Paper - The later development of the bursa pharyngea - Homo

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Snook T. The later development of the bursa pharyngea: Homo. (1934) Anat. Rec. 58(3): 303-318.

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This historic 1934 paper by Snook described development of the human bursa pharyngea or pharyngeal bursa. A blind sac or cystic notochordal remnant found inconstantly in the posterior wall of the nasopharynx above the adenoids and at the lower end of the pharyngeal tonsil.




Postnatal abnormalities in this region are also named after two German anatomists who historically first described them:

  • Luschka's bursa, after Hubert Luschka (1820-1875) a German anatomist.
  • Tornwaldt's bursa or Tornwaldt's cyst, after Gustavus Ludwig Tornwaldt (Thornwaldt) (1843-1910) a German physician.


See also by this author: Snook T. The development of the human pharyngeal tonsil. (1934) Amer. J Anat. 55(2): 323-341.


Modern Notes

Mouth | Gastrointestinal Tract Development

Search PubMed pharyngeal bursa development

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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Later Development of the Bursa Pharyngea: Homo

Theodore Snook

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

Three Plates (Twenty-Seven Figures)

Introduction and Historical

The frequent occurrence of median out-pocketings from the pharyngeal roof in the region of the pharyngeal tonsil has been a point of interest and contention among anatomists for nearly a century. Although probably nothing more than a local expression of peculiar developmental relations (except in certain cases of cyst formation), a voluminous literature has accumulated describing varied developmental origins and anatomical configurations for these pharyngeal appendages.


The terminology and classification used by different workers has led to much confusion concerning the identity of the structures described. Normal and pathological as well as embryonic and mature cases have all been considered together.


Those structures under consideration are the bursa pharyngea, bursa pharyngea embryonalis, and the median pharyngeal recess. Before presenting the problems which have formed the basis of this investigation, it would be advisable to review briefly the literature concerning them.


In the original sense as it was first used by Mayer (1840 and 1842), the term bursa pharyngea was employed to desig-nate an infrequently occurring pathological depression found. in adults in relation to the pharyngeal tonsil.


A similar type of pathological formation was fully described by Luschka (1868) as having a large orifice situated in the median line at the inferior limit of the adenoid tissue and leading into an elongated pocket extending diagonally backward into the periosteum of the occipital bone and having a maximum length of 1.1; cm. and a diameter of 6 mm. He believed it to be the persistence of the oral-hypophyseal duct. It is occasionally referred to as the ‘bursa of Luschka.’

Tornwaldt (1885 and 1887) found by rhinoscopic examination an opening into the pharyngeal mucosa which accorded with Luschka’s description. He attributed to the bursa a special pathology by which, during the course of a chronic pharyngitis, its cavity became filled and dilated and transformed into a cyst. He termed the structure an 'anatomisch selbstandiges G-ebilde'.


The term recessus pharyngeus medius was first used by Ganghofner (1879) to designate the simple depression occupying ordinarily the most posterior part of the median tonsillar groove. He believed that the structures called bursa pharyngea by Mayer, Luschka, and Tornwaldt were nothing more than the pathologically altered median tonsillar fissure which became deepened through the growth of the adenoid tissue. Inflammatory adhesions bridged over the median recess; retention of secretion caused the bulging and enlargement to form the bursa.


The investigations of Schwabach (1887) led him to agree with Ganghofner. In recognition of the prior development of the median recess, he went so far as to designate it as the first anlage of the pharyngeal tonsil. This View has led certain investigators to the conclusion that the recess is comparable to the sinus tonsillaris of the palatine tonsil.


The term bursa pharyngea was also employed by Froriep (1882) to designate a well—developed pocket which he found in the roof of the pharynx of a 38 mm. fetus. Because of the fact that the apex of the bursa was in intimate relation with a mass of notochordal tissue, he concluded that the notochordal contact must have been instrumental in a mechanical Way in the production of the bursa (figs. 11, 12, 13).


In his classical researches, Killian (1888) Was unable to observe the connections seen by Froriep between the notochord and bursa in human foetuses. He believed that the embryonic bursa resulted as the consequence of active formative processes and not from any developmental stress such as notochordal adhesions would indicate.


Excellent summaries of this older literature are given by Killian (1888) and by Oppel (’00).


Conclusive evidence that the formation of the embryonic bursa is in some way linked with notochordal contacts with the pharyngeal epithelium has since been offered by a number of investigators, among whom may be mentioned Meyer (’l0), Link (’1l), Huber (’12), Tourneux (’12), and Radford (’13).


Huber’s careful work has shown that the bursa pharyngea embryonalis is formed at the point where the pharyngeal segment of the notochord has retained in a point its original union with the pharyngeal entoderm. The bursa thus formed lies in the median plane and is separated from Rathke’s pouch by nearly the whole pharyngeal roof.


J. P. Tourneux ( ’12) distinguished between bursa and median recess. He believed the two to be independent structures either occurring separately or superimposed. Thus, the recess was believed to result from the inflection of the head and the adherence of the fascia pharyngobasilaris to the mucous membrane at the level of the angle of the pharynx above the superior constrictor muscle. It forms there a coni-cal depression at the posterior extremity of the median furrow of that organ.


The bursa pharyngea embryonalis is the name Tourneux: gave to the simple depression whose end, in younger embryos, is intimately united with the pharyngeal segment of the basilar notochord, a causal relationship supposedly existing between the two.


In other animals, homologues of the bursa pharyngea embryonalis in man have been found in the horse (Tourneux), ferret (Radford), and after the interpretation of Killian in Arctomys marmota. Radford for the ferret and Meyer for homo both believed that the bursa (median pharyngeal recess) is identical with Seesel’s pocket.


The terms bursa pharyngea embryonalis and median pharyngeal recess will be used in the present discussion as they were defined by Tourneux.

The outstanding problems concerning the bursa and median recess are three in number. The exact role played by the notochord in the formation of the bursa pharyngea embryonalis has not been fully determined. Doubt has recently been expressed concerning the adequacy of the tension hypothesis of Froriep (and others). After the degeneration of the notochord, other factors must be involved in the later transformations of the bursa. Finally, the fate of the embryonic bursa after birth, i.e., the relation between bursa pharyngea embryonalis and the bursa of adult life, has not been definitely established. These are the problems dealt with in the present paper.

Materials and Methods

This study was made incidental to an investigation of the development of the human pharyngeal tonsil. A total of 221 human embryos ranging in size from 7 mm. OA.R. length to newborn were examined. Serial sections of entire embryos and heads out in three planes constituted the majority of the material. In addition to these, the pharyngeal vault and adjacent skull base were removed from thirty-one foetuses (3 months to newborn), studied macroscopically and then sectioned and stained. Of the embryos and fetuses studied, 152 belonged to the Carnegie Institution Department of Embryology. The remaining specimens were from the Cornell collection}

Observations

Frequency of occurrence of bursa

Statistics concerning the frequency of occurrence of the bursa pharyngea vary considerably. The most reliable are

1 I wish to express my thanks to Dr. G. L. Streeter for the use of the Embryo1ogical Collection of the Carnegie Institution and supplying figures 15, 16, and 17. I also wish to thank Prof. B. F. Kingsbury, of Cornell University, for his guidance throughout the course of the work. BURSA PHARYNGEA : HOMO 307

those of Killian. Out of seventy cases examined, bursae were present in forty—two, or 60 per cent. Link found the bursa to be present in over 50 per cent of the cases he examined.

In the present investigation, a distinct burse was not recognizable in embryos under 15 mm. in length. Disregarding twenty embryos under this length, distinct bursae were found in 41 per cent of the 201 remaining specimens. In 45 per cent bursae were lacking; the remaining 14 per cent were questionable or doubtful (extremely thick sections, etc.).

The distribution in the embryos is given in the chart:

Length Number examined Bursae 7n‘e>.s-ant Per cent present Mm. 15-191) 42 6 14 20-24.!) 42 17 40.3 25-299 29 1-1 -18.2 30-50 43 24 55.8 51—99 19 11 57.8 100-200 23 10 43.4 ‘.200—N.B. 3 1 33.3 Totals 201 83 41

These figures, except for the first group, compare favorably with those of other Workers. The low figure for the 15 mm. group may be due to the shallowness of the bursae at that stage, or it may indicate that factors other than notochordal contacts become operative around 20 mm.

External appearances

The size and extent of the bursa pharyngea embryonalis is subject to wide variation. Compare figures 1 to 10. Of special interest is figure 1 and its transverse sections, figures 20 and 21. It possesses, relatively, the largest opening and longest lumen of any bursa studied. No median recess is present. Figures 4 and 9 have distinct median recesses, but no bursae, whereas in figures 8 and 10 the median recess leads directly into a Well—developed bursa (figs. 25 and 27 ).

Intermediate and aberrant forms occur which are difficult to classify. See figures 2 and 5. Sections (fig. 2) give little aid since the relations are masked by extravasated blood, a common occurrence in this portion of the pharynx.

In the region of the attachment of the pharyngeal hypophysis to the pharyngeal epithelium, i.e., in the region of the union of the nasal septum with the pharyngeal Vault, a slit-shaped depression sometimes appears. This was described by Citelli (’11). It may be well marked as in figure 10 or less so, figure 9. The fact that a ‘bursa’ appears at the former site of Rathke’s pouch as well as at the other extreme of the vault necessitates a separate origin for both structures. Inasmuch as Seesel’s pocket, when present, is formed immediately behind Rathke’s pouch, it follows that the bursa pharyngea is an entirely separate structure and not identical with the pocket as postulated by Meyer and Radford. A pharyngeal hypophysis was found in practically every specimen examined.


In sections, the bursa appears in a variety of forms. Extremes are shown in figures 26 and 20 and intermediate types in figures 22, 23, 24 and 25.

Notochordal relations and discussion

From the extensive researches of Meyer, Link, Huber, Tourneux and others it appears to be a well—established fact that the notochord plays an important role in the formation of the bursa pharyngea embryonalis. This notochordal relationship has been found to hold true during the course of the present investigation. See figures 11, 12, 13, 14, 15, and 17.


However, there exists some uncertainty as to the exact nature of this relationship. According to the older views, i.e., those of Froriep and Tourneux, etc., it is the mechanical tension exerted by a strand of chordal cells at the point of fusion with the pharyngeal epithelium which causes the formation of the bursa. Kingsbury (’32) Voices the opinion that it is not clear “hoW such soft fusions of notochordal cellular material and pharyngeal epithelium may be effective in a mechanical way in producing the bursa.” Band (’17) had previously suggested that it was not so much the notochordal cells themselves as the connective tissue sheath forming around them which exerts the tension. There are several specimens in the material examined in which the influence of a notochordal sheath would be out of the question. For example, in figure 14 the notochordal cells and epithelial cells are so intimately fused that it is impossible to tell them apart. In figures 15 and 17 the end of the bursa is embedded in a mass of chordal tissue and is therefore completely separated from any outer connective tissue sheath. Even in figure 11, where a connective tissue sheath appears, the tip of the bursa is in connection with a strand from the mass of ehordal tissue..


The majority of cases show no definite attachments with the connective tissue fascias of the pharyngeal roof. It is a striking feature of the older embryos that the bursa possesses a definite tunica propria of its own (figs. 20 and 25). This tunica propria becomes transformed into lymphatic tissue, however, generally after that for the posterior part of the pharyngeal tonsil has been laid down (figs. 23 and 27).


It thus becomes of importance to analyze more completely the existing relations between notochord, bursa, and fascias during all stages of development; first, to see if the same or different forces act in bursa formation at different stages of growth; and, secondly, to determine what these forces are.


The bursa pharyngea lies at the junction of the vault with the dorsal or posterior pharyngeal wall. It extends between the heads of the musculi longus capitis and a short distance cephalad of the uppermost fibers of the superior constrictor muscle. These relations are characteristic and have been described by Huber.


The fibers of the fascia pharyngobasilaris as they come from the occipital periosteum diverge to form two distinct bundles lying medially to the longus capitis muscles. The antebasilar segment of the notochord reaches the pharyngeal region through this bifurcation, whether a bursa is present (figs. 12 and 13) or absent (fig. 18). Thus, in figures 12 and 13, the tip of a bursa pharyngea is seen attached to a mass of chordal tissue, both lying between the halves of the fascia pharyngobasilaris and the heads of the longus capitis muscles.


Throughout its later development the bursa always retains the above relations. The pharyngeal segment of the notochord begins to degenerate in embryos of about 25 mm. (second month). Examination of the sections of later fetuses reveals that the bursa has followed the former course of the notochord to the periosteum of the occipital bone in some cases (figs. 20 and 25). Since the pharyngeal segment of the chorda appears in such a wide variety of configurations, it is to be expected that the form and extent of the bursa will vary accordingly.


In the younger embryos, one occasionally finds bursae anterior to (rostrad of) the definitive bursa. They are formed at places where other points of contact between epithelium and notochord remain. It is a significant fact that ‘double’ bursae were not found in any of the older fetuses examined. Apparently, the only spot in which a bursa can reach its fullest development is at the region indicated above. Anterior to this point the fibers of the fascia pharyngobasilaris approach the mucosa and the fibers from each half intermingle forming a dense fibrous sheet, thus preventing the ‘bursa’ from enlarging.


Therefore, it is evident that the factors involved in bursa formation are: 1) an interruption of the pharyngeal epithelium by a more or less close union with the notochordal tissue; 2) an independent proliferation of epithelial cells in a region which is neutral as far as developmental stresses are concerned; 3) a continuation of this growth along a line of least resistance, i.e., along the course of the degenerating notochord, is responsible for the later development of the bursa and not tension directly exerted by the chordal cells or the connective tissue sheath surrounding them.

The question whether the embryonic bursa persists after birth to form the cyst-like bursae which were the first described has not been fully answered. The presence of very large bursae in fetuses of 4 months Would lead one to expect that such bursae could, under proper conditions, form a cyst. At birth, the tunica propria of the bursa is occupied by dense lymphatic tissue (fig. 27), a preliminary stage of which is shown in figure 23. The newborn bursa of figure 27 is in the exact location of, and has the typical structural relations, i.e., to musculature and fascias, of a true bursa pharyngea embryonalis. This one example offers strong evidence that the embryonic bursa may persist into post—nata1 life. It is easy to imagine how hypertrophy of the tonsil might occlude the mouth of the bursa and result in the formation of a cyst.

Conclusions

  1. The bursa pharyngea embryonalis is found in at least 40 per cent of the cases from 15 mm. to newborn.
  2. In its later development the bursa probably depends upon epithelial proliferation along the path of the degenerating notochord.
  3. The bursa pharyngea embryonalis persists after birth and forms the bursa pharyngea of the adult.

Literature Cited

CITELLI 1911 L’Ipofisi faringea nella prima e seconda infanzia. Suoi rapporti colla mucosa faringea. e coll’ip0fisi centrale. Anat. Anz., Bd. 38, S. 242-256; 279-302; 334-349.

FRORIEP, A. 1882 Kopfteil der Chorda dorsalis bei menschlichen Embryonen. Beitréigc zur Anat. u. Embryo1., Festgabe Jacob Henle, Bonn, S. 26-40.

GANGHOFNER, FR. 1879 Ueber die Tonsilla und Bursa pharyngea. Sitzungsber. d. k. Akad. d. Wiss. in Wien, Bd. 78, S. 182-212.

HUBER‘, G. C. 1912 On the relation of the chorda dorsalis to the anlage of the pharyngeal bursa or the median pharyngeal recess. Anat. Rec., vol. 6, pp. 373404.

KILLJAN, G. Ueber die Bursa und Tonsilla pharyngea. Eine entwickelungsgeschichtliche und vergleiehen-anatomische Studie. Morphol. Jahrb., Bd. 14, S. 618—711.

Kmcssuxv, B. F. 1932 The developmental significance of the mammalian pharyngeal tonsil: cat. Am. J. Anat., vol. 50, pp. 201-231.

LINCK, A. 1911a. Beitrag zur Kenntnis der menschlichen Chorda dorsalis im Hals und Kopfskelet. Anat. Hefte, Bd. 42. 1911b Ueber die Genese der Bursa pharyngea embryonalis. Zeitschr. f. Ohrenheilk. u. f. d. Krankh. d. Luftwege, Bd. 62, S. 158-181.

LUSCHKA, H. 1868 Das adenoid Gewebe der Pars nasalis des mensehliehen Sehlundkopfes. Arch. f. mikr. Anat.., Bd. 4, S. 1-9.

MAYER, A. F. C. J. 1840 Bursa seu cystis tubae Eustaehianae bei einigen Siiugethieren. Neue Notizen aus dem Gebiete der Natur— und Heil— kunde von Froriep, Bd. 14.

1842 Neue Untersuchungen aus dem Gebiete der Anatolnie und Physiologie. Bonn.

LIEYER, R. 1910 Ueber die Bildung des Reeessus pharyngeus medius, Bursa, pharyngea, in Zusammenhang mit der Chorda. bei menschliehen Embryonen. Anat. Anz., Bd. 37, S. 449-453.

OPPEL, A. 1900 Mundhohle, Bauchspeieheldriise, und Leber, S. 103-123, in Lehrbuch der vergleichenden mikroskopisehen Anatomic der Wirbe1tiere. Teil 3. Ed. Albert Oppel.

RADFOKD, M. 1913 A note on the development of the pharyngeal bursa in the ferret embryo. Anat. Anz., Bd. 44, S. 371-377.

RAND, R. 1917 On the relation of the head chords. to the pharyngeal epithelium in the pig embryo, etc. Anat. Rec., vol. 13, pp. 465-491.

SCHWABACH 1887 Ueber die Bursa pharyngoa. A1-eh. f. mikr. Anat., Bd. 29, S. 61-74.

TOR.N\VALD’1‘ 1887 Zur Frage (ler Burst: plm1'_\'x1g<-:1. Deutsche med. Woch., No. 23, S. 501-502; No. 48, S. 1042-1044.

TOURNEUX, J. P. 1912 Bourse pharyngienn et recessus median de pharynx chez 1’homme et chez le cheval, fossettes pharyngienn et naviculaire chez 1’homme. J. de 1’Anat. et de la Ph_vsiol., Année 48, pp. 516-544. PLATES

Plates

Plate 1

1 Homo; 115 mm. fetus. Pharyngeal vault, showing opening into a large bursa pharyngea embryonalis (below). Nasal septum is shown above. Sections are shown in figures 20 and 21. X 2.8.

2 Homo; 126 mm. fetus. Pharyngeal vault showing an eccentrically placed median pharyngeal recess. Nasal septum above; posterior pharyngeal wall below. X 3.2.

3 Homo; 127 mm. fetus. Pharyngeal vault with opening into a small bursa pharyngea embryonalis. Posterior wall of pharynx is below. X 2.4.

4 Homo; 135 mm. fetus. Pharyngeal vault showing a typical median pharyngeal recess. No bursa is present. The pharyngeal openings of the eustachian tubes are shown on either side. Nasal septum is above. X 2.

5 Homo; 144 mm. fetus. Vault and posterior pharyngeal wall with opening into a bursa at their junction. Atypical shape for the region. X 2.4.

6 Homo; 145 mm. fetus. Pharyngeal vault with a depression at the usual site of the bursa. No bursa is present. X 2.4.

7 Homo; 148 mm. fetus. Pharyngeal vault showing the converging tonsillar folds. A small bursa pharyngea( is seen at the lower (posterior) pole of the tonsil. X 3.2.

8 Homo; 150 mm. fetus. Pharyngeal vault with a deep median recess terminating below in a deep bursa pharyngea. See figure 25. The discoloration is due to extravasated blood. X 2.4.

9 Homo; 180 mm. fetus. Pharyngeal vault with well-developed tonsillar folds, along which are seen centers of lymphocyte proliferation. A median recess is shown below. No bursa is present. X 2.4.

10 Homo; newborn. Pharyngeal vault with adenoid tissue. The deep median groove (recess) terminates below in a bursa (fig. 27). Above is a median depression marking the site of attachment of the pharyngeal hypophysis. X 2.4.

11 Homo; 39 mm. fetus. Median sagittal section. Occipital cartilage above; pharyngeal epithelium below. The tip of the bursa pharyngea embryonalis is in contact with a strand from the notochordal mass. X 32.

12 Homo; 36 mm. fetus. Frontal section. Occipital cartilage above; pharyngeal cavity below. Between the heads of the m. longus capitis and the fascia pharyngobasilaris is the tip of the bursa, directly above which is a mass of notochordal tissue. X 32.

13 Homo; 30 mm. fetus. Transverse section. Occipital cartilage below. Between the two strands of fascia pharyngobasilaris is the tip of a bursa in contact with a notochordal mass. The heads of the m. longus capitis are shown laterally. X 32.

l4 Homo; 18 mm. embryo. Median sagittal section. Occipital cartilage above; pha.r_vngeul cavit_v below. Strands of cells from the notochord are seen in intimate contact with the epithelial cells. It represents an early stage in the formation of the bursa pharyngea embryonalis. X 280.

15 Homo; 23 mm. embr_vo. Frontal section. Occipital cartilage above: pharynx below. Embedded within the mass of notochordnl tissue (center) is seen the tip of the bursa pharyngea. X 160.

16 Name. Section taken more dorsad, showing relation of the notochord to occipital cartilage above, Ill. lougus eapitis laterad, and cavity of pharynx below. X 60.

17 Homo; 33.2 mm. embryo. Frontal see.tiou. Oceipital cartilage above, pharyngeal cavity below. 'l"he extremit_v of the bursa pharyngea (solid black) is shown almost completely surrounded by uotochordal tissue. Between the heads of the m. longus capitis are seen fibers of the fascia pharyngobasilaris. X 60.

18 Homo; 95 mm. fetus. Transverse section of head. A single mass of notochordal material remains between the fascia. and occipital cartilage (above). It illustrates the normal relations of the notochord when no bursa is present. x 24.

19 Homo; 18:’) mm. fetus. The light area below the occipital ossification contains remnants of the chordal sheath, which can be followed for some distance. No bursa. i present. x 16.

20 Homo; 115 mm. fetus. Section cut at right angles to occipital bone (above). Sce figure 1. 'l‘he tip of the large bursa is seen to have exactly the same relations as the corresponding segment of notochord. Longitudinal muscles are laterad: superior constrictor muscle is below. x 16.

Plate 1

21 Same as 20. More ventrad showing opening of bursa into the pharyngeal cavity. X 16.

22 Homo; 125 mm. fetus. Sagittal section through bursa pharyngea embryonalis. Lymphatic tissue is forming ahead of the bursa. Fascia pharyngebasilaris is above. X 26.

23 Homo; 143 mm. fetus. Sagittal section through bursa. The tunica propria around bursa is becoming transformed into lymphatic tissue. X 24.

24 Homo; 144 mm. fetus. Cut transversely to basis cranii. The bursa is surrounded by fascia pharyngobasilaris above, longitudinal muscles laterad, and constrictor muscles below. X 16.

25 Homo; 150 mm. fetus. Transection showing same relations as above. A distinct tunica propria is shown around the epithelium of the bursa. Section of figure 8. X 16.

26 Homo; 80 mm. fetus. Sagittal section showing small bursa pharyngea at lower right. At upper left is seen the cerebral hypophysis Within the sella turcica. At lower left the pharyngeal hypophysis has been plotted in from other sections. The cranio-pharyngeal canal is still open. A portion of the large median vein is shown near center. X 16.

27 Homo; newborn. This bursa possesses the same relations as the younger ones previously described. Its tunica propria has been transformed into dense lymphatic tissue. X 12.


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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

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