Paper - The development of the pharyngeal derivatives in the calf (Bos taurus)

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Anderson EL. The development of the pharyngeal derivatives in the calf (Bos taurus). 24(2): 25-38.

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An historic 1922 paper by Anderson studying bovine pharyngeal arch development.

Modern Notes: pharyngeal arch | cow

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The development of the pharyngeal derivatives in the calf (Bos taurus)

The development of the pharyngeal derivatives in the calf (Bos Taurus)

Ethel Louise Axderson

Department of Histology and Embryology, Cornell University, Ithaca, New York

One Plate (Five Figures)


Despite the vast amount of work on the pharyngeal derivatives in many animals, hterature shows but few references to these bodies in the calf, ^'erdun has given a short description of the pharjTigeal derivatives as found in one embryo, 160 mm. in length, together with a reference to a description of a smaller embryo by Woelfier, whose paper, however, is not accessible to the present writer. Groschuff ('96) worked with considerable accuracy on several animals, including the calf, and he has been quoted by a number of authors, among whom are Maurer and Simon. This latter author, whose chief interest was in the fate of the so-called 'lateral th}Toid' (L'ebauche lateral de la glande thjToide), included in the material which he studied more than twenty- calf embryos, none of which were under 20 ram. in length.

It is the purpose of this paper to present the early development of the phar^^lx of the cah with reference particularly to the pharyngeal derivatives. In the parathjToids especially onecan see a peculiarity in development which is apparently quite different from other forms. But brief reference will be made to the general literature; for a detailed review of the early research the reader is referred to the review by Verdun ('98) as well as to the papers of Grosser ('11), Hammar ('11), and Camp ('17). A series of calf embryos, the property of the Department of Histology and Embryology of Cornell University, was placed at my disposal. It consisted of twenty embryos, ranging from 3.5 to 50 mm. in length and cut in transection, and the heads of eight older embryos, 58 to 163 mm. long, which were cut in sagittal section. Twelve frontal or sagittal series of younger embryos were also employed, chiefly for orientation.

The median thyroid

The development of the median thyroid is essentially that described for other mammals. The youngest embryo of the series (3.5 mm. estimated length) shows four branchial pouches, only three of which have an ectodermal contact; the fourth pouch was not observed to reach the ectoderm in any of the embryos which were examined. The 'median thyroid' appears in this embryo as a hollow bud from the floor of the pharynx, in the region just posterior to the first pouch. With the rupture of the 'thyreoglossal duct' (8.5 mm. embryo) the thyroid is left as a short solid cord or plate of cells, morphologically, as at the time of its origin, cephalodorsal to the tinincus aorticus. A sliglit depression on the floor of the pharjmx, the foramen caecum, marks the upper extremity of the duct and the point of origin of the gland. The 8.5-mm. embryo was the only one in which the foramen caecum was evident. The lower extremity of the duct, the 'ductus thyreoideus," extends about 0.12 mm. above the body of the gland.

At about this age (8 to 11 mm.) the lateral expansion of the thyroid is dependent apparently on the growth tensions in the individual embryo, and presents considerable variation. But in every case it has maintained its position on the cephalodorsal side of the truncus aorticus. The ductus thyreoideus can be traced forward sometimes as much as 0.3 mm., depending on the length of the downward shifting and somewhat on the angle of the section. Though the base of the 'duct' is moderately thick, the upper part dwindles down to no more than two or three cells' to the section.

In their expansion the lateral lobes come into close contact topographically, with the derivatives of the caudal pharyngeal complex — the ultmiobranchial body and parathyroid IV In the 14-nmi. embryo the ultimobranchial body lies medial to and close up against the lateral lobe of the thyroid, and in the early stages, when the ultimobranchial body is large, it constitutes nearly the entire lateral lobe, while the thyroid itself is represented by slender cords or plates of cells, loosely strung together by connective tissue, as shown in figures 2 and 4; the median portion of the thyroid is more compact. Parathyroid IV lies median to the dorsal aspect of the lateral lobe, entirely outside of the parenchj-ma of the gland. As the embryo grows the parathyroid and the ultmiobranchial body sink lower in the lateral lobe and the thyroid material comes to nearly surround the latter.

Though in earlier embryos the derivatives of the caudal pharyngeal complex he in or near the cephaUc end of the lateral lobe m those of 30 mm. and over they are found well down within the body of the lobe; parathyroid IV is sometunes visible even after the sections have passed below the level of the thyroid itself ihis shifting m position is due partly to the upward expansion and growth of the lateral lobe and partly to the continued 'descent of the other bodies. In the 50-mm. embryo the lateral lobes contain the characteristic dark patches of cells (cf fig 3) the cords of the ultimobranchial body. There is, as yet' no loosening of the cells of the thyroid cords to form vesicles and no secretion of colloid until the embryo has reached 140 mm in length. Simon ('96) also described the appearance of colloid at this time.

Complex III

In the calf embryos one finds four well-formed pouches. Only the first three of these were ever observed to establish an ectodermal contact; the fourth pouch was never observed to reach the ectoderm in the series of embryos which was studied. The 8-mm. embryo showed the rupture of the membrane separating the second pouch from the exterior; this condition is quite common in calf embryos (and occasionally observed in human); in some instances it may be due to rough handling, but as the rupture was observed in several embryos which were well preserved and showed good morphological relations it was concluded to be a normal occurrence. The first of the aortic arches — which form on the anterior aspect of each pouch — has already broken its connection with the dorsal aorta in the .3.5-mm. embrj'o; the second, though small, is still intact; the third is large and fills most of the space in the third branchial arch, and the fourth and sixth aortic arches are not yet formed. In the 8-mm. embryo the forward growth of the anterior pouches has broken the second as well as the first arch; the remaining three arches (third, fourth, and sixth) are well formed.

The 8.5-nmi. embryo is the youngest in wliich there is to be noted from the medial border of the third pouch the ventral elongation which is to form the entodermal thj-mus. As the embryo develops (9.5 to 10 mm.) th>^nus III becomes elongated, extending down from the pouch, directed ventrally and medially and pointed toward the truncus aorticus. In the more cephalic sections it is seen in the form of a hollow tube, dorsal and a little external to the third aortic arch (the primitive carotid). It follows the line of the carotid, swinging to the lateral and finally to the ventral side of that vessel.

When the embryo is 14 mm. in length the thymus and parathyroid III have lost their connection with the pharjnix. The head of the thymus is lodged in the caudal and dorsal part of parathyroid III and the gland extends back from this as a slender cord with the lumen nearly obliterated, and follows roughly, as before, the line of the carotid. In the thoracic region the two sides of the thymus make a rather marked medial turn and come to lie over the pericardial cavity, a little to the left of the midline. Here the walls of the thpnus become enlarged and lobulated; the branching cords from either side are apparently fused along their region of contact.

In connection with the development of the thjTiius it may be stated that a cer\ical vesicle is formed essentially as in man and possesses the same relations to the ganglion nodosum. It forms no part of the thj-mus, as it does in the pig.

In the 30-mm. embryo the division of the thjTnic cord and body into segments is definitely noted for the first time. T he h ead of the thjTiius, slightly enlarged, lies, as before, in connection with the lower pole of parathyroid III and the whole group has shifted a little to the median side of the carotid artery, on its dorsal aspect. From the head extends a thin cord of cells, called by Badertscher ('15, who adopted the terminology of Kastschenko, '87) the 'intermediary cord,' which connects the thymic head with the 'mid-cervical segment.' In jthe^region of the thsToid the 'intermediary cord' is very small and lies ventral to, and a Uttle anterior to the brachiocephalic vein which is formed by the union of the subclavian and jugular veins. Below this, in the region of the truncus proper and also ventral to the superior vena cava, the thjTnic cord diminishes markedl.v in caliber to form the 'cervicothoracic cord' which connects the 'midcerxdcal' with the 'thoracic segment.' The thoracic segment hes in the upper section of the thorax, is expanded in contact with the pericardium, and is markedly lobulated.

The above description will hold, in the main, until the 80-mm. stage is reached. Only the following differences need be noted. In the 39-mm. embryo there is no enlargement in the midcervical region. The 40-mm. stage shows a shifting of parathyroid III so that it (and consequently the head of the thymus) lies below the bifurcation of the carotid and well medial to that vessel.

After the 80-mm. stage the head of the th\Tnus becomes markedly enlarged and lengthened. At 110 mm. the intermediary cord begins to enlarge, and at 130 mm. shows slight lobulation. Complete older series would undoubtedly show a transformation of the entire thj-mic cord as in the pig (Badertscher).

The dorsal element of complex III, parathyroid III, appears for the first time in the 9.5 to 10-mm. embryo in which the thymus has already elongated. It lies on the anterior and dorsal surface of the third pouch, and extends well from the pharynx to the free margin of the pouch. Histologically, it is composed, from its earliest appearance, of cords of epithelial cells, proliferated by the entoderm of the pouch and associated from the start with a rich network of fine capillaries.

The question of the vascularization of the parathyroids is an important one and involves possibly the question of the cause of their appearance. In the human embryo they appear as rather thick, but definitely limited proliferations of epithelium on the dorsal side of the third and fourth pouches, and it is not until late in their history that they are broken by vascular channels. In the calf, on the other hand, blood vessels appear along the anterior side of the third pouch before the epithelial proliferation is even noted (9 mm. Sag.) and, after the proliferation, there is a subepithelial plexus of blood vessels not only between the cords of cells, but also to the outside of the gland. The connection of this vascular network appears to be with the anterior side of the third aortic arch, and with the dorsal side of the external carotid, going to parathyroid III on either side of the common carotid; a few of the younger embryos show direct vascular connections between the posterior side of the carotid and the parathyroid (fig. 5), and still others show combinations of these sources. In all cases the third aortic arch lies along the anterior and dorsal surface of the third pouch and is unquestionbly the source of some of the blood for the parathyroid.

In the early embryos parathyroid III lies dorsal to the common carotid artery, between it and the anterior surface of the pouch, and the surface of the parathyroid is slightly concave to conform to the shape of the carotid about which it fits. Topographically it is anterior to the bifurcation of the carotid.

In the 14-mm. embryo, in which the derivatives have broken from the phar^nix, the parathyroid has the shape and position which characterize it for a number of stages; it is in the form of a thick crescent, slightly elongated in the vertical plane. On its anterior side it is concave toward the carotid and forms a cap around that vessel, just cephalad of the bifurcation of the carotid. It lies a trifle lower than the carotid body, which is seen here for the first time. The horns of the crescentic parathyroid seem to be shaped about the sides of the carotid by the hj'poglossal nerve (XII) on the exterior, and the superior larj-ngeal nerve on the interior surface. In the younger embryos the hypoglossal nerve lay entirely caudal and ventral to the third complex, lateral to the fourth complex and its aortic arch. A sUght descent of the head of the third complex together with the forward growth the more lateral material is responsible for the altered relations. The head of the thymus is lodged in the lower pole of parathjToid III.

Subsequent stages (30 mm. and up) see a backward shifting of parathjToid III, so that most of its body now lies caudal to the bifurcation of the carotid and hence posterior to the carotid body. It does not, however, come into contact with the lobes of the thjToid as does the other parathyroid. In its shifting it comes to lie well medial to the carotid and offers a flat or sUghtly concave surface to that vessel. Numerous small blood vessels are seen which enter parathyroid III from the carotid both directly (fig. o) and out through the carotid body.

The caudal pharyngeal complex

The caudal pharyngeal complex — to include under a common heading, the derivatives parathyroid IV, the ultimobranchial body, and thjTnus IV, of the more caudal pouches — has been a frequent source of discussion among writers, both from the standpoint of origin and from the standpoint of fate. Especiallj' is this true of the ultimobranchial body (the 'lateral thyroid,' 'post-branchial boch',' 'suprapericardial bod}-' of other writers).

Briefly, the morphology of the fourth or caudal pharj-ngeal complex as it appears in successive stages in the calf embryos of the series studied is as follows:

The fourth pouch, as stated above, does not reach the ectoderm, but lies in the posterior region of the pharjTix caudal to the third pouch and, because of its tardy development, is smaller than and median to the wings of the third pouch. In the 8. 5mm. embryo a long posterior and a short anterior diverticulum are evident on the ventral side of the complex and the fourth aortic arch forms to the lateral side of the pouch. The anterior diverticulum elongates (9.5 to 10 mm.) to form the so-called 'thjTuus IV' with its axis directed toward the truncus as in the case of thjanus III. The posterior diverticulum forms the ultimobranchial body, and in the angle between^t and thymus IV, on the lateral side of the pouch in the region toward the fourth aortic arch is parathjToid I^'. Like parathyroid III, parathj'roid IV is from the first an epithelial proliferation from the wall of the pouch and is supplied with a rich subepithelial network of blood channels. But here it has been impossible to determine any definite and constant connection of the vascular network. In the 11-mm. embryo there is one direct blood vessel from the posterior side of the fourth aortic arch to parathjToid IV. The ultimobranchial bodj' and thjinus IV have a common opening into the pharj-nx, but their relative size soon changes so that tlmnus IV (14.5 mm.) appears to be an appendage of the ultimobranchial l)ody: parathjToid IV, a vascularized prohferation, lies between them on the dorsolateral aspect of the pouch.

The ductus pharyngeo-branchialis I^', which early connects the complex with the pharjiix, has ruptured and entireh' disappeared in the 14-mm. embrj'o; thymus IV, nicely shown in sagittal section in the 14-mm. stage,, has disappeared as such, and of the complex there only remain parathyroid IV and the ultimobranchial body. These come to lie close to the upper pole of the lateral lobes of the thyroid as that gland develops. Parathyroid IV is the more dorsal and medial; the ultimobranchial body is fast agahist the inner surface of the lateral lobe, but separated from the th^Toid by a distinct connective-tissue sheath. A cord of cells connects the anterior side of the ultimobranchial with the parathyroid, and in the parathj^roid, at the head of this cord, is a cavity — the remains of the cavity of the fourth pouch.

Even at 15 mm. the ultimobranchial bodj' shows, in its scalloped edge, the tendency to 'bud,' which has led some authors to the behef that this, the 'lateral thjToid,' after its inclusion in the lateral lobe of the thj-roid, is transformed into a part of the thyroid gland.

While the relative size and position of parathj'roid IV and the ultimobranchial body vary in embryos 20 mm. to 50 mm. in length, the sanie general relations hold. Parathyroid l\ is round or oval in form, always situated in the dorsomedial a.spect of the lateral lobe of the thyroid, sometimes above and sometimes below the level of that gland. Often, especially in the later stages, the parathyroid will he low on the lateral lobe. Some of the blood enters it directh' from the dorsal side of the carotid artery (24 mm.), while in other cases (40 mm., 50 mm.) theparath\Toid is supphed with a branch from the accessory thyroid artery. It always contains, on its ventral side, a cavity from which a sohd cord of cells runs forward to join v\-ith the ultimobranchial body (&g. 4). This latter structure is embedded more or less intimately in the lateral lobe of the thyroid and shows in the early stages a heavy wall and a narrow, cresentshaped cavity. About it the cords of the thvToid tend to be thin and separated by connective tissue: below the level of the ultimobranchial body the material of the thvToid is more closely packed. Gradually the thick wall of the ultimobranchial bodj- loosens and sends out buds which shape themselves into narrow cords or plates of cells, interminghng with those of the thyroid proper. Though in form resembling the material of the thyroid, histologically they are quite different. The nuclei of the epithelium of the thyroid are of varving size and shape and contain mmierous small bits of chromatin, peripherally placed. The nuclei of the ceUs of the ultimobranchial body, on the other hand, are smaller, rounder, more nearly of a size, and more closely packed ; they contain two or three large nucleoli, centrally located. Even in the oO-mm. embryo, in which the sections are rather thick, the material of the ultimobranchial bodies can be easily distinguished in the midst of the substance of the thyroid by its darker staining quaUties. Figure 3. of a 33-mm. embryo, may be compared.

From this time on, with the marked increase in the size of the thvToid, the ultimobranchial body becomes relatively smaller and smaller and shows as thick branching cords of darkly staining cells at the dorsal side of the lateral lobe of the thjToid and at the 'hilus,' around the entrance of the blood vessels. These cords of cells branch out, but do not join with the parenchvTna of the thyroid.

In the 40-mm. embryo, in connection with the lower pole of the parathyroid, is found an instance of an accessory thymus (IV). Its appearance is that of the thymus (III) and its relation to the posterior pharyngeal complex would suggest that it represents a thymus IV. A calf of 130-mm. length shows a similar structure.


The following points have been noted in the morphology of the pharjaigeal derivatives in the calf:

  1. The median thyroid undergoes a typical evolution.
  2. Thymius III, of entodermal origin only, divides into head, intermediary cord, midcervical segment, cervicothoracic cord, and thoracic segment.
  3. Of these, the intermediary and cervicothoracic cords show thymic transformation only in the older stages.
  4. The parathyroids appear as proliferations of the epithelium of the pouches, adjacent to the corresponding aortic arches, and are highly vascular from the first.
  5. Parathyroid III is but little involved in the descent of the heart; it is not associated with the thyroid as an external parathyroid, but remains near the bifurcation of the carotid and medial to that vessel.
  6. Parathyroid IV becomes lodged on the mediocaudal aspect of the lateral lobe of the thyroid, but is never embedded in that gland. It is connected, in all the embryos examined, by a cord of cells to the ultimobranchial body.
  7. The ultimobranchial body can still be clearly distinguished from the material of the thyroid in the oldest embryo examined.
  8. 'Thymus IV' is but a transitory structure, not recognizable after the 14-mm. stage.
  9. In only two cases in the older embryos was an accessory thymus noted which might possibly be considered as 'thymus IV.'
  10. From the evidence it may be concluded that: a) The second pouch normally opens in the calf; 6) the fourth pouch fails to reach the ectoderm.

I wish to take this opportunity to thank Dr. B. F. Kingsbury for the material he has put at my disposal and for helpful criticisms and suggestions. I am also indebted to Prof. S. H. Gage for the material which he has loaned to me.

Literature Cited

B.^^DERTACHER, J. A. 1915 a The development of the thymus in the pig. I. Morphogenesis. Am. Jour. Anat., vol. 17, no. 3.

1915 b The development of the thymus in the pig. II. Histogenesis. Am. Jour. Anat., vol. 17, no. 4.

1918 The fate of the ultimobranchial bodies in the pig (Sus scrofa). Am. Jour. Anat., vol. 23. C.\^p, W. E. 1917 The development ~Jf the suprapericardial (postbranchial, ultimobranchial) body in Squalus acanthias. Jour. Morph., vol. 28,

Groschufp, K. 1896 Bemerkungen um der vorliiufigen iMitteilung von Jacoby; Ueber die Entwickelung der Xebendrijsen der Schilddrlise. Anat. Anz., Bd. 12, no. 21.

Grosser, H. 1911 Zur Entwieklung des Vorderdarmes menschlicher Embryonen bis 5 mm. grosster Liinge. Sitzungsber. d. Kaiserl. Akad. d. Wiss. Wien. Math.-Xaturf. Kl., Bd. 120; Abt. III. Hammar, Acg. 1911 Zur groberen Morphologie und Morphogenie der Men sehenthymus. Anat. Hefte, Bd. 43,

H. 1. Kastschexko, X. 1887 Das Schicksal der embryonalen Schlundspalten bei S.iugetieren. Arch. f. mikr. Anat., Bd. 30.

Kingsbury BF. The development of the human pharynx. (1915) Amer. J Anat. 18(3): 329-397.

KiNGSBURY, B. F. 1915 The development of the human pharynx. I. The pharyngeal derivatives. Am. Jour. Anat., vol. 18, no. 3.

Kingsbury BF. The interstitial cells of the mammalian ovary: Felis domestica. (1914) Am. Jour. Anat. 16: 59-90.

1914 On the so-called ultimobranchial body of the mammalian embryo; man. Anat. Anz., Bd. 47, no. 24.

Maurer, F. 1906 Die Entwicklung des Darmsystems in Handbuch d. Entwges. der Wirbeltiere. Edited by O. Hertwig, Bd. 2, s. 108-252. Prexant, a. 1900 Contribution a I'etude du developpement organique et histologique du thymus, de la glands thyroide, et de la glande carotidienne. La Cellule. T. 10.

Saxdstrom, J. 1880 Om em negKoertel hosmenniskan ochitskilliga doggdjur. Upsale Lakerefoerenings Foerhandlinger, 15.

SiMcv, C. 1896 Thyroide laterale et glandule thyroidienne chez les mammi feres. These, Xancy. Verdux, p. 1898 Derives branchiaux. These, Toulouse.

WoELFLER 1880 Ueber die Entwickelung und den Bau der Schilddrlise. Berlin.


Plate 1


1 Section through the phanoix, showing the third branchial pouch and the formation of parathyroid III on the anterior and (dorsal) side of the pouch. Section also shows direct vascular connection from the posterior side of the third aortic arch to the anterior surface of the corresponding pouch. The second pouch is open. Embryo calf, 11.5 mm. Photograph, X 33j.

2 Section through the caudal pharj'ngeal complex, to show the characteristic relations. Parathyroid IV, on the right, shows the characteristic cavity at the head of the cord which connects the parathyroid with the ultimobranchial. Embryo calf. 14 mm. Photograph, X 33J.

3 Section through the lateral lobe of the thyroid in a more advanced stage. The cords of the ultimobranchial body are clearly distinguishable. Embrj'o calf, 33 mm. in length. Photograph, X 33j.

4 A section through the caudal pharyngeal complex, to show the connection rf the ultimobranchial body to the parathyroid IV by a cell cord. Compare with figure 2. Calf embryo of 20-mm. length. Photograph, X 33§.

5 Section through parathj-roid III and the carotid artery, to show the direct vascular connections between the two. Embrj'o calf, 30-mm. length. Photograph, X 125.


A. Ill, third aortic arch A. IV, fourth aortic arch A. VI, sixth aortic arch C, carotid artery £p.,'epibranchial placode G. X.. ganglion nodosum (X) P. Ill, parathyroid III

P. 7F, parathyroid IV

S. Ill, sacculus branchialis III (pouch HI) T. A., truncus aorticus Th., thymus Thy., thyroid U ., corpus ultimobranchiale