Paper - Major features in the developmental history of the human stapes (1940)
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Anson BJ. Major features in the developmental history of the human stapes (1940) Q Bull Northwest Univ Med Sch. 14(4): 250–257. PMC3802317
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Major Features in the Developmental History of the Human Stapes
Barry J. Anson, Ph.D. (Med. Sci.) 1
- Contribution No. 327 from the Anatomical Laboratory of Northwestern University Medical School. An investigation conducted under the auspices of the Central Bureau of Research of the American Otological Society. Received for publication, Sept. 29, 1940.
Most of the bones of the human body arise through the gradual replacement of cartilaginous models by bony material; all the bones of the upper and lower extremities, those of the vertebral column and thorax, the hyoid bone, and the greater part of the bones of the base of the skull belong in this category. Regularly, too, authors include the auditory ossicles.
But the stapes, at least, departs very early from the conventional developmental plan: It begins as a ring—not as a column or a plate—and becomes stirrup-shaped; its full size is attained, by dramatically rapid growth, in the midterm fetus; with the appearance of its single center of ossification, the stapes has already attained its adult dimensions; while still a fetal bone, a longitudinal half of each of its subdivisions is absorbed, marrow and cancellous bone concurrently removed; the ossicle lacks epiphyses, its periosteum is unosteogenic.
These features will now be discussed in connection with a description of histological series of human stapes from prenatal and postnatal stages. The stapes, when first discernible in the embryo of 17.5 mm., is a complete cartilaginous ring (see Anson, Karabin and Martin, 1938),? thus differing in shape from the cartilaginous predecessor of any long bone—clavicle, femur or phalanx. In the embryos of 40, 43 and 50 mm. the primordial annular shape has been altered to such an extent that basal flattening and capital elongation are evident. In the 100-mm. stage the cartilage is definitely stirrupshaped; the base is broadened and lipped marginally, the head is lengthened and foveate on the articular surface, the column-like crura convergent at the capital extremity. The 115-mm., the 120-mm. and the 126-mm. stages are, except for size, like the preceding;® they exhibit progressive increase in length and width, and in thickness of their several parts; in all of them—as an evidence of chondral growth—the perichondrium is thick and poorly delimited.
2 See ‘References Cited’’ in the following article by L. E. Beaton and B. J. Anson.
In the 135-mm. fetus the stapes has already attained its full dimensions (reconstruction, figs. 7, 24 and 25 in Anson, Karabin and Martin, 1938); it is still entirely cartilaginous, and remains so in the 147-mm. fetus. The stapes now resembles an embryonic long bone which has been divided longitudinally in its middle two fourths (fig. 1; cf. fig. la); the capital end retains the typical cylindrical form, but the basal end is flattened (fig. 1).
In the stapes of the 150-mm. and 161 mm. fetuses osteogenesis has just begun (fig. 4).4 The ossification center is oval in outline, basal in position (loc. cit., figs. 9, 28 and 29). The more advanced changes are occurring near the center; marginally in the plaque calcification is the only mark of change, the perichondrial wall being still intact, i.e., unbroken by osteogenetic buds. Centrally, vascular buds, entering the cartilage from the surrounding tissue, produce shallow excavations. So far, the crura and the head are unaltered in fabric, being simple hyaline cartilage.
8 For the opportunity of studying the fetal series herein described, the author is indebted to Professor T. H. Bast of the University of Wisconsin. While a guest in the latter’s laboratory the author was graciously permitted to study the numerous otological series, upon the results of which investigation the present article is an introductory report.
Ossification, then, occurs through spread from a single center situated on the tympanic aspect of the base. Whereas in long bones ossification begins at or near the middle of the ‘‘bone,’”’ in the stapes it is initiated in the flattened, basal, part of what was originally a ring of cartilage. Since the primordial form will be retained in the subsequent stages, the ossification center develops at what might be considered an “extremity”? of the stapes.
It is important, at this point, to recall the regular features in the development of a long bone; with some of them the stapes conforms, from others it differs profoundly.
Ossification begins in a localized area, the center of ossification, which is usually situated near the middle of the cartilage of the future long bone. The first center in the human skeleton appears during the second month of intrauterine life, the last in the third decade of postnatal life. Ossification begins as a deposition of calcareous salts; in this calcifying tissue cartilage is converted into true bone, first through destruction of the calcified cartilage by osteoclasts, second through production of bone by osteoblasts. Secondary (epiphyseal) centers appear during infancy or early childhood, only one later than the ninth month.
4 The photomicrographs in figs. 4 to 9 were prepared from the following series: Fig. 4, 150 mm., no. 39 (slide 22, section 8); fig. 5, 205 mm., no. 129 (20, 3); fig. 6, 210 mm., no. 51 (38, 5); fig. 7, 180 mm., no. 45 B (15, 5); fig. 8, 180 mm., no. 45 B (17, 9); fig. 9, 290 mm., no. 59 (36, 5). The original magnifications are as follows: fig. 4, 23 diameters; figs. 5 and 6, 18; figs. 7, 8 and 9, 130. All have been reduced in reproduction. Abbreviations used in figs. 4 to 9: A.c., anterior crus, A.l., annular ligament, B., -base., C., cartilage, E.b., endochondral bone, H., head, I., incus., Is.j., incudo-stapedial joint, M., marrow, N., neck, O.c., ossification center, P.b., perichondrial bone, P.c., posterior crus, T.c., tympanic cavity, V., vestibule.
In fig. 5 the circle indicates the approximate area photomicrographed in fig. 8 (older stage).
Within the core of cartilage endochondral bone formation occurs; the chondral matrix, first calcified, disintegrates through the activity of vascular buds derived from the perichondrium; upon the persisting spicules of cartilage the osteoblasts deposit bone matrix. This process goes on until the original cartilage is entirely replaced by bone. On the outside the perichondrium is converted into an osteogenic layer; as it deposits bone matrix, central resorption concurrently destroys the endochondral tissue. As a result, in the middle region of a long bone an extensive open cavity develops, cancellous bone remaining only at the extremities. The cartilage at either end grows rapidly and progressively ossifies; usually between birth and puberty, osteogenic tissue invades these terminal cartilages and secondary ossification centers (epiphyses) are established; on both surfaces of the cartilaginous plate which intervenes between epiphysis and diaphysis new cartilage develops as long as the bone lengthens, and is in turn steadily replaced by bone matrix. When the adult length is attained, proliferation ceases, the epiphyses becoming united with the diaphysis.
In the stapes, as has been shown, secondary centers do not occur; stapedial development, therefore, resembles that obtaining within the diaphyseal portion of a long bone: both endochondral and perichondrial plates are formed; marrow tissue is produced within excavations in the cartilage. But as soon as these ‘“‘diaphyseal”’ features are established, the ensuing formative stages become specialized, are of a unique type; these will now be discussed.
In the 163-mm. fetus the basal portion of the stapes is in the stage preparatory for perichondrial ossification: the surface is broken by osteogenic buds, perichondrial bone is not yet formed; the production of endochondral bone, however, has just been initiated, cartilage remaining in the crypts in the form of elongate, eroded, spicules. In each of these cartilage remnants the same series of changes is occurring: the cartilage is excavated, the lacunae opened; their original cells are in part removed, the latter being replaced by those derived from the mesenchyma. Externally, the mesenchymal tissue is gradually modified to form a perichondrium; internally, along certain of the persisting spicules, the tissue is definitely osteoblastic, the cells being arranged in lines. Calcification is spreading along the inner surface of each crus at the basal end; but in the capital portions of the crura, and in the head, cartilage is as yet unaltered. In skeletal elements generally, at this stage in fetal development, cartilage is extremely active. But in the stapes multiplication of cartilage cells is scarcely perceptible after bone formation has begun. Cartilage is as inactive in the fetal stapes as it is in a long bone after puberty has been reached.
In the 146-mm. fetus excavation of the stapedial base and crura is pronounced, as is concurrent formation of periosteal bone;® the periosteal bony plate is foraminous, osteogenic tissue passing through the openings from the perichondrium. The tissue within the excavated crypt, being a primitive marrow, is already distinguishable from the surrounding mesenchyma.
In the 160-mm. fetus ossification is even further advanced. Excavation of the stapedial base is deep and has progressed peripherally to the point of junction of base and crus.
With the formation of a perichondrial shell of bone around an excavated cartilaginous core within which endochondral spicules are being laid down, the mechanism is set in operation by which a solid chondral “‘ossicle,’’ of stapedial shape, is converted into a hollowed osseous element of similar size and outline. The endochondral bone, as will be shown, is transitory, being later removed entirely; a portion of the perichondrial bone is likewise destined to be destroyed; the bone of the completed ossicle is totally of the compact variety, and is persistent along what would correspond to a longitudinal half of a long bone.
5 The recorded crown-rump length is not an index to stapedial morphogenesis; actually, the developmental series is as follows: 126 mm. (no. 11); 135 mm. (no. 5.); 147 mm. (no. 38); 161 mm. (no. 13); 146 mm. (no. 30); 160 mm. (no. 41).
Complete destruction of cartilage, save as terminal cylinders, characterizes stapedial anatomy in the 183-mm. embryo (fig. 2);° progressive invasion has resulted in the destruction of all but basal and capital cartilages. But in this same stage a further step in erosion is observed which does occur in long bones: the surfaces of the entire stapes which face the obturator foramen are being gradually destroyed by osteoclasts, leaving a foraminous inner wall (see following article, fig. 2). The crura, base, and neck of the stapes now constitute continuous parts of a tubular bone, the capital and basal openings in the latter being occupied by cartilage —of cylindrical and of plate-like form, respectively (depicted as separated in fig. 2). The stapes may now be likened to a hypothetical long bone double through its middle two-fourths (fig. 2, cf. fig. 2 a); it resembles a long bone which is incompletely bifid, diaphyseal in character (since it lacks epiphyses), flattened at one extremity into a basal portion. Unlike a long bone, its growth ceases just as soon as it is formed in osseous tissue.
In the stage just described destruction of bone on the inner walls of the crura is a slow process; osteoclasts, in many sections in a series, are not to be found. Their absence is not, however, astonishing, since they are also wanting in portions of the otic capsule which are, simultaneously, undergoing remodeling. The crura are columns of periosteal bone, extensively fenestrated on the facing aspects; within them is a marrow tissue; endochondral bone occurs only at the head (fig. 7) and at the base (fig. 8). Both the foraminous wall and the contained spicules will subsequently be destroyed; this is a curious developmental fact, since, unlike conditions in the developing long bones, the permanent parts of the crura are already present (being the externally placed longitudinal half of each crus); it is as if the crura, in the process of remodelling, passed through developmental stages which were not requisite to their ultimate structure — governed by unalterable laws of construction, serviceable in bones generally, but a vestigial succession of architectural changes in the case of the ossicle. The cartilage of the base is excavated in such a way that an oval crypt is formed; upon this excavated surface bone has not yet been deposited—in fact, deposition of bone does not begin until erosion of cartilage has progressed so far that the original base remains merely as a thin plate.
6 See figs. 1 to 4 in the following article by L. E. Beaton and B. J. Anson; the latter illustrations trace major stages in stapedial morphogenesis (161 mm. fetus to adult of 57 years).
Figures 1 to 3. Diagrammatic representations of stages in the development of the stapes. Figures 1a, 2a, 3a. Comparable stages in the formation of a hypothetical long bone.
In the fetus of 205-mm. the internal foraminous wall of each crus is largely removed; the cartilaginous part of the base is characteristically lipped marginally (fig. 5). On the tympanic surface of the cartilaginous basal lamina bone is now being deposited. The space within the base and crura still contains marrow. Developmental change is slower in the head than in the base; the head resembles a short solid cylinder; its outer surface is smooth (for articulation), its inner one is still undergoing excavation.
In the 210 mm. fetus the stapes resembles more closely the ossicle in the child (fig. 6). The crura are thin; their facing (internal) walls are entirely removed.’ In the base the earlier hollowed character is represented by the persistence of a ledge; between it and the basal plate marrow is still present. New bone has crept along the floor of the excavated crypt to form an osseous lamina. The bone of the newly formed lamina is not everywhere contiguous with the old cartilage, space, at several points, existing between the two; it is possible that this represents the space —haversian in function if not in character and mode of formation—which is seen in the stapes of some early postnatal specimens (Anson, Karabin and Martin, 1939, fig. 41). The head is deeply excavated, yet removal of cartilage is not complete; bone has not covered its internal aspect. All phases of the process which is here operative in the neck and head were observed in the remodelling of the base, but at an appreciably earlier stage.
- Within the stapes, then, all of the original endochondral, some of the early perichondrial, bone is removed to produce an ossicle whose form suggests that of a deeply guttered diaphysis. But within the otic capsule both types of bone persist (figs. 5, 6 and 7); by their progressive spread the capsule is rendered solid, or ‘‘petrous.” Yet, just as cartilage remains throughout adult life in certain areas of the stapes, so it does also in fissular tracts situated in the otic capsule in front of and behind the vestibular window; these are respectively, the fissula ante fenestram (figs. 5 and 6) and the fossula post fenestram. These structures have been described in recent articles by Bast (1930, 1933, 1936, 1938), Anson and Martin (1935), Anson, Karabin and Martin (1938, 1939), Anson and Wilson (1939).
The process by which a foraminous inner wall of the stapedial ‘‘ring’’ is gradually removed is an interesting one; in a sense it is comparable to that through which marrow tissue in the young temporal bone is replaced by pneumatic spaces. In the case of the ossicle, however, the erosion produces a continuous trough, not a series of intercommunicating air-cells. The separate foramina which are present along the base, crura and neck in the stapes of the 193-mm. fetus become coalescent as the intervening bone is absorbed. The hollow thus produced faces the obturator foramen; it is continuous, being gutter-like along the crura, a lozenge-shaped excavation on the base, a deep cup-like recess in the neck and head (cf. fig. 3). Concurrently primitive marrow is replaced by connective tissue, the latter becoming a submucosal tissue as the lining membrane of the tympanic cavity is draped over the ossicle. Cartilage persists on the two extremities, laterally forming an articular surface for the incus, medially being articular on the circumference of base, merely covered by an extension of the annular ligament on the vestibular surface. Internal to each cartilaginous lamina bone spreads across the gap as it does in closing the extremities of a diaphysis. The gradual extension of the bone across the pre-existent cartilaginous lamina, and the concurrent removal of the fenestrated internal layer of periosteal bone, are then, the two principal features marking the second stage in the development of the osseous stapes. These alterations are accomplished without over-all increase in size; once bone has formed a complete ring—i.e., a continuous annulet from the head through the crura across the base—no appreciable increase in dimensions occurs; unlike a long bone, the stapes possesses no epiphyseal areas which would permit of growth.
Figures 4 to 9. Photomicrographs of sections of fetal stapes (see footnote 4). Fig. 4, x 16; figs. 5 and 6, x 12; figs. 7 to 9, x 88. For abbreviations see footnote 4.
The changes observed are in the nature of reshaping, not of enlargement. The persistent cartilage occurs as stratum to which bone is applied, not as an area of epiphyseal character. From a modified osseous ring whose basal and capital openings (externally situated) are covered over by cartilage (fig. 2; cf. fig. 2 a), the ossicle is thus converted into a truly stapedial element whose open portion (now internally placed) is continuous along its inner circumference (fig. 3; cf. fig. 3 a). In its major features the stapes is now an adult ossicle.
In the 260-mm., 275-mm. and 290-mm. fetuses the base consists of two complete layers, the vestibular lamina being the remnant of the primordial cartilage, the tympanic being new bone of periosteal form; between the two there is seemingly no space (fig. 9). The head is deeply excavated; the articular portion is thin and bilaminar, bone has invested the internal surface. The crura are thin and of the simple channelled form.
In the fetus of 310 mm. the stapes could be mistaken for the ossicle in a postnatal stage. The vestibular surface of the base is smooth, the tympanic surface is irregular, the irregularities in the cartilage layer fitting into corresponding ones on the contiguous bony layer.
In the 345-mm. and 370-mm. fetuses the stapes resembles, in every respect, that of an adult; the base is bilaminar, in thickness being three-fourths cartilage, one-fourth bone. The crura are channelled, their cavities being continuous with the excavations in the head and neck and the base. The base, in undergoing final remodelling, comes to resemble, in certain respects, the extremity of a long bone; it is cartilaginous on its outer, osseous on its inner, surface; it is terminal; marginally it fits into a space—i.e., is in part articular. But it differs profoundly from an extremity of a long bone in being open to the tissues in which it is lodged, in being composed of a compact type of bone only, and finally, in being immediately invested by a liga ment, and not associated with a synovial cavity.
The ossicle as a whole is remarkable in its retention of fetal dimensions. While in a typical long bone increase in breadth is accomplished through the deposition of matrix in the deeper layer of the perichondrium, in the stapes periosteal bone formation is minimal. Whereas in a femur the diameter increases by ten times between midfetal life and puberty, the corresponding dimension of a stapedial does not increase at all; the persistence of cancellous bone and associated marrow, so characteristic of long bones generally, is never a feature in the anatomy of the fully formed stapes; both marrowtissue and endochondrial bone are removed when the parts of the stapes are converted from tubular into channelled members. While long bones lack osteogenic periosteum on their articular surfaces, the stapes lacks it on all surfaces. And while, through the possession of an adaptive mechanism—the secondary center of ossification—the long bones increase in length, the stapes loses all potentialities for elongation in the want to epiphyseal areas of growth. Some bones retain epiphyses through the twenty-fifth year of life; the stapes, on the contrary, does not possess secondary centers at any stage in its development, develops from a single primary center situated in its base. The stapes, having no means of lengthening, is as long in the midterm fetus as it will ever be. Instead of having to fuse with epiphyseal ossification center, the crura, etc.,—which are modified diaphyses—merely close over terminally, the bony laminae of head and base lying internal to thin cartilaginous plates. Only the lateral (tympanic) extremity of the stapes is of true articular type; the medial (vestibular) extremity is articular marginally, the flattened surface closing a fenestral orifice in the otic apsule.
Anson BJ. Karabin JE. and Martin J. Stapes, fissula ante fenestram and associated structures in man: I. From embryo of seven weeks to that of twenty-one weeks (1938) Arch. Otolaryng. 28: 676-697.
Anson BJ. Karabin JE. and Martin J. Stapes, fissula ante fenestram and associated structures in man: II. From Fetus at Term to Adult of Seventy (1938) Arch. Otolaryng. 28: 676-697.
Anson BJ. and Martin J. Fissula Ante Fenestram: Its Form and Contents in Early Life. (1935) Arch. Otolarying. 21; 303-323.
Anson, B. J. and Wilson, J. G.: Structure of the Petrous Portion of the Temporal Bone with Special Reference to the Tissues in the Fissular Region, Arch. Otolaryng., 1939, 30;922-942.
Bast TH. Ossification of the Otic Capsule: in Human Fetuses. (1939) Contrib. Embryol. (no 121) 21: 52-93.
Bast TH. Development of the Otic Capsule: II. The Origin, Development and Significance of the Fissula Ante Fenestram and Its Relation to Otoscerotic Foci. (1939) Arch. Otolaryng. 18: 1-20.
Bast TH. Development of otic capsule III. Fetal and infantile changes in fissular region and their probable relationship to formation of otosclerotic foci. (1936) Arch. Otolaryng. 23: 509-525.
Bast TH. Development of otic capsule IV. Fossula Post Fenestram. (1938) Arch. Otolaryng. 27: 402-412.
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