Paper - The early development of the mammalian sternum

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Whitehead RH. and Waddell JA. The early development of the mammalian sternum (1911) Amer. J Anat. 12: 89-106.

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In this study, the human embryos provided by Franklin Mall from the Johns Hopkins Embryological Collection later became the Carnegie Collection. These human embryos are a mix of stage 18 and stage 19 embryos.

"The embryos which we found adapted to our purpose were those represented by the serial numbers Carnegie stage 18 424, 17.2 mm long; Carnegie stage 18 296, 17 mm long; Carnegie stage 19 409, 16 mm long; Carnegie stage 18 423, 15.2 mm long; Carnegie stage 19 144, 14 mm long; 175, 13 mm long; and Carnegie stage 18 109, 10.5 mm long. In embryos of less length than no. 109 we were unable positively to identify any sternal anlage."



See also Paterson The sternum - its early development and ossification in man and mammals. (1900) J Anat Physiol. 35(1): 21-32 PMID 17232454
Fell HB. The origin and developmental mechanics of the avian sternum. (1939) The Royal Soc. Series B. 229: 407-463


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The Early Development of the Mammalian Sternum

R. H. Whitehead And J. A. Waddell

From the Anatomical Laboratory of the University of Virginia

Eight Figures

Introduction

In the text-books of human anatomy it is usually stated that the sternum is formed by the union in the median plane of two longitudinal cartilaginous bars, which are derived on each side from a fusion of the ventral extremities of the embryonic ribs; and that, after this union is established, the costal cartilages are segmented off from the sternum with the formation of costosternal articulations. This account is based chiefly upon the studies of Ruge[1] in 1880, although these had to do almost entirely with the sternum after chondrification had begun, that is to say, with a comparatively late stage of development.


The accuracy of this account, with respect to some of its details at least, was first questioned by Paterson.[2] This author describes the sternal anlage in a human embryo 'in the second month' as consisting of an aggregation of mesoblastic cells in the median line of the anterior (cranial) part of the thoracic wall. There is no indication, he says, of bilaterality in the mass. The ventral ends of the clavicles and ribs are composed of cartilage. The first three ribs 'join' the cellular sternum, the fourth and fifth join those above them, while the sixth and seventh have free pointed ends. The meaning of the word 'join' is not entirely clear, but subsequent use of the term in the article indicates that the author does not intend to imply fusion of these structures.


This observation led Paterson to make a study of the development of the sternum in embryos of the rat. In the rat of 9 mm. he finds the sternal anlage as a structure quite similar to that just described in the human embryo - a median mass of cells in the anterior part of the thoracic wall without bilateral subdivision except in front, "where the cells are consolidated into two horns which are concerned with the formation of the clavicles and sternoclavicular articulations and with the anterioi parts of the prester- num." The sternal anlage is not connected with that of any of the costal cartilages. In the embryo 10 mm. long the sternum is still cellular. Here there is added to the single median anlage of the presternum the anlage of the mesosternum in the shape of two strands of cells which diverge caudally. The strands are joined by the ventral extremities of the first six ribs, but, he states, there is an obvious difference between the cells composing the two structures. Later on the two cellular strands unite with each other in the median plane forming an unpaired mass of cells which is connected with the first seven ribs on each side. Ultimately the cartilaginous sternum of the ra1 is laid down as a single median band separated from the clavicles by connective tissue, but in complete fusion with the first seven costal cartilages on each side.


Paterson's observations on the human embryo are probably of little value ; but his findings in the rat led him to challenge the traditional account of the development of the sternum. In a subsequent article[3] he holds that the anlage of the sternum is at first single, median in position, and directly continuous with the mass of cells which is to form the shoulder-girdle on each side ; and that the shoulder-girdle and the presternum are derived from the same elements. This anlage of the presternum bifurcates into two strands, which grow caudalward and become connected secondarily with the ventral extremities of the ribs. Thus in the final analysis, according to Paterson's view the sternum is derived from the shoulder-girdle.


Kravetz[4] has studied the development of the sternum in the pig, using embryos which measured from 24 to 50 mm. in length. In the 24 mm. embryo he describes the sternal anlage as consisting of two bands of condensed mesenchymal cells which are fused with each other at their anterior extremities, while caudally they diverge and extend as far as the level of the ventral extremity of the seventh rib on each side. He denies that there is any true continuity of tissue between the ventral extremities of the ribs, which are in the early stage of chondrification, and the sternal anlage; indeed, the first rib, he states, does not reach the sternal anlage at all. Later on the sternal bands become differentiated into the cartilaginous sternal bars, chondrification proceeding faster in their more cranial portions; and only after this differentiation "tritt eine engere Verbindung der Leisten mit der Ventralenden der Rippen ein." This stage, he thinks, was incorrectly regarded by Ruge as primary.


Finally, Charlotte Mueller[5] in the course of an extensive study of the development of the thoracic walls in man has made very careful observations upon the development of the sternum. In an embryo of 13 mm. she could find no evidence of the sternum, but in one 17 mm. long the anlage was present in the form of two widely separated bands of precartilaginous tissue — the term 'precartilaginous' being used in the chronological and not the histological sense. These bands were connected with each other at their cranial ends by a bridge of less closely aggregated mesenchymal cells. Caudally they diverged and were in direct continuity with the ventral extremities of the first seven ribs, the tissue of the ribs shading off gradually into that of the sternal anlage without any demarcation. In an embryo 15 mm. long she found much the same condition as in the preceding case, except that the bands were not so widely separated, their cranial ends being almost in contact with each other; so that this embryo presented a more advanced stage of sternal formation than the preceding one. In an embrj^o of 23 mm. the sternal bands had fused with each other at their cranial ends in the region of the first pair of ribs. The anlage of the ensiform process was seen here for the first time as a caudal prologation of the sternal band on each side. Histologically the bands now showed chondrification from the level of the first to the fifth rib inclusive, and there was distinct continuity of tissue between the ends of the ribs and the bands, cartilaginous in the more cranial portion, precartilaginous in the caudal part. Her study of the later stages confirms Ruge's account, and need not be reviewed here. From her observations Mueller concludes that the sternal bands originate directly from the ventral ends of the first seven ribs; andshehomologizes the bridge of mesenchymal cells which connects the cranial extremities of the bands in the early stages with the episternum of other forms. ^


From this review of the literature it is seen that the earliest stages of the sternum as observed by Paterson, Kravetz, and Mueller, while not identical, were still very similar; and yet these authors give very different interpretations of their observations. The median portion of the anlage, which Mueller regards as the homologue of the episternum, Paterson considers to be the earliest part of the entire anlage, and thinks that the two sternal bands grow caudalward from it ; this median portion he thinks is derived in its turn from the shoulder-girdle. Kravetz, on the other hand, apparently attaches no special morphological significance to it in the pig. Again, Mueller believes that the sternal bands are derived directly from the ventral ends of the ribs, while Kravetz and Paterson hold that the connection of the bands with the ribs is purely secondary. It has seemed clear to us that none of these investigators has had the earliest stages of the sternum before him, and that justifiable conclusions could be reached only through a study of such stages. Accordingly we have undertaken to find such stages in several mammals.

Material Employed

We have studied first the pig, thinking that the appearances at the cranial end of the anlage would be less complicated in this form owing to the absence of the clavicles; and then have followed this with an examination of corresponding stages in the cat, in which animal the clavicle is a rudimentary bone not articulating with the sternum. Finally we have studied the development of the sternum in human embryos, the clavicle here reaching its full development.

Observations in Pig Embryos

We shall begin the account of our findings by a description of the sternal anlage as presented by a pig 24 mm. long.^ The anlage is first encountered about 12 sections anterior (cranial) to the level of the ventral extremities of the first ribs as an aggregation of mesenchymal cells lying transverse to the median plane of the body. At the level of the first ribs (fig. 1) it is somewhat triangular in cross section, with the apex of the triangle directed ventralward. Each lateral angle of the base is connected with the corresponding first rib. The rib is in an early stage of cartilage formation, but its extremity is capped by a zone of sclerogenous tissue which fades ofT into the sternal anlage without any definite demarcation, that is to say, there is direct continuity of tissue between the anlage of the rib and that of the sternum. In the figure the ventral portion of the triangle is labeled ' median anlage' because, as will appear later, it has a different origin from the more lateral portions. As the series of sections is examined proceeding in the posterior (caudal) direction, indications of a division of the triangular mass can be seen beginning on the dorsal aspect, until, just posterior to the level of the ventral extremities of the first ribs, two somewhat crescentic bands of mesenchymal cells united across the median plane by embryonic connective tissue separate out from the mass (fig. 2). Before the level of the second rib is reached the band changes shape, the con- cavity of the crescent being directed lateralward. From here on the anlage consists of two diverging, uninterrupted bands of mesenchymal cells extending, one on each side, as far as the ventral extremity of the seventh rib. The extremities of these six ribs, as in the case of the first rib, are undergoing chondrification, but each is capped by a zone of sclerogenous tissue the cells of which are entirely similar to those composing the sternal bands; and the anlages of the two structures, ribs and sternal bands, shade off into each other without any definite demarcation. It is worthy of note, however, that while the first rib joins the lateral angle of the triangular portion of the anlage (fig. 1), the remaining ribs join in the concavity of the crescent. This embryo thus presents a stage of sternal formation quite similar to the youngest embryo of Kravetz (24 mm.). Kravetz stated, however, that the first rib did not reach the anlage of the sternum in his embryo ; and he held, moreover, that the connection between the other six ribs and the sternal band was too feeble to have any special significance. To us, on the other hand, this connection seems marked; and we should not feel able from an examination of this stage alone to conclude that the sternal bands either are or are not derived from the ventral ends of the ribs.


All the embryos were fixed in Zenker's fluid, and the measurements were made in 80 per cent alcohol.


Fig. 1 Pig, 24 mm Transverse section at level of ventral extremity of first rib; rl, ventral extremity of first rib; sb, sternal band; 7na, median portion of sternal anlage; pm, pectoral muscle. X 60.


Fig. 2 Pig, 24 mm Transverse section caudal to ventral extremity of^firgt rjb; r/, first rib; -sb, sternal band; pm, pectoral muscle. X 60.


A considerably younger stage was found in a pig 20 mm. long. Here the pericardial cavity extends into the neck, and the ventral extremities of the ribs are separated by a greater interval than in the preceding embryo. A section anterior to the level of the ribs shows that in this region the sternal anlage consists of three parts : the sternal band on each side, and a wide band of less condensed mesenchyme reaching across the median plane and connecting the two sternal bands with each other (fig. 3). The latter are made up of more densely aggregated cells, and consequently appear darker in the stained sections. The anlage in this stage differs from the appearance presented in the preceding embryo mainly in two respects: 1. The sternal bands exist as separate structures well in advance of the ventral ends of the first ribs. 2. There is a median portion of the anlage consisting of less densely aggregated mesenchymal cells connecting the cranial extremities of the sternal bands anterior to the level of the ribs. In other respects there is no essential difference. The sternal bands still extend as diverging, uninterrupted strands of cells along the ventral extremities of the first seven ribs, and are in direct conti- nuity with the tips of these ribs. The condition of the anlage in this embryo seems to accord very well with Mueller's description of the youngest stage found by her in the human embryo. So that in the two embryos just described we have encountered stages practically identical with the youngest stages described by those who have studied the subject before us. But, as we have seen, these stages are susceptible of very different interpretations, and accordingly we have sought for still younger stages.


Such a stage was found in an embryo 22 mm. long. In this pig the sternal bands are still quite distinct anterior to the level of the first ribs but the median portion of the anlage is less well developed. There is an appreciable thickening of the mesenchyme in the region mentioned, but it is not so well defined as in the preceding embryo. The pericardial cavity reaches into the neck and separates the first rib and sternal bands of the two sides. As one proceeds caudalward through the series he is struck by the fact that the ventral extremity of the first rib falls short of the sternal band, and is connected with it only by embryonic connective tissue. Fig. 7 shows the corresponding stage in the cat. The ventral extremity of the second rib approaches the band more closely, and the evidence as to continuity is not so clear as in the case of the first rib; but, if there be any continuity of tissue between the ventral extremity of this rib and the sternal band, such continuity is very slight. The remaining ribs, however, third to seventh inclusive, present the same continuity of tissue between their tips and the sternal bands as was noted in preceding stages. In the more cranial portion of the band, the longest diameter in the cross sections is dorso-ventral in direction, whereas posterior to the level of the second rib this dorso-ventral diameter is much reduced, and the bulk of the anlage tends to lie ventro-lateral ward from the tips of the ribs; moreover, the band becomes considerably reduced in size in its posterior portion.


Fig. 3 Pig, 20 mm TransveiTse section 10 sections anterior to level of 1st rib, right side; mxt, median plane of body; s6, sternal band; ma, median portion of anlage; pw, pectoral muscle. X 60.

Fig. 4 Pig, 18 mm long. Transverse section at level of 3d rib, right side; tB, ventral extremity of 3d rib; sh, sternal band. X 200.


We find the next stage in an embryo 18 mm. long. Here the pericardial cavity and the heart are well forward in the neck, and the anterior extremities of the sternal bands are widely separated thereby. There is no evidence whatever of the median portion of the anlage encountered in the previous embryos, so that the sternal anlage now consists of the two lateral portions, or sternal bands, alone. These can be traced from a point about 10 sections of 15 microns each anterior to the level of the ventral extremities of the first ribs to the level of the seventh ribs. Each band, while it presents about the same structure as in the preceding embryos, is smaller, the aggregation of the cells composing it is less dense, and the band is not so well defined from the sur- rounding mesenchyme. This is particularly true as to the more posterior portion. Still the thickening is quite perceptible, and is uninterrupted throughout. In cross sections the band occupies a position dorsal to the junction of the axilla with the lateral wall of the body, between the pectoral muscle laterally and the pericardial cavity medially. Into this region the ventral ends of the ribs project. They are now entirely free from cartilage, and the cells composing them are very densely packed together, so that the tips of the ribs are very deeply stained in the sections. The first and second ribs fail to reach the sternal band, but the succeeding five are fused with it, and offer the same evidences of continuity with it shown in preceding stages (fig. 4).


In embryos 16 and 15 mm. long the bands were still present, but less clearly defined from the surrounding tissues. In the 16 mm. pig the bands stopped caudally at the level of the fourth ribs; while in the 15 mm. embryo they could be traced no further than the third rib. In both cases the first and second ribs failed to reach the band. In embryos of less length than 15 mm. we were not able to detect any sternal anlage with certainty. There could be found a thickening of the mesenchyme in the region occupied by the band in embryos 15 and 16 mm. long, but it was too poorly defined to allow us to differentiate it from surrounding tissues. Judging from the behavior of the ventral extremities of the first and second ribs in somewhat older stages, w^e think it probable that a stage exists in which no rib is connected directly with the sternal band, but we were unable to detect such a stage.


To recapitulate : We first find the anlage of the sternum as a blastema occupying a region on each side of the body dorsal to the juncture of the axilla with the lateral bodj^ wall between the pectoral muscle laterally and the pericardial cavity medially. At first the blastema is found only in the more anterior portion of this region, reaching as a column of cells from a point well anterior to the level of the first rib as far as that of the 3rd rib on each side in embryos 15 mm. long. It extends rapidly in the caudal direction, so that in the embryo 18 mm. long it reaches as far as the level of the ventral end of the seventh rib. It is uninterrupted throughout its entire extent. Into the region occupied by these sternal bands the ventral ends of the growing ribs project, and soon fuse with the sternal anlage. At first they are not cartilaginous, but are composed entirely of sclerogenous tissue in embryos 18 mm. long. In the earliest stages the first and second ribs do not reach the sternal anlage ; it could not be determined whether or not this is also true of the more posterior ribs of the series. However, at the time the embryo is 20 mm. long the ventral ends of the first seven ribs are firmly fused with the sternal band on each side. At first, owing to the projection of the heart into the neck, the two sternal bands are widely separated throughout their entire extent; but as the heart sinks into the thoracic cavity, the bands are allowed to approach each other, the approximation being greatest in the neck, until their anterior extremities finally meet and fuse. Coincident with the sinking of the heart, there appears a third division of the sternal anlage in the shape of a transverse bridge of mesenchymal cells in the ventral wall of the neck which unites the anterior extremities of the sternal bands. As the latter approach each other, this median anlage becomes incorporated with them, and thus assists in the formation of that part of the sternum which lies anterior to the level of the first pair of ribs. At no stage could we detect any evidence of continuity between the sternal anlage and any element of the shoulder girdle.

Observations in Cat Embryos

Our study of the development of the sternum in the cat was made possible by the courtesy of Professor C. F. W. McClure, who gave us the opportunity of examining the beautiful series of cat embryos which form a part of the Princeton Embryological Collection. As the early stages of the sternum in this form agree very well with those already described in the pig, we may make our account brief.


In the cat embryo 18.5 mm. long (series 21) the anterior extremity of the sternal anlage appears as an unpaired, median mass of mesenchymal cells, the cells being arranged more densely on the sides than in the center of the anlage. Just anterior to the level of the ventral extremities of the first ribs the two sternal bands separate out from this median mass, and can be traced as far as the level of the ninth ribs. The ventral ends of the ribs are cartilaginous, but the cartilage is surrounded by a zone of sclerogenous tissue which fuses with the similar tissue composing the sternal bands. Anteriorly these bands lie side by side diverging very slightly until the level of the fourth ribs is reached; but posterior to this region they are separated by the pericardial cavity, and their divergence is more marked. In this posterior region also the bands rapidly diminish in size; and, instead of being crescentic in outline on cross section, they are flattened out so that the long diameter of their sections nearly corresponds in direction with that of the ribs. The clavicles lie almost entirely anterior to the anterior end of the sternal anlage. They contain cartilage, but their medial ends are capped by sclerogenous tissue which is prolonged medialward and caudalward so as to fuse with the sides of the anterior extremity of the sternal anlage (fig. 5). This connection is, however, very slight, extending only through two or three sections (fig. 6). In the progress of development this connection is soon lost. Thus in the embryo 25 mm. long (series 22) there is no connection between the anlage of the clavicle and that of the sternum, and the clavicles lie entirely anterior to the level of the sternum.


The embryo 17 mm long (series 36) presents the same appearances as those just described, except that the sternal bands are more divergent.


In the embryo 16 mm. long (series 64) the clavicles are still connected to the anterior extremity of the sternal anlage in the way previously noted. The sternum extends about twenty sections anterior to the level of the first ribs as an irregularly oval mass of cells less densely arranged in the center. The sternal bands separate out just before the first ribs are reached, and extend caudahvard as far as the eighth pair of ribs. At first they are circular on cross section, but soon become crescentic, and finally are flattened out so as almost to meet each other across the median plane. They are uninterrupted throughout. Under the low power there is an appearance suggestive of a line of demarcation between the sternal bands and the tips of the first and second ribs, but under the high power the two structures - ribs and sternum - appear intimately united.


In the embryo 14 mm. (series 37) and 13 mm. long (series 35) the median portion of the sternal anlage noted in the pig makes its appearance as a distinct structure just posterior to the level of the clavicles. It consists of a band of cells somewhat larger and less compactly arranged than the cells of the sternal bands stretching across the median plane. Its lateral extremities are fused with the anterior ends of the sternal bands about fifteen sections anterior to the level of the first ribs. The sternal bands are widely separated throughout their extent by the pericardial cavity, and diverge markedly. They occupy a position in the sections dorsal to the line of junction of the axilla with the body wall, and extend as far as the seventh ribs. They are united with the ends of these ribs.


Fig. 5 Cat embryo, 18.5 mm. long. Cross section of junction of clavicles with sternum. Princeton Embryological Collection, series 21, slide 13, section 2;c, clavicle; s, sternum; x, connection between clavicle and sternum. X 60.

Fig. 6 Same embryo as in fig. 12. Slide 13, section 5. X 60.

Fig. 7 Cat embryo, 12 mm. long. Princeton Embryological Collection, series 401, slide 10, section 24; r 1, tip of first rib: sb, sternal band; pm, pectoralmuscle; pc, peri-cardial cavity; a, axilla. X 60.

Fig. 8 Transverse section of sternal band and tip of second rib. Embryo no. 109, 10.5 mm. long, Mall collection. Slide 18, section 1, right side; r2, second rib; sb, sternal band. X 250.


In the embryo 12 mm. long (series 401) the heart and pericardial cavity are well forward in the neck, and there is no evidence of the median portion of the sternal anlage. The clavicles are present as a short bar of cells lying far out in each side of the neck, the two being widely separated by the pericardial cavity. The sternal bands still extend as far caudalward as the seventh ribs. The ventral ends of these ribs are now composed entirely sclerogenous tissue. The first three fail to reach the sternal bands (fig. 7) ; it is uncertain if the fourth does, but the remaining three are connected with the bands as in the older embryos.


The embryo 10 mm in length (series 402) which, however, was from the same litter as the previous one, shows no differences with respect to the sternal anlage, except that the clavicles could not be detected, and the sternal bands could not be traced farther than the level of the sixth pair ot ribs.


From this account it appears that the early stages of the development of the sternum in the cat are practically identical with those observed in the pig. There are some minor differences such as the fact that there are nine vertebro-sternal ribs in the cat, and the further fact that there is a rudimentary clavicle in the cat connected for a short time with the anterior end oi the sternal anlage. The presence of this clavicle, however, does not influence the median portion of the anlage, which develops in the same way in both forms.

Discussion and Conclusions

Our findings make it clear that the theory of Paterson, according to which the mammalian sternum begins as a single median blastema which bifurcates and sends a prolongation caudalward on each side, is untenable. For in all three forms studied by us the appearance of the paired portion of the anlage, the sternal bands, antedates that of the median portion.


The evidence is almost as strong against the view of Ruge and Mueller that the sternal bands are derived from the ventral extremities of the ribs. If the formation of these bands is due to the proliferation of cells composing the ventral ends of the ribs, i.e., if they are segmental in the beginning, one would reasonably expect to find in the early period of their development breaks in their continuity; yet we were not able to detect interruptions in any of the many series of the sternal bands in their precartilaginous stages. A much stronger argument than this, however, is the fact that the more anterior ribs did not reach the sternal hands in the earliest stages that we examined. It is undoubtedly true, in our opinion, that continuity of tissue between the ventral ends of the ribs and the sternal bands does exist at an early stage in the development of the sternum; but in the earliest stages in both the pig and the cat such continuity is lacking between the bands and the first and second ribs, while in the human embryo at 10.5 mm. none of the ribs directly reached the sternal band.


As to the derivation of the median portion of the sternal anlage the evidence is not so conclusive. The fact that in both pig and cat embryos this portion of the anlage originates independently of the clavicles enables us to conclude at once that it is not derived from the medial ends of the clavicles. Either of two other inter- pretations, however, seems possible so far as our observations go: (1) it may be formed in situ, or (2) it may be derived from the anterior ends of the two sternal bands by each of them sending a prolongation medialward to join its fellow in the median plane. The fact that we never found this anlage in a paired condition, but always as a single band of cells uniting the anterior ends of the sternal bands leads us to believe that the first interpretation is the more probable.


In conclusion, the conception which we have gained of the early development of the mammalian sternum may be stated as follows: The sternum is developed from three anlagen. First to arise are the lateral portions, the two sternal bands, which make their appearance one on each side of the body wall as a longitudinal blastema dorsal to the junction of the axilla with the lateral wall of the thorax and ventral to the tips of the ribs. The vencral extremities of a certain number of the ribs soon reach this region and fuse with the sternal band. A little later, as the heart begins to sink into the thorax, the third or median anlage makes its appearance as a transverse bridge of cells extending bet ween the anterior extremities of the two lateral anlagen, and the entire blastema now presents the shape of a two-pronged fork. As the heart sinks still more into tne thorax, the anterior ends of the lateral anlagen are allowed to approach each other and soon fuse, the median anlage being incorporated with them.


With respect to the morphological significance of the median anlage, we incline to the view that it is the homologue of the episternum of certain of the lower vertebrates, or, perhaps we should rather say, of the prosternum of the monotremes.


References

  1. Ruge, G. 1880. Untersuchungen ueber Entwicklungsvorgaenge am Brustbein und an der sterno-clavicular Verbindungen des Menschen. Morph. Jahrb. Bd. 18.
  2. Paterson, A. M. 1900. The sternum, its early development and ossification in man and mammals. Jour. Anat. and Physiol, vol. 33.
  3. Paterson, A. M. 1902. The development of the sternum and shoulder girdle in mammals. Brit. Med. Jour., vol. 2, p. 777.
  4. Kravetz, L. P. 1905. Entwicklungsgeschichte des Sternums unci des Episternalapparates der Sauegethiere. Bull, de la Soc. Imper. des Natural. deMoscou. Annee 1905, nos. 1-2.
  5. Mueller, Charlotte. 1906. Zur Entwicklung des menschlichen Brustkorbes. Morph. Jahrb. Bd. 35.



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