Paper - A study of the development of the mammalian pelvis
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Ruth EB. A study of the development of the mammalian pelvis. (1932) Anat. Rec. 53(2): 208 -
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- 1 A Study of the Development of theMammalian Pelvis
A Study of the Development of theMammalian Pelvis
Elbert Bresee Ruth
Department of Zoology, University of Wisconsin
Two Plates (Eleven Figures)
The eutherian pelvis has been an object of study for many years. The earlier investigations were mostly concerned with the gross morphology and the developmental history in the different orders. More recently, the interest has centered about the age changes, and particularly the changes effected during pregnancy and parturition, from the standpoint of the speciﬁc activities of the sex hormones. In most of the past studies of the pelvis, however, the investigations have been concerned with the pelvis as a whole, or, in comparative studies, with the homologies in the different groups. Comparatively few investigations have dealt with the os pubis and pubic symphysis alone.
Investigators agree that the os coxae is a bilateral structure, arising from three separate chondrogenous centers in the scleroblastema on each side. These primary centers of chondriﬁcation, representing the anlagen of the ilia, ischia, and pubes, ﬁnally fuse together to form a continuous cartilaginous plate on each side; the anterior ends meeting ventrally to form the symphysis pubis, after the usual method of formation of an amphiarthrosis. Development is completed by the appearance of centers of ossiﬁcation in each pelvic element, and the ﬁnal fusion of these centers. This account, however, fails to take into consideration the fact that there are three types of pubic symphysis found in the mammalian orders (Todd, ’21). 1. Those in which the innominate bones are fused at the ischiopubic, or pubic symphysis, as the case may be, forming a synostosis. 2. Those in which the innominate bones are separated by cartilage at the symphysis, forming a synchondrosis. 3. Those i11 which the innominate bones have no connecting medium at the symphysis; or are connected by a ligamentous band, forming a syndesmosis. The fact of the occurrence of all three types even within a single order, would suggest that the development of these types might differ from the usual concept. At least, the opportunity is presented for further investigation into the details of development in each case.
Considering the usual concept of the development of the pelvic girdle, the question arises as to the sequence of events leading up to the formation of the typical adult pelvis, of the species in question. What is the ontogenetic history of the interosseous medium at the symphysis? How does the osseous connection of type 1, the cartilaginous connection of type 2, or the ligamentous connection of type 3 arise‘? That, brieﬂy, is the problem with which this investigation attempts to deal.
In a more recent series of investigations concerning the development of the fetal pelvis of the pocket gopher, mole, and guinea-pig, among the Eutheria (Hisaw, ’23, ’25, ’27, ’29), and Ornithorynchus and Echidna, among the Prototheria (Low, ’29) new light is thrown upon the problem. It IS to be noted that there is speciﬁc mention of the fact that at some time the innominate cartilages of these fetal pelves have been fused into a continuous cartilaginous girdle. This fusion takes place at the pubic symphysis, and frontal or transverse sections through this region show no sign of fusion from two distinct halves. Except for these discussions there is no other literature concerning the development of the mammalian pelvic girdle wherein it has been noted that the innominate cartilages of the fetal pelvis are ever continuous ventrally, indicating no suggestion of a symphysis. And further, that the symphysis, whatever its type, is developed secondarily from this bar of cartilage which forms the midventral continuity between the innominate cartilages. This suggested a study of the development of the symphyseal region of all of the available Eutheria, in order to ascertain whether a like sequence of events, e.g., the formation of the os coxae in cartilage, the fusion of the two lateral plates of cartilage in the symphyseal region, and ﬁnally the formation of the type of symphysis that is typical of the species in question, could be demonstrated in other species.
The problem presented the difficulty of obtaining embryonic material in suﬂicient variety and abundance, and at the proper stages of development. The common laboratory animals that could be readily obtained in all stages of development offered the most complete studies. The less common forms had to be studied as they beca.me available. In these rarer forms, where age data could not be obtained, the stage of development is indicated by the crown-rump measurement.
The present investigation has included ﬁve orders: Edentata (Dasypus novemcinctus, Linn); Rodentia (Mus norvegicus albinus, Lepus cuniculus, Cynomys ludovicianus); Artiodactyla (Sus scrofa); Carnivora (Felis domestica), and Primates (Homo sapiens). Here I wish to express my thanks to Dr. F. L. Hisaw for his valuable criticism of the work as it progressed, and for the prairie-dog and pocket-gopher material which he let me examine; and to Dr. H. W. Mossman for the rabbit material.
Methods and Material
The rat fetuses were obtained from the rat colony of the Department of Zoology of the University of Wisconsin. Rats were mated and fetuses were obtained at fourteen, sixteen, twenty, and twenty-two days. The fetuses were sectioned transversely, and stained with hematoxylin and eosin. This was the routine technique for all of the forms studied. Gross specimens of the adult male, and the adult virgin and multiparous female pelves were cleaned and studied in the fresh condition; and frontal sections of a ﬁfteen-day pregnant multiparous female Were made. The ages of the rat fetuses were counted from the ﬁrst of thedaily vaginal smears to show the presence of spermatozoa. The rabbit material included four fetuses—‘two seventeen and two eighteen days. The prairie—dog fetuses were of various stages of development, from 10 mm. to 25 mm. crown-rump length. By sectioning fetuses of each stage represented, it was found that the important stages, in regard to this investigation, were at 15 mm. and at 20 mm.
The pig fetuses were collected at a local abattoir. Embryos of 16 mm., 20 mm., 25 mm., 30 mm., 35 mm., and 55 mm. crown—rump length were sectioned transversely through the pelvic region. The 35—mm. and 55-mm. stages were found to be the stages of greatest interest in this investigation.
The cat fetuses were obtained from pregnant cats that happened to be among the embalmed cats that were used in the course in comparative anatomy at the University of Wisconsin. In many cases the material was found to be fairly well ﬁxed by the embalming ﬂuid, so that satisfactory studies could be made of the tissues when sectioned. Fetuses of 35 mm. and 43 mm. were studied.
Through the kindness of the Department of Zoology of the University of Wisconsin, I was permitted to remove the symphysis pubis of each of three armadillo fetuses, that form a part of the embryology museum. These symphyses were sectioned transversely, and the serial sections were studied for the points having a bearing upon this investigation. Unfortunately, these fetuses were all of the same length, being three of a mounted quadruplet group. Each measured 80 mm.
A study was made of the symphyseal region of several human fetuses, but no deﬁnite conclusions were reached, as it was impossible to obtain fetuses of the desired ages at the time.
Observations on the Development of the Symphyseal Region in Various Mammals
In this order all three of the types of pelves described by Todd (’21) are found. In this group, then, a great degree of Variation may be expected in the symphyseal region. Flower (’85) states that the rodent symphysis is long, and that it usually becomes osseous, except in the guinea-pig, where in the female it is ligamentous——the pubic bones being widely separated at parturition. In the completion of the symphyseal face the tendency is toward bilateral rather than medial ossiﬁcation.
Lepus cuniculus. In the seventeen-day fetus no ossiﬁcation centers are present in the os innominatum. The pubic and ischial cartilages surround the obturator foramen, and the symphyseal region shows the pubic cartilages to be closely approximated. They are, however, separated by undifferentiated mesenchyme, which blends insensibly with the chondrogenic layer of the pubic cartilages. In the eighteen-day fetus the ilia and ischia show incipient ossiﬁcation centers—the lacunae and cells being greatly enlarged, and showing a tendency to line up in columns, although no calciﬁed cartilage is yet apparent. The pubic cartilages show no sign of ossiﬁcation, but the chondrogenic layer is extremely active, especially in the symphyseal region. The pubic cartilages are fused at the symphysis, forming a continuous cartilaginous connection between the two innominate cartilages (ﬁg. 1).
Mus norvegicus albinus. The symphysis, pubis of the adult male, and both the sexually mature Virgin and the multiparous female, is a synchondrosis. In the old male the cartilage separating the pubic bones is gradually replaced by bone. Frontal sections through the pubic symphysis of a multiparous female, ﬁfteen days pregnant, show the symphysis to be a false synchondrosis (ﬁg. 2). In the sixteen-day fetus the cartilaginous anlagen of the pubis, ischium, and the ilium are present, and each innominate cartilage is a continuous plate of hyaline cartilage. The pubic elements are separated in the symphyseal region by undifferentiated tissue resembling the precartilage blastema surrounding the chondrogcnous areas (ﬁg. 3). The eighteen-day fetus shows the cartilaginous pelvis to be a completed structure. The pubic elements are fused together at the symphysis, so that they are continuous, forming a bar of hya.line cartilage that connects the two innominate cartilages (ﬁg. 4). Incipient ossiﬁcation centers a.re present in the ischial and iliac cartilages. The twenty-one-day fetus presents a similar picture as far as the general structure of the symphyseal region is con cerned. All of the pelvic elements at this stage show ossiﬁcation centers. Small, closely packed cells in the symphyseal region indicate active proliferation at this point, suggesting that by growth in this region the pelvic canal is widened, while the pelvis is mostly cartilaginous; and that after the pelvic elements are completely ygssiﬁed except for this interpubic synchondrosis, growth, and therefore widening of the pelvic canal, takes place from this region after the manner of growth at an epiphyseal synchondrosis.
Cynomys ludovicianus. In the 10-mm. embryo some hyaline cartilage has been laid down in the region of the ilium. No other cartilaginous elements are present, although a condensation of the scleroblastema in the region of the ischium and the pubis indicates the presence of incipient chondrogenous centers for these parts. The 15-mm. fetus shows the cartilaginous pelvis complete, the elements of each innominate cartilage forming a continuous lateral plate on each side. The pubic cartilages, however, are separated at the symphyseal region by undifferentiated mesenchyme (ﬁg. 5). In the 30-mm. fetus the ilium shows a deﬁnite ossiﬁcation center. A layer of calciﬁed cartilage underlies the periosteum, and a reticulum of calciﬁed cartilage marks out the greatly enlarged lacunae in which the enlarged cartilage cells are present. Except for this ﬁne reticulum, the hyaline matrix has been resorbed. Between the periosteum and the layer of calciﬁed cartilage a row of osteoblasts is present. The ischium shows an incipient ossiﬁcation center, but no center is indicated in the pubis at this stage. The pubic cartilages, however, are fused in the symphyseal region, forming an uninterrupted cartilaginous arch connecting the two lateral innominate cartilages into a single structure (ﬁg. 6). At the point of fusion the crowded and small cartilage cells indicate the rapid proliferation of cells in this region. Artiodactg/la
In the Ungulates the true symphyseal face is not only pubic in nature, but is conﬁned to the body of the pubis (Todd, ’21). The domestic pig was the only member of this group found available for this study, but the ease with which embryonic material of this form is collected made it possible to get an abundance of material at the stages of development that indicate the process of development of the cartilaginous pelvis. It has been impossible to ﬁnd an adequate description of the adult pelvis of this representative of the Artiodactyla, or of the fresh pelves in any other representatives of the group. Todd, (’21), however, gives several descriptions of the dried pelves of the group, in which he found the two halves of the pelvis separate in what he designates the ﬁrst, second, and the ﬁrst half of the third life period. In the second half of the third life period he found the two halves of the pelvis fused at the anterior end, and in the fourth life period the whole symphyseal face was completely ossiﬁed. The nature of the interpubic connective tissue in the fresh condition, in the stage where the two pubic bones were separate, was not suggested.
Sus scrofa domestcia. In the 16—mm. fetus the outline of the pelvis is just being suggested by the condensation of the scleroblastema—a center of condensation being present for each element of the innominate bone. These centers are characterized by closely packed and very small mesenchymal cells that stain darkly so that they are readily observed. The 24-mm. fetus shows the cartilaginous pelvis just being differentiated. Chondriﬁcation centers for each element of the innominate bone are present, but they are separated from each other by undifferentiated blastema. In the centers of chondriﬁcation the cells are dense and relatively small, but the hyaline matrix is present, and the lacunae surrounding the cartilage cells are easily visible, although the cells nearly ﬁll them. In the 30-mm. and in the 35~mm. fetus the pelvis is completely formed of hyaline cartila.ge—the pelvic elements of each side being fused into a single lateral plate of cartilage (fig. 7). There is little difference in the appearance of the two stages—the pubic elements being fused at the symphysis in both cases, so that the two innominate cartilages are joined into one continuous piece. In the 55-mm. fetus the pubic cartilages are fused so that it is almost impossible to make out the line of fusion (ﬁg. 8).
The representative of this order in this study is the domestic cat. In the adult Carnivora the pelvis is generally long and narrow, and the ischium is usually in almost a straight line with the ilium, and of nearly equal length. The ilia are usually ﬂat and straight, with very little, if any, eversion or the anterior ends. The symphysis is long, and in adult animals usually becomes osseous. The ischium takes part iii the posterior part of the symphysis, but for the most part the pubic elements form the symphysis, although, as age increases it extends more onto the ischial ramus.
Felis domestéca. The two stages chosen for study were 35-mm. and 43-mm. fetuses. I11 the 35-mm. fetus the two innominate cartilages are present and complete. The pubic elements are separated at the symphyseal region by undifferentiated mesenchyme. The 43-mm. fetus shows the pelvis completely formed of hyaline cartilage. It differs, however, from the 35-mm. stage in that the pubic elements are fused together at the symphysis, so that the two innominate cartilages form one continuous piece (ﬁg. 9). The cells at the symphyseal region are small and closely packed, indicating the rapid proliferation of the cartilage cells at this point of fusion of the two halves.
In this order the symphysis is short and is formed by the pubic elements alone. Between the opposed surfaces of bone is a plate of ﬁbrocartilage. A rudimentary joint cavity is usually present in the adult. Ankylosis at this spot, so common in the lower Mammalia, very rarely takes place in man. Todd (’21), in his excellent study of the pubic bones, concludes — that the symphysis of the ancestral primate was short, probably conﬁned to the body of the pubis,, or but slightly extending onto the pubic ramus. In the Primates, so far as the Lemurs, and the giant Anthropoids, and Man are concerned, the symphysis involves the body and part of the ramal portion of the pubis. In the giant Anthropoids frequently, and in Man always, fusion of the t.wo pelvic halves at the symphysis is lacking. In certain forms, of which Man is one, the primitively fused symphysis is resolved again into two non-uniting components.
The lack of material of the proper stages of development prevented the study of the development of the Primate pubic region, as represented in man, from being carried to a deﬁnite conclusion. The picture obtained, however, is extremely suggestive, in the light of the ﬁndings in the other orders. It is hoped that the missing stages may soon be ﬁlled in, so that a more closely graded study of the development of this region may be made. Here I wish to thank Dr. Edgar Allen for the loan of a serially sectioned human embryo; and Dr. Chas. R. Bardeen for the opportunity of examining several sectioned embryos in his collection.
Homo sapiens. Further discussion of the development of the cartilaginous pelvis in man would be superﬂuous, in the light of the work that has been done already. All investigators have agreed that three centers of chondriﬁcation appear in the blastemal os coxae—one for the ilium, one for the ischium, and one for the pubis. These centers grow until they fuse to form a continuous plate of hyaline cartilage representing the os coxae, and in which ossiﬁcation centers for each of the pelvic elements will appear. The symphysis pubis is formed at about the beginning of the third month of development (Bardeen, '05). The ﬁrst appearance of the symphysis is a dense blastemal tissue from which ﬁrst hyaline and later ﬁbrocartilage is diﬂerentiated. In the 30—mm. fetus the cartilaginous pelvis is formed, but the pubic cartilages of each side are separated at the symphyseal region by undifferentiated blastemal tissue. In the 35—mm. fetus the picture is quite the same, except that the pubic elements are very close together, so that it is diﬁicult to see whether the cells separating them are very small cartilage cells, or whether there is a thin line of undifferentiated tissue present (ﬁg. 10). The appearance of these two stages suggests the similar appearance of the pelves of other forms at this stage of development, when the two pubic elements have just fused, or are on the verge of fusing.
This study conﬁrms the concept that the representatives of the eutherian orders studied show a like sequence in the order of changes that result in the development of the adult pelvis common to the species in question. Chondriﬁcation centers arise in the scleroblastema for each of the pelvic elements—the ilium, the ischium, and the pubis. These eventually fuse together to form an innominate cartilage on each side. The pubic cartilages then fuse at the symphysis, forming a complete cartilaginous pelvis in one uninterrupted piece. The last-mentioned stage has been observed to occur in all of the forms studied, except man. However, as has already been suggested, in the 35—mm. human embryo the pubic elements appear to be on the verge of fusion at the symphysis. Whether fusion ever does occur has not been observed.
While the cartilaginous pelvis is being laid down, ossiﬁcation centers for each of the pelvic elements appear. In the case of the pubic bones, ossiﬁcation proceeds, gradually encroaching upon the interpubic hyaline cartilage (ﬁg. 11) which becomes progressively narrower until it is ﬁnally obliterated in the course of ossiﬁcation, when the two innominate bones become fused at the symphysis. A few exceptions are found, of which the female guinea-pig is an example, wherein the interpubic cartilage is replaced by an interpubic ligament; and among the Primates, where a ﬁbrocartilage is differentiated from the embryonic hyaline cartilage, and where ossiﬁcation of the symphyseal region resulting in the ankylosis of the pubic bones, is rare.
These results indicate that the classiﬁcation of the pubic symphysis depends upon the age and sex of the form in question. That is, in all forms studied, except the Primates, the pubic symphysis is at ﬁrst a true synchondrosis, gradually changing by progressive ossiﬁcation of the pubic cartilage, as the animal develops, into a synostosis, with the exception of the female guinea-pig and a few other forms in which it has been observed that the action of speciﬁc sex hormones results in the formation of an interpubic ligament (syn~ desmosis) during pregnancy. Another exception to the above is found in the Talpidae, and any other forms in which the adaptations of the animal has caused a loss of the symphysis before this process is carried out. In man, the symphysis is very soon differentiated into a false synchondrosis, with a more or less rudimentary joint cavity; and never becomes a synostosis.
In addition to the study of the development of the symphysis in the forms already described, some additional evidence in support of the concept of development that has been brought forward in this study has been found in two additional orders —Edentata and Chiroptera. The representative of the edentates is the nine-banded armadillo (Dasypus novemcinctus, Linn.). A paucity of material in this and the following case prevents any detailed discussion. Observations were conﬁned to the three 80-mm. fetuses mentioned earlier. The pubic cartilages in each case were fused at the symphysis, forming a solid bar of cartilage with no indication of a line of fusion. The representative of the Chiroptera is the little brown bat (Myotis luciﬁgus Miller). In a study made of the development of the pelvis of the little brown bat, in an unpublished investigation made by two of my associates, Dr. C. J. Hamre and Dr. R. K. Meyer (who kindly permitted me to examine their material), it was found that at one stage the embryonic pelvis of the bat is a continuous structure of hyaline cartilage, the pubic cartilages being fused to form a continuous cartilaginous union between the two innominate cartilages. Unfortunately, Dr. Hamre, who now has the material, is in Hawaii, so that the measurement of the embryo is not available.
In a form such as the pocket gopher (Hisaw, ’25) the pubic elements are still completely cartilaginous at two weeks of age, and the process of ossiﬁcation in this region through the stage of synchondrosis to synostosis occurs When the animal is two-thirds grown. After that, the sex factor enters to cause a gradual resorption of the pubic bones at the symphysis of the female, to form the open-type pelvis characteristic of the mature female of this group. This form is interesting in that the cartilaginous continuity between the pubic elements disappears relatively early in the life of the animal, leaving a complete bony arch formed by the fusion of the pubic bones. In most forms the obliteration of the interpubic hyaline cartilage and fusion of the pubic bones through completion of the symphyseal face by ossiﬁcation, is a process found in old individuals. However, the process, and at whatever age completed, in these forms studied (exclusive of exceptions aleady noted) at some time in the cartilaginous stage, the pelvis is a continuous structure of hyaline cartilage: the two innominate cartilages being fused at the pubic symphysis. There follows a gradual progressive change from a symphyseal synchondrosis to a fusion of the pelvic halves to form a synostosis, through the completion of the symphyseal face by progressive ossiﬁcation. It can then be said that, in these forms, the pelivs is a homogeneous continuity at two stages of its development——ﬁrst as embryonic hyaline cartilage, and, in the adult, as bone.
- In the Monotremes the embryonic pelvis was found to be a continuous structure of hyaline cartilage at one time — the two innominate cartilages being fused at the symphysis.
- The condition stated above was found in ﬁve eutherian orders, among eight different species; exclusive of observations made on human embryos.
- The embryonic pelvis of the forms studied (except Primates) is at one time a continuous structure of hyaline cartilage, with the pubic cartilages fused into a continuous bar at the symphysis. Ossiﬁcation of the pubic elements progressively obliterates the interpubic cartilage, forming a continuous bony pelvis through the fusion of the pubic bones.
- The symphysis pubis, whatever its type, is developed secondarily from the original bar of hyaline cartilage, which forms the midventral continuity between the innominate cartilages, in the forms studied.
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1 Transverse section through the pubic symphysis of an eighteen-day rabbit fetus, showing fusion of the pubic cartilages at the symphyseal region. Approx. X 1.5.
2 Frontal section through the symphysis of a multiparous female rat, ﬁfteen days pregnant. Approx. X 15.
3 Transverse section through the symphyseal region of a sixteen-day rat fetus. Note the pubic cartilages separated by undifferentiated blastemal tissue. Approx. X 15.
4 Transverse section through the symphyscal region of an eighteen—day rat fetus, showing the fusion of the pubic cartilages at the symphysis. Approx. X 15.
5 Transverse section through the symphyseal region of a 15-mm. prairie-dog fetus. Note the separation of the pubic cartilages by undiﬁerentiated blastcmal tissue at the symphyseal region. Approx. X 15.
6 Transverse section through the pelvic girdle of a 30-mm. prairie dog fetus. Note the continuity of the pubic cartilages at the symphysis.
7 Transverse section through the pubic symphysis of a 304 mm. pig fetus. Note the close approximation of the pubic cartilages at the symphysis. Approx. X 15.
8 Transverse section through the pelvic girdle of a 55-min. pig fetus. Note the complete continuity of the pubic eartilages at the symphysis. Approx. X 25.
9 Transverse section through the pelvis of a 43-mm. eat fetus. Note the continuity of the pubic cartilages at the symphysis. Approx. X 15.
10 Transverse section through the pelvis of a 35-mm. human fetus. Note the close approximation of the pubic cartiluges at the syinphysis and the apparent continuity superiorly. Approx. X 15.
11 Transverse section through the pubic symphysis of a young male guineapig, showing the plate of hyaline cartilage between the encroaoliing ossiﬁcation processes of the pubic bones.
Cite this page: Hill, M.A. 2018 Embryology Paper - A study of the development of the mammalian pelvis. Retrieved January 19, 2018, from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_A_study_of_the_development_of_the_mammalian_pelvis
- © Dr Mark Hill 2018, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G