Paper - The development of the sphenoidal sinus in man and its homology in mammals (1927)
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van Gilse PH. The development of the sphenoidal sinus in man and its homology in mammals. (1927) J Anat. 61(2): 153-166. PMID 17104130
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The development of the sphenoidal sinus in man and its homology in mammals
By P. H. G. Van Gilse, M.D. (Amsterdam)
The hinder part of the nasal cavity in the Mammals, with the exception of the Primates, is provided, as has been observed by Dursy, with a double floor. Of this double floor, the lower stage is the palate, the upper transversales and between the two is the ductus naso-pharyngeus which is continuous with the lower part (pars respiratoria) of the nasal cavity.
Dursy states that a similar division of the hinder part of the nasal cavity into olfactory and respiratory parts would be present in man if the conchae Bertini, which form the front wall of the sphenoidal sinus, were turned downwards, as in his opinion the conchae Bertini correspond to the laminae transversales. He compares them to a drawbridge which is pulled up in man and lowered in most other Mammals (fig. 2).
Before Dursy the homology of the conchae Bertini and the laminae transversales had already been formulated by Cleland. Dursy pursued the subject further by studying mammalian embryos in which the nasal capsule is still cartilaginous. He states that even in early stages similar conditions are to be seen: an upper or olfactory chamber of the nasal cavity being separated from a respiratory chamber or ductus naso-pharyngeus by the laminae transversales (cartilagineae) (fig. 3).
In human embryos he observed very small prolongations of the upper part of the nasal cavity extending backwards on either side of the cartilaginous sphenoid. These small recesses are, in his opinion, the rudiments or Anlage of the sphenoidal sinuses (fig. 4). The cavum naso-pharyngeum is situated below these recesses.
Dursy came to the conclusion that the recesses observable in the human embryo represent the posterior part of the olfactory chamber of Mammals. He says: ‘“‘Somit besitzt auch der Mensch im hintersten Abschnitt der Nasenhéhle eine Abscheidung in eine obere und eine untere Partie, jedoch mit dem Unterschied, dass die obere Partie nur einen Ausserst kleinen Anhang der Regio olfactoria oder die Anlage der Keilbeinhéhlen darstellt.”” These recesses grow into the sphenoid, where they give rise to the permanent sphenoidal sinuses. Later authors (Toldt, Zuckerkandl, etc.) confirm Dursy’s opinion.
It seems to me, however, that the problem needs further investigation, for: (1) The comparison of the conchae Bertini to a drawbridge, which is pulled up in man, is open to criticism. Primitively, the conchae Bertini are not concerned in providing the front wall of the sphenoidal cavity only, as Bertini himself described them as plates bent upon themselves. Toldt has taught us that originally the concha Bertini is the ossified cartilaginous capsula posterior nasi which is completely closed behind. A bony capsule, which is closed on all sides with the exception of an opening in front and which is separated from the sphenoid by connective tissue, can be isolated in young children. At a later stage this capsule fuses with the sphenoid. After this fusion has taken place the posterior wall is absorbed, and the pneumatisation of the sphenoid begins as the result of an invasion by the mucous membrane which lines the nasal cavity. These changes I have described and briefly discussed in the Zeitschrift f. Hals-, Nasen- und Ohren-heilkunde. Thus of the original bony capsule the front wall and part of the floor alone persist and they also form the front wall and part of the floor of the sphenoidal sinus. These persisting parts of the nasal capsule are the “conchae sphenoidales” of Bertin. (2) Dursy states in his article (p. 197): ‘““Auch bei den Saugetieren greift das hintere Ende der Regio olfactoria in die Keilbeingegend ein, aber in viel starkerem Masse, sodass aus diesem Grunde besondere Keilbeinhéhlen nicht verkommen, oder es bilden vielmehr diese Héhlen bei den Saéugern keinen Anhang der Nasenhohlen, sondern gehen ganzlich in die Nasenhéhlen auf.” According to this view the part of the nasal cavity which lies above the laminae transversales is represented by. the widened sphenoidal sinus (p. 96). He particularly emphasises the fact that he never found a true sphenoidal sinus in adult Mammals. The view that a sphenoidal sinus is non-existent in Mammals is, however, a misconception. Certainly there are Mammals which have no sphenoidal sinuses, e.g. Canis familiaris, but there are others in which a true sphenoidal cavity exists, e.g. Felis domestica, where the sphenoidal cavity communicates with the general nasal cavity by a somewhat narrow entrance.
Fig. 4. Human embryo of 26 mm. length. Frontal section through the posterior part of the nose.
If there is a strict homology between the laminae transversales and the conchae Bertini, it should be possible to demonstrate: (1) that the osseous laminae transversales of the adult animal are simply parts of a bony capsule limiting the posterior part of the nasal cavity; (2) that the real sinus within the sphenoid, as occurs in the adult cat, is the result of a pneumatisation of the sphenoid by the mucous membrane lining the posterior part of the nasal cavity. ,
In order to determine these points I studied the development of the posterior part of the human nasal cavity and compared it with that in several Mammals, more especially with that in the cat.
If a sagittal section of the nose of a human embryo of 50 mm. length (fig. 5) be examined, the posterior part of the cartilaginous nasal capsule (cupula nasi posterior) is seen to be entirely separated from the basal plate (the cartilaginous precursor of the bony sphenoid). The recess of the nasal cavity lodged in the cupula is the rudiment or Anlage of the sphenoidal sinus. Below the recess is a small piece of cartilage. In a coronal section through the posterior part of the nose of a younger human embryo of 25 mm. (fig. 4) ' the same piece of cartilage again appears below the recess. This cartilage is the remnant of the lamina transversalis, which in animals forms a continuous floor for the regio olfactoria (fig. 3).
As a result of examining a large number of serial sections of human embryos, I found that there were three chief stages in the developmental history of the posterior end of the nasal capsule surrounding the sphenoidal sinus.
The first stage was seen in three human embryos (of 84, 55 and 56 mm. length). The cartilaginous skeleton is here composed of a median part, which develops later on into the bony presphenoid, and two lateral parts, one on either side. There is a slight fusion between these medial and lateral parts in the upper part of the nasal cavity (fig. 6, embryo of 56 mm.).
In the second stage, which was found in four embryos of 36, 59, 70 and 90 mm. respectively, not only has the upper connection between the medial and lateral cartilages become more extensive, but a second and lower connection has made its appearance between them. Further, in coronal sections of the anterior part of the sinus capularis a downwardly growing process of the medial cartilage is apparent. If serial sections of these embryos are traced from before backwards, a closed cartilaginous ring surrounding the recess of the nasal cavity eventually comes into view. The connections between the lateral and the medial cartilages do not extend throughout the capsule. Thus it comes about that in the hindmost sections the medial and lateral cartilages are entirely separated from each other by connective tissue (fig. 7).
Fig. 5. Human embryo of 50 mm. length. Sagittal section of the nose.
Fig. 6 (a-d). Human embryo of 56 mm. length. Frontal sections: a, through the entrance of the recessus cupularis; d, behind the recessus.
In the third stage, which was found in three embryos, all 90 mm. long, the sinus cupularis is surrounded on all sides by cartilage, which in this stage is more extensive and is disposed in the form of a tube unconnected with the median cartilage (fig. 8). In a sagittal section of an older human embryo of 43 months (fig. 9), it is seen that the hinder wall of the cupula posterior and the front part of the still cartilaginous sphenoid are separated from each other by connective tissue.
In a sagittal section of the head of a new-born child (fig. 10), it can be seen that the ossification of the posterior end of the nasal capsule has commenced, but it is still separared by connective tissue from the sphenoid which is now ossified.
When ossification, the details of which need not be described here, is completed, the recessus cupularis (posterior) is surrounded on all sides, even posteriorly, by a bony capsule which, however, has an opening or deficiency in its front wall (fig. 11). This bony capsule is the fully developed concha, or perhaps it would be better to term it the “capsula,” Bertini.
The connective tissue between the osseous cupula nasi posterior and the sphenoid disappears. It is not until the fusion of these parts is completed that the pneumatisation of the sphenoid, by absorption of bone as a result of its invasion by the mucous membrane lining the sinus cupularis, commences.
Fig. 12 is a drawing of the front of the sphenoid bone (the capsulae Bertini are not present) of a child of about four years. Here the absorption of the sphenoid has commenced on either side at the “‘planum resorptionis” in the typical situations. _
Pneumatisation gradually progresses and the posterior boundary of the sinus recedes until at the twelfth or fourteenth year, in normal cases, the sella turcica is reached and penumatisation is mainly completed (fig. 18).
In a sagittal section of a foetal cat (some days before birth) (fig. 14) the recessus cupularis is seen to occupy the still cartilaginous cupula posterior of the nasal capsule, which is separated from the sphenoid by connective tissue. Ossification, both endo- and peri-chondral, is commencing in the lamina transversalis which provides a floor for the recessus cupularis.
Here again the ossification of the posterior part of the capsula nasi is seen to be independent of the sphenoid which has already ossified.
A similar section of a kitten a few weeks old (fig. 15) shows that the sphenoid is still unoccupied by a sinus; the (posterior-) inferior ethmo-turbinal now projects into the recessus cupularis.
Fig. 7 (a-f). Human embryo of 70mm. length. Frontal sections: a, through the entrance of the recessus cupularis; f, behind the recessus.
Fig. 8 (a-d). Human embryo of 90mm. length. Frontal sections: a, through the entrance of the recessus cupularis; d, behind the recessus.
In a young cat with milk teeth (fig. 16) pneumatisation of the sphenoid has commenced and a cavity extends backwards about half-way through the pre-sphenoid.
In a paramedian section of the skull of an adult cat (fig. 17) a large cavity is seen occupying the pre-sphenoid and extending backwards nearly as far as the post-sphenoid, in other words, a true sphenoidal sinus is present.
The situation of the original recessus cupularis is indicated by the inferior ethmo-turbinal.
Fig. 9. Human embryo of 44 months. Sagittal section of the nose.
As has already been noted, a coronal section of an embryo of 60 mm. in the region of the posterior end of the cartilaginons cupula nasi shows that the regio olfactoria of the nasal cavity is separated from the regio respiratoria by the lamina transversalis (fig. 3). The postero-inferior concha projects into the sinus cupularis, the lining wall of which is invaginated.
If sections of the structures situated further backwards are examined it is seen that the cartilage of the cupula posterior is separated from the sphenoid by connective tissue.
The examination of a sagittal section of the skull of an adult dog (fig. 1) shows that a recessus cupularis exists and that the ossified cupula posterior is fused with the sphenoid, but as no pneumatisation of the sphenoid has taken place, no true sphenoidal sinus exists.
Thus the conditions of affairs in the adult dog correspond in general with those in the cat of a few weeks old: the recessus cupularis posterior exists in both, but in neither is there a pneumatic cavity within the sphenoid.
In the cat, however, as in man, the recessus extends backwards by a secondary pneumatisation of the sphenoid, after the ossified has fused with the ossified sphenoid. In the cat and in man the cupula posterior and the sphenoid ossify independently of each other.
Fig. 11. Child of about 6 years. Schematic horizontal section through the sphenoid and posterior part of the ethmoid. Beginning of (secondary) pneumatisation.
Fig. 12. Frontal aspect of the sphenoid of a child Fig. 13. Schematical sagittal section of about 4 years. of the human sphenoid with indication of different stages of development of the sinus.
The human sphenoidal sinus, in which the recessus cupularis is included, is to be compared with the conditions existing in the cat, to the sphenoidal cavity of which animal the recessus cupularis posterior must be added.
Zuckerkandl said that in animals with five and more “ Riechwiilste in der medialen Reihe”’ a part of the fifth (or more) is situated in the “ Keilbeinnische.” In man a remnant of such a “‘Keilbeinmuschel” is to be found as the supero-lateral part of the front wall bounding the opening into the “‘sinus sphenoidalis.”
In fig. 9, which represents the conditions in a human embryo of 44 months, the position of this rudimentary turbinal is indicated by an arrow. The rest of the front wall is formed by an upgrowing fold of mucous membrane containing connective tissue (fig. 10) in which dermal ossification occurs, whereas the upper part ossifies by endochondral ossification.
Occasionally a fine fissure is found in the front wall of the sphenoidal sinus in adult human skulls and when present indicates the line of junction of the two parts of which this wall is composed. The curved spiral edge bounding the opening into the’ sinus which was found in the specimen represented by fig. 18, may be explained as an exhibition of a characteristic feature of a turbinal.
An irregularity, which may have the form of a process, of the lateral cartilaginous wall of the recessus cupularis found in some human embryos (fig. 7) can be considered as a remnant of another turbinal.
The body of the sphenoid normally consists of two parts, viz. the ossified anterior part of the basal plate (post- with pre-sphenoid) and the ossified cupula posterior of the nasal capsule.
The front wall of the sphenoidal sinus together with the anterior part of the sinus in man and the anterior part of the sinus in those animals which possess a true sphenoidal sinus belong to the cupula posterior of the nasal capsule (recessus cupularis posterior). In animals in which a pneumatised sphenoid does not exist, the front wall of the pre-sphenoid together with a recessus behind the inferior ethmo-turbinal (“‘Keilbeinnische”) also belong to the cupula. The lamina transversalis, or its rudimentary representative in man, is a part of this cupula.
That the rudiment (Anlage) of the sphenoidal sinus of man is homologous with the posterior part of the regio olfactoria may be taken as proved, but that in man as compared with other animals a relative “withdrawal” (“sich Zuruckziehen”’) of the ethmoid or of the turbinals from the sphenoidal sinus has taken place (Zuckerkandl) is not a legitimate conclusion. The rudimentary turbinal, which forms part of the front wall of the sinus in man, occupies very nearly the same position in the recessus cupularis as does the posterior end of the fully developed concha sphenoidalis in the cat.
Zuckerkandl’s statement that: ‘den Héhlen des Keilbeins fallt demnach bulbus olfactorius vielfach die Aufgabe zu, Riechwiilste zu beherbergen” is inexact. Paulli’s opinion that the sinus sphenoidalis is an “‘abgeschnittener Teil der Regio olfactoria,” which in appearance only has the characteristics of a pneumatic cavity, is a fallacy. The cavity, which is bounded by the cupula nasi posterior cartilaginea or ossea (concha) Bertini, I propose, at the suggestion of Professor Bolk, to call lamina cribrosa the palaio-sinus (sphenoidalis). The cavity within the sphenoid, which appears after the fusion of the cupula posterior with the sphenoid and results from the absorption of bone due to the growth activity of the mucous membrane, may be called the neo-sinus.
Fig. 14. Felis domestica some days before birth. Sagittal section through the posterior part of the nose. Ossification of the lamina transversalis in beginning.
Fig. 15. Felis domestica a few weeks old. Sagittal section of the skull.
Fig. 16. Felis domestica with milk-teeth.
Fig. 17. Adult Felis domestica. Sagittal Beginning of pneumatisation of the section of the skull. A sinus within the sphenoid. sphenoid is present.
Fig. 18. Inner aspect of the sphenoidal sinus of an adult man.
Thus the sphenoidal sinus of man, as it is normally described, consists of a palaio-sinus plus a neo-sinus.
The palaio-sinus is present in those animals which have no cavity in the sphenoid and is represented in them by the recessus cupularis posterior.
In animals with a pneumatised sphenoid, e.g. the cat, the part of the “‘sphenoidal sinus” which contains the posterior end of the inferior (‘‘sphenoidal”’) turbinal is palaio-sinus, the rest of the cavity being neo-sinus.
Finally I wish to emphasise the fact that the epithelium which lines the — cavity of the recessus cupularis in the human embryo (fig. 19 a) is obviously thinner than in those parts of the nose where olfactory mucous membrane never appears (fig. 19). This thicker epithelium, which is especially obvious in the upper part of the recessus, resembles the epithelium in those parts where, at a later stage, the olfactory mucous. membrane makes its appearance.
Fig. 19 (a-c). Schematic drawings of the thickness of the epithelium in different parts of the human embryonic nose.
That this epithelium is peculiar is very evident under high magnification, as an indication of a membrana limitans can be detected, while here and there nerve fibres of the bulbus olfactorius seem to be connected with the epithelial cells.
This histological evidence supports the view, that the Anlage of the sphenoidal sinus in the human embryo is a part of the olfactory chamber.
All investigators, indeed, are of the opinion that in adults the sphenoidal sinus, including even its anterior part, has no sensory epithelium. The investigations of E. Read, however, show that in the noses of young individuals the surface of olfactory epithelium is relatively more extensive than it is in adults. Consequently, a diminution of the sensory epithelium of the recessus cupularis in later developmental stages is not a matter for surprise. The epithelium of the mucous membrane of the sinus in a new-born child is also of the same non-olfactory character as that of the accessory sinuses of adults.
- The “sphenoidal sinus” of adult man consists of two parts, viz. the recessus cupularis posterior capsulae nasi (palaio-sinus) and the proper cavity in the ossified front part of the basal plate (neo-sinus).
- The neo-sinus is formed by a secondary pneumatisation of the bone.
- In animals which have no pneumatised sphenoid the palaio-sinus is represented by the recessus cupularis posterior of the olfactory chamber.
- In those animals which have a cavity in the sphenoidal bone, this is the result of a secondary pneumatisation and corresponds to the neo-sinus of man.
- The epithelium of the mucous membrane in the palaio-sinus of the human embryo presents the features of embryonic olfactory epithelium.
- The opinion of Dursy, viz. that the sphenoidal sinus of man is homologous with the posterior part of the olfactory chamber of quadrupeds, is essentially correct, but his argument supporting this view cannot be accepted.
1. Berrrini (1744). “Description de deux os inconnus.” Ac. roy. d. sc. 29 Juillet.
2. CLELAND, JoHN (1863). ‘On the relations of vomer, ethmoid and intermaxillary bones.” Philos. Trans. of the Roy. Soc. London, vol. cuit.
3. Dursy, Emm (1869), Zur Entwickelungsgeschichte des Kopfes des Menschen und der hoheren Wirbeltiere. Tiibingen.
4, v. Gitsg, P. H. G. (1922). “Zur Pneumatisation der Keilbeinhéhle.” Z. f. Hals-, Nasenund Ohren-heilkunde, Bd. 111.
5. Pav, Smmon. “Ueber die Pneumacitét des Schidels bei den Saugetieren.” Morphol. Jahrb. Bd. xxvii.
6. Rzap, E. A. “A contribution to the knowledge of the olfactory apparatus in dog, cat and man.” Amer. Journ. of Anat. vol. vat, No. 1.
7. Toxprt, C. (1883). “ Osteologische Mitteilungen.” Lotos Jahrb. f. Naturw. Neue Folge, Bde. 3 u. 4.
8. ZUCKERKANDL, E. (1893). Normale und pathologische Anatomie der Nasenhdhle und der pneumatischen Anhdnge, 2e Aufl. Bd. 1.
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