Paper - The normal changes in the position of the embryonic kidney
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Gruenwald P. The normal changes in the position of the embryonic kidney. (1943) Anat. Rec.
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- 1 The Normal Changes in the Position of the Embryonic Kidney
- 1.1 Introduction
- 1.2 Material and Methods
- 1.3 Observations
- 1.4 Discussion
- 1.5 Failure of Normal Displacement - Pelvic Kidney
- 1.6 Summary
- 1.7 Literature Cited
The Normal Changes in the Position of the Embryonic Kidney
Department of Histology, Middlesex University School of Medicine, Waliham, Massachusetts
It has long been known that the kidney undergoes a remarkable change in position during early stages of its development. Most of the studies on this process were conducted in an effort to decide whether the kidney moves “actively,” or is carried passively to its new position by other parts to which it is attached. However, the majority of the reports in the literature fail to indicate the mechanism of this active or passive movement held responsible by the respective authors. Preliminary studies suggested that the conditions involved in this process are too complex to be adequately described by one of these two terms without further explanation. The present detailed investigation was carried out in an effort to trace the mechanism of displacement of the kidney, as far as feasible with descriptive methods.
Material and Methods
From the author’s collection of serially sectioned human embryos of 7.5 to 48 mm., the best suitable specimens were used to obtain graphic reconstructions of those organs which had to be considered as possibly inﬂuencing the position of the kidney. In these reconstructions, the adrenal, kidney, urogenital ridge, and umbilical artery of the right side appear projected on a sagittal plane, along with the liver and vertebral column. Reconstruction of the organs of one side was deemed suﬂicient since the changes in question are identical on both sides. Fourteen reconstructions were obtained from cross sections and one by superimposing sagittal sections. One of the 9—mm. embryos showed agenesis of the ureteric buds, as described previously (’39). The segments of the vertebral column were determined by counting from the first cervical segment, and also by the position of the first and last ribs. The original magnifications of the reconstructions varied from 15 to 50; In the early stages represented, the outlines of the ' adrenals are inaccurate because the boundaries of their early primordia are very indistinct. The segments occupied by the various organs were read from the reconstructions and compiled in curves (fig. 8). The vertical lines representing individual embryos in this figure are placed in such distances as to correspond very roughly to the time intervals during development.
In addition to this material, early stages of metanephros development were studied in embryos from the Minot Embryological Collection. A reconstruction was made of a 6.7-mm embryo from that collection. However, it turned out that in these earliest stages the segments can not be determined with sufficient accuracy because of the low degree of differentiation of the vertebrae. For this reason, the results of the reconstruction of this '6.7-mm. embryo and the author’s 7.5-mm. series are not entered in figure 8.
The following descriptions are based on the findings in the sixteen embryos whose organs were graphically reconstructed. The embryos will be described in groups representing the most important steps of the processes under consideration.
Embryos up to 7.5 mm
In embryos showing the earliest stages of metanephros formation, the caudal nephrons of the mesonephros are just differentiating and the adrenal cortex blastema appears with indefinite boundaries near the cranial portion of the mesonephros. The kidney is found caudal to the mesonephros. Its relation to the segments of the vertebral column can not be determined exactly by graphic reconstruction, because on cross sections the vertebrae of this region can not be definitely delimited from each other. However, it is certain that the kidney primordium arises at the level of the sacral segments, as described by Starkenstein. Approximate determination of the segments carried out in the reconstruction of a 6.7-mm. embryo, makes it probable that the kidney is located slightly farther caudally than in the embryos of the following group.
Embryos of 9 mm
(figs. 1 and 8). The axial organs of these embryos, as represented in figure 1 by the notochord, show a considerable and fairly uniform curvature throughout the trunk. The mesonephros is just reaching its full length and extends from the lower cervical to the lower lumbar segments. Near its cranial end appears the adrenal cortex primordium, not yet distinctly bounded. Its position is dorsal or dorso— cranial to the liver. The metanephros is found caudal to the mesonephros, and shows the dilated end of the ureteric bud beginning to form cranial and caudal extensions. It is located opposite the first and second sacral segments of the vertebral column, and ventro-caudal to the origin of the umbilical artery from the aorta.
Embryos of 9.5 and 10 mm
(figs. 2, 8, 10). In the lumbar a11d sacral regions the curvature of the vertebral column is approximately the same as in the previous stage, but the thoracic portion of the axial organs has straightened somewhat. The cranial border of the mesonephros shows the very beginning of a movement in the caudal direction which will be discussed later. The boundaries of the adrenal cortex are still indistinct. The curvature of the mesonephros is not, as in the previous stage, concentric with that of the vertebral column, but approaches the form of a chord. This is most probably an effect of the straightening of the axial organs, a11d will appear to a greater extent in the following stage (fig. 3). An instructive diagram of the changing curvature of the vertebral column may be found in the work of Bardeen (’05, fig. 44). If the axial organs and the mesonephros, figs. 1-7 Graphic reconstructions based on serial sections of human embryos of 9mm. (fig. 3), 12 mm. (fig. 4), 15.5mm. (fig. 5), 18 mm. (fig. 6) and 25 mm. (fig. 7). Vertebral column (in fig. 1: notochord): heavy lines, lumbar segments stippled; liver; dotted heavy line; ventral body wall and right mesonephros: thin lines; right gonad: horizontally lined; right adrenal: broken thin line; right kidney: heavy line; right umbilical artery at the aorta: ring with cross. The (fig. 1), 10mm. (fig. 2), 10.5mm. outlines of these organs appear projected on sugittal planes. X 9.
originally occupying concentric arches, straighten, the mesonephros will straighten more than the axial organs if it is to extend over the same number of segments. From this stage on, all embryos of the investigated period show a large amount of loose mesenchyme in the lumbo-sacral region, apparently filling the space between the diverging retroperitoneal and axial organs (figs. 2-7). In spite of this mechanism, the mesonephros and other viscera can not keep pace with the straightening vertebral column, and consequently the segmental extension of the viscera decreases during this and the following stage, as is apparent in figure 8. These changes have considerable bearing on the position of the small metanephros which is in close proximity with the caudal end of the mesonephros. It moves slightly in the cranial direction (fig. 8) and its longitudinal axis does not remain parallel to the vertebral column. This latter change is probably caused in part by the changed position of the mesonephros (fig. 2), and partly by the presence of the umbilical artery which interferes with the growth of the primordium in the cranial direction, and thus forces it to tilt. This relation of the metanephros to the umbilical artery is easily seen in reconstructions (fig. 2) and sagittal sections (fig. 10).
Embryos of 10.5 to 13.5 mm
(figs. 3, 4, 8). The changes observed in the embryos of this group bring the metanephros almost to its definitive position. figure 8 shows that the viscera in the upper thoracic region, including liver, adrenal, and cranial border of the mesonephros, are uniformly displaced in the caudal direction. Detailed description and investigation of this change in the thoracic region are beyond the limits of the present work. (Here as in several other parts of the present report, the description is abbreviated by taking the Vertebral column as a fixed scale, thus neglecting the inﬂuence of growth of the vertebral column itself.) In the lumbar and sacral regions, the structures under consideration show only slight changes in their segmental locations, with the exception of the kidney. figure 8 shows the caudal border of the mesonephros and the umbilical artery moving slightly in the cranial direction, in continuation of the process described in the preceding paragraph. The caudal border of the kidney follows this movement, but the cranial border shows a steep cranial displacement between the stages of 10 a11d 11 mm. This is the expression of extensive growth of the kidney in the cranial direction alone. It can be explained on the basis of the above described tilting of the primordium. Its caudal end is turned toward the sacral vertebrae. It is fixed because the small amount of tissue between it and the skeleton can not yield. The cranial end, however, is free; hence all of the considerable longitudinal growth of the organ expresses itself as displacement of the cranial pole. Thus the center of the kidney passes the narrow space between the umbilical arteries. At this stage the kidney is a relatively thin oblong body (fig. 3). Immediately after its center has passed the umbilical artery, it begins to round itself out (fig. 4). It appears as if the kidney were mechanically forced to stretch temporarily in order to bypass the umbilical artery and leave the narrow pelvic region. This is, however, not a deformation of an existing mass of tissue, but rather an inﬂuence upon the direction of growth of a rapidly expanding primordium. At the end of this period, the cranial pole of the kidney has reached the lower border of the first lumbar segment and is thus almost in the position which it is to occupy during a long period of embryonic life (fig. 8).
Embryos of 15.5 to 21 mm
The most striking change during this period is the reduction of the segmental length of the mesonephros (fig. 8). There is only a slight variation in the position of the caudal end of this organ, but the cranial end moves from the eighth thoracic segment in the 15.5—mm. embryo to the second lumbar segment in the 21-min. embryo. The role of degeneration of the cranial portion of the mesonephros in these changes will not be discussed here. There is also a displacement of liver and adrenal cortex during the same period, but to a far lesser degree. The kidney rounds itself out as described in the previous section. The result is, that its cranial pole keeps approximately the same distance from the umbilical artery during the previous and present stages (13.5 to 21 mm.), whereas the caudal pole undergoes a relative movement in the cranial direction and thus approaches the level of the umbilical artery (fig. 8). In the 18-mm. embryo the kidney is found in contact with the adrenal for the first time. figure 8 shows that this contact is not established by cranial movements of the kidney, but by caudal displacement of the adrenal (see above). In the 21-mm. embryo the adrenal occupies the most caudal position encountered in the present series of stages.
Embryos of 25 to 48 mm
The only organ under consideration which still undergoes considerable displacement during this late period is the mesonephros. It is now attached to the inguinal region by a well developed gubernaculum and there can be little doubtthat this attachment accounts for the removal of the mesonephros from the posterior abdominal wall. A detailed description of development and action of the gubernaculum in the human embryo was given by Moszkowicz (’35). The cranial borders of liver and adrenal keep their position at the lower borders of the seventh and tenth thoracic segments, respectively, while the caudal border of the adrenal and the cranial pole of the kidney show a slight cranial displacement. It appears as if these changes were due to a relative decrease in size of the adrenal. The kidney is now definitely rounded; this rounding and the slight cranial displacement just mentioned have resulted in bringing the lower pole of the organ to a level cranial to that of the umbilical artery. It appears that a slight caudal displacement of the artery, whose mechanism was not determined, also plays a role in this process (fig. 8). During the oldest period investigated (25 to 48 mm.) most organs under consideration have reached a stabile position. It can only be conjectured at the present time that the slight further ascensus which the kidney has to undergo in order to reach its final position, may be caused by a relative decrease in size of liver and adrenal, with the cranial border of the liver as the fixed point and the kidney remaining in contact with the lower surface of the adrenal.
In his classic description of the development of the urogenital tract Felix (’l2) holds that the kidney primordium moves craniad by growth of the ureteric bud until the end of that bud begins to branch. By this time, that is, in embryos of 9.5—13 mm., the pelvis of the kidney has reached its definitive position opposite the second lumbar vertebra. Further growth of the ureter occurs only as far as is necessary to keep up with the increasing distance of its end points. In other words, Felix assumes that the kidney reaches its final position after a brief period of active migration by growth of the ureteric bud. This opinion is reﬂected in most of the text-books.
Brockmann (’36) traced the position of the kidney in human embryos and arrived at a different conclusion. He holds that straightening of the body causes a change in relations, resulting in a displacement of the kidney in the cranial direction when compared with the vertebral column. A similar mechanism was hinted above in the description of embryos of 9.5 and 10 mm. Starkenstein (’38) opposes Brockmann’s conclusion and points out that Brockmann failed to examine the earliest stages during which most of the displacement occurs. He advocates active ascensus of the kidney without specifying how the organ accomplishes active movement. Brockmann maintains in a second publication (’38) his previous view for the stages which he had investigated, and objects to Starkenstein’s failure to differentiate between migration and displacement.
fig. 8 Graphic presentation of the position of the right kidney, adrenal and mesonephros (cranial and caudal border), liwfer (cranial border) and the level of origin of the right umbilical artery from the aorta, after graphic sagittal reconstructions. Each vertical line connects all points related to one embryo whose length in millimeters is given at the bottom. These lines are placed in distances very roughly proportionate to the time intervals during development. The embryo designated by 9 A shows agenesis of the ureteric buds (Gruenwald, ’39). In this case the kidney measurements refer to the metanephric blastema alone.
fig. 9 Diagrams illustrating the displacement of the kidney in relation to vertebral column and umbilical artery. Changes in the curvature of the vertebral column are not considered. The diagrams represent approximately the following stages: a, 7mm.; b, 10 mm.; c, 11mm.; (1, 18 mm.; e, 25 mm. Drawn as figures 1-7. Gruenwald (’38) points out that the ureteric bud is covered with a thick cap of nephrogenic tissue from its earliest stages. This makes a displacement of the whole primordium by growth of the ureter alone (Felix) highly improbable. A later finding (’39) showed that in a 9-mm. human embryo with agenesis of the ureteric buds the nephrogenic tissue had moved away from the caudal end of the wolffian duct exactly like a normal kidney primordium (see also the present fig. 8, embryo 9 A). This disproves an inﬂuence of the ureter upon the position of the kidney in those early stages in which the primordium might be small enough to yield to pressure by the ureter.
As suggested in the introduction to the present report, no uniform explanation should necessarily be expected for all phases of displacement of the kidney primordium. It was found that up to the 10—mm. stage the kidney keeps a constant relation to the caudal pole of the mesonephros while moving craniad. This is strongly in favor of displacement by differential growth as against “active” movement. As suggested in the description of the observations, straightening of the body is probably the cause of this change, in a similar manner as suggested by Brockmann for later stages. As soon as the kidney reaches the umbilical (common iliac) artery, it tilts and thus loses its previous close relation to the mesonephros. Its caudal end is now directed dorso-caudad toward the sacral vertebrae, and thus prevented from moving caudad again when the urogenital ridge begins its descensus at the 13.5-mm. stage (fig. 8). For the same reason the caudal pole does not yield during the following period of rapid growth of the kidney, and the cranial pole must move upward that much more (fig. 8). In this manner the pelvis of the kidney reaches approximately its final position, and rounding and relative shortening finally remove the kidney completely from the crotch of the umbilical arteries. The remaining slight cranial displacement is probably the result of a relative decrease in size of the liver and adrenal. These latest stages are not covered by the present investigation.
According to the present view all displacement of the kidney is effected by differential growth, although not in the simple and uniform manner as suggested by previous investigators. Participation of active ascensus (Starkenstein) appeared improbable from the beginning since no mechanism is known by which an organ of the structure of the kidney can move actively. The only process which might be considered as active movement of the primordium, is displacement by pressure of the growing ureter. It is obvious that this could only occur in very early stages, but the above quoted findings in agenesis of the ureteric buds exclude this possibility, as does the constant relation of kidney and mesonephros in the stages in guestion.
In conclusion, the ascensus of the kidney can be described as follows (fig. 9). In embryos up to 10 mm. the retroperi— toneal tissues of the lumbar and sacral regions, including mesonephros and kidney, move in the cranial direction (fig. 9 a, b). Shortly before this movement comes to an end, the upper pole of the kidney deviates ventrally (fig. 9 b). In this new position the caudal pole of the kidney is directed against the anterior surface of the sacral vertebrae and thus prevented from moving downward. There follows a period of very fast lengthening of the kidney (10-11 mm., fig. 9 c) which, according to this peculiar position of the organ, can result only in cranial displacement, with the caudal pole remaining in a constant position. In the course of this growth period the pelvis of the kidney passes the level of the umbilical arteries. The shape of the kidney changes now, perhaps because the organ has emerged from the narrow passage between these arteries. The transverse diameter increases simultaneously with a decrease in length (fig. 9 d). The kidney thus rounds itself out and the caudal pole moves craniad until it reaches the level of the umbilical arteries (21—mm. embryo). Meanwhile the kidney has come in contact with the adrenal (18—mm. embryo) and moves now, along with the caudal border of the adrenal, slightly craniad (fig. 9e). The nature of this last slight movement was not ascertained; changes in the size of liver and adrenal may play a role. In the 25-min. embryo the kidney is found entirely above the level of the umbilical arteries, and keeps a constant position in the upper three lumbar segments during the remainder of the period covered by the present investigation.
Fig. 10. Parasagittal section of a 10 mm human embryo (see also fig. 2). Azan stain.
Failure of Normal Displacement - Pelvic Kidney
Most authors regard congenital pelvic kidney as the result of arrested development, that is, retention of the kidney in its early embryonic position. Laughlin (’42) lately disputed this concept and held that in the malformation in question the kidney is pulled down into the pelvis from the lumbar region by abnormal attachment to organs moving in that direction. He based his theory on Hinman’s (’35) statement that the kidney is found in embryos of 9-10 mm. in its final position with its pelvis at the level of the second lumbar vertebra, and that from that time on other structures move away from the kidney in the caudal direction. It is obvious that Hinman failed to consider sufficiently early stages. The present findings show, in accordance with the data given by Starkenstein, that the kidney POSITION or EMBRYONIC KIDNEY 175 primordium is at first located in the pelvis, at the level of the sacral segments. In the course of its cranial displacement it must pass the crotch of the umbilical arteries. This is important from the viewpoint of teratology not only, as Lewis and Papez point out, because the two kidney primordia come very close to one another and may fuse, but also because the kidneys can pass the arteries only after tilting as described here. Failure of this complicated movement would trap them below the umbilical arteries and keep them in the pelvis. The resulting condition would be pelvic kidney. We can thus describe the formal genesis of that malformation as an arrest of displacement of the kidney, favored by the peculiar relations to the umbilical (later common iliac) arteries or failure of the early kidney primordium to follow the caudal end of the mesonephros in its cranial movement.
The relation of the kidney primordia to the surrounding organs was examined in human embryos of 6 to 48 mm., mostly by means of graphic reconstruction from transverse serial sections.
The kidney moves craniad from its original position in the sacral region, along with the caudal portion of the mesonephros. This displacement is probably due to a diminution of the body curvature. The cranial pole of the kidney reaches the umbilical artery and avoids it by deviating ventrally. The caudal pole is thus directed dorso-caudad toward the sacral vertebrae (10—mm. embryo).
The following rapid growth of the kidney causes its pelvis to pass the umbilical artery in the cranial direction because the caudal pole cannot yield (11—mm. embryo). The kidney then rounds itself out and shortens relatively, thus escaping the crotch of the umbilical arteries in the cranial direction (21—mm. embryo). A slight further movement in the same direction brings it into the upper three lumbar segments (25mm. embryo) where it remains for the rest of the period investigated. No active cranial migration of the kidney takes place at any time.
Congenital pelvic kidney is the result of failure of the organ to undergo its normal change of position. The obstacle of the umbilical artery favors this arrest of displacement.
I wish to acknowledge the generosity of the Department of Anatomy, Harvard Medical School, in permitting me to use the Minot Embryological Collection.
BROCKMANN, A. W. 1936 Form— und Lageentwicklung der Niere. Morphol. Jahrb., vol. 77, pp. 605-665.
1938 Bemerkungen zu einer Arbeit Starkenstein: “Ueber die Anlage und Wanderuug der Nachniere beim Menseheu.” Morphol. Jahrb., vol. 81, pp. 21-23.
GRUENWALD, P. 1938 Embryologische Beitrage zur Kasuistik und Genese dcr Nierendystopien. Virchow’s Arch., vol. 303, pp. 47-59.
Gruenwald P. The mechanism of kidney development in human embryos as revealed by an early stage in the agenesis of the ureteric buds. (1939) Anat. Rec. 75(2) 240-247.
HINMAN, F. 1935 The principles and practice of urology. Philadelphia; Saunders.
LAUGHLIN, V. C. 1942 Renal dystopia (ectopia): a report of an interesting case and brief review of the literature. J. Urol., vol. 47, pp. 632-64].
Lewis FT and Papez JW.Variations in the early development of the kidney in pig embryos, with special reference to the production of anomalies. (1915) Anat Rec 9: 105-106.
MOSZKOWICZ, L. 1935 Das Gubernaculum Hunteri und seine Bedeutung fur den Descensus testiculorum beim Menschen. Zeitschr. f. Anat. u. Entwicklungsgesch., vol. 105, pp. 37-71.
STARKENSTEIN, W. 1938 Ueber die Anlage und die Wanderung der Nachniere beim Menschen. Morphol. Jahrb., vol. 81, pp. 8-20.
Gruenwald P. The normal changes in the position of the embryonic kidney. (1943) Anat. Rec.
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