Paper - The development of the serous glands (von Ebner's) of the vallate papillae in man (1917)

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Baumgartner EA. The development of the serous glands (von Ebner's) of the vallate papillae in man. (1917) Amer. J Anat. 22(3): 365-384.

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This historic 1917 paper by Baumgartner described serous gland development of the tongue in human.



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The Development of the Serous Glands (von Ebner's) of the Vallate Papillae in Man

E. A. Baumgartner

Department of Anatomy, Washington, University Medical School, St. Louis

One Text Figure And Three Plates (Ten Figures)

  • I wish to thank Prof. J. Playfair McMurrich for the privileges of his laboratory during a part of the time while this study was in progress.

Introduction

In 1873 von Ebner described the acinal glands in the base of the tongue. Since then contributions to our knowledge of these glands have been mainly of a topographical or comparative nature. Surprisingly little work has been done on the development of the lingual glands. Graberg's ('98) figures of sections showing the early origin of the serous glands of the vallate papillae in man form the basis of the description of the development of the serous glands in Keibel and Mall's Embryology. He figured them as early lateral outgrowths from the epithelial walls of the papillae which in later development branch considerably but are not fully developed in a 56 cm. child. This work, together with Oppel's ('99) excellent figure of the topography of the lingual glands in various mammals, is particularly enlightening. Oppel's study of the arrangement of the lingual glands in man is based upon a single specimen. Maziarski ('01) gives a brief illustrated descrii^tion of a model of a small portion of the glands of a child of fourteen years.


Since there has been so little work done on the development of these glands and on their adult condition, an intensive study of the glands in various stages of development as well as a further iiKiuiry into their topographical distribution in late fetuses and the newborn, may be of interest. The to]3ographical distribution in the newborn, the arrangement of ducts and gland masses, the distribution of blood vessels and the topographical relations of ducts, glands and blood vessels are considered in this study.


The greater part of the material used was preserved in formalin. Serial sections of the entire caudal region of the tongue of the younger fetuses form the basis for the study of the glands. Wax reconstructions of various stages of glandular development were made according to Born's method.


Development of the Glands

As indicated by Graberg, the vallate papillae first appear as solid epithelial do^\^lgrowths. A surface view of the tongue of a 6.5 cm. fetus shows no papillae under a low power lens although the foramen caecum is well developed. However, sections show seven papillae, well defined by epithelial downgrowths. Their arrangement is characteristic. No glandular outgrowths are distinguishable.


The earliest glandular outgrowths from the epithehum appear in an 8.5 cm. fetus. There are nine well developed papillae, the fifth lying in the foramen caecum and forming the apex of the 'V.' As yet there are no grooves outlining the papillae. A reconstruction of the anterior papilla of the right side shows a slight indication of a groove surrounding it and the papilla slightly raised above the surface of the tongue. The anlagen of four glands project from the lower border of the epithelial wall, two occupying a lateral position and two a medial (fig. 2). The caudo-lateral anlage is ridge-like wdth two protruding ends; the antero-lateral and the caudo-medial are rounded elevations; and the antero-medial has two slightly extended ends.

Several bulb-like outgrowths are found on the lower border of the epithehal wall of a vallate papilla from a 9 cm. fetus.


Of the eight papillae in the tongue of a 10 cm. fetus the one in the foramen caecum is the largest. This one and the two adjoining it on the right side were reconstructed. Deep furrows separate the papillae from each other. Of the three papillae modeled, the anterior one is di\dded into four parts by epithelial partitions. Both the partitions and the surrounding wall bear glandular outgrowths. The second papilla is simple. Five glands project from the lower border of the epithelial wall, two of which have enlarged ends and slightly constricted necks. The third papilla modeled, that in the foramen caecum (fig. 3) shows many glands at its lower border, some having the same appearance as the two above described. The lateral walls of this papilla also bear gland anlagen resembling in some cases folds of epithelium.


Nine papillae are present in an 11.5 cm. fetus. One papilla on the left side, near the foramen caecum, was reconstructed. Most of the glands extend downward and slightly caudal ward. Three glands (fig. 4) are longer than the others, the constricted necks having apparently elongated. Gland anlagen are to be found on the outer surface as well as on the lower border of the epithelial wall.


The tongue in a 12.5 cm. fetus shows twelve papillae. In sections, a very slight furrow is present indicating the site of the developing groove. This groove is only indistinctly indicated in a model of the two right anterior papillae. A model of one of these papillae, with its glands, is shown in figure 5. The glands are elongated greatly, their ends are enlarged and the stalks constricted. The stalks and occasionally the bulblike ends have lumens. The walls of the ducts are formed by two rows of epithelium but the walls of the bulbous ends contain four or five rows. In both of the papillae modeled the greater number of glands are found at the anterior and posterior ends. These glands are longer than those at the sides. Five of the nineteen glands arise from the outer wall, one from the inner, and the remaining thirteen from the lower border of the epithehal wall of the papilla. Two of the caudal glands have arisen so close to each other that they give the appearance of branches from a single outgrowth. The larger of these glands divides almost immediately, one branch extending caudalward almost in a horizontal plane, the other extending downward and caudalward for a short distance, then again dividing. At the pomt of the latter division, the duct is somewhat enlarged and has a well-defined lumen. The two subdivisions project straight down ward, one sc^iuliiig off n short caudal branch. Fi'oni the origin of the caudal branch, the duct enlarges gradually up to the end piece.


The condition just described seems to be true of all of the longer glands. That the end pieces are distinctly enlarged is apparent in sections as well as in reconstructions (fig. 5). The glands of the papilla occupying the foramen caecum are more highly developed than those of the other papillae, as evidenced by more branching and the greater length of the ducts.


Nine vallate papillae are present in the tongue of a 15 cm. fetus. Reconstructions were made of the two anterior papillae on the right side. In one a very long gland extends deeply into the tongue (fig. 6) . At its origin from the lower border of the wall of the papilla two short glands are found. The long gland extends downward about 0.5 cm. then divides into two branches. Both of these subdivide, a subdivision of each branch going lateralward. All carry enlarged knob-like masses at their ends. These show beginning subdivision into several parts. About 0.15 mm. from its origin, several branches are given off from the long gland. The latter show small rounded masses constricting from the end bulb of each (fig. 6).


Other glands of the same papilla are short and show occasional anlagen of lateral branches on the stalks. Some small glands, \\dthout terminal enlargements, are present on the lateral walls of the papilla.


A tongue from, a specimen slightly smaller than the previous one (14.5 cm.) also has nine papillae. In this and other specimens, some papiUae, when examined under low power lenses, appear to consist of several small, closely crowded papillae enclosed by one furrow. The condition described in the 10 cm. fetus, viz., epithelial downgrowths subdividing the papilla into smaller, closely associated ones, is foimd here. Four of the nine papillae in a 14.5 cm. specimen were of this compound form, and for the first time, a well-formed surrounding groove is present. The papillae are somewhat raised above the level of the dorsum of the tongue. A reconstruction of the right anterior papilla shows fourteen glands in various stages of development.


They are more branehccl than those of the 15 cm. specimen studied, this being particularly true of the terminal portions of the ducts. The gland ducts frequently divide dichotomously, although occasionally they resolve into three or four branches, ^^onie of the glands extend down into the muscular tissue as far as the transverse muscle layer, where they spread into terminal branches. The terminal branches, as a rule, ran horizontally, sometimes with many turns. A few, however, are so situated that their secretions are emptied into the main duct against its stream. The three largest glands of the papilla occupy a medial position. One of these shows especially well a terminal arborization similar to that seen in figure 6, as well as beginning alveolar subdivision of the end masses. In the shorter glands the end pieces do not show^ as yet this formation of alveoli. Only two glands arise from the outer wall of the papilla. Another, possibly the anlage of a mucous gland, has its origin from an epithehal fold lateral to the papilla. It shows, howe^'er, the same terminal enlargement as is characteristic of the glands of the vallate papilla.

One papilla of a specimen 19 cm. long was reconstructed. This specimen was singular in that it presented so many gland ducts to each papillae. The papilla chosen for reconstruction lies on the left side near the foramen caecum. With this papilla seventy-seven ducts are associated, w^hile with another papilla on the left side, one hundred and four are present. In the one reconstructed, tW'O glands arise from the inner w^all of the papilla, the others coming from the lower border and outer wall. Some ducts are 2 mm. long, others very short. The short glands are characterized by short side branches and enlarged end pieces (fig. 7) The breaking up of the end pieces is advanced far beyond that in younger specimens and is apparently a constricting of parts to form small round, or ridge-like alveoli, the latter connected by a long narrow base. Older stages demonstrate that these may first sejiarate in the middle, having the ends attached, and thus form anastomosing alveoli. The serous glands of the vallate papillae can, therefore, in later fetal stages, be considered as branched alveolar glands. Both the end pieces and the stalks have lumens. In another specimen 19 cm. long, a spherical thyroid-like mass is present in the base of the tongue above the hyoid bone. It is made up of follicles which contain a colloid-like substance. No connection between this mass and any duct system is apparent.


Sections of a tongue of a 23.5 cm. fetus show twenty-six and forty ducts respectively in connection with the first and third papilla on the right side. The second papilla on the left side is provided with forty-five ducts. One of the ducts in this specimen has a greatly dilated end from which small ducts radiate in all directions. This cystic enlargement, irregular in shape, is lined by a layer of flattened epithelium and measures 0.6 by 0.4 by 0.15 mm. in its greatest diameters.


The vallate papillae of a fetus 25 cm. in length, of a new born, and of a nine months old child, all show the characteristic short and long glands sending off many branches wdth terminal arborization of alveolar-like glands with occasional anastomoses. The longest ducts extend into the upper strata of the transverse muscle, the gland masses being broken up by the vertical and the longitudinal muscle fibers. A small group of glands in the tongue of the nine months old child were modeled (fig. 8). Some of the glands are irregular in shape, showing constrictions, outpouchings and anastomoses. The method of formation apparently is as pre\'iously described. The main ducts frequently present many small, solid outpouchings, the anlagen of other gland groups. Two such anlagen attached to the large duct near the gland appear in the model (fig. 8).


Two papillae in a newborn have associated with them thirtyeight and forty-three ducts respectively. In another specimen three papillae have thirty-two, thirty-three, and thirty-eight ducts resj>ectively. One of the latter with its gland gi'oups, from the caudal end of a papilla, was reconstructed. Twentyone groups of glands are attached to this main duct by means of small lateral or terminal branches (fig. 1). The gland masses extend beyond all sides of the papilla, spreading antero-posteriorly 2.2 mm., laterally 1.3 mm. and projecting into the tongue tissue about 1.2 mm. Since the antero-posterior diameter of this papilla is only 0.5 mm. and the lateral diameter 0.56 mm., one can readily see that there must be great intermingling of glands when there are thirty or forty such ducts, or one hundred as was found in a younger specimen (19 cm.).

A graphic reconstruction from the newborn to show the position of the papillae and the distribution of the serous glands resembles in all respects the reconstruction of Oppel ('99).

Since the glands of the newborn are not of the branched, tubular type of the child of fourteen years as modeled and described by Maziarski, reconstructions of glands from specimens of intermediate ages were made in order to determine the character of the transition between these forms. From a reconstruction of a small group of glands of a nine months old child it appears that these resemble closely those of the newborn (fig. 8). The alveolar masses occasionally anastomose although this may not be apparent from a surface view. As stated above the method of development readily accounts for this anastomosing of end-pieces. In the newborn and nine months old child, the larger ducts frequently present small irregular outpouchings connected by short, constricted stalks. Some of these show the beginnings of secondary alveolar-like sacs. These groups may develop into glands similar to those already formed, or remain in a more or less undeveloped state.



Fig. 1 Drawing made from a photograph of a reconstruction of a papilla and one duct with its gland groups from a newborn. X 65.



In the specimen from a child of five years, as also in specimens from older individuals, mucous glands, either as single alveoli or in groups, join the ducts of serous glands. Occasionally a part of an alveolar group is formed of serous cells, which are succeeded by cells distinctly mucous in type.


A reconstruction of the glands from a twenty-two year old specimen shows anastomoses between the closely crowded alveoli. Some of the glands are somewhat tubular, although they generally appear to be more of the alveolar type (figs, 9 and 10). The main ducts are distinctly different in structure from the end pieces, but the terminal ducts, breaking up within a group or lobule, may be similar to the glandular end-pieces. Anastomoses occur between alveoli of two terminal ducts as well as between those from one duct (fig. 9). Irregular outgrowths of the main ducts noted in younger specimens are present also in this specimen; these outgrowths extend in every direction and some are just beginning to break up into end-pieces (fig. 9). Figure 9 shows a gland from one terminal duct anastomosing with one of these gland anlagen. The lumen in the specimen could not be traced from one duct to the other through the gland mass. However, the lumens are sometimes very minute, even in larger end-pieces. Figure 10a shows an alveolar-like endpiece connected with the terminal duct; from the former three alveolar-like end-pieces project in various directions. Figure 10 shows a group of glands from which a portion has been removed in order to show the terminal duct with its various end-pieces.


The histological structure of the serous glands from the twenty-two year old specimen varies greatly. In some of the glands the secreting cells are large and deeply-stained; in others the lumens are large, whereas the cells appear flattened. These differences are probably due to different stages of functional activity.


Serial sections of a vallate papilla from a man fifty years old presented very closely crowded glands.

Although this work is mainly a study of the development of the serous glands and their topographical relations, some attention is given to their histological structui'e, especially in the better preserved material from older individuals.


An attempt to include the taste buds in the models was met with only partial success. Few taste buds appear in stages before that of the 19 cm. fetus, but in this specimen the number is relatively large. In all cases taste buds are more numerous on the sides of the papillae although some are present on the summit. They are also found on the dorsal surface in the newborn. In none of the specimens is there any definite arrangement of the taste buds in rows and tiers as has been described in sheep and pig by Schwalbe ('68).


In several specimens the lingual artery was injected and the materia) sectioned and studied. A number of rather large arteries ascend obliquely toward the serous glands about the vallate papillae. Smaller vessels enter a gToup of glands and then subdivide. Some of the latter vessels leave the glandular tissue and supply the surrounding musculature. The arteries do not follow the main ducts, or the terminal ducts of the lobules.

Discussion

As has been stated, the earliest glands are downgrowths of the lower border of the papilla. Graberg ('98) figures the first outgrowths from the lateral wall of the papilla. My models show that lateral outgrowths are not infrequent but that the gland anlagen which first appear in about 8.5 cm. fetuses are on the lower border (fig. 2) of the papilla. Oppel ('99) gives us an excellent figure showing the topography of the serous glands. The conditions there sho^\^l are confirmed in the present study of the serous glands in a newborn. These glands extend 3-5 mm. on all sides of the vallate papillae as has been observed by Oppel and by von Ebner ('73). The extent of the area occupied by the group of serous glands about a papilla can be estimated by reference to figure 1 which shows a single duct with its gland groups. With thirty to fifty such ducts associated with a papilla it is apparent that the glandular tissue must be crowded and extend considerably beyond the surrounding furrow. I have not "found glandular tissue within the connective tissue of any papilla although von Ebner and others have noted this.


The ducts open into the bottom of the furrow or along the lateral side of the epithehal wall, and occasionally into the medial wall. No ducts are observed opening into the dorsum of the papilla or into other grooves in the surface of the tongue (except those belonging to the folliate papillae). Nor are any ducts lined by ciliated epithelium as described by Schwalbe ('68), von Ebner ('73) and'Gmellin ('92) found in my material. Von Ebner stated that small alveoli either poorly developed or not fully formed, and separated by considerable connective tissue are not infrequently present. It is apparently such a group of glands which Maziarski ('01) has reconstructed and figured. In my material I have seen such a condition in only one group of glands from a five year old child, and in this it is rather that considerable connective tissue separated the more or less tubuloalveolar components of the glands than that the glands themselves are small. This group of glands approaches the alveolar type more nearly than does the one figured by Maziarski and as in his, no anastomoses are present. For the most part, although the lobules may be closely crowded or scattered, the individual end-pieces are usually very much crowded, and as a result are often rounded or irregular in shape. This fact may account for the occasional anastomosing of glands observed in my material. It is possible that the anastomoses are not permanent and that anastomosing end pieces may separate in older specimens. Absence of lumens in these anastomoses may indicate beginning separation. However, as stated, the lumens are often very minute and may appear discontinuously in other places.


Simple outgrowths from larger ducts are present in several of the specimens studied (figs. 8 and 9). That these are gland anlagen seems probable since various stages from the earliest outpouchings to those showing beginning glandular division are present. The serous glands therefore are not fully developed at birth nor even at five years. At twenty-two years simple outgrowths and anastomoses are still present (fig. 9).


Schmidt ('96) and Erdheim ('04) have described several cases in which cystic glands are found associated with the thyreoglossal duct, or, as isolated structures containing no ducts. In the present study, the occurrence has been noted of a spherical, thyroid-like mass, made up of follicles and containing a colloid-Hke substance, situated in the base of the tongue of a 19 cm. specimen. In another specimen dilatations of the ducts of some of the serous glands of the anterior papillae have been observed. A homogenous mass filled the cystic parts, and a duct connected the largest cyst to the groove surrounding the papilla. It appears, therefore, that besides the cystic glands associated with the thyreoglossal duct, cystic enlargements of serous glands of the tongue might also occur.


Frequently taste buds are found on the dorsal surfaces of the vallate papillae in the newborn. In other specimens they are noted only incidentally and occasionally are reconstructed mth the papillae. It has been stated above that in some of the newborn and older specimens, mucous glands intermingle with serous glands and join with the ducts of the latter. This condition has also been observed by Maziarski and others. It is possible therefore that the ducts and glands of the vallate papillae although usually serous in type are capable of developing mucous cells or alveoli or of being transformed into mucous alveoli, or that secondary connections are established between mucous end-pieces and the ducts of serous glands. It is noteworthy that mucous alveoli joined to ducts of the serous glands are observed only in adult material.


From the distribution of the blood vessels in the gland groups, it does not appear that the latter conform to our usual conception of lobules or histological units of organs.

Conclusions

Serous glands first appear in 8.5 cm. fetuses as outgrowths, originating usually from the lower border, but sometimes from the outer wall of the vallate papilla.


The first outgrowth is knob-hke. Soon a stalk develops givmg rise to lateral branches with enlarged end pieces. In a 19 cm. fetus, these enlargements present bulgings of the surface and beginnings of alveoli. These retain various connections with the ducts and with each other, so that in the newborn the serous gland is of the alveolar type with some anastomoses between the alveoli. In the adult (twenty-two years) some of the glands are of the tubular type with, some anastomoses between end-pieces of the same and separate ducts.


In the newborn, many knob-like outgrowths appear on the large ducts; in older specimens the number is less. These outgrowths are probably the anlagen of future glands, or at least potential anlagen.


Cystic dilatations of the serous ducts may occur. Mucous end-pieces occasionally open into the ducts of serous glands of the vallate papillae.


The serous glands of the vallate papillae of man belong therefore to the branching tubulo-alveolar and not to the branched tubular type as stated by Maziarski.


Bibliography

Von Ebner, V. 1873 Die acinosen Drlisen der Zunge und ihre Beziehungen zu den Geschmacksorganen. Graz.

Erdheim, J. 1904 I. Ueber Schilddriisenaplasie. II. Geschwiilste des ductus Thyreoglossus. III. Ueber einige menschliche Kiemenderivate. Beitr. z. path. Anat. und allg. Path., Bd. 35.

Gmelin, a. 1892 Zur Morphologie der Papilla vallata und foliata. Arch. mikr. Anat., Bd. 40.

Graberg, J. 1898 Beitrage zur Genese der Geschmackknospen des Menschen. Morph. Arb., Bd. 8.

Maziarski, S. 1901 Ueber den Bau und die Einteilung der Drlisen. Anat. Hefte, Bd. 18.

McMuRRiCH, J.P. 1912 Grosser O. Lewis FT. and McMurrich JP. The Development of the Digestive Tract and of the Organs of Respiration. (1912) chapter 17, vol. 2, in Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

Oppel, a. 1899 Zur Topographic der Zungendriisen des Menschen und einiger Saligethiere. Festsch. z. 70. Geburtstag von C. v. Kuptfer.

PoDWisoTZKY, V. 1878 Anatomomische Untersuchungen iiber die Saligethiere. Inaug. Diss. Dorpat.

ScHMiTT, M. B. 1896 Ueber Flimmercysten der Zungenwurzcl und die drlisigcn Anhjinge des Ductus Thyreo-glossus.

Fesctsch. f. B. Schmitt. Jena. ScHWALBE, G. 1868 Ueber die Geschmacksorgane der Siiugethiere und des Menschen. Arch. mikr. Anat., Bd. 4.

Plates

Plate 1

EXPLANATION OF FIGURES

2 Ventral view of a reconstruction of the right anterior j^apilla of an 8.5 cm. fetus showing gland anlagen from the lower border of the papilla. X 135.

3 Same view of a reconstruction of the papilla from the foramen caecum of a 10.0 cm. fetus. X 135.

4 Same view of a model of a papilla of the left side from an 11.5 cm. fetus, showing enlarged end-pieces and constricted stalks. X 135.

Plate 2

EXPLANATION OF FIGURES


Plate 3

EXPLANATION OF FIGURES

7 Lateral view of a reconstruction of some short glands from a 19 cm. fetus. X 135.

8 Reconstruction of a small group of glands connected by a terminal duct to a larger collecting duct from a nine months old child. X 135.

9 Reconstruction of a small group of glands, a larger collecting duct and a small simple outgrowth anastomosing with the glands of the group, from an adult specimen of twenty-two years. X 166.

10 Reconstruction of another group of glands showing alveolar-like endpieces from a specimen twenty-two years of age. X 166. a, alveolar end-pieces opening through an alveolus into the terminal duct; D, main duct; d, terminal duct to gland group; ^, early gland anlagen from main duct.




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