Paper - The developmental anatomy of the human osseous skeleton during the embryonic, fetal and circumnatal periods
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The Developmental Anatomy Of The Human Osseous Skeleton During The Embryonic, Fetal And Circumnatal Periods
Charles R. Noback
Department Of Anatomy, University Of Minnesota, Minneapolis
Four Plates (Eight figures)
The literature of the developmental anatomy of the gross human prenatal osseous skeleton has been primarily concerned with the time of appearance, the number and location of the ossification centers, the determination of fetal age on the basis of the presence and absence of specific centers, the interpretation of osseous anomalies, the development of the individual bones, and the relation of certain extrinsic and intrinsic factors to skeletal development. A few systematic researches have been made presenting pictorial and Verbal descriptions of the general morphological development of the osseous skeleton as a unit (Kerkring, 1670, 1717; Albinus, 1737; Rambaud and Renault, 1864; Lambertz, ’00; Alexander, ’06; Mall, ’06; Hess, ’17; Dorland and Hubeny, ’26, and others). No worker has figured the development of the prenatal skeleton in a series of orthoscopio drawings held to some constant dimension.
With this in mind, the purpose of this paper is to present, first, a pictorial and a brief verbal description of the development of the human skeleton up to and including the time of birth, by seven stages based on the examination of a series of stained transparent embryos and fetuses; second, some observations of the developmental anatomy of some of the individual bones; and third, some general concepts pertaining to the prenatal skeleton. No attempt is made to assay the determination of fetal age by fetal osteology.
- Portion of the thesis submitted to the faculty of the Graduate School of the
University of Minnesota in partial fulfillment of the requirements of the degree of Doctor of Philosophy.
- 2 Manuscript prepared at the University of Georgia School of Medicine, Augusta, Georgia.
For his advice, aid and counsel during the entire progress of this problem, I wish to express my sincerest thanks to Dr. Richard E. Scammon. I am indebted to Mr. Lawrence Benson for the precise execution of the series of skeletal illustrations and to the Department of Anatomy, University of Minnesota, for the facilities and materials supplied for this research.
From the time of Galen (ca. 130-200 A.D.) to the present, the gross developmental anatomy of the human prenatal osseous skeleton has been the object of much research. In a general way the bibliography of this field may be classified as: (1) literature concerned with the problems of the various aspects of the development of a single bone or a group of bones, and (2) literature concerned with the problems related to the development of the skeleton as a whole.
Most of the literature may be placed in the first group. Galen, who described seven ossification centers in the ossifying sternum and two centers for the mandible, and Fallopius (1561), who noted five centers in the prenatal sphenoid bone, three centers in each vertebra, four centers in the axis and eight centers in the newborn sternum, are examples of the pioneer workers. Weber (1830), and Rambaud and Renault (1864), presented excellent reviews and bibliographies of the work in this period. Descriptions of the ossification and development of the sphenoid bone by Huxley (1864), of the mandible by Low (’09), of the diaphyses of the long bones by Horand (’08), of the clavicle by Hanson (’20) and of the petrosa.l bone by Bast (’30) are examples of the literature since the time of Rambaud and Renault (1864). Von Spee DEVELOPMENT OF OSSEOUS SKELETON
(1896), Bardeen (’10), Bryce (’15), deBeer (’37) and other references are bibliographical sources of this phase of the literature. The problems of the number and location of the ossification centers of each bone, of the prenatal developmental anatomy of each individual bone, and of the interpretation of congenital anomalies have been the primary topics of this literature.
The main topics of the literature of the second group are: ( 1) the attempt to establish the state of skeletal maturation as a criterion for the determination of fetal age and term (Hess, ’17; Hill, ’39 and others) ; (2) the developmental anatomy of the skeleton as a unit (Kerkring, 1670; Mall, ’06 and others) ; and (3) the determination and evaluation of the factors (intrinsic: such as endocrine, hereditary and parity; and extrinsic: such as the nutritional and mechanical) influencing the appearance of the ossification centers and the growth of the bones (Noback, ’-13, for examples of this literature).
The classical researches of Kerkring (1670, 1717), Albinus (1737) and Rambaud and Renault (1864) present excellent original accounts of the ossification of the prenatal and circumnatal skeleton. Detailed, accurate and proportional drawings in these papers illustrate the skeleton and its parts. The analysis of the development of the prenatal and circumnatal skeleton from roentgenograms has been the subject of numerous papers from the pioneer researches of Bade (’OO) and Lambertz (’00) to the recent work of flecker ( ’42) and others. Mall (’06) appears to be the only worker to utilize either the clearing or clearing and staining techniques to analyze some aspects of the development of the entire skeleton during even a portion of prenatal life.
For further bibliography of the literature of the developmental anatomy of the human osseous skeleton during the embryonic, fetal and circumnatal periods, see Noback ( ’43).
Materials and Methods
A series of forty human embryos, fetuses and a newborn infant, distributed throughout the period from the 23 mm. CR stage to birth, were cleared with potassium hydroxide and their osseous skeletons were stained with alizarin red S by a technique described by Noback (’43) and Noback and Noback (unpublished). These specimens were distributed as follows: 2 embryos in the second lunar month, 12 fetuses in the third lunar month, 8 fetuses in the fourth lunar month, 5 fetuses in the fifth lunar month, 4 fetuses in the sixth lunar month, 4 fetuses in the seventh lunar month, 1 fetus in the eighth lunar month, 2 fetuses in the ninth lunar month, 1 fetus in the tenth lunar month and 1 newborn infant. In addition, 10 other late fetal and newborn infant skulls were dissected.
From the cleared and stained series, seven specimens were selected and were used to illustrate a series of seven stages (figs. 2-8). An anterior View, a posterior view, and a lateral View of each specimen was drawn. All drawings were made to constant crown rump length.
The technique for making the drawings of the specimens selected to illustrate the stages consisted of the following five steps:
1. The specimen, floating in glycerin, was pinned down as desired to a paraffin base. Three views (anterior, posterior and lateral) of each specimen were photographed with a mounted 35—mm. camera.
2. The 35-mm. negative was then enlarged on a projecting machine to the predetermined CR length selected for all drawings, and a preliminary sketch was made.
3. The preliminary sketch was retouched freehand to add minor details observed directly from the specimen.
4. The retouched sketch was transferred to Ross board.
0. The Ross board drawing was finished in detail by observation of the specimen.
By this method it is felt that the illustrations were proportional and that they were drawn with a negligible amount of distortion.
The development of the prenatal and the circumnatal osseous skeleton is briefly described and illustrated (figs. 2-8) in a series of seven stages. The rate of differentiation of the skeleton determined the length of the intervals between the stages. When differentiation is rapid there is a short time interval between two stages, as 14 days between stage I (fig. 2) and stage II (fig. 3). When differentiation is slow there is a long time interval between two stages, as 5 months between stage VI (fig. 7) and stage VII (fig. 8). The drawings illustrating these stages were made from cleared and stained specimens that were selected as being representative for these stages. Variations, which are frequent in the developing skeleton, are illustrated in some of the figures. For example, in stage IV (fig. 5) an enlarged frontal and metopic fontellar area is shown in the anterior View and a Kerkring’s ossicle, rarely present, is illustrated in the posterior view. The seven stages follow.
STAGE NUMBER °"?;V§G:¥ltM" °R$;’§'G,'I',':m‘ mzommnrc mus ‘ mm. mm. I 38 64 days II 56 75 78 days III 88 125 3.25 lunar months IV 105 156 3.5 lunar months V 139 205 4.25 lunar months VI 175 255 5 lunar months VII 352 520 10 lunar months
‘Probable age determined from the linear dimensions (CR and CH length)
from formulae computed by Scammon and Calkins (’23), Seammon (’37) and Boyd (’41).
Stage I (fig. 2,)
Length, 38 mm. CR. Age, (54 days (approximately).
Bones present Facial bones: mandible, maxilla, premaxilla, nasal bone, vomer, palate bone, zygomatic bone and internal pterygoid plate. 96 CHARLES R. NOBACK
Calvarial bones: frontal bone, parietal bone, interparietal bone. supraoccipital bone, squamosal bone and tympanic annulus.
Basicranial bones: exoccipital bone and great wing (alisphenoid bone) of the sphenoid bone.
Thoracic bones: clavicle, scapula, and all ribs.
Vertebral column bones: cervical arches 3, 4, 5, 6 and 7, and thoracic arches 1 and 3 present on the right side; and cervical arches 3 and 5 and thoracic arches 1 and 2 present on the left side.
Upper extremity bones: diaphyses of the humerus, ulna, radius, metacarpal 2, 3, and 4, and all terminal phalanges.
Pelvic bones: ilium.
Lower extremity bones: diaphyses of the femur, tibia, fibula, metatarsals 2 and 3, and terminal phalanx 1.
The differences in the amount of differentiation among the facial bones, the calvarial bones, and the basicranial bones are the most striking features in the skull at this stage. The facial bones, except for the lacrimal bone which is absent in the specimen drawn, are all present and are more fully differentiated than the calvarial bones which are all present. Few of the basicranial centers have appeared. Each facial bone is characterized by the same general features as the corresponding adult bone. The facial sutural spaces are broad when compared to their definitive size but they are relatively narrow when compared to the broad sutural gaps of the calvarial bones. The calvarial bones are relatively small, rapidly differentiating bones With broad membranous areas separating them from each other. Except for the small ossification centers present, the basicranium is essentially cartilage.
The maxilla has well developed frontal, alveolar, zygomatic, palatine and orbital processes. The sutura notha is indicated by small unossified intervals at the premaxi-llary junction especially superiorly and on the palatine process. The interpremaxillary suture is rather wide and the infraorbital canal is a groove in the orbital facies. Characteristically the mandible is depressed as it is throughout prenatal life. The fetal mandible is discussed in detail by Wissmer (’27). The zygomatic bone is a flat membrane bone with identifiable infra orbital, frontal and zygomatic processes. As the malar tubercle is only slightly indicated the bone has a triangular outline instead of the adult diamond form. The bone has a uniform thin depth, for the orbital facies, which deepens the bone, is not well developed. A large unossified gap is present between the zygomatic processes of the zygomatic bone and the temporal bone. The palate bone has so differentiated that the horizontal and vertical lamina are approximately of equal size; and the orbital, sphenoidal and pyramidal processes and the incisura sphenopalatine are all recognizable. The two bilateral centers of the vomer are located on the inferior border of the medial nasal cartilages.
The open reticulated parietal bones show evidence of ossifying from one center. The interparietal bone is a line of open reticulated bone just superior to the supraoccipital bone. The two bones are connected medially by a sliver of bone. Although Augier ( ’31b) and La Coste ( ’31) stated that the interparietal bone fuses with the supraoccipital bone initially at the lateral margins, the specimens of this stage (fig. 2) and stage II (fig. 3) show that at least there may be an initial medial fusion between the two bones. The exoccipital bones, which lie inferior to the posterior border of the parietal bone at the level of the angle of the mandible, are in series with the more medially placed neural arch centers. The tympanic annulus is an ovoid nodule of bone located just inferior to the posterior border of the squamosal bone in the region of the future superior anterior region of the annulus. The squamosal bone with the slightly differentiated squama is mainly zygomatic process and squamal base. The mandibular fossa is undeveloped.
The clavicle is sigmoid shaped. The lateral edge is superclateral to the acromial process of the scapula and the medial edge is medial to the upper thoracic neural arches. The seapula is lunate. The curved vertebral border and the curved glenoid border, which is relatively large, are parallel to each other. The scapular spine is only slightly developed. There is no osseous acromial process. The ribs have almost reached the same proportions to each other and to the costal cartilages as exist during postnatal life. The angle and the body of each rib are well formed but the neck, tubercle and capitulum of each rib are unossified. The proximal ends of the ribs are in a parasagittal line that is lateral to the parasagittal line of the neural arches. In other words, the proximo-medial ends of the ribs of each side are relatively far apart.
Asymmetry in the appearance of bilateral ossification centers is illustrated by the cervical and thoracic neural arches present. Thoracic neural arch I is the largest arch center present and therefore it was presumably the first to appear.
Stage II (fig. 3)
Lengtli. 56 mm. CR, 75 mm. CH. Age, 78 days (approximately).
Bones present that were absent in stage I Facial bones: lacrimal bone.
Basicranial bone: basioccipital bone.
Vertebral column bones: neural arches from cervical 1 to lumbar 3 inclusive are present; except for thoracic centrum 7, thoracic centra from thoracic 6 to lumbar 4 inclusive are present.
Upper extremity bones: metacarpal diaphyses 1 and 5; proximal phalangeal diaphyses 2, 3 and 4.
Lower extremity bones: metatarsal diaphyses 1, 4 and 5; terminal phalangeal diaphyses 2, 3, 4 and 5.
Description The facial bones have increased in absolute size and, with respect to the facial area, in relative area; and they have reached a size that is almost proportional to their definitive area. The membranous calvarial bones, which have not as yet reached the size that is proportional to their definitive area, have grown rapidly iii the interval since the last stage. The small alisphenoid bones, the elongated exoccipital bones and the nodular basiocciptal bone are the only osseous elements in the predominately cartilaginous basicranium.
The frontal processes of the maxillae have grown superiorly to flank the elongating nasal bones. The nasal notches are enlarged and the sutura notha is absent. The growth of the malar tubercle gives the corpus of the zygomatic bone a diamond shape. The thin attenuated maxillary process of the zygomatic bone extends to the region of the future infraorbital
canal; and the orbital facies, which is commencing to form,
gives the bone some depth. The vomer consists of the two lateral alae and the median ventral keel. Each parietal bone and each half of the interparietal bone shows evidence of ossifying from two centers of ossification, one superior to the other.
The zygomatic process of the squamosal bone has elongated almost to articulate with the zygomatic process of the zygomatic bone. The squama of the squamosal bone has three interconnected plates of bone radiating superiorly from the base of the bone. The tympanic annulus is a semicircular rod with an enlarged antero—superior portion.
The relatively more rapid growth of the vertebral border as compared with the glenoid border, since stage I (fig. 2) has altered the shape of the scapula. The scapular spine is larger than in stage I (fig. 2). The neural arches are small bars consisting of the radices and the laminae. They are further apart in the cervical region than in the thoracic and lumbar regions. The centra are larger than the arches. The great antero—posterior distance between the line of the neural arches and the line of the centra with respect to the depth of the thorax is marked.
Stage III (fig. 4)
Length, 88 mm. CR, 125 mm. CH. Age, 3.25 lunar months (approximately).
Bones present that were absent in previous stages Basicranial bones: basisphenoid bone, orbitosphenoid bone.
Vertebral column bones: lumbar neural arches 4 and 5, and sacral neural arch 1, cervical centra 3, 4, and 5, lumbar centrum 5, and sacral centra 1, 2 and 3.
Upper extremity bones: all phalangeal diaphyseal centers are present.
Lower extremity bones: cliaphyses of proximal phalanges 1, 2 and 3.
The facial bones have differentiated to a size that is proportional with respect to their definitive areas. The orbital facies of the zygomatic bone completes the general form of this bone. In the specimen used to illustrate this stage the metopic fontanelle appears to be formed as a result of the accelerated growth of the supero-medial border of the frontal squama of the frontal bone. The unossified notch on the posterior border of the parietal bone is probably an indication of a space separating the two parietal ossification centers. The tympanic annulus forms three quarters of a circle. The basisphenoid centers are paired nodules in the cartilaginous sella turcica and the orbitosphenoid bone is a nodule in the metopic root of the orbital cartilage.
By this stage the relative proportions of each osseous rib to its costal cartilage and to the other ribs are, in general, similar to these proportions in the adult.
The differentiation as well as the appearance of the neural arches follows a cranio—caudal pattern. The cervical arches have narrow laminae and radices while the lumbar neural arches are small osseous nodules. The laminae, where developed, are directed caudo-posteriorly from the radices with which they form approximately a 120 degree angle. The rela,tive sizes of the centra are directly related to their order of appearance.
The alar portion of the ilium is formed, but is only slightly indicated. The angle of the greater sciatic notch is more obtuse than in later stages.
Stage IV (fig. 5)
Length, 105 mm. CR, 156 mm. CH. Age, 3.5 lunar months.
Bones present that were absent in previous stagesBasicranial bones: lingula. Pelvic bones: ischium.
Lower extremity bones: proximal phalangeal diaphyses 4 and 5, all middle phalangeal diaphyses.
In the specimen used the membranous area between the frontal squama of the frontal bone is large for this stage. A cartilaginous Kerkring’s ossicle is present in the inferior su« praoccipital notch. The basisphenoid has the shape of a block 0 with the vertical line of the C posterior in position. The lingula is a short rod extending laterally from the basisphenoid bone.
The laminae and radices of the neural arches are longer and broader than in previous stages. The nodular ischiatic bone is located in the cartilaginous ischiatic superior ramus.
Stage V (fig. 6) Length, 139 mm. CR, 205 mm. CH. Age, 4.25 lunar months.
Bones present that were absent in previous stages — Facial bones: maxillary turbinates.
Basicranial bones: posterior lateral presphenoid bones, incus, malleus, petrosal centers, ossicles of Bertini.
Thoracic bones: manubrium, right 7th cervical rib (inconstant).
Vertebral column bones: sacral neural arches 2 and 3, sacral centrum 1.
Lower extremity bones: middle phalangeal diaphyses 2 and 3.
At approximately this stage the membranous calvarial bones have differentiated to a size that is proportional with respect to their definitive areas (Inman, ’33; Noback, ’43). The sutural spaces of the calvarium are narrow and the fontanelles are discrete structures. The orbitosphenoid bone, shaped like a boomerang, is ossified in the regions of the anterior clinoid process and of the superior portion of the optic foramen. The alae of this bone are unossified. The paired postero-lateral presphenoid centers are small nodules in the lateral ends of the groove of the optic chiasma. The basisphenoid bone has invaded the dorsum sellae posteriorly and the tuberculum sella anteriorly. It is notched anteriorly. The incisura between the body and the squama of the alisphenoid bone representing the site of the future foramina ovale and the foramen spinosum is deep.
A supero-medial notch and rounded infero—lateral edges characterize many of the centra.
Stage VI (fig. 7) Length, 175 mm. CR, 240 mm. CH. Age, 5 lunar months.
Bones present that were absent in previous stages — Facial bones: superior concha.
Basicranial bones: anterior lateral presphenoid centers, stapes, petrosal centers, ethmoidal centers, ossicles of Bertini.
Vertebral column bones: dens (omitted in figures 7 and 8), neural
arches 4 and 5. Pelvic bones: pubis. Lower extremity bones: calcaneus (all phalangeal diaphyses are
present soon after this stage). Description The cartilage bones of the skull are the most actively differentiating bones of the skull since the last stage as attested by the appearance of several cartilage ossification centers and by the relatively rapid growth of these bones. None of these cartilage bones have assumed a size that is proportional with respect to its definitive area. The small ethmoidal turbinate centers may be present in the superior a11d middle nasal conchae. No further ethmoidal ossification is indicated. The anterior lateral presphenoid centers may be present. The posterior presphenoid centers are elongated, extending toward the anterior ramus of the lesser wing of the sphenoid. The orbitesphenoid consists of a posterior ramus (anterior clinoid process), of an anterior ramus (supraoptic portion) and of a small lateral ala. Each lingula is broad. The ossification of the petrosum during this portion of fetal life is discussed by Bast (’30). In the lateral view the petrosum is visible posterior to the squamosal bone. This is due to the lateral growth of the petrosum subsequent to the appearance of its ossification centers. The large unossified petrosal foramen (fig. 7c)
is the subarcuate fossa.
The form and anatomical relations of the post cranial bones are obvious in the figures.
Stage VII (fig. 8) Length, 352 mm. CR, 520 mm. CH. Age, 10 lunar months.
Bones present that were absent in previous stages Facial bones: mental ossicles. Basicranial bones: tympanohyal center.
Hyoid bones: body of the hyoid bone. Thoracic bones: manubrium and first three sternal corpus centers
Vertebral column bones: sacral centrum 5, sacral costal centers 1, 2 and 3 (omitted in figure 8).
Lower extremity bones: talus, distal femoral epiphysis, proximal tibial epiphysis.
The description of the newborn infant osseous skeleton is summarized by Hess (’17), Scammon (’23), Testut (’21), standard anatomical textbooks, and the literature.
Except for the ribs the cartilage bones have not as yet reached sizes that are proportional with respect to their definite areas. Broad cartilaginous synchondroses separate the bones from each other. The peripheral margins of the calvarial bones are characterized by short peripherally projecting osseous trabeculae while the calvarial suture spaces have a varying number of small osseous nodules of bones detached from the bone proper. These may possibly be potential sutural bones. The peripherally projecting osseous trabeculae of the margins of the bones are not characteristic of cartilage bones and they are not prominent features of the facial bones. The bone superior to the occipital bone is either an enlarged sutural bone or a preinterparietal bone (Augier, ’31a).
The pubis and the ischium are restricted to the superior rami of their respective cartilages. Occasionally the epiphyses of the head of. the humerus, the cuboid, the hamate, the cuneiform III bones and the epiphyses of the head of the femur are present in the newborn infant (see Noback, ’43, for bibliography).
THE DEVELOPMENTAL ANATOMY OF SOME OF The PRENATAL BONES
Some miscellaneous observations of the developmental anatomy of certain bones during prenatal life are presented. N o attempt is made to give a complete account of the prenatal developmental anatomy of any bone, nor a complete discussion of the controversial aspects of any phase of the development of any bone.
Mandible. From an examination of the published and original roentgenograms and from cleared and stained embryos, fetuses and newborn infants, the prenatal and circumnatal mandible appears to be normally always depressed and not opposed to the maxillary bone as it is generally illustrated (figs. 2-8).
Frontal bone. The prenatal developmental anatomy of the frontal bone as presented by Inman and Saunders ( ’37) has been fully confirmed. Each half of the frontal bone ossifies from a single center appearing just above the superciliary ridge.
Parietal bone. The parietal bone ossifies from one ossification center (Rambaud and Renault, 1864; Pendergrass and Pepper, ’39; Arey, ’42) or from two ossification centers, appearing close together one above the other (Toldt, 1883; Augier, ’31a). The normal ossification of the parietal bone from three or four ossification centers (reviewed by Bardeen, ’10) is not acceptable as this conclusion is based on rare anomalies and not on any direct observations of the ossifying bone. The parietal bone of a series of nine cleared and stained fetuses ranging from 38 mm. OR to 71 mm. CR length showed evidence of ossifying from one center in one fetus of 38 mm. CR (fig. 2) and from two centers in eight fetuses (fig. 3 and fig. 4). All the parietal bones interpreted as ossifying from two centers, one superior to the other, have the constriction of the hour glass shape described by Mall (’06) on the anterior and posterior borders midway between the superior and inferior borders of the bone (fig. 3). The assumption is made that these constrictions are the remnants of the membranous spaces between two centers. On the basis of these observations it may be provisionally concluded that each parietal bone normally ossifies from two ossification centers.
Tympamc cumulus. The tympanic annulus appears as a small round nodule, which represents the anterior superior portion of the annulus, just inferior to the posterior border of the temporal squama (fig. 2). With the posterior growth of the temporal squama the tympanic annulus becomes located just inferior to the junction of the zygomatic process of the temporal squama and the temporal squama proper. This relation is maintained throughout prenatal life. The annulus has a semicircular shape at the 56-min. CR stage (fig. 3) and a three-quarter circle form at about the 75-mm. CR stage (fig. 4). During early fetal life the annulus has a small osseous appendage on its superior anterior border (fig. 2). The bone grows in depth until birth when it commences to fuse to the squamosal bone.
Occipital bone. The changes in the relative sizes of the interparietal portion (membrane bone) and the supraoccipital portion (cartilage bone) of the occipital bone illustrates the rapid growth of membrane bone as compared to slow growth of cartilage bone. Until the 88-mm. CR stage (fig. 4) the supraoccipital bone has a larger surface area than the interparietal bone. At approximately the 88-mm. CR stage these two bones have approximately the same surface area. After this stage the interparietal bone has a larger surface area than the supraoccpital bone. The interpretation of the ossification of the interparietal bone from one or two pairs of bilateral centers is discussed bv Augier ( ’31b). No evidence was obtained to substantiate Mall’s (’O6) observation that the supraoccipital bone ossifies from four centers. It appears that this bone ossifies normally from one center.
Scapula. The changes in the form of the scapula during prenatal life may be expressed in terms of the relative growth of the axillary and vertebral borders. Throughout prenatal life the vertebral border is growing absolutely faster than the axillary border (figs. 2-8).
Clcwicle. By stage I (fig. 2) the definition of the clavicle is similar to that of the mature clavicle. Unlike the postnatal clavicle, which lies in a horizontal plane, the fetal clavicle is inclined in an oblique plane from latero—superior to medioinferior. The prenatal obliquity of the clavicle is present in all the cleared specimens examined and it is confirmed by published roentgenograms in the literature.
Ribs. At the 56-mm. CR stage (fig. 3) the breadth of each rib is the same throughout its length (the superior and inferior borders are almost parallel to each other). At the costal angle there are indications of a constriction in the depth of the ribs. Just distal to this constriction an increased breadth of the rib is definitely present by the 88-mm. CR stage (fig. 4). This increased depth, characteristic of the posterior 7 or 8 ribs, is due mainly to ossification on the inferior border of the ribs.
Vertebral column. Roentgenologists and anatomists refer to the cranio—caudal appearance of the primary neural arch ossification centers (Ruckensteiner, ’31). However, except for an observation by Mall ( ’06), all published data report the findings of either no neural arch centers present in a specimen or never less than the cranial 9 neural arch centers. As the arch centers caudal to the second thoracic arch can be easily demonstrated to appear craniocaudally, the assumption has been made that the cranial 9 neural arches likewise appear craniocaudally. Mall ( ’06) described a 33-mm. CR stage fetus as having cervical arches 1, 2 and 7, and thoracic arches 1 and 2 present on the right side; and cervical arches 1, 2 and 3, and thoracic arches 1, 2, 3 and 4 on the left side. A fetus of the 38-mm. CR stage (fig. 2) has the cervical arches 3 and 5 and the thoracic arches 1 and 2 present on the right side; and cervical arches 3, 4, 5, 6 and 7, and thoracic arches 1 and 2 present on the left side. None of the other arches are present in either specimen. In both specimens the left side has the greater number of centers and the first thoracic arch center is the largest neural center. On the basis of these two specimens it may be suggested that the cervical neural arches do not appear craniocaudally, that the thoracic arch 1 is the first to appear, and that there is probably no systematic order of appearance of the cranial 9 arch centers. More data are needed to clarify the order of appearance of these centers.
On the basis of anomalous centra, several. authors (Beadle, ’31, and others) have concluded that each centrum ossifies from two bilateral ossification centers. Most Workers (Alexander, ’06; Mall, ’06 and others) are of the opinion that each centrum ossifies from one center. In the entire series of cleared and stained specimens examined in this study, all of the centra appeared to ossify from one center. The further development of the supero—medial notch on some of the centra, as noted in stage III (fig. 4), may explain the formation of the anomalous bipartite centra occasionally observed in postnatal life by Beadle (’31) and others.
Ilium. At the 38-min. CR stage (fig. 2) the osseous ilium is enlarged anteriorly and attenuated posteriorly. The greater sciatic notch is large and its angle between the attenuated posterior portion of the ala and the cartilaginous iliac body is obtuse. By the 88—mm. CR stage (fig. 4) this angle of the greater sciatic notch is as acute as it is in the newborn infant. At the 175-mm. CR stage (fig. 7) the iliac crest, the anterior and posterior iliac spines, the greater sciatic notch and the ala proper resemble, in general, their definitive form. The body has not as yet fully invaded the acetabulum and a broad cartilaginous synchrondrosis separates it from the ischium and the pubis. The relative distance between the twelfth rib and the superior border of the ilium, and the cranio-caudal distance between the fifth lumbar vertebra and the superior border of the ilium are reduced with fetal age (fig. 2-8). The secondary iliac ossification centers appearing during prenatal life in the region of the posterior inferior iliac spine and the anterior iliac spine, described by Lambertz ( ’00) but not seen by Adair (’18), were not observed.
Centric and Eccentric Ossification Centers
“Every bone develops from one or more bony nuclei or centers of ossification. The localization of this center is subject to but slight variation” (Spalteholz, ’33). On the basis of the relation of the location of an ossification center to the geometric center of the bone or of the part of the bone that the center forms, there are two types of ossification centers, (1) centric centers and (2) eccentric centers. A centric center is an ossification center which appears approximately in the geometric center of the bone or of the part of the bone that the center forms. An eccentric center is an ossification center which appears in a loci removed from the geometric center of the bone or of the part of the bone that the center forms.
The prenatally ossifying bones with centric centers are the zygomatic bone, lacrimal bone, nasal bone, palate bone, vertebral centra, clavicle, diaphyses of the long bones of the extremities, body of the hyoid bone, basioccipital bone. cuboid bone and the talus. The palate center appears at the junction of the horizontal and Vertical plates (Mall, ’O6) or in the vertical plate immediately internal to the palatine nerves (Fawcett, ’10). The basisphenoid bone and the presphenoid bone are both ossified from more than one ossification center. The fusion of these centers occurs soon after their appearance and thus these two bones may be considered as ossifying from one multiple center. If this premise is accepted these bones may be considered as ossifying from centric centers; otherwise, from eccentric centers. The locations of the other centric centers require no explanation.
The prenatally ossifying bones with eccentric centers are the frontal bone, parietal bone, mandible, maxillary bone, squamosal bone, tympanic annulus, interparietal bone, supraoccipital bone, orbitosphenoid bone, alisphenoid bone, vomer, lingula, medial pterygoid plate, exoccipital bone, inferior concha, petrosum, scapula, ribs, ilium, ischium, pubis and calcaneus.
The frontal bone’s center appears just superior to the superciliary ridge (Inman and Saunders, ’37), while the geometric center of the definitive bone is higher on the frontal squama. The parietal bone ossifies from two centers, one superior to the other (see above). The mandibular center appears at a point one-third of the length of the bone from the symphysis (Fawcett, ’05; Low, ’09). The maxillary center ossifies on the outer side of the nasal cavity just above the cuspid tooth germ (Mall, ’06). The center for the squamosal portion of the temporal bone arises in the region of the midpoint of the base of the squama (fig. 2). The tympanic annulus appears at the antero—superior region of the bone (fig. 2). The bilateral centers of the interparietal bone appear at the inferior border of the bone just lateral to the midsagittal line from which region ossification proceeds superiorly, laterally and medially (LaCoste, ’31; Augier, ’31b) (fig. 2). The center of the orbitosphenoid bone which appears in the metopic root of the orbital cartilage (Mall, ’06), and the center of the alisphenoid bone which appears lateral and inferior to the foramen rotundum (Sutton, 1885) are located in the medial portions of their respective bones. Subsequent ossification is predominately lateral in each bone while in the alisphenoid bone ossification also extends inferiorly into the lateral pterygoid plate. The medial pterygoid plate center appears in the region of the hamulus and ossification extends superiorly (Fawcett, ’10). The center of the lingula appears basally (Rambaud and Renault, 1864) and the main ossification extends distally. The vomerine centers appear as bilateral centers in the inferior portion of the definitive bone and subsequent ossification proceeds predominately superiorly into the alae (Fawcett, ’10). The exoccipital center appears in the region of the hypoglossal foramen while the inferior concha appears in the supero-medial aspect of the inferior chonchal cartilage. The multiple centers of the petrosal portion of the temporal bone appear adjacent to the membranous labyrinth (Bast, ’30).
The scapula center ossifies in the corpus in the middle of the spine (Mall, ’06) while the neural arch centers appear at the base of the superior articular processes in the laminae (Ramband and Renault, 1864). The rib centers ossify at the angle of the costal cartilages. The iliac center arises in the inferior medial portion of the ala above the greater sciatic notch (Lambertz, ’00; Falk, ’01) while the ischiatic and pubic centers appear in their respective superior rami (Rambaud and Renault, 1864). The calcaneal center arises slightly anterior to the center of the calcaneal cartilage (Bryce, ’15).
The sites of the frontal eminence and the parietal eminence are not necessarily coincident with the sites of the ossification centers of these bones. The eminences are evident at the region of the greatest curvature and thus they seem to be a response to a mechanical stimulus. The ossification centers appear in a constant location, a condition which would seem to indicate a response to a genetic stimulus. The frontal center appears below the site of the future frontal eminence. In a parietal bone which arises from one center, the locations of the eminence and the center of ossification could be coincident. When the early fetal parietal bone, ossifying from two centers, is enlarged to the definitive size, the site of the future parietal eminence can be plotted as being located between the two centers. Thus the absolute coincidence of the location of the eminences and the ossification centers of the frontal bone and the parietal bone does not appear to be acceptable.
Asymmetry In The Time Of Appearance Of The Bilateral Ossification Centers
The unilateral presence of one and the unilateral absence of the other of a pair of bilateral ossification centers during prenatal and circumnatal life has been reported for the lacrimal bone in a 4.25—cm. fetus by Macalister (1884); for some ribs in a 30-mm. CR embryo, for some cervical and upper thoracic neural arches in a 34—mm. CR fetus (noted above) and of the tympanic annulus of a 42—mm. CR embryo by Mall (’06); for some of the sternal centers by Borovansky (’31); and of thirty—two cases of seven different circumnatally appearing centers (head of the humerus, coracoid process, capitate, hamate, distal femoral epiphysis, cuboid and external cuneiform) in 640 newborn infants by Menees and Holly (’32). Borovansky and Hnévkovsky (’29), Pryor (’36) and flecker (’42) present similar data for some of the bones appearing after birth.
The asymmetrical presence of some of the cervical and upper neural arches is discussed above and illustrated in stage I (fig. 2). The posterior lateral presphenoid center was present on the left side and absent on the right side in the fetus illustrated by stage III (fig. 4). The twelfth rib was present on the left side and absent on the right side of a 56-mm. CR fetus, and the right twelfth rib was much larger than the left twelfth rib in the fetus illustrated by stage I (fig. 2). In the latter case the assumption is made that the larger rib appeared first.
The paucity of reported observations of the asymmetrical appearance of ossification centers during early fetal life, when most centers are appearing, may possibly be accounted for by the infrequent use of sensitive techniques, like the clearing and staining methods, in examining specimens; and by the fact that bilateral centers probably appear at the same time or within a short time of each other. In some cases the interpretation of the congenital absence of a bone is possible.
These observations suggest that although the asymmetrical appearance of bilateral centers occasionally occurs the appearance of bilateral centers is essentially symmetrical.
THE “SEQUENCE” OF CRANIO-CAUDAL DEVELOPMENT AND THE APPEARANCE OF THE OSSIfiCATION CENTERS
The sequence of the appearance of the ossification centers during prenatal life shows varying degrees of conformity and nonconformity to the “sequence” of cranio-caudal development (the so-called “law” of antero-posterior development or “law” of developmental direction).
The regional order of the appearance of the primary ossification centers during prenatal life appears to be roughly as follows: ( 1) Diaphyseal centers of the two proximal segments of the extremities, (2) centers of the facial bones, (3) and (4) centers of the calvarial bones and centers of the thoracic bones (except for the centers of the sternum), (5) primary centers of the free vertebral column, (6) diaphyseal centers of the hand, (7) and (8) centers of the basicranial bones (except for the ethmoidal centers) and centers of the pelvic bones, (9) diaphyseal centers of the foot, (10) centers of the sternum, and (11) centers of the hyoid complex (Mall, ’O6; Adair, ’18; Augier, ’31a; Ruckensteiner, ’31; Noback, ’43, and others). From this order it may be concluded that the sequence of the time of the appearance of the ossification centers of the body as a whole does not fully conform to the “ sequence” of craniocaudal development.
The intraregional order of appearance of some groups of ossification centers does conform with the “sequence” of cranio-caudal development. For example, the order of appearance of the head branchial arch centers is (1) centers of the facial bones, (2) centers of the calvarial bones, ( 3) centers of the basicranial bones and (4) centers of the hyoid bones. The centers of the sternum appear cranio—caudally (Borovanskv, ’31). Except for the first phalangeal centers, the diaphyseal centers of each row of the metacarpals the metatarsals and the phalanges appear, as a rule, cranio-caudally with respect to their embryonic position (Mall, ’06, Ruckensteiner, ’31). VVith possible exception of the cervical neural arches, the neural arch centers appear cranio-caudally (Mall, ’06).
The intraregional order of appearance of other groups of ossification centers show degrees from partial to total nonconformity to the “sequence”. The order of appearance of the vertebral centra, the ribs and the diaphyses of the upper and lower extremities are examples. The lower thoracic are the first centra centers to appear. The sixth and seventh costal centers are probably the first ribs to appear. Subsequent ossification in these two groups of bones is cephalad and caudad to the initially appearing centers (Mall, ’06). Those centers that appear caudally conform to the “sequence” while those appearing cranially do not. The diaphyseal centers of the upper extremity ossify in the following sequence: (a) humerus, (b) radius, (c) ulna, (d) metacarpals, (e) terminal phalanges, (f) basal phalanges, (g) middle phalanges, and (h) carpals. The diaphyseal centers of the lower extremities ossify in the same order but later than those of the upper extremity. The appearance of the more proximal elements follows the “sequence” while the appearance of the more distal elements does not appear to do so.
SHORT CRITIQUE OF THE LITERATURE OF THE TIME OF THE APEARANCE OF THE OSSIfiCATION CENTERS
Pathology, race, sex, nutrition and other factors have been shown to influence the time of the appearance of ossification. To obtain sufiicient data to properly evaluate these factors, consolidation of the data in the literature should be helpful. However, even a short review of the literature reveals the difficulty of such consolidation because of the omission of much vital data and because of the variety of techniques employed in observing the prenatal skeleton.
The ages of the specimens examined are often given but the method used to calculate fetal age or the linear dimensions of the specimens are frequently omitted. The number of specimens examined is often omitted. In order to get an accurate idea concerning the range of the time of the appearance of ossification centers the absence of a center should be reported. Most papers only report the earliest observed presence of an ossification center. Many recent publications ignore the data of accurate investigations (flecker, ’42)
To obtain an accurate consolidation of data, account must be taken of the techniques employed in observing the time of the appearance of the centers. Ossification of a given center is observed first by the sectioning technique, followed in order by the KOH clearing and alizarin red S staining technique, by the roentgenographic method and by gross dissection. The time difference between the clearing and staining technique and the roentgenographic technique, in indicating the appearance of a center is approximately 1 week (Hess, ’17). A striking difference illustrating the relative sensitivity of these two techniques in revealing calcification is shown by the parietal bone which, according to Mall (’06) using the clearing technique, appears at the 31 mm. CR stage and which, according to Hill (’39) using the roentgenographic method, appears at the 194-mm. CR stage.
1. Aspects of the developmental anatomy of the prenatal and circumnatal macroscopic osseous skeleton are outlined and illustrated in seven stages. These stages are the 38-mm. CR, 56-mm. CR, 88—mm. CR, 105—mm. CR, 139—mm. CR, 175mm. CR and 352—mm. CR stages.
2. Some special phases of the normal prenatal developmental anatomy of the mandible, frontal bone, parietal bone, tympanic annulus, occipital bone, scapula, clavicle, ribs, centra, neural arches and ilium are briefly discussed.
3. On the basis of the relation of the location of an ossification center to the geometric center of the bone or the part of the bone that the center forms, there are two types of ossification centers, viz., (1) centric centers and (2) eccentric centers. A centric center is an ossification center which appears approximately in the geometric center of the bone or the part of the bone that the center forms. An eccentric center is an ossification center which appears in a loci removed from the geometric center of the bone or the part of the bone that the center forms. Each prenatal ossification center is classified into one of these two types.
4. The asymmetrical time of appearance of the bilateral ossification centers and the relation of the order of appearance of the ossification centers appearing during the prenatal and circumnatal periods to the “sequence” of cranio-caudal development are briefly discussed. Although the asymmetrical appearance of the bilateral centers occasionally occurs their appearance is essentially symmetrical. The sequence of the appearance of the ossification centers during prenatal life shows Varying degrees of conformity and nonconformity to the “sequence” of cranio—caudal development. 5. A short critique of the literature of the time of the appearance of the prenatal ossification centers is presented.
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Each plate consists of two figures. Each figure (except fig. 1) illustrates three views, anterior, posterior, and lateral of one of the seven developmental stages discussed in the observations. figure 1 is a key figure to facilitate the interpretation of figures 2 to 8 inclusive. All figures are drawn to the same crown-rump length. The manner of drawing the figures is outlined in the material and methods.
The increased flexibility of the vertebral column in the fragile cleared speci« mens is reflected in the figures by the degree of the column ’s curvature. When the curvature of the thoracic segment of the vertebral column is reduced there is a reduction in the obliquity of the ribs. Conversely, when there is an increase in the curvature of the thoracic segment of the vertebral column, there is an increase in the obliquity of the ribs. The anterior view of the specimen in figure 4 illustrates the horizontal position of the 'ribs when the vertebral column is held straight. Varying degrees of costal obliquity are illustrated in the other figures.
ABBREVIATIONS A1i., alisphenoid bone (great wing of P., palate bone sphenoid bone) Pe., petrosum
Bo., basioccipital bone Pu., pubis
Eo., exoccipital bone So., supraoccipital bone
Ip., interparietal bone T.A., tympanic annulus (tympanic Is., ischium bone)
K.O., Kerkring’s ossicle Z., zygomatic bone
EXPLANATION OF‘ fiGURES
1 Three fetuses at different age stages with the bones, which are not easily recognizable, labeled to facilitate the interpretation of figures 2 to 8 inclusive.
(a) Lateral View of fetus approximately 78 days old (56-mm. CR, 75-mm. CH).
(b) Posterior view of a fetus approximately 3,5 lunar months old (105-mm. CR, 156-mm. CH).
(c) Lateral view of a fetus approximately 5 lunar months old (175 mm. CR, 255-mm. CH).
2 Three drawings of the osseous skeleton of a human fetus approximately 64 days old (38~mm. CR) illustrating stage I.
(a) Anterior view. (b) Posterior view. (c) Lateralview.
PLATE 1 PLATE 2 EXPLANATION or fiGURES
3 Three drawings of the osseous skeleton of a human fetus approximately 78 days old (56-mm. CR) illustrating stage II.
(a) Anterior view. (b) Posterior view. (c) Lateral view.
4 Three drawings of the osseous skeleton of a human fetus approximately 3.25 lunar months (88-mm. CR) illustrating stage III.
(a) Anterior view. (b) Posterior view. (c) Lateral view.
DEVELOPMENT OF OSSEOUS SKELETON F tqure 8
PLATE 2 PLATE 3 EXPLANATION or fiGURES
5 Three drawings of the osseous skeleton of a human fetus 3.5 lunar months (105-mm. CR) illustrating stage IV.
(a) Anterior view. (b) Posterior view. ((2) Lateral view.
6 Three drawings of the osseous skeleton of a human fetus 4.25 lunar months (139-mm. CR) illustrating stage V.
(a) Anterior view. (b) Posterior view. (c) Lateral view.
DEVELOPMENT OF OSSEOUS SKELFJON PLATE 3 PLATE 4
EXPLANATION OF fiGURES
7 Three drawings of the osseous skeleton of a human fetus 5 lunar months (175-mm, CR) illustrating stage VI.
(a) Anterior view. (b) Posterior view. (c) Lateral view.
8 Three drawings of the osseous skeleton of a human fetus 10 lunar months (352-mm. CR) illustrating stage VII._
(a) Anterior view. (b) Posterior view. (0) Lateral view.
CHARLES R. NOBAC K
DEVELOPMENT OF OSSEOUS SKELETON PLATE 4
Cite this page: Hill, M.A. (2019, June 16) Embryology Paper - The developmental anatomy of the human osseous skeleton during the embryonic, fetal and circumnatal periods. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_developmental_anatomy_of_the_human_osseous_skeleton_during_the_embryonic,_fetal_and_circumnatal_periods
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