Paper - The history of the earliest stages in the human clavicle

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Hanson FB. The history of the earliest stages in the human clavicle. (1920) Anat. Rec. -323.

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This historic 1920 paper by Hanson is a description of the development of the human clavicle.

See also Fawcett E. The development and ossification of the human clavicle. (1913) J Anat Physiol. 47(2): 225-34. PMID:17232952 | PMC1289013

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The History of the Earliest Stages in the Human Clavicle

Frank Blair Hanson

Department of Zoology, Washington University, Saint Louis, Missouri

Four Plates (Thirteen Figures)


The clavicle is one of those elements of the human skeleton concerning which the last word has not yet been spoken..

Beginning with Gegenbaur in 1864, an enormous literature has arisen, the earliest of which would be now of historic interest only, were it not for the fact that the most recent paper on the clavicle (Huntington, ’18) attempts to restore the old Gegenbaurian hypothesis of a cartilaginous precoracoidal core in the human clavicle, thus opening again an old controversy on the origin of the clavicle as a dermal or cartilage element.

The point of interest, then, in this present paper is whether the human clavicle originates in cartilage or as a dermal element or is derived in part from both cartilaginous and membranous elements.

Gegenbaur (’64) considers the clavicle in man to be a pure cartilage" bone; Broom (’99) and Fawcett (’13) claim that the cartilage present has no morphological significance and that the clavicle is as purely a dermal bone as is the dentary; while Paterson (’02) and fitzwilliams (’10) combine these two views, holding that the clavicle is of dual origin, its inner end being formed in cartilage and its outer as a dermal element.

This confusion in the literature of the clavicle is reflected in the text—books of human anatomy and puts new and uncalled-for difficulties in the by no means rosy pathway of the first-year medical student.

Theories of Clavicular Origin

Gegenbaur (’64) thought that he had found the human clavicle developing in cartilage, and probably with the anuran shouldergirdle in mind, claimed that the cartilage present was a remnant of the old precoracoid, thus determining the character of the clavicle as a cartilage bone. It is certainly true that in the frog the precoracoid does enter into and constitute the core of the clavicle, which is overlaid on the anterior side by a membranous element, and it is also true that in many of the mammals the clavicle contains a relatively large amount of cartilage at a fairly early stage. In man the cartilage is of a peculiar kind called by Mall a ‘precartilaginous tissue’ (figs. 4 to 6).

Gegenbaur has been supported in his View of a precoracoidal contribution to the clavicle by Huntington (’l8), and in a private communication to the author concerning the matter Huntington states his position not only on the clavicular complex, but also on the entire shoulder-girdle as follows:

this structure (shoulder-girdle) as a whole represents all the various possible combinations which result from the fact that it develops by the union of two originally distinct and separate elements, the exo skeletal and the primordial cartilaginous girdle, in different degrees in different types.

As regards the clavicle the different proportional amounts of the dermal and cartilaginous contribution is well shown in the difierent vertebrate classes. The process of envelopment of the procoracoid by the clavicle is developed to a widely varying degree in individual

Anure types, up to the complete replacement of the cartilage by an element originally dermal in origin.

In the above statement of Huntington’s is a somewhat plausible explanation of the widely different views expressed as to the constitution and homology of the clavicle. Two distinct "elements, exoskeletal and cartilaginous, have contributed to it unequally in different classes of vertebrates, and even in different genera of the same class. This is apparently the case in the Amphibia and Reptilia, where the cartilaginous and dermal elements Vary from a nearly pure precoracoidal cartilage bone to a purely dermal bone such as that found in many of the reptiles.

The hypothesis of Gegenbaur and Huntington has much to recommend it at first sight and does seem to account for the variations met with in the clavicle of the different groups of vertebrates by the inclusion of a greater or lesser amount of the cartilaginous precoracoid into this element. Assuming that the coracoid process of man is the homologue of the metacoracoid or posterior coracoid of Permian reptiles and the precoracoid to be the cartilaginous part of the clavicle, a most direct and beautiful homology can be drawn between the shoulder—girdle complexes in the frog and man, for which comparison examine figures 1 to 3.

However, as Watson (’17) remarks, the anuran shoulder-girdle is of totally unknown ancestry, and the group as a. whole being characterized by extraordinary specialization, any comparisons between the frog and other forms are very hazardous and should receive most careful checking and corroboration. And this is especially true in a comparison with the human shoulder—girdle so long as the homology of the coracoid process is still in doubt. Further on I shall attempt to show that the coracoid process is the homologue of the precoracoid rather than the metacoracoid, and, if this be true, the theory of Gegenbaur and Huntington is no longer tenable.

Broom (’99) was the first to cast doubt upon Gegenbaur’s hypothesis. He claimed that, while cartilage was present in the clavicle, it did‘ not appear until after ossification had begun in the dense connective tissue, and concluded therefore that the clavicle was a purely membrane bone. Broom examined a numBer of marsupials, reptiles, and other Tetrapoda, including man, and found that in all these ossification of the clavicle preceded the appearance of true cartilage cells.

Mall (’06) studied by the Schultze method of clearing, the ossification centers in an extensive series of human embryos less than 100 days old. He was the first to announce the dual origin of the clavicle from two distinct centers of ossification, a medial and a lateral. Mall did not, however, give an opinion on the significance of these two centers.

Fawcett (’13) examined a series of human embryos sectioned transversely and otherwise, andifound in serial sections the two centers of ossification Mall had seen in cleared specimens. Ossi— fication began in the outer end of the inner half of the clavicle and in the inner end of the outer or acromial part of the clavicle. No cartilage cells were present until after the appearance of these two ossified centers. At this stage the inner and outer parts of the clavicle had no connection, but were separated by the investing perichondrium. In the 19-mm. stage (crown-rump measurement) a bony bridge develops and connects the two centers (figs. 6 to 9).

Another important point made by Fawcett is that the connection of the coracoid-clavicular ligament is always with the acromial half of the clavicle, and not, as fitzwilliams (’10) thought, with its sternal end. In cases of cranio-cleido-dysostosis _fitz_williams found a ligament connecting the inner part of the clavicle with the base of the coracoid process. He identified this as the coracoid-clavicular ligament and urged that it was in cases of this disease a prolongation of the coracoidal contribution to the sternal part of the clavicle. That fitzwilliams is incorrect in his identification of this ligament is beyond all doubt, as is shown very clearly in figures 6 and 7. In all the specimens I have examined in the Mall Collection, the coracoid-clavicular ligament extends from the acromial half of the clavicle to the coracoid process, and Fawcett found the same thing in his material. Watson (’17) publishes a photomicrograph of a cross-se'ction through the shoulder region of the marsupial Trichosurus, which shows that in this group also, as in the primates, the coracoid-clavicular ligament is attached to the acromial part of the clavicle.

It is admitted by all investigators that at a comparatively early stage cartilage does appear in the clavicle _in considerable quantity and contributes to the ossification process. The question seems to hinge on the amount and character of the cartilage present and whether this has morphological significance such as is attributed to it by Gegenbaur, Huntington, fitzwilliams, and Paterson or is merely a neomorph comparable to the cartilage in the mandible and other membrane bones (Broom, Fawcett, Watson).

Paterson has a number of papers on the shoulder-girdle and has briefly stated his views on the homology of the clavicle in his 1902 paper as follows: that the clavicle possibly contains more than one morphological unit (judged by its ossification, directly in the outer part, indirectly through cartilage in the inner part).

Fitzwilliams (’ 10) also maintains that there are two distinct elements involved in the origin of the clavicle, one is a dermal element and is confined to the outer half of the clavicle, while the other is cartilaginous and represents the precoracoid of the lower forms. His arguments for the dual origin of the clavicle are the most complete and strongest on that side of the question. They may be summed up as follows:

a. There are two centers of ossification present in the clavicle, and this may well indicate that the bone is a composite one and may be traced back to_ dissimilar elements in lower forms.

b. It is pointed out that the inner end of the element is a round bone, and here is found the greater amount of the cartilage present. Round bones are, in general, cartilage bones, and this argues in favor of the inner half of the clavicle being of cartilage origin. On the other hand, the outer half is flattened and has more the characteristics of the flat bones of the skull which are membrane bones. The first center of ossification also appears in the outer half and is well advanced before cartilage appears.

c. The disease known as cranio-cleido-dysostosis attacks membrane bones principally, and when present in the clavicle the outer part is usually the one affected, while the inner half remains normal. This again points to the inference that the outer half of the clavicle is of membranous origin, the inner half cartilaginous.

d. There is, after all, a rather large deposit of cartilage present in the developing clavicle, and as this cartilage enters into and becomes a part of the bony product, it may have had an ancestral history.

e. The above points are emphasized by the known conditions in the Anura, where the precoracoid becomes the cartilaginous core of the investing dermal tissue, the two elements quite clearly uniting to form the anuran clavicle.

f. The clavicle, therefore, according to this point of View, is the result of two interacting tissues, one a dermal element and the other cartilage, which contribute unequally in the different classes of vertebrates to this structure, so that investigators finding one or the other elements greatly in excess in the form immediately under observation were led to take such divergent views as above indicated. . '

The three theories of clavicular origin now in the literature are set forth with their respective sponsors in the following table:


Broom (’99) . . . . . . . . . . . . . . . . . . .. *

Fawcett (’13) . . . . . . . . . . . . . . . . . . . *

fitzwilliams (’10) . . . . . . . . . . . . . . . _ *

Gegenbaur C64) . . . . . . . . . . . . . . .. '*

Gotte (’77) . . . . . . . . . . . . . . . . . . . . . *

Hoffman (’79) . . . . . . . . , . . . . . . . . . *

Huntington (’18) . . . . . . . . . . . . . . . *

Paterson (’02) . . . . . . . . . . . . . . . . .. *

Watson (’17) . . . . . . . . . . . . . . . . . . . * OBSERVATI ON S

Recently I have had the privilege of examining the cleared specimens of human embryos upon which Mall (’O6) based his paper on ossification‘ centers, and also have studied the earliest stages of the clavicle in the splendid collection of serial sections of human embryos in the Carnegie Laboratory of Embryology at the Johns Hopkins Medical School} My purpose was to determine, if possible, between the View of Broom and Fawcett that the human clavicle is a pure membrane bone, and that of

other investigators who see in the clavicle a persisting remnant of the old precoracoid.

1 It is my pleasure to acknowledge the courtesy extended me by Dr. George L. Streeter, of the Carnegie Laboratory of Embryology, in placing the facilities

of the laboratory and the series of human embryos in his charge at my disposal during the summer of 1919.

So far as I an1 aware, there was no prejudicial bent of mind toward either theory, and I am not committed to either side of the controversy by any statement in my published papers on shoulder-girdle problems.

The result of my examination of all the evidence available may be summed up briefly as follows:

A. The material at my command, the Mall Collection, than which there is no better or larger collection of human embryos anywhere to be found, confirmed in all essential particulars the observations of Broom and Fawcett. Ossification begins approximately about the thirty-ninth day and is by two -distinct centers, one in the lateral half and one in the medial half of the clavicle. At this time the bony centers are surrounded by the ‘peculiar precartilaginous tissue,’ which certainly is not hyaline cartilage. It seems quite clear that the earliest stage of 0ssz'ficat2'on in the clavicle, both in its medial and lateral halves, is a dermal ossification, and that cartilage is entirely lacking at the time of the appearance of the two centers of bony tissue. This one fact was sufficient to justify Broom and Fawcett in excluding the precoracoid as a morphological element of the human clavicle (figs. 10 to 13).

B. In addition to the confirmation above, my special contribution to the "subject consists in an attempt to show that the precoracoid has a history so different from that contemplated by those who see in the cartilage the old precoracoid, that this cartilage could not possibly be that element. I have traced the history and homologies of the precoracoid recently (Hanson, Anat. Rec., vol. 19), and the conclusions therein set forth may be recapitulated briefly here.

  1. It has been shown by Broom for Australian marsupials, and the author for the American opossum, that in the embryo and fetus of these forms the shoulder—girdle consists of a scapula, clavicle, and two coracoid elements, one of which, the posterior (fig. 2), extends from the scapula to the sternum and is comparable directly with the coracoid of the monotremes. The anterior element of the marsupial fetus is a broad fan-shaped sheet of mesenchyme, of short duration in embryonic life, and is the homologue of the epicoracoid of monotremes.
  2. Development shows that the posterior of the two coracoid elements of the fetal marsupial girdle becomes the small rudimentary coracoid process attached to the scapula in the adult. which process undoubtedly is homologous with the same-named process in man. This gives a clear line of genetic relationship from the coracoid process of man to the posterior element in the girdle of the monotremes.
  3. Gregory and Camp (’18) and the author have shown that the conditions in the monotreme girdle are so clearly reptilian in character and approximate so closely in every respect to the structure of the girdles in Sphenodon and lizards that genetic relationship and homology exist between them.
  4. Williston (’11) has practically demonstrated that the coracoid of living reptiles is derived from the anterior bony co1'acoid element (precoracoid) of Permian reptiles.
  5. Therefore, if the coracoid process of man is the same element as the posterior coracoid of monotremes, and this latter is directly comparable with the posterior of the two coracoids of Sphenodon and lizards, which is in turn a derivative of the precoracoid of Permian reptiles, then the coracoid process of man equals the anterior bony element of Permians, and the precomcozfd is the true coracoid.
  6. It seems to be pretty well established that the coracoid process of placentals is a precoracoid, so that this bone is fully accounted for without reference to the clavicle. It might be suggested that the part of the precoracoid which has aborted is the piece found in the clavicle, but it has been shown clearly by Broom that the clavicle is fully formed and contains its maximum amount of cartilage long before the degeneration of the precoracoid, i.e., the fully formed precoracoid extending from scapula to sternum (fig. 2) persists for a considerable time after the ossification of the clavicle has begun and the cartilage at its ends is present. The two, fully formed clavicle and precoracoid, are in marsupials coexistent and separated by a considerable space. There is, therefore, no way for the cartilage of the precoracoid to enter the clavicle in mammals.


The fact that the cells in the early clavicle are clearly not hyaline cartilage cells, but a peculiar tissue of which little seems to be known, coupled with the demonstration by the author that the well-developed clavicle and complete precoracoid extending from the scapula to the sternum are coexistent in the embryo, and the stages of the degeneration of the precoracoid having been followed completely in marsupials by Broom, excluding the possibility of the entry of precoracoidal tissue into the clavicle, apparently indicates that there are pretty solid grounds for considering the human clavicle to be a purely dermal bone.

Literature Cited

BROOM, R. 1899 On the development and morphology of the marsupial shoulder girdle. Trans. Roy. Soc. Edinb., vol. 39. pt. III, pp. 749—770.

Fawcett E. The development and ossification of the human clavicle. (1913) J Anat Physiol. 47(2): 225-34. PMID:17232952 | PMC1289013

FITZWILLIAMS, D.C.L. 1910 Hereditary cranio-cleiclo-dysostosis. The Lancet, Nov. 19, 1910. _

GEGEXBAUR, C. 1861 Ein Fall von erblichem Mangel clcr Pars acromialis Claviculare, mit Bemerkungen fiber die Entwickelung cler Clavicula. Jen. Zeitschrift, Bd. 1.

GOTTE, A. 1877 Morphologie des Skelettsystems der Wirbeltiere: Brustbein und Rcliultergfirtel. Arch. f. Mikr. Anat... Bd. 14.

GREGORY, W. I{., AND CAMP, C. L. 1918 Studies in comparative myology and osteology. No. III. Bull. An. Mus. Nat. Hist., vol. 38.

H01-‘F)IA.\’, C. l\'. 1879 Zur Morphologie des Scliultiergflrtiels und des Brustbeins bei Reptilien, Vfigeln, Sfitlgetieren, und dem Menschen. Niederlancl. Archiv. f. Z00l., vol. 5.

HUNTINGTON. G. 1918 Modern problems of evolution, variation, and inheritance in the anatomical part of the medical curriculurn. Annt. Rec.. vol. 14. no. 6.

Mall FP. On ossification centers in human embryos less than one hundred days old. (1906) Amer. J Anat. 5:433-458.

PATERSON, A. M. 1902 Development of the sternum and shoulder girdle in mammals. Brit. Med. Jour., vol. ‘.2.

WATSON, D. M. 1917 The ‘evolution of the tetrapod shoulder girdle and forelimb. Jour. Anat., vol. 522, pt. 1.

WILLIs'1‘o.\'. W. 1911 American Permian Vertebrates. University of Chicago Press, Chicago.



1 Shoulder-girdle and lateral half of sternum and epicoracoidal cartilages of the bull frog. The precoracoid becomes the cartilaginous basis of the clavicle. In this form the clavicle is derived from two sources, the precoracoid and the dermal ossification.

2 Reconstruction of the shoulder-girdle of a marsupial fetus. Note that the coracoid reaches to the sternum. This is the same coracoid that a little later in development aborts, the only remains of which is the rudimentary coracoid process attached to the anterior side of the neck of the scapula. The complete coracoid is present, however, long after the clavicle is fully ossified, and if this element (coracoid) is the precoracoid, as I hold, there is no possibility of its contributing to the cartilage of the clavicle. After Broom.

3 Schematic diagram of shoulder—girdle of man. Compares pretty closely with figure 1 of the anuran shoulder-girdle. However, the resemblance is superficial only (see text) and not genetic. After Huntington.


Ac, acromian Oss, os suprasternalia CC, costocoracoid ligament 0St, omosternum

Cl, clavicle PCr, precoracoid

C7‘, coracoid R1, first, rib

ECr, epicoracoid Sc, scapula

Ep, sternal epiphysis of clavicle SSC, suprascapula Hiu, humerus St, sternum

I c, interclavicular ligament



4 to 9 A series of stages showing the ossification of the clavicle from two distinct centers. Note that the coracoid-clavicular ligament is attached to the acromial half of the clavicle. This series of figures is modified after Fawcett

and checked in all particulars by a careful examination of a large series of human embryos.

ABBREVIATIONS B, ossification center 0 Cl Lig, coracoicl clavicular ligament Br, bridge of connective tissue between CT, connective tissue two parts of clavicle DT, deltoid tubercle

C, cartilage 0, bony bridge, connects two centers CC, young cartilage cells PC, precartilaginous tissue



10 Photomicrograph of developing clavicle, showing two centers of ossification. This and the following three photomicrographs are introduced to show several stages of the developing clavicle as it actually appears under the microscope. Together with a large number of others, they constitute the basis for the schematic figures 4 to 9 and the conclusions reached in this paper. Series 240, slide 26, section 1. X 29. Mall Collection, Carnegie Laboratory of Embryology.

11 Older stage than above. Outer half of clavicle fully ossified, inner half lags in ossification process and more cartilage is present in this part. Ossification is ectochondrial. Series 460, slide 19, section 7. X 29. Mall Collection, Carnegie Laboratory of Embryology.



12 The two parts of the clavicle are beginning to fuse, Series 1324, slide 26, section 6. X 55. Mall Collection, Carnegie Laboratory of Embryology.

13 Photomicrograph of developing clavicle, showing acromial center of ossification well established and inner center just beginning around the lower outside edge of clavicle, an ectochondrial ossification. Series 240, slide 26, section 8. X 48. Mall Collection, Carnegie Laboratory of Embryology.

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