sciurus niger (East- ern fox squirrel)

2

2

2 1

5

2

3

3

1

2

278

TABLE 1 (continued)

Classification and number of specimens

GENUS AND SPECIES ~~~~E~~

Superfam. Geomyoidea Fam. Heteromyidae

Subfam. Dipodomyinae

Suborder MYOMORPHA Superfam. Muroidea

Fam. Cricetidae Subfam. Cricetinae

Tribe Cricetini

Fam. Muridae Subfam. Murinae

Suborder HYSTRICOMORPHA

Superfam. Cavioidea Fam. Caviidae

Subf am. Caviinae Superfam. Chinchilloidea

Fam. Chinchillidae

Cohort FERUNGULATA Superorder FERAE

Order CARNIVORA

Fam. Canidae Superf am. Canoidea

Subfam. Caninae

Superf am. Feloidea Fam. Felidae

Subf am. Felinae Superorder MESAXONIA

Order PERISSODACTYLA

Superf am. Equoidea Suborder HIPPOMORPHA

Fam. Equidae Subfam. Equinae

Superorder PARAXONIA Order ARTIODACTYLA

Suborder SUIFORMES Inf raorder SUINA

Superfam. Suoidea Fam. Suidae

Subfam. Suinae Superfam. Bovoidea

Fam. Bovidae Subfam. Bovinae

Tribe Bovini

Dipodomys sp. (‘ ‘kangaroo r a t ’ ’)

Mesocricetus auratus (Syrian hamster)

Rattus rattus ( ra t ) Mus musculus

(mouse)

Cavia sp. (guinea pig)

Chinchilla sp. (chinchilla)

Canis f amiliaris (dog) 2

Felis domesticus (cat) 5 Felis tigris (tiger) 1

Equus caballus (horse)

Sus scrofa (pig)

Bos sp. Ovis sp.

1

2

2 2

279

280 MARIAN WILLIAMS

bilaterally in one specimen, both above and below the intra- articular ligament. In the other two specimens, such a cavity was present in one instance in the lower right portion of the articulation, and in the other in the upper right portion.

The interzones between the costal cartilages and sternum were similar at all levels, and when a cavity was present it appeared to have developed first as a fissure in the interzone. The tissues of the interzone resembled loose connective tissue, with parallel fibrous strands crossing transversely. The cells between the strands were acidophilic and arranged in rows parallel to the fibers. When cavities were present in the third through seventh joints, they varied from small discontinuous spaces between the fibers of the interzone to wide cavities with smooth margins which apparently had replaced the entire interzone.

When narrow fissures had formed in the interzone they appeared toward the medial margin of the zone (fig. 5 ) . On the costal margins of the interzone, the rows of cells retained some semblance of their transverse direction across the zone. The interzone cells adjacent to the cavity were hypertrophied, acidophilic and irregular in their arrangement. On the sternal side of the cavity the cartilage cells were closely packed and flattened with their long axes parallel to the surface. Thus the sternal wall of the cavity resembled definitive articular cartilage while the interzone residuum attached to the costal wall was still undergoing dissolution (fig. 6).

Hylobates sp. (gibbon; two adult specimens) The first sternochondral juncture was made up of continuous

hyaline cartilage. The second joints of one specimen contained no cavity, while in the other specimen only poorly formed spaces were seen at this level.

Well-formed cavities were present in all the sternochondral joints from the third through the seventh. The third articulations closely resembled the second joints in the human newborn specimens in that the end of the costal cartilage was pointed and the cranial and caudal cavities were divided by

MORPHOLOGY O F S T E R N O C H O N D R A L J O I N T S 281

fibers crossing from the end of the costal cartilage to the sternum (fig. 9). The walls of the spaces consisted of hyaline cartilage, containing rows of flattened lacunae and covered by a thin layer of amorphous material. One specimen had only caudal cavities bilaterally.

The 4th, 5th and 6th joints contained a well-formed space in the caudal portion. Here the cavity extended for a distance along the side of the caudal sternebra, and was enclosed by a thick capsule (fig. 8). The walls of the well-formed portion of the cavity, which contained a caudal synovial fold, consisted of basophilic hyaline cartilage. Cranially, the union between the costal cartilage and sternum resembled the interzone described in the human newborn. Immediately within the capsule, fibers crossed transversely, while farther centrally they became more oblique in direction. Many fissures separated the latter fibers but these spaces were discontinuous. In one joint of this group (6th left) the situation was reversed. Here the smooth-walled synovial cavity appeared cranially, while the caudal portion of the joint contained discontinuous fissures and obliquely crossing fibers.

The seventh joints had complete cavities. The sternal notches at this level were remarkable for their depth, which approached a half circle.

Cynonzolgus. (monkey; 5 udzclt specimens) Although well-formed cavities were found in the sterno-

chondral joints of each specimen, their number and location varied considerably from one specimen to another. In one case, only the caudal half of the second sternocliondral joints had spaces. In others, 4 or 5 joints were found to have cavities bilaterally. These were most frequently present in the fourth and fifth joints. The appearance of the right and left joints at any given level mas usually similar in each animal (fig. 13).

A well-formed cavity is illustrated in figure 11. I n this type of joint, the costal cartilage end and the sternal notch were congruent, and their hyaline cartilage surfaces were often covered by a thin layer of amorphous material. The cartilage

282 MARIAN WILLIAMS

of the sternal notch sometimes contained areas of chromophobic tissue relatively poor in cells a t the deepest point of the notch. A synovial fold usually protruded into the joint space from the cranial or caudal side of the cavity or from both sides. In several instances cavities were found with irregular margins and numerous strands crossing obliquely between the borders.

At the first sternochondral union an interzone was present between the costal cartilage and manubrium in three of the specimens. In the first left joint a clear cavity with a synovial fold was present in the caudal portion. The second sternochondral joints, bordering the manubrio-gladiolar articulation, resembled those at this level in the human newborn and the third sternochondral joints in the gibbon ; however, in the monkey the costal cartilage extremities and sternal notches were less flat and the transverse fibrocartilage strip separating the manubrium and body was relatively much wider, nearly approximating the width of the second costal cartilages in some instances.

In one specimen the general arrangement of the second joint was suggested also in the structure of the third through the sixth joints. A transverse fibrous or chromophobic zone crossed the middle of the sterncbral discs and was continuous with a fibrous area surrounding the medial end of the costal cartilages (interzones). In the third joints of this specimen, clear cavities appeared in the caudal portion of the sternochondral union, and in the fourth and fifth joints, both cranial and caudal cavities were present (fig. 12).

My Otis velif er, Arctrozous pal l idus pacificus (bat; three adul t specimens)

All the sternochondral joints had complete cavities except the first in Aw2ozous, where there was no demarcation between costal cartilage and manubrium. The joints of the third through the sixth costal levels were remarkably similar in appearance (fig. 16). The articular surfaces were congruent and the joint space was slightly enlarged peripherally. Usu-


ally the tissue at the medial end of the hyaline costal cartilage was relatively acellular adjacent to the cavity. On the opposite side of the joint the thin layer of hyaline cartilage lining the sternal notch overlay an equally thin bony compacta adjacent to the marrow cavity. The bone was deficient in places, so that the marrow space i\-as bounded by a cartilaginous wall.

The first sternochondral joint facets in Myot is were shal- lower than those farther caudalward. The curvature of the first costal cartilage extremity closely followed that of the sternal notch. Caudal to the joint cavity and communicating with it were rounded spaces enclosed by capsular fibers. These sac-like structures contained fatty tissue and were present also in Auztroxous, which lacked a cavity in the first sternochondral joints.

The cavity of the second joint communicated with that of the manubriogladiolar articulation (fig. 15). The costal cartilage extremity was pointed and the cranial and caudal facets of the notch were flattened. The layer of hyaline cartilage lining the second sternal facet was considerably thicker than that in the other joints. The cartilage of the sternal notch and along the borders of the transverse manubriogladiolar cavity contained lacunae which were small and sparse but not flattened.

Talpa scaparzus latimunus (mole; two adult specimeizs) No sternochondral joint cavities were found in the mole.

Very small fissures appeared in the second joints, and small peripheral (cranial) cavities were present in the sixth and seventh left joints of one specimen and in the sixth right joint of the other. In one specimen an irregular transverse fissure appeared in the manubriogladiolar disc.

At the fifth and sixth sternochondral joints, where an intersternebral disc was absent, the interzones were crossed transversely by columns of lacunae; these were similar to the interzones of the more proximal joints. Although the seventh costal cartilages were adjacent to each other in the midline,

284 MARIAN WILLIAMS

they were attached to the caudal surface of the neighboring sternal segments rather than to each other (fig. 14).

Oryctolagus sp. (rabbit; three adult specimens)

Many well-formed cavities were present, with the majority in the more cranial joints. Mature cavities were present in 5 of the 6 third sternochondral joints and in 4 of the 6 second joints. In the second joints, the lacunae on the costal surface were generally larger than those on the sternal side and the cavity surfaces were lined by a thin, amorphous layer.

Well-formed cavities were found in all the first sternochondral joints. The spaces were shaped like an inverted “v” - pointed cranially and widened caudally. The sternal facet was flat. A large synovial fold extended into the joint cavity from the caudal side.

Most of the remaining joints with cavities resembled one another. I n one specimen with complete cavities in the fourth joints, the sockets were deep, slightly angular, and notched at the innermost point (fig. 24). From the deepest part of the notch, small rows of flattened lacunae radiated medialward for a short distance into the disc. The ground substance surrounding these lacunae was particularly basophilic.

In one fifth joint a cavity was present in the cranial portion of the interzone. The walls of the space were irregular and basophilic strands crossed the zone caudally. The joint appeared to be in the process of cavity formation or to have been arrested earlier at this stage of development.

Megamys sp. (chi!nchilla; one adult specirnew)

No extensive cavities were present in the chinchilla, although a fissure appeared in the first sternochondral joint bilaterally and a few very limited peripheral cavities were found in the caudal joints. I n the first joints the marginal parts of the interzone consisted of zones of hyaline cartilage. The remaining sternochondral joints had interzones which varied in appearance. The more cranial usually appeared as

MORPHOLOGY O F STERNOCHONDRAL JOINTS 285

crescent-shaped, light areas enclosed within deeper basophilic margins. Very limited caudal peripheral cavities were present in the third, fourth, and fifth left joints and in the fourth right joint (fig. 20).

Cavia sp . (gu inea p ig ; 5 specimens, ranging in age from approz imate ly three moa ths t o six: and one-half m o n t h s )

Although irregular spaces and fissures were found frequently, well-formed synovial cavities with smooth walls were present only in the first joints. Here the sternal notch and costal cartilage end were flattened (fig. 17). Close to the surface of the cavity the lacunae were sparse, and medial to the sternal surface in a wide basophilic zone were a number of very large, scattered lacunae containing as many as 8 acidophilic cells.

In the second, third, and fourth joints the appearance of the interzone and disc tissue was distinctive at each level. Extensive regions of degenerated, chromophobic tissue formed what seemed to be potential cleavage planes in various parts of the intersternebral disc and sternochondral joints. At the second costal level, such regions were found in the lateral parts of an H-shaped area of cartilage (fig. 18). The cross bar of the H traversed the disc and the uprights curved around the medial ends of the costal cartilages. Fissures appeared at intervals in the regions of degenerated tissue. I n some areas where the chromophobic regions were discontinuous, small discrete clumps of similar degenerated tissue were found at intervals.

The third sternochondral joints resembled the second, although the dimensions of the joints were smaller in relation to the total size of the disc. At the fourth costal level the disc was wider and thinner than at other levels and its cartilage was homogeneous, lacking a transverse band. Many of the acidophilic cells of the interzones were contained in giant lacunae such as those previously encountered. In some joints, cavities appeared peripherally beneath the capsule. In the fifth and sixth sternochondral joints the areas of

286 MARIAN WILLIAMS

degenerated tissue marking the juncture of the costal cartilages and sternum were located far medially in what appeared to be the substance of the sternum.

M u s musculus (mouse; 8 specimens, ranging in age from 5 days to over one year )

No true joint cavities were found. Irregular fissures appeared around the medial ends of the costal cartilages in some of the sections, but these were believed to be artifacts. The interzones were made up of hyaline cartilage. The lacunae were usually small and most often appeared in rows which were arranged concentrically around the medial end of the costal cartilages. The lacunae in the medial end of the costal cartilage became smaller toward the joint and the ground substance increased in basophilia. The cartilage of the interzone and adjacent disc was particularly basophilic (fig. 19).

R a t t u s ra t tus ( ra t ; 4 specimesns, three of which were 23 weeks old; t he age of the f o u r t h was mot know%)

Cavities were present in the form of narrow fissures in the caudal portion of the first sternochondral joints. These small spaces were shaped like an inverted “v” and contained a fold of connective tissue which projected into them from the caudal margin. A few very limited peripheral cavities with synovial folds were seen in the more caudal sternochondral joints.

Mesocricetus au,ratus (hamster; 4 specimems, three of which were 20 weeks old; the age of t he f o u r t h was mot known) There were no complete joint cavities in the specimens

studied. However, in many instances in the third to seventh joints there were extensive peripheral cavities (fig. 23). Some of these spaces extended for a considerable distance laterally along the costal cartilage. The medial part of these cavities extended around the sternal end of the costal cartilage for a short distance so that a notch-shaped space was formed between the costal cartilage and the adjacent sternebra. A synovial fold often protruded into the cavity.


The costal cartilage increased in basophilia toward its medial end and the lacunae became smaller (fig. 22). The sternochondral interzone was deeply basophilic and contained lacunae which were usually small and arranged in rows aligned concentrically around the end of the costal cartilage.

Dipodomys sp. (kangaroo rat; 4 adult specimens)

Well-formed cavities were present in many of the second to fifth sternochondral joints. The most frequent site was in the third joints, where cavities or fissures appeared bilaterally in each specimen. The joint cavities were usually crescent- shaped, although occasionally the sternal notch appeared slightly angular and the end of the costal cartilage was pointed. The walls of the cavities were of hyaline or fibrocartilage on the costal side of the cavity. The cells of the sternal notch cartilage were markedly flattened and acidophilic. The first, sixth, and seventh sternochondral joints consisted of continuous hyaline cartilage with little modification of the cells and ground substance at the joint.

Sciurus niger ( f o s squirrel; two adult specimens)

?So complete sternochondral joint cavities were present. However, well-formed peripheral cavities appeared in the 4th to 7th joints of one specimen (fig. 21). At these levels the costal cartilage was broad toward its medial end and then it narrowed abruptly before uniting with the sternum. Where cavities were present, the notchlike space surrounding the cartilage union was enclosed by a capsule, and an extensive synovial fold projected inward in most instances. The cavities on the cranial side of the 7th joints appeared to be particularly large ; the right space contained degenerated fibers.

Aplondontia rufn (mou.ntai.12 beaver or sewellel; one adult specimen)

There were well-formed cavities in all the sternochondral joints. The space in the first joint was narrow and the walls

288 MARIAN WILLIAMS

were flattened. The cranial portion of the slit-like cavity was enclosed by a thick fibrous capsule ; caudally the capsule was thin and surrounded an area of fatty tissue. A large synovial fold extended into the joint space from the caudal margin. I n the second, third, and fourth joints, the general shape of the hyaline costal cartilage extremity and sternal notch resembled that of the fourth through sixth joints in the gibbon. The cavity extended for a distance along the side of the adjacent caudal sternebra. The walls of the space were lined by a thin amorphous, chromophobic layer in many sections. Syn- ovial folds extended into the joint space from both the caudal and cranial margins.

Calzis familiaris (dog; two specirnelzs of appror;imately 4 months )

Complete cavities were found in several sternochondral joints of one specimen ; most of these were in the more cranial joints. I n the other specimen, only the fifth joint cavities were complete, although several joints located farther cranially had incomplete spaces.

In the joints with complete cavities, the sternal notch and the costal cartilage surface were congruent (fig. 26). A narrow region of the articular cartilage on either side of the cavity differed from the surrounding tissue which was basophilic to an unusual degree in the dog. The surface layer was char- acterized by decreased basophilia and small, sparse cells. De- generated, chromophobic tissue lined the cavity in a thin, irregular layer, and synovial folds frequently extended far inward from both the cranial and caudal sides of the joint.

In several joints, well-formed cavities were present which were not complete. Spaces appeared in the caudal portion of the first joints of both animals. A long fissure extended cranially from these inverted v-shaped spaces and a fold of synovial tissue was present caudally.

A few joints had the appearance of having been arrested in the process of cavitation. Here fissures extended inward

MORPHOLOGY O F STERNOCHOBDRAL JOINTS 289

from the periphery between the costal cartilage and sternum (fig. 25).

Felis domesticus (cat; three adult specimens, two o f one year and one of 8 years;

two specimens of 6 weeks)

A complete joint cavity was found only in the eighth sternochondral joints of the 8 year animal. Elsewhere cavities were seen frequently at the periphery of the joints. These notchlike spaces around the costal cartilage extremities were commonly present only at either the caudal o r cranial margin and usually contained a synovial fold which extended inward from the capsule (fig. 27). Such peripheral cavities were extensive and occurred most frequently in the articulations toward the caudal end of the sternum.

In the third to seventh joints of both young and adult animals, a large triangular basophilic region containing a criss- cross arrangement of cartilage elements often was present medial to the costal cartilage (fig. 29). This pattern resembled the arrangement at some costal levels in the squirrel; in both species whitish fissures which were presumed to be preparation artifacts were present between the fibers where they were interlaced at the apex of the triangular re,' mion.

Extensive peripheral joint cavities were found in many of the eighth and ninth joints, usually in the cranial portions. In several ninth joints the cartilage differed very little from that of the adjacent sternum and costal cartilage. In the one instance where a complete cavity appeared bilaterally in the eighth joints, its borders were fibrous and irregular and the articular surfaces gave the impression of degeneration. No synovial membrane was evident.

Felis tigris (tiger; one specimen of advanced age)

All the sternochondral joints had complete synovial cavities. The fourth, eighth and ninth right joints were sectioned and stained f o r histological study. I n these joints a narrow strip

290 MARIAN WILLIAMS

of basophilic hyaline cartilage bordered the cavity on either side. The arrangement of the lacunae varied; in a few areas the rows were aligned perpendicularly to the joint surface and fibrous bundles were evident between the rows.

Equus caballus (horse; one adult specirnew)

All the sternochondral joints had synovial cavities. The central portion of the first joint was sectioned. The greater portion of the surfaces of the first joint consisted of hyaline cartilage. At the periphery of both the costal cartilage end and the sternal facet, near the attachment of the capsule, the hyaline cartilage merged into a small area of fibrocartilage. The fibrocartilage of the costal extremity extended farther inward along the joint surface than did that of the facet, so that in some regions of the joint the fibrocartilage of the costal surface lay opposite the hyaline cartilage of the facet.

Bos sp. (cow; two adult specimelzs)

All the sternochondral joints contained synovial cavities. The second and fifth joints were sectioned. In a distinct zoiio bordering the surface, the cartilage of both articulating elements decreased in basophilia. The edge of the lighter marginal zone on the side away from the cavity was very irregular, especially in the sternal articular cartilage.

Ovis sp. (sheep; two young specimens)

All of the sternochondral joints of both specimens had synovial cavities. Portions of the second, seventh and eighth joints of one specimen were sectioned. The cavity of the second joint communicated with a well-formed joint space between the manubrium and the first sternebra in each specimen. I n some of the sections obtained from the second joint, no fibers crossed between the end of the costal cartilage and the sternum, so that the sternochondral joint cavity was continuous with the manubriogladiolar cavity. The hyaline cartilage bordering

MORPHOLOGY O F STERNOCHONDRAL JOINTS 291

the niaiiubriogladiolar joint was similar in appearance to that of the second sternochondral joints.

The articular cartilage of the seventh and eighth joints resembled that of the second joint, although in some itreas the cartilage bordering the cavity was less basophilic and the cells of the costal surface less flattened than in the second joint. The joint elements were congrucnt (fig. 30).

Sus scrofa ( p i g ; t w o adult specimens)

All the sternochondral joints present in both specimens had synovial cavities. The central part of the fourth and fifth joints of one specimen were sectioned. In the hyaline costal cartilage adjacent to the joint surface, the lacunae were closely packed and were grouped in small clusters. With the exception of tlic area near thc sternochondral joint, the costal cartilage contained cells grouped in lacunae which were surrounded by a wide zone of matrix deeply basophilic in character. The ground substance between these chondrones was lighter. The articular surfaces wcrc less basophilic than the surrounding area.

Diclelphis virginicincr (Virginin opossum ; two adult specimens)

Although the costal cartilages of the second to fifth ribs approached the sternum at the discs between adjacent sternebrae, they were attached primarily to tlir cranial stcrnebra in each case (figs. 31, 32). The costal cartilage was often separated from the sternebra on its caudal side by a space which was continuous with a transverse fissure crossing the middle of the interstcrnehral disc between the medial ends of the costal cartilages.

One specimen contained only peripheral cavities in the cranial portion of the sternochondral joints. I n the other specimen, partial cavities were present bilaterally in the fourth and fifth joints. The sixth right joint in one specimen had a complete cavity which was riot crossed by strands. Most of

292 MARIAN WILLIAMS

the caudal joints in both specimens had peripheral cavities on the cranial side beneath the capsule. These spaces were frequently filled with a large synovial fold or with degenerated fibers arid cells resembling similar tissue seen in the guinea pig.

DISCUSSION

Variation in the occurrence and distribution of synovial cavities such as that found in the sternochondral joints of man was seen in the monkey, dog and rabbit. In these genera the incidence of synovial cavities decreased caudalward, which parallels the findings in man (Tschaussow, 1891 ; Musgrove, 1892; Gray and Gardner, '43). Right and left joints at any given costal level were fairly similar in the monkey and dog but varied in the rabbit. I n the rabbit there were instances in which a complete synovial cavity had formed on one side while no evidence of cavitation appeared on the opposite side.

Among the species studied, there appeared to be some relation between the size of the animal and the development of synovial cavities. In general, the larger animals were found to have well-formed cavities while only peripheral spaces or no cavities were present in many of the smaller animals. Exceptions were the full set of cavities in the bat (Myo t i s ) arid the absence of complete cavities in the cat. Data from many additional individuals and species would be necessary to clarify this point. In a few instances, distinctive arrangements of the joint

and disc elements appeared which were peculiar to a given species and to a certain costal level. Outstanding examplcs were the joints of the gibbon and the joints and intersternebral discs of the guinea pig. Broadly speaking, however, there was basic similarity in appearance of the joints of the various species studied. Where cavities were lacking, the articular cartilage was usually basophilic and contained small, flattened cells which lay with their. long axes parallel to the joint. Where peripheral cavities were present there were similarities in form among certain species.

M O R P H O L O G Y O F S T E R N O C H O N D R A L J O I N T S 293

Pcripheral cavities of the myomorpha (hamsters, rats) and of the chinchilla extended primarily in a transverse direction along the costal cartilages. In the squirrel and cat, a large notch-like space circled the medial end of the costal cartilage and extended into the side of the sternebrae; a synovial fold usually protruded into this cavity from the capsule. These cavities were found primarily in the caudal joints. Partial cavities in the sternochondral joints of the opossum sometimes extended far inward between the articular elements so that it was difficult t o determine whether or not these spaces should bc considered peripheral. Thc large number of peripheral synovial cavitics observed, especially in the rodents, may account f o r reports in thc literature of complete synovial cavities which were not substantiated by present findings (Anthony, 1898 ; Reighard and Jennings, ’01 ; Bradley, ’48). I t is possible that with gross inspection, particularly of small specimens, such peripheral cavities might be mistaken for complcte spaces.

Cavities which lacked smooth walls and a synovial membrane were found in many instances. Frequently in a given joint such an amphiarthrosis appeared in part of the articulation while the remainder of the cavity was diarthrodial, with smooth walls and a well-formed synovial fold. This arrangement, which was typical of the fourth to sixth joints of the gibbon, is of interest in view of divergent opinions regarding joint formation. Schulin (1879) maintained that an amphiar- tlirosis is distinct from a diarthrosis and that these two types undergo parallel development. Luhosch ( ’10) supported this vicw, contending that the definitive form of the joint depends on the inherent tendency of the interzone tissue. On the other hand, Lushka (1855) believed that the “unfinished” appearance of an amphiarthrosis represents an arrested stage of development before diarthrosis is achicved. Pohlman ( ’33) and Dziallas ( ’52) also described sternochondral ampliiar- throses as joints whose cavities had remained at an early stage. The latter vicw would seem to be supported by the

294 MARIAN WILLIAMS

present findings, in which there was considerable variation among individuals in the form of the joint cavities observed. The “hereditary tendency” theory is particularly questionable in the light of cavities which are partly diarthrodial and partly amphiarthrodial. Aging and degeneration is another possible explanation which has been suggested for cavities with irregular walls.

Nearly all the sternochondral articular surfaces appeared to bc remarkably congruent in the specimens prepared for this study. Even in instances in which the curvature of the sternal facet was somewhat complex, as in the mid-sternal joints of the gibbon and mountain beaver, the costal cartilage configuration fitted it closely. It is possible that movement is so limited in the sternochondral joints that these articulations may ap- proach the “geometrically pure’’ configuration said by Bu- bosch (’ lo) never to occur in animal forms. The requirements of shape of the articular surfaces necessary to adapt the joint for weight-bearing and extensive motion (Walmsley, ’28 ; MacConaill, ’32) do not apply to the joints of the thorax. Furthermore, the demands of lubrication, to which Haines ( ’47) attributed the need for incongruence, can apparently be satisfied in the case of relatively congruent articular surfaces.

The sternochondral joints were examined to determine whether any difference in form might be found which could be related to the presence or absence of an intersternebral disc. I n several specimens a portion of the sternal body had fused into a bony unit, while in the remainder of the body cartilaginous discs still separated the sternebrae (mole, mouse, cat). I n each instance there was no apparent difference in the joints at the level of discs and those adjacent to a solid plate of bone. An area of hyaline cartilage always bordered the joint on the sternal side, and whether this tissue was limited to the region of the joint or whether a cartilaginous strip extended transversely across the sternum did not affect the joint structure. In a number of instances, after intersternebral discs had

MORPHOLOGY O F STERNOCHONDKAL J O I N T S 295

disappeared and the sternal body had become synostosed, a bony spicule extended partially or completely across the marrow cavity between the costal cartilage ends at the site of the former disc.

The first sternochondral joints in many species were found to differ in form from the remaining joints, as is the case in man. Where partial cavities were present (dog, chinchilla, and one specimen of cynomolgus and rabbit), the first joint space was shaped like an inverted ‘ ‘v’ ’ and occupied the caudal part of the articulation. The sternal facet was likewise flattened in those first joints which had complete synovial cavities. The first sternochondral articulations of nearly all the individuals in 11 species (487%) were synchondrodial. The joint structure here varied from well defined interzones to continuous unmodified hyaline cartilage extending between the costal and sternal elements. Ruge (1880) reported that in the development of the human sternochondral joints there is frequently a very early separation of the first rib from the sternal bar, which is soon followed by fusion. This segmentation mas said to take place phylogenetically first and then to be repeated ontogenetically. Ruge quoted Hoffman who believed that the division is an “inherited factor,” as in most mammals the first rib is united with the sternum in a “jointed” fashion (“gelenkig”). If this is interpreted to mean that the first union is diarthrodial in a large majority of mammals, the findings in the present study do not support Hoffman’s observations.

The articular surfaces of the sternochondral joints observed were nearly all of hyaline cartilage. Fibrocartilage was present in some joints of the gibbon, monkey and mole. Fibrous areas were seen in the cartilage of certain first joints, cranial to partial cavities. Small regions of fibrocartilage were found near the attachment of the capsule in joints of the horse and sheep. On the basis of these findings, no species could be recommended as a favorable source of material f o r the study of fibrocartilage development. However,

296 MARIAN WILLIAMS

for this purpose it might be profitable to investigate specimens of more advanced ages.

SUMMARY

1. The sternochondral joints of 63 specimens, representing 23 genera of 9 mammalian orders, were sectioned, stained and examined microscopically.

2. Complete synovial cavities were present in all the sternochondral joints of approximately one-third of the genera : horse, cow, sheep, pig, tiger, mountain beaver, and one species of bat (Myot i s ) . Cavities were lacking in only the first joints of Afitroxous and in the first and second joints of the gibbon. Genera in which the number of diarthrodial joints was found to be variable, as in man, included the monkey, dog and rabbit ; in these specimens the incidence of synovial cavities decreased caudalward.

3. Peripheral joint cavities with synovial folds were seen in many instances. The spaces were large in the opossum, cat, squirrel and hamster, and limited in the rat, chinchilla and mole. Such cavities often appeared on either the cranial or caudal side of the joint. 4. Amphiarthroses were found principally in species in

which the incidence of sternochondral joint cavities was variable. In some cases amphiarthroses were continuous with smooth-walled cavities which contained a synovial membrane.

5 . Where cavities were absent, the cartilage of the joint was usually basophilic and the cells were flattened with their long axes parallel to the joint; thcse compressed cells were arranged in concentric rows around the end of the costal cartilage.

6. The diarthrodial articular cartilage was nearly always hyaline and contained small flattened cells near the surface. In a few regions, surface cells were rounded or sparse. The costal articular cartilage was usually similar in structure to that on the sternal side, although occasional differences were


apparent in t.he shapc, number and arrangement of the cells. Fibrocartilagc was seen infrequently.

ACKNOWLEDGMENT

The author is grateful to Dr. Donald Gray for criticism and suggestions during the course of this study and in the preparation of the manuscript.

LITERATURE CITED

ASTHONY, R. Du Sterrium et de ses Connexions avec le Membre Thorarique dans la Sdric des M a m m i f h s . L Bourgeon, Lyon.

BRBDLEY, 0. C. 1948 Topographiral Anatomy of the Dog, 5th edition. The Mac- millan Company, New York.

T)ZIALLAS, P. 1952 Zur Entwicklung und Histogenese der Sternokostalverbin- duiigen und Sternalfugen. Zeitschrift f u r Zellforschung und Mikro- skopische Anatomie. Band 37, hefte 2. 127-143.

G R ~ Y , D. J., AND E. D. GARDNER 1943 The human steriiochondral joints. Anat. RPC., 87: 235-253.

HAINES, R. W. 1947 The development of joints. J. Anat., 8 2 : 33-35. LUBOSCH, W. 1910 Rau und Entstehung der Wirbeltiergelcnkr. Gustav Fischer,

Jena. LUSHKA, H. 1855 Ziir Entwickelungsgeschichte der Gelenkc. Muller 's Archiv.

f u r Anat., Physiol. und wissenschaftliche Medicin, 481-488. MACCONAILL, M. R. 1932 The function of intra-articular fibrocartilages with

special referenre to the knee and inferior radio-ulnar joints. J. Anat., 66: 210-227.

MUSGROVE, J. 1892-1893 The eovtosternal articulations. J. Anat. and Physiol., 27: 14.

POHLMANN, 11. 1933 Entwicklung, Wachstum und Altersveranderungen der In - tersternalsynchondrose mit Beruchlichtigung der zweiten Sternocostal verbindung. Ztschr. f. Konstitutionslehre, 17: 641-687.

REIGGTTAED, J., AND H. S. JENNINCS 1901 Anatomy of the Cat. Henry Holt and Company, New York.

RUGE, G. 1880 Untersuchungen iiber Entwicklungsvorgange am Brustbeine und an der Sternoclavicularverbindung des Menschen. Morph. Jahrbuch, 6 : 362414.

1879 Ueber die Entwickelung unci weitere Ausbildung der Gelenkc des menschlichen Korpers. Arch. f. Anat. u. Physiol. Anat. Abth., 3: 240-274.

TSPHAUSSOW, M. Zur Frage iiber die Sternocostalgelenke und den Respira- tiontypus. Anat. Anz., 6: 512-524.

WALMSLEY, T. 1928 The articular mechanism of the diarthroses. J. Bone and Jo in t Surg., 10: 4 0 4 5 .

YOUPTG, J. Z. 1950 The Life of Vertebrates. Clarcndon Press, Oxford.

1898

SCIIULIN, K.

1891

PLATE 1

EXPLbNATION OF FIGURES

1

2

3

4

9

Caudal par t of the sternum and fourth to seventh costal cartilages of a human newborn specimcn. Three-layered interzones are evident at the sternochondral joints. x 1%.

Caudal par t of the interzone between the first left r ib and the manubrium of the human newborn. Fibers crossing the zone curve outward near thc periphery of the articulation. X 27.

Second right sternochondral joint of the human newborn with smooth-walled upper and lower cavities. I n this instance the niariubriuni is joined to the upper sternebra by continuous hyaline cartilage. x 8.

Second left sternochondral joint of the human newborn with upper and lower cavities. Here a fibrous interzone separates the manubrium from the upper sternebra. X 7 .

Seventh left sternoehondral joint of the human newborn in which cavitation has progressed farther in the caudal par t than cranially. x 12.

Stcrnochondral joint cavity and residual interzone in the fourth left joint of a human newborn spwimen. The transverse orientation of cell rows is still discernible in the interzone adjacent to the costal cartilage. Kext to the cavity, the interzone cells are hypertrophied, acidophilic and scattered. Cells of the sternal facet are flattened with their long axes parallel to the cavity surface. Fibers are no longer visible in the interzone tissue.

Caudal par t of the sternum and fourth to seventh pairs of costal cartilages of thc gibbon. A cavity is present i n each sternochondral joint. x 2 $/la. Fourth right joint of gibbon, with a syuovial cavity extendiiig caudally along the sternebra. Basophilic fibers cross the joint cranially and form the margins of the cranial amphiarthrodial cavity. X 11.

Third right joint of the gibbon, with synovinl cavities in both cranial and caudal portions. Medial to the extremity of the costal cartilage is an area of f a t ty and fibrous tissue from which a fold projects into the caudal space. X 13.

x 80.

298

MORPHOLOGY O F STHRXOCHONDR.4L J O I N T S MARIAN WILLIAMS

299

PLATE 2

EXPLANATION OF FIGURES

10

11

12

13

14

15

16

Caudal part of the sternum and fourth to eighth pairs of costal cartilages of the monkey. Well-defined sternochondral interzones are present in this specimen but no cavities. The eighth costal cartilages are separated from the sternum and from each other by a three-layered interzono.

Well-formed fifth left cavity of the monkey, with long villi extending inward. The cartilage near the center of the sternal facet is chromophobic. X 19.

Fourth left joint of the monkey in which iiitra-articular strands separate the cranial and caudal portions of the cavity. The general arrangement suggests somewhat the form commonly found at the second costal level. x 12.

Right and left fifth joints of the monkey, showing congruence of the articular surfaces. A chromophobic zone of cartilage extends medially into the disc from the ceiiter of each sternal facet. x 14.

Sixth and seventh sternochondral joints of the mole, with small peripheral cavities on the cranial sides. Areas of ossification appear toward the inner end of the seventh costal cartilages. X 30.

Second right sternochondral joint of the bat (Hyotis) . The sternal facets are flattened, the costal extremity is pointed, and a large synovial fold extends into the caudal portion of the cavity. x 50.

Fif th and sixth sternochondral joints of Yyotis, in which peripheral enlarge- ments of the cavities beneath the capsule are evident. A synovial fold extends inward from the caudal Dortion of the sixth rieht ioint. X 40.

x 29.

300

PLATE 3

EXPLANATION O F FIGURES

1 7 First right steriioclioiiilral joint of the guiiica pig, with a shallow sternal facet and a syiiovial fold in both the cranial and caudal parts of the cavity. Several very large lacuiiae may be seen in the basopliilic strip medial t o the joint cavity. x 45.

Second sternocbondral joints atid disc of the guinea pig, with characteristic ‘‘11” arrangement of the tissuc3 at the niidtlle of tho diw and adjacent to the costal cartilages. Areas of degeneratccl, chromophobic tissue may be seen in the sternochondral joints and between tho stcrnebrae.

18

X 21.

19 Third costal cartilage attachincnts and disc of the moue ( C 57 BL). Thc cartilage of the sternochondral joints axid intrrsternebral disc is hasophilie. x 75.

Fif th left sternochondral joint of the chinchilla. A very limited peripheral cavity is present on the caudal side. The interzoiie consists of a light area. of liyaline cartilag? bordered by basophilic zones.. X 19.

F i f th left steriiochoiidral joint of the Eastern fox squirrel. A small periphcral cavity is present on the esudal side of the joint. Cells arc sparse in thc car tilage medial to the articulation. X 23.

22 Third stcriiochondral joints of the hamster (Meuocrzcrtus uuratus). The hyaline cartilage a t the joints and between the steriiebrae is basophilic and contains flattcned lacunae. Note the arcas of ossification in the adjaceiit sternebrac. X 58.

Fourth strriiocliondral joiuts of the hamster with peripheral cavities. Herr areas of ossification are present only in the cranial sternebra. x 39.

20

21

23

302

~ I O R P l l O I ~ O G Y OF STERNOCHONDRAL JOINTS MAKId\N WILLIANS

303

PLATE 4

EXPLANATION OF FIGURES

24

25

26

27

28

29

30

31

32

Fourth right joint of the rabbit. The ribs extend far inward into the disc.. I n this specimen there is a notch at the deepest point of the sternal facet, with a few basophilic fibers crossing between the costal cartilage extremity and the lower margin of the notch. x 30.

Second left sternochondral joint of a dog of approximately 4 months. The fissures extending inward around the medial end of the costal cartilage arc lined with a thick layer of chromophobic, degenerated tissue. The cartilage at the middle of the joint and ad jwent to thc fissures is of decreased basophilia. X 14.

Fif th left joint of a 4-month dog, with a well-formed synovial cavity and congruent surfares. The articular cartilage is of decreased basophilia. X 8.

Sixth left joint of a cat of one year. A large peripheral cavity on the caudal side extends laterally along the costal cartilagc. x 17,

Seventh left sternochondral joint of a kitten ( 6 wecks). Rows of cells cross thc joint transversely and a small space is prescnt beneath the capsule on the cranial side of the joint. X 27.

Seventh left joint of a one-year rat. A triangular area of cell row8 and fibers is present medial to the joint, and a peripheral cavity appears on the cranial side. X 31.

Scvmth and eighth left steriiorhondral joints of the sheep. The cavities arc continuous. x 3.

Third right joint of tlie opossum, showing a synchondrial union between the cranial sternebra and the costal cartilage. A few fibers cross the cavity between the costal cartilage arid the caudal stcriiebra. X 20.

Fourth right joint of the opowuni, with a partial cavity extending f a r inward bctween tlie articular elements. Fibcrs cross between thc costal cartilage and sternum farther caudally. A transversc cavity separates thc adjacent sternebrae from one another. X 20.

MORPIIOT~OC~T OF STERNOCHONDRAL J O I N T S >I ARIAN WILL1 AYS

PLATE 4

morphology of the sternochondral joints of mammals

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