Paper - On the fate of the ultimobranchial body within the human thyroid gland
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Kingsbury BF. On the fate of the ultimobranchial body within the human thyroid gland. (1935) Anat. Rec. 61(2): 155–173.
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On the Fate of the Ultimobranchial Body within the Human Thyroid Gland
Benjamin Freeman Kingsbury
Laboratory of Histology and Embryology, Cornell University, Ithaca, N .Y .
Three Plates (Seventeen Figures) 1935
Since the observations of Stieda (1881) and His (1885), it has been known that three cell groups from the embryonic pharynx unite to form the human thyroid gland. One is median and more cephalic, two are lateral and more caudal. While the contribution from the first source is undoubted, the ultimate fate of the material from the second source has been far from clear. It is derived from the most caudal lateral out-pocketing of the pharynx which upon reaching the ectoderm establishes the branchial membrane of the fourth pharyngeal pouch and cleft. Since a parathyroid (IV) and, frequently in other mammals, a thymus as well (the so-called thymus IV) are differentiated from its epithelium, the term ‘caudal pharyngeal complex’ is a convenient designation for the entire out-pocketing. Conditions in other mammals, or indeed other Vertebrates, cannot be ignored in considering developmental relations in man. It need only be stated that the extent to which such material from the caudal pharyngeal complex is engulfed by the expanding lateral lobes of the thyroid varies in different animals and individually Within the same species. Practically the entire ‘complex’ may be included, as in the cat, or only the more caudal portion as in man — the so-called ultimobranchial (post-branchial) body No extensive comparisons need be made here. It may only be mentioned that in monotremes and all lower vertebrates the three structures remain quite separate and distinct.
- 1 The term ultimobranchial body is employed as perhaps the most adequate, but without subscribing to its value as a physiological ‘organ’ of unknown function of the homologue of a fifth or any other pharyngeal pouch.
The complete separation in lower vertebrates of the median thyroid and the two lateral components, in itself strongly contradicts the View that they possess the same potentialities. Nevertheless, from the mode of development in the mammal, the interpretation originally made was very natural; namely, that the deﬁnitive thyroid Was, in these forms, derived from three sources and so the caudal pharyngeal contribution should be designated ‘lateral thyroid’ (Born, 1883). In the pig (Badertscher, ’18) and in the rat (Rogers, ’27) detailed examination of many developmental stages has supported this conclusion. In man, however, the fate of the material incorporated from the caudal pharyngeal complex has remained inadequately determined. The most recent investigator of thyroid development in man (Weller, ’31) it is true, accepts the interpretation of a tripartite origin and names what is here termed the ultimobranchial body the lateral thyroid. Weller, in a ﬁnely illustrated article, fully conﬁrms the previous observations upon the early morphogenesis of the thyroid. The development is, however, not illustrated beyond the period of fusion (23-mm. stage), which was already Wel.l known. The description of the transformation of ‘lateral thyroid’ to typical thyroid parenchyma is brief and not sufficiently detailed to be convincing, particularly since it is unsupported by adequate illustration at the critical period.
To determine the fate of the ‘caudal pharyngeal inclusion within the expanding thyroid, the present writer had earlier (Kingsbury, ’14) examined in detail some ﬁfty series of human embryos with indecisive results. It was then stated that “Despite careful study, I have been unable to satisfy myself as to the actual fate of the material so included in the medial portion of the lateral lobes of the thyroid” (p. 623). However, the general conclusion was (p. 626) that after “the caudal portion becomes fused with the thyroid, . . . . its epithelial syncytium rapidly undergoes reticulation,” and while “at first clearly circumscribed within the expanding thyroid, it soon becomes indistinguishable and apparently ﬁnally in man, disappears typically without trace.” Since that time the problem has been kept in mind and at intervals received some consideration. The present paper gives the results of a careful examination of some forty additional series?
The caudal pharyngeal complcrv. The early history before fusion with the thyroid need not be considered in detail, since it is Well described by several previous investigators. As is well known, man develops i11 cepl1alo—caudal and chronological sequence four well—deﬁned pharyngeal pouches, all of which reach the ectoderm and establish well-deﬁned branehial membranes. The transformation during this period of the caudal or pouch IV complex was diagramrned in my earlier paper (Kingsbury, ’14, ﬁg. 9). Contact. with the ectoderm is made when the embryo attains a length of 5 mm. Molded apparently by the associated arch material, the expanding pouch (IV) develops (5 to 7 mm.) a ventral diverticulum and a caudoventral extension, the latter the so—eallcd ultimobranchial body. With the expansion of the mesoderm the ectoderrnal contact is drawn out into a cord which soon ruptures (ea. 10-mm. length). In turn, the communication of the pouch with the pharynx becomes prolonged, attenuated and interrupted (ca. 12 mm.). In the meantime (ca. 8 mm.) a thickening of the epithelium upon the dorsal side of the pouch produces parathyroid IV and under a remolding of the pouch complex any clear distinction between the ventral diverticulum and ultimobranchial outpocketing is lost. Finally, in man the portion of the pouch between the parathyroid and the ultimobranchial body becomes interrupted (ca. 20 mm.). The caudal portion of the epithelial wall becomes markedly thickened and the cavity reduced, though traces of it may persist for some time. At approximately a stage of 12 mm. length, the lateral wings of the thyroid, molded medially about the common carotid arteries, have become interpolated between the latter and the ultimobranchial bodies which thus lie medially. Fusion of the two structures and inclusion of the ultimobranchial bodies within the thyroid have now begun.
- Collections of the human embryos in the Department of Comparative Anatomy of the Harvard Medical School and at Cornell University, Ithaca, New York, furnished the material in the earlier investigation (Kingsbury, ’14, footnote, p. 612). The supplementary series likewise include embryos in both collections. I wish to thank Dr. J. L. Bromer for the privilege of examining those in the Harvard Collection. The supplementary series listed in millimeters length include the following stages (the C and the H indicating, respectively, the Cornell and the Harvard collections): 0. 13.0; G. 13.5; C. 15.0; H. 16.5; H. 17.5; H. 18.2; H. 18.8; H. 21.7; H. 22.8; H. 23.0; C. 23.0; H. 24.0; II. 24.0; H. 25; 25.0; C. 25.0; C. 25; C. 25; H. 27.0; H. 29.0; H. 30.0; C. 30.0; C. 30.0; H. 31.0; C. 31.5; C. 32.0; C. 34.0; C. 36.0; H. 36.0; II. 40.0; C. 40.0; C. 42.0; C. 44.0; C. 44.0; C. 46.0; C. 46.0; C. 55.0.
The stage when thyroid and ultimobranchial body ﬁrst become fused is illustrated in figure 1. The lateral wings of the median thyroid are crescentic in shape with the common carotid artery Within the concavity. On its dorsal edge it is fused with the ultimobranchial body which is still joined to the parathyroid IV by means of a stalk. In the early mammalian embryo, the relative position of thymic cord (pouch III), common carotid, thyroid and complex IV, vagus and internal jugular vein are characteristic. The topographical relation of these structures is clearly determined by the mechanical shiftings of material in the developmental transformations which the region undergoes (Kingsbury, ’15). Figure 2 illustrates the same fundamental relations, save that at this later stage the carotid has shifted dorsally. The fate of the ultimobranchial body within the human thyroid may be considered for convenience under four epochs.
The ﬁrst is the epoch of fusion and incorporation. During this period the ultimobranchial body is a well—deﬁned mass, roughly pear-shaped (ﬁgs. 1, 2), the stem or stalk connecting with the parathyroid IV. It is mainly epithelioid, although the cavity, which is variable, is usually represented at least in the dorsal, less expanded, portion. In ﬁgures 1 and 2, the cavity is typical. Not infrequently it is relatively larger. A papillary projection from the stalk into the cavity (ﬁg. 2) is sometimes encountered. While in earlier stages the body is quite compact, in later stages the interior of the epithelioid mass is markedly looser, that is, reticulated, with a narrow denser layer superﬁcially next the mesenchyme, or next the thyroid plates where they adhere. In ﬁgure 3, five sections from the level illustrated in ﬁgure 2, there is shown the incipient central reticulation. Tl1e boundary between the ultimobranchial body and the fused thyroid plate to the right is clearly indicated. Laterally (i.e., below), a thyroid plate is (at this level) nearly in contact with the body. During this period the nuclei of the ultimobranchial body are distinctly smaller and more chromatic than the clear and Vesicular nuclei of the thyroid plates. This very characteristic difference between the two components was illustrated by Grosser (’10), commented on by myself (’14) and noted by Weller (’31). Of the embryos examined the following may be listed by millimeter length as falling within this epoch: 13, 13.5, 15, 16.5, 17, 18.2, 22.8, H 23.0.
The second epoch is less well deﬁned, of shorter duration and probably not constantly present. It expresses a continuation of the loosening and reticulation which become apparent in the ﬁrst epoch. At the sa.me time, the nuclei lose their markedly chromatic character, while the thyroid plates seemingly stain more intensely, with the result that the contrast between the inclusion and the thyroid is temporarily reversed, but nevertheless sharp. Figure 6 (25 mm. embryo) in my earlier paper (Kingsbury, ’14) illustrated this stage. In the present series embryos of 21.7, 23, 24, 25, 31.2 mm. length may be grouped together as exhibiting in varying degrees the structural features of this epoch. In a 24-mm. embryo (Harvard ser. no. 2307) the relation was most characteristic. It is diﬂicult to sharply separate this from the next epoch, in which the boundary of the ultimobranchial body is vaguely deﬁned. The third epoch might thus be described as the period of confusion. Figures 4 to 10 represent embryos of 23, 24, 25, 30 mm. and as a quite exceptional late persistence, an embryo: of 36 mm. length. In the last two embryos the conditions on both right and left sides are illustrated. It may be noted that in three of these embryos (ﬁgs. 4, 7 and 8, 9 and 10) the cavity of the complex is still evident. In ﬁgure 6 the reticulation and pyknosis subsequently to be discussed are well advanced.
During the fourth and last period the inclusion as such fades from view. The disappearance might conceivably be due to either a) transformation to thyroid parenchyma or b) degeneration or c) both. Furthermore, it would be expected that in any event the place of ‘disappearance’ in one of the ways suggested would be marked as a ‘center’ by a different arrangement of the thyroid material. In man the Vasculo—stromal hilus of Prenant (1894) is at least insigniﬁcantly represented. The period of disappearance may be given as including embryos of approximately 25 to 40 mm. length. Save for the exceptional 36 mm. embryo as already noted, embryos of this size or larger consistently revealed no parenchyma other than the typical thyroid plates and masses.
In this period, diﬁicult of interpretation as it is, pyknosis and nuclear degeneration are marked features. During the ﬁrst, second and third epochs a certain pyknosis within the inclusion is obvious. In the fourth period it becomes marked. In earlier stages of this period (ﬁg. 6, 25 mm.) the pyknosis accompanies the loosening or reticulation; in later stages (ﬁgs. 12 to 14, 25 mm., and 16 and 17, 31 mm.) the pyknosis and degeneration prevail, and the concentrated area where they occur seems to mark quite sharply within the thyroid lobe the disappearing ultimobranchial body. In the ﬁrst of the two embryos just mentioned (25 mm.) there is found on the left a cord of cells which leads from an unincluded more dorsal portion of the complex (fig. 12) to an area of pyknosis (fig. 13).
On the opposite side in this embryo the inclusion seems to have been complete and the area of pyknosis is more deeply enclosed by thyroid parenchyma (figs. 14 and 15). In the older embryo (31 mm., figs. 16, 17) the regions of pyknosis, upon both right and left sides, are more fully surrounded by thyroid. At the close of the period this distinguishing feature no longer holds, and such typical areas of pyknosis were not encountered.
While the main and central mass of the inclusion undergoes loosening, reticulation and apparently ultimat.e degeneration, it by no means follows that the denser superﬁcial layer of the ultimobranchial body, particularly at the points where it is in contact and intimate fusion with the thyroid plates, may not undergo. transformation to thyroid parenchyma. However, careful examination failed to furnish evidence of such a fate. Despite the fact that it could not be disproved, the writer considers it highly unlikely, although possible. Comparative evidence does not strongly support such an interpretation, as will be briefly presented below.
It should be appreciated that - as was expected - considerable variability exists between stage and age as determined by embryo length. This is clearly in part — but only in part — due to the inadequacy of length as a measure of developmental stage. The.re is also a marked variability as between right and left sides, expressed as differences in the extent of inclusion and the degree of transformation. As an illustration, a marked instance in a 32-mm. embryo is presented (ﬁg. 11). Here, on the right lack of inclusion is accompanied by an absence of transformation. In ﬁgures 12 and 13 a portion of the complex lies outside the thyroid and is untransformed. The cavity is shown in ﬁgure 12. A number of similar instances of persistence of a portion of the complex outside the thyroid were encountered in the series of embryos examined. N o attempt has been made to ascertain whether or not a fundamental asymmetry underlies differences in the development of the two sides. Nor has any consideration been given to the question of how far such frequent developmental variability may underlie pathologic conditions. Some of these doubtless arise as expressions of such developmental fluctuations. Examination of a large number of thyroids from later fetal life would be necessary, and might indeed yield results of interest.
No instance of thymic transformation (so-called thymus IV) of any portion of the caudal pharyngeal complex was encountered in any of the embryos examined. Whether the epithelioid bodies (ﬁgs. 11, 12) just referred to may be so interpreted is, I think, questionable.
When the term ‘lateral thyroid’ was introduced by Born (1883), who derived it from the fourth pharyngeal pouch in the pig, little was known of the transformation of the pharynx of lower vertebrates. At the present time the origin of an outpocketing from the most caudal branchial pouch, or just caudal thereto, is known for all orders of vertebrates save the eyclostomes. Certain information has also been gained as to its fate, position and structure in all such lower vertebrates (W'atzka, ’33). The so—called lateral thyroid of mammals has the same place and mode of origin, and the inclusion within the thyroid is clearly determined by an altered growth mechanics in the developmental transformation of the pharyngeal region (Kingsbury, ’15). Since this most caudal pharyngeal derivative, however named, can hardly be suspected of being thyroid in birds, reptiles, amphibians or ﬁshes, it is a. priori exceedingly unlikely that in the higher vertebrates it possesses thyroid potentialities. However, the possibility of a secondary induction of thyroid out of material of caudal pharyngeal complex origin exists, as will be referred to below.
As has been stated, Badertscher (’18) and Rogers (’27) employing abundant and excellent material, pig and rat, respectively, concluded that the ultimobranchial body in these two mammals became transformed to thyroid, although in both forms it was recognized that relatively little thyroid parenchyma of the lateral lobes was so derived. Badertscher, at the earlier date, did not olfer any suggestion of how such a diﬁerentiation was possible. Rogers, however, was enabled to do so, and I quote from him in full (p. 365) :
- Mangold’s (’22) experiments suggest a basis upon which the transformation of the ultimobranchial body into thyroid or thyroid-like tissue is comprehensible. It is very probable that the ultimobranchial body represents a more or less indifferent structure with no strongly marked inherent potentialities. Vt-Then, in the course of growth, it becomes embedded in the thyroid gland, which has already undergone some degree of diﬁerentiation, it is possible that, in effect, we have a natural transplant. The more- or less indifferent material of the ultimobranchial body seems to be inﬂuenced in its further development by its thyroid environment. The suggestion is strong that We have to do here with conditions similar to those produced experimentally by Mangold, who has shown that when indifferent embryonic material is transplanted into a new environment, it differentiates not according to its origin, but in harmony With its surroundings. A comparison With those forms in which the ultimobranchial body never becomes embedded in the thyroid strengthens the above comparison.
This suggestion is quite in accord with the results of the experimental analysis of development. The writer earlier (Kingsbury, ’15) expresses the conviction that in interpreting development the emphasis should be ﬁxed differently from where it is ordinarily placed; not that organs develop in and from such places; but that organs owe their character to their origin. Expressed differently: that the body is not an aggregate of distinct organs, but that the body is. a unit Whose different portions are variously differentiated (as organs) the character of the differentiation depending upon the way adaptation is met, determined by the past history.
The opinion as expressed was directed primarily against the branchiomeric concept—that intrinsically each pharyngeal pouch embodied speciﬁc regions of thymus and parathyroid forming potencies. As far as the thyroid is concerned, while it is probable that the pharyngeal lining and pouches express a growth expansion of a limited region, and granted that thyroid forming potencies may be at ﬁrst relatively more extensive, there is little to support the interpretation of His (1885) that the lateral thyroids, so-called, are derived from the same material as the ‘median’ thyroid. The characteristics of the thyroid (median thyroid) from the beginning of its growth are marked. Equally distinctive are the structural peculiarities of the ultimobranchial body, and in its morphology it is totally unlike the growing thyroid. The intense staining of the ultimobranchial body during the ﬁrst epoch, already referred to, is a striking peculiarity which at this stage distinguishes it sharply from the thyroid. Whether the smaller size and markedly chromatic character of the nuclei, which determines the sharp differentiation, is indicative of an embryonic condition is at least questionable. The possibility that there is thus expressed a tendency toward pyknosis and degeneration may also be mentioned. The suggestion of Rogers (’27) which presupposes that the ultimobranchial body, the most caudal outpocketing of the pharynx, is at the time of inclusion undifferentiated, without determined potentialities, is at least plausible. However, there is also the suggestion that thyroid induction — granted that it may exist — is quite variable, since it would depend not only in part upon the indiﬁerent or embryonic character of the inclusion, but also upon the intimacy of the incorporation. It might thus be very varyingly effective in different mammals, or even in the same mammal. Depending upon the character and the degree of inclusion very different fates might thus be anticipated for non-thyroid material embedded within the thyroid. WY: may list as possible, or probable: a) degeneration, b) cyst-formation, the cysts being of varying size, content and persistence, c) thymic transformation, and d) a transformation to thyroid parenchyma. through induction. In any specific instance, one particular fate might be expected to prevail, or a combination of any or all. In man the evidence indicates an early and marked degeneration. Persistence with cyst-formation may be expected occasionally, especially When incorporation is imperfect or lacking. Thymic transformation of any part of the caudal pharyngeal complex must from the evidence be rare or lacking in man. Thyroid transformation, if indeed it occurs, must be slight. In the pig it is evident from the detailed descriptions and ﬁgures of Badertscher that the early stages of the transformation are quite like those characteristic of man. Reticulation early sets in, scattered nuclear degenerations occur and occasionally are marked (Badertscher, ’18, ﬁg. 7). Neither of these features appear to be as marked in the pig as they are in man. Cyst forma tion (Badertscher’s cystoid follicles) appears to be of frequent occurrence.
In the rat the reticulation, pyknosis and degeneration appear to be much less marked than in either pig or man. Rogers reports no cyst—formation (in the prenatal period) nor was there any evidence of a thymic transformation. Tl1e smaller size and chromatic character of the nuclei Within the ultimobranchial body of man, already twice commented upon, are equally obvious in the pig and rat, as judged by the published ﬁgures. In the calf this nuclear characteristic of the ultimobranchial body is even more marked and persistent as Will appear in a subsequent publication.
The differentiation of colloid-ﬁlled vesicles, usually considered a criterion of thyroid tissue, should, in the opinion of the writer, be so interpreted with caution. Any cyst arising within an epithelial or epithelioid mass appears by virtue of a secretion or retention of ﬂuid often obviously rich in coagulable material. Thickening of such content through reabsorption of Water or desquamation and degeneration of epithelial cells produces the picture of colloid. Indeed, the presence of the colloid-filled vesicles of the thyroid is from the vieW—point of the physiology of the gland, itself an enigma. The formation of colloid—filled vesicles within the ultimobranchial body or the presence of such which may be suspected to be from that source, is at most suggestive. The ultimobranchial body of lower vertebrates usually exhibits vesicles and cysts often of marked irregularity and containing obvious ‘secretion’ not infrequently of colloid character (Watzlza, ’33). As illustrating thyroid nature little reliance should thus be placed upon cases of congenital hypoplasia of the thyroid such as that of ‘Ophelia P’ presented by Weller (’31) as evidence of the lateral thyroid character of the ultimobranchial bodies in man. The bodies described as containing large irregular cysts with an obvious secretion undoubtedly originated from the right and left caudal pharyngeal complex, which had not become joined to the undescended thyroid. As judged by the ﬁgures and description the suggestion of a thyroid parenehyma is, however, very remote. It would seem that t.he ultimate and conclusive test of thyroid parenchyma would be- the demonstration of the thyroid hormone(s). Obviously, such evidence would be diﬂicult to obtain. Uhlenhuth and McGowan (’24) indirectly made such a test of the amphibian ultimobranchial body with negative results. Aside from this single instance, the writer knows of no attempt to ascertain the physiological value, if any, of this unique vertebrate structure. Watzka (’33), from an extensive study of its structure in all vertebrate classes, concludes that in man and mammals it can hardly possess signiﬁcant physiological value. In the non-mammals he suggests a. probable, but unknown, endocrine function. To the present writer it would seem unnecessary to ascribe any speciﬁc function to that curious pharyngeal derivative, the ultimobranchial body.
The detailed examination of forty selected human embryos, 13 mm to 55 mm in length, has furnished the author with no conclusive evidence of the development of thyroid parenchyma from material contributed by the caudal pharyngeal complex. On the contrary, the evidence has indicated that after fusion with the median thyroid gland, the complex undergoes reticulation and progressive degeneration. Thus there seems to be no justiﬁcation for substituting the term ‘lateral thyroid’ for that more usually employed—‘ultimobranchial body.’ In conclusion, certain general and comparative considerations are discussed - considerations related to the fate of the ultimobranchial body within the thyroid.
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Weller GL. Development of the thyroid, parathyroid and thymus glands in man. (1933) Contrib. Embryol., Carnegie Inst. Wash. 24: 93-139.
1 Homo. CU no. 87. Transverse. 15.0 mm X 143. Thyroid just fused with ultiniobranchial body. Median plane (larynx) to the right. P‘, paratl1yroid IV; U, ultin1obra.nchia.l body; Th, thymie cord; ’l_‘11r, thyroid; 0, common carotid artery; X, vagus nerve.
2 Homo. Harvard no. 2246. Transverse. 18.8 1mm X 4.8. Thyroid fused laterally and ventrally. A portion (only) of pouch Ill. complex included on either side. Abbreviations as under ﬁgure 1.
3 The same. X 285. The left ultimobranohial body, 5 sections caudal of ﬁgure 2. Dorsal side to the left, median plane above.
4 Homo. CU no. 70. Transverse. 23 mm X 143. The right ultiniobmncliial body, rather diffuse, within the dorsal portion of the right thyroid lobe. A remnant of the cavity is shown.
5 Homo. CU no. 79. 25 mm X 41. Au oblique section, showing both ultimobranohial bodies, rather diffuse. A ‘stalk’ is evident on the right.
6 Homo. CU no. 64. Sagittal. 25 mm X 285. The ultimobranchial body (center) is. markedly reticulated, with extensive pyknosis. Thyroid plates above and to the right.
7 and 8 Homo. CU no. 93. Transverse. 30 mm X 76. Left and right thyroid lobes showing diffused ultimol>ranchia.l bodies with marked pyknosis. A residuum of the cavity is obvious in each figure. Parathyroid III is at the lower right of ﬁgure 8.
9 and 10 Homo. CU no. 61. Transverse. 36 mm X 76. Right and left thyroid lobes with persistent diffuse ultimobranchial bodies in each. Remnant of the cavity in each body. Dorsal side to the left.
11 Homo. CU no. 63. Frontal. 32 mm X 152. An unincluded body (left), with blood vessels outside. Dorsal side to the left. At the right, most dorsal thyroid cords with four blood channels.
12 Homo. Harvard no. 2042. Transverse. 25.0 mm X 152. On the right an uninclucled portion of the complex with a cord leading to an area of diffuse pylmosis (fig. 13). Thyroid plates below and to the left.
13 Homo. Harvard no. 2042. Transverse. 25.0 mm X 152. Right, two sections below ﬁgure 12, showing the area of diffuse pyknosis, with the edge of the unincludcd body above.
14 and 15 The same embryo. X 152. Left side. Four sections intervene between the two sections. To show the area of diffuse reticulation and pyknosis. In ﬁgure 15 the edge of parathyroid IV is above (dorsal).
16 and 17 Homo. Harvard no. 2043. Transverse. 31.0 mm X152. The dorsal portions of the right and left lobes of the thyroid, marking the degenerating ultirnobranchial bodies. Dorsal side to the left.
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