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Q Bull Northwest Univ Med Sch. 1949;23(4):428-31.
The morphogenesis of the systems of juxta-aortic tissues in human embryos.
Jimenez-Castellanos J.
https://www.ncbi.nlm.nih.gov/pubmed/18148736
PMID: 18148736 PMCID: PMC3802928
THE MORPHOGENESIS OF THE SYSTEMS OF
JUXTA_AORTIC TISSUES IN HUMAN EMBRYOS1
JUAN JIMENEZLASTELLANOS”
INTRODUCTION
HE chromaffin system of tissues has
been reviewed as to origin, morphogenesis, relationships and functions by
Kohn (1), Zuckerkandl (2), Iwanow (3),
and Hollinshead (4). Reconstructions of
the juxta-aortic bodies have been made
in various mammals. Kohn (1), Zuckerkandl (2), and Iwanow (3) have presented
planographic reconstructions of this system in human embryos and fetuses of
various ages, and Wrete (5) has presented
models prepared from human embryos
of 38 and 39 mm.
In order to contribute to the better
understanding of the sympathochromaffin
system in the human embryo, three
stages in the morphogenesis of this system
have been reconstructed planographically. The two older stages have also
been reconstructed as wax models. The
three embryos so utilized were of 9 mm.
(greatest length), 14 mm. (greatest length)
and 40 mm. (crown-rump length). It was
judged that stages intermediate between
14 and 40 mm. did not offer sufficient
differences to warrant separate consideration. The 9 mm. embryo was fixed in
Zenker’s solution; the 14 mm. and 40 mm.
specimens were fixed in 20 per cent
formalin. All three embryos were embedded in paraffin, sectioned transversely
at 10, 11 and 30 micra, respectively, and
stained in hematoxylin and eosin. The
original models and the planographic reconstructions were made at magnifications of 22.5 diameters (40 mm. embryo)
and 62.2 diameters (14 mm. embryo).
The original planographic reconstruction
of the 9 mm. embryo was made at a
magnification of 156 diameters.
This investigation was carried out in
the laboratory of Prof.-Dr. José Escolar
‘Contribution no. 517 from the Department of Anatomy,
Northwestern University Medical School. Received for
publication, June 1. 1949.
‘From the Department of Anatomy. University of Granada, Spain, and Northwestern University Medical School.
428
at the University of Granada, to whom
I wish to express gratitude for many
excellent suggestions. The author is also
grateful to Dr. John Jacobs and Dr.
Alberto Vaz Ferreira of Northwestern
University Medical School for their kind
assistance in preparing the original manuscript in English and to Professor L. B.
Arey, who has recast that manuscript
into its present form.
OBSERVATIONS
1. Embryo of 9 mm.
At this stage the reconstruction (fig. 1)
shows that the suprarenal glands have
not yet appeared, the metanephroi are
at the beginning of their development,
the mesonephroi are fully developed and
the gonads are prominent, elongate folds
along the ventromedian surfaces of the
mesonephroi. The ganglionated sympathetic cords descend dorsolateral to the
aorta, and near the cranial ends of the
mesonephroi gradually disappear as such
and become continuous with paired juxtaaortic masses. These latter extend caudad ventrolateral to the aorta, and in
their more caudal extents interconnect by
three bridges ventral to the aorta.
In the sections the juxta-aortic tissue
shows as masses that stain deeply with
hematoxylin (fig. 4).
2. Embryo of 14 mm.
As the reconstruction (fig. 2) shows,
this stage is marked by the increasing
prominence of the metanephroi and by
the suprarenal glands, which not’ only
have appeared since the previous stage
but also have grown to relatively large
size. The juxta-aortic substance differs
from that in the previous stage by being
dispersed into 31 discrete masses. These
lie both in front of the aorta and on
both sides of it; indeed, some that are
not shown in figure 2 are even included
in the interior of the suprarenals themJIMENEZ-CASTELLANOS~—]UXTA-AORTIC TISSUES 429
fig. '1. Planographic reconstruction of the juxtaaortic masses and the adjacent organs of a human
embryo of 9 mm. :3 5.9. (1) metanephroi; (2) mesonephros; (3) gonad; (4) sympathetic cord; (5)
juxta-aortic body; (6) post-cardinal vein; (7)
coeliac axis; (8) superior mesenteric artery.
fig. 2. Planographic reconstruction of the juxtaaortic masses and the adjacent organs of a human
embryo of 14 mm. :c 47. (1) Aorta; (2) coeliac axis;
(3) superior mesenteric artery; (4) middle sacral
artery; (5) common iliac artery; (6) metanephros;
(7) suprarenal gland; (8) mesonephros; (9) gonad;
(10) sympathetic cord; (1 1) splanchnic nerve;
aortic bodies (of Zuckerlcandl).
fig. 3. Planographic reconstruction of the juxtaaortic masses and the adjacent organs of a human
fetus of 40 mm. :13 8.5. (1), (2), Vertebral body and
arch; (3) aorta; (4) common iliac artery; (5) renal
hilus; (6'), (7'), suprarenal glands; (8) superior
mesenteric artery; (9), inferior mesenteric artery;
(10), (16), (24), aortic body; (11) middle sacral
artery; (12) common iliac vein; (13) inferior vena
cava; (14), (17), (20), renal vein; (15), (19) vein
from aortic body; (18) left suprarenal vein; (21)
splanchnic nerves; (2.?) right vagus nerve; (23)
sympathetic cord.
430
selves. In the region located between
the suprarenals and between the cranial
halves of the metanephroi, there are
numerous small masses, the more caudal
ones tending to be larger than those at
higher levels. Between the caudal halves
of the metanephroi there are two masses,
much larger than any others in the
embryo. These are the forerunners of
the aortic bodies of Zuckerkandl. The
sympathetic cords continue caudad beyond the region reconstructed. The
splanchnic nerves also descend to the
level of the juxta—aortic masses and end
in association with them; the nerve fibers,
however, do not actually enter the cellular masses.
In sections (fig. 5) there is no particular
tinctorial difference between the large
inter-renal masses and the small masses
located between the suprarenal glands.
Both stain deeply with hematoxylin.
Certain of the small masses can be observed in the process of being incorporated into the interior of the suprarenal
glands. This, of course, is a normal
initial stage in the development of the
suprarenal medulla.
3. Embryo of 40 mm.
The distribution or Juxta-aortic tissue
is much as in the previous stage (fig. 3).
Mostly lateral to the aorta, and roughly
coincident with the extent of the suprarenal glands, are small masses composed
of small cells that stain deeply with hematoxylin. In size and stainability, at least,
they resemble closely the syrnpathoblasts
in the ganglionated sympathetic chains.
These latter cells, likewise, are not far
along in the course of differentiation into
ganglion cells. All of these small juxtaaortic masses that were examined for the
purpose were proved to be in intimate
relationship with the terminations of
fibers from the splanchnic and right
vagus nerves. It is possible, under high
magnification, to observe the nerve fibers
penetrating into the interior of such
masses.
There are two large inter-renal masses
which represent the future aortic bodies.
These are elongate and irregularly lobed;
they interconnect, ventral to the aorta,
by two prominent bridges of tissue. A
similar, smaller mass is displaced down
QUARTERLY BULLETIN, N.U.M.S.
fig. 4.
Photomicrograph through a human
embryo of 9 mm. at the level indicated in fig. 1. :1:
59. (1) Aorta; (2) posterior cardinal vein; (3)
mesonephros; (4) gonad; (5) liver; (6) juxtaaortic body; (7) body of vertebra.
fig. 5. Photomicrograph through a human
embryo of 14 mm. at the lower level indicated in
figure 2. 1: 47. (1) Metanephros; (2) juxtaaortic body; (3) sympathetic cord; (4) aorta;
(5) mesanephros; (6) body of vertebra.
fig. 6. Photomicrograph through a human fetus
of 40 mm. at the middle level indicated in fig. 3.
ac 15. (1) Suprarenal gland; (2) aorta; (3) body of
vertebra; (4) duodenum; (5) metanephros; (6)
crus of diaphragm; (7) sympathetic cord; (8)
right splanchnic nerve; (9) masses of sympathoblasts; (10) paraganglia; (11 ) renal vein; (12)
inferior vena cava.
JIMENEZ-CASTELLANOS—JUXTA—AORTIC TISSUES 431
the middle sacral artery. All three bodies
stain more weakly than do the smaller
masses at higher levels, already mentioned. Their paler color with hematoxylin is like that observed in the most
central part of the suprarenal gland.
Intermediate between the two levels
already mentioned is a zone containing
small masses that have a double structure (fig. 6). The main material of such
a complex consists of the larger, pale type
of cell; at the periphery are aggregations
of the smaller, dark type of cell.
DISCUSSION
This study sheds no light on the origin
of the juxta-aortic tissue since at 9 mm.
it is already present as paired, continuous masses. At this period this common
substance is not visibly differentiated in
its definitive directions: ganglion tissue
of the coeliac plexus; suprarenal medulla;
and the chromaffin tissue of the aortic
paraganglia. This lack of differentiation
is in accord with the observations of
other investigators and is not only shown
by routine methods of staining but also
by the application of specific methods
for chromaflin tissue and by silver procedures.
The 14 mm. stage likewise fails to provide information concerning divergent
differentiation in the common juxtaaortic tissue. It does, nevertheless, illustrate the subdivision of the common
primordia into multiple small masses superiorly and two large inter- renal masses
(aortic bodies of Zuckerkandl) that lie at
a more caudal level. Likewise, the invasion of some smaller masses (future
suprarenal medulla) into the cortical primordium has begun.
At 40 mm. some specialization, as indicated by staining differences with hematoxylin, can be detected readily; Zuckerkandl (6) was the first to notice this
divergent stainability. The sympathoblasts of the small, cranial masses are
larger, paler elements. These are coming
into relationship with nerve fibers, all of
which are preganglionic elements (Hollins
head, 4). The small masses at an intermediate level between the ganglionic
primordia and the aortic bodies tend to
show representations of both cell types,
as do also the later paraganglia.
SUMMARY
Planographic reconstructions have been
made of the sympatho-chromaffin tissue
in human embryos of 9, 14 and 40 mm.
The two older stages were also modelled
in wax.
The 9 mm. stage possesses two elongate, interconnecting juxta-aortic masses
which consist of small, dark-staining cells.
At 14 mm. the suprarenal glands are
beginning to be invaded by some of this
tissue which also has subdivided into
many small masses cranially and into
two large masses located caudally between the metanephroi.
At 40 mm. the differentiation has taken
three directions: (1) suprarenal medulla;
(2) sympathetic ganglia; (3) paraganglia;
(including the aortic bodies of Zuckerkandl). The cells of the future suprarenal
medulla and paraganglia are large and
stain palely. The small masses, located
cranially (between the suprarenal glands),
consist of small, dark-staining cells that
are becoming similar to the sympathoblasts. In a location intermediate between
these two extremes are compound, small
masses containing both kinds of cells.
Raferences
1.Kohn, S.: Die Paraganglien, Arch. f. mikrAnat., Bd. 62, S. 263-365, 1903.
2. Zuckerkandl, E.: The Development of the
Chromaffin Organs and the Suprarenal Bodies.
In Keibel and Mall: Manual of Human
Embryology, 2:157-179, 1912.
3.Iwanow, G.: Das Chromafline and Interrenales System des Menschen, Ergeb. d.
Anat., Bd. 29, S. 87-280, 1932.
4. Hollinshead, W. H.: Chromaflin Tissues and
faigganglia, Quart. Rev. Biol., 152156-171,
5. Wrete, M.: Beitrag zur Kenntnis von der
Entwicklung des Chromaffinen Gewebes der
Bauchregion beim Menschen, Zeitschr. f.
mikr.-anat. Forsch., Bd. 9, S. 79-98, 1927.
6. Zuckerkandl, E.: Ueber Nebensorgane des
Sympathicus in Retroperitonealraum des
Menschen, Anat. Anz. (Ergéinzrheft), Bd. 19,
S. 95107, 1901.
{{Footer}}
[[Category:Historic Embryology]][[Category:1940's]]
[[Category:Draft]]

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Jimenez-Castellanos J. The morphogenesis of the systems of juxta-aortic tissues in human embryos. (1949) Q Bull Northwest Univ Med Sch. 23(4):428-31. PMID: 18148736

Online Editor Note 
Mark Hill.jpg
This historic 1949 paper byJimenez-Castellanos is a description of the development of the juxta-aortic tissues.



Modern Notes:

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Mark Hill.jpg
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Q Bull Northwest Univ Med Sch. 1949;23(4):428-31. The morphogenesis of the systems of juxta-aortic tissues in human embryos.

Jimenez-Castellanos J.

https://www.ncbi.nlm.nih.gov/pubmed/18148736

PMID: 18148736 PMCID: PMC3802928


THE MORPHOGENESIS OF THE SYSTEMS OF JUXTA_AORTIC TISSUES IN HUMAN EMBRYOS1

JUAN JIMENEZLASTELLANOS”

INTRODUCTION

HE chromaffin system of tissues has

been reviewed as to origin, morphogenesis, relationships and functions by Kohn (1), Zuckerkandl (2), Iwanow (3), and Hollinshead (4). Reconstructions of the juxta-aortic bodies have been made in various mammals. Kohn (1), Zuckerkandl (2), and Iwanow (3) have presented planographic reconstructions of this system in human embryos and fetuses of various ages, and Wrete (5) has presented models prepared from human embryos of 38 and 39 mm.

In order to contribute to the better understanding of the sympathochromaffin system in the human embryo, three stages in the morphogenesis of this system have been reconstructed planographically. The two older stages have also been reconstructed as wax models. The three embryos so utilized were of 9 mm. (greatest length), 14 mm. (greatest length) and 40 mm. (crown-rump length). It was judged that stages intermediate between 14 and 40 mm. did not offer sufficient differences to warrant separate consideration. The 9 mm. embryo was fixed in Zenker’s solution; the 14 mm. and 40 mm. specimens were fixed in 20 per cent formalin. All three embryos were embedded in paraffin, sectioned transversely at 10, 11 and 30 micra, respectively, and stained in hematoxylin and eosin. The original models and the planographic reconstructions were made at magnifications of 22.5 diameters (40 mm. embryo) and 62.2 diameters (14 mm. embryo). The original planographic reconstruction of the 9 mm. embryo was made at a magnification of 156 diameters.

This investigation was carried out in the laboratory of Prof.-Dr. José Escolar

‘Contribution no. 517 from the Department of Anatomy, Northwestern University Medical School. Received for publication, June 1. 1949.

‘From the Department of Anatomy. University of Granada, Spain, and Northwestern University Medical School.

428

at the University of Granada, to whom I wish to express gratitude for many excellent suggestions. The author is also grateful to Dr. John Jacobs and Dr. Alberto Vaz Ferreira of Northwestern University Medical School for their kind assistance in preparing the original manuscript in English and to Professor L. B. Arey, who has recast that manuscript into its present form.

OBSERVATIONS 1. Embryo of 9 mm.

At this stage the reconstruction (fig. 1) shows that the suprarenal glands have not yet appeared, the metanephroi are at the beginning of their development, the mesonephroi are fully developed and the gonads are prominent, elongate folds along the ventromedian surfaces of the mesonephroi. The ganglionated sympathetic cords descend dorsolateral to the aorta, and near the cranial ends of the mesonephroi gradually disappear as such and become continuous with paired juxtaaortic masses. These latter extend caudad ventrolateral to the aorta, and in their more caudal extents interconnect by three bridges ventral to the aorta.

In the sections the juxta-aortic tissue shows as masses that stain deeply with hematoxylin (fig. 4).

2. Embryo of 14 mm.

As the reconstruction (fig. 2) shows, this stage is marked by the increasing prominence of the metanephroi and by the suprarenal glands, which not’ only have appeared since the previous stage but also have grown to relatively large size. The juxta-aortic substance differs from that in the previous stage by being dispersed into 31 discrete masses. These lie both in front of the aorta and on both sides of it; indeed, some that are not shown in figure 2 are even included in the interior of the suprarenals themJIMENEZ-CASTELLANOS~—]UXTA-AORTIC TISSUES 429

fig. '1. Planographic reconstruction of the juxtaaortic masses and the adjacent organs of a human embryo of 9 mm. :3 5.9. (1) metanephroi; (2) mesonephros; (3) gonad; (4) sympathetic cord; (5) juxta-aortic body; (6) post-cardinal vein; (7) coeliac axis; (8) superior mesenteric artery.

fig. 2. Planographic reconstruction of the juxtaaortic masses and the adjacent organs of a human embryo of 14 mm. :c 47. (1) Aorta; (2) coeliac axis; (3) superior mesenteric artery; (4) middle sacral artery; (5) common iliac artery; (6) metanephros; (7) suprarenal gland; (8) mesonephros; (9) gonad; (10) sympathetic cord; (1 1) splanchnic nerve; aortic bodies (of Zuckerlcandl).

fig. 3. Planographic reconstruction of the juxtaaortic masses and the adjacent organs of a human fetus of 40 mm. :13 8.5. (1), (2), Vertebral body and arch; (3) aorta; (4) common iliac artery; (5) renal hilus; (6'), (7'), suprarenal glands; (8) superior mesenteric artery; (9), inferior mesenteric artery; (10), (16), (24), aortic body; (11) middle sacral artery; (12) common iliac vein; (13) inferior vena cava; (14), (17), (20), renal vein; (15), (19) vein from aortic body; (18) left suprarenal vein; (21) splanchnic nerves; (2.?) right vagus nerve; (23) sympathetic cord. 430

selves. In the region located between the suprarenals and between the cranial halves of the metanephroi, there are numerous small masses, the more caudal ones tending to be larger than those at higher levels. Between the caudal halves of the metanephroi there are two masses, much larger than any others in the embryo. These are the forerunners of the aortic bodies of Zuckerkandl. The sympathetic cords continue caudad beyond the region reconstructed. The splanchnic nerves also descend to the level of the juxta—aortic masses and end in association with them; the nerve fibers, however, do not actually enter the cellular masses.

In sections (fig. 5) there is no particular tinctorial difference between the large inter-renal masses and the small masses located between the suprarenal glands. Both stain deeply with hematoxylin. Certain of the small masses can be observed in the process of being incorporated into the interior of the suprarenal glands. This, of course, is a normal initial stage in the development of the suprarenal medulla.

3. Embryo of 40 mm.

The distribution or Juxta-aortic tissue is much as in the previous stage (fig. 3). Mostly lateral to the aorta, and roughly coincident with the extent of the suprarenal glands, are small masses composed of small cells that stain deeply with hematoxylin. In size and stainability, at least, they resemble closely the syrnpathoblasts in the ganglionated sympathetic chains. These latter cells, likewise, are not far along in the course of differentiation into ganglion cells. All of these small juxtaaortic masses that were examined for the purpose were proved to be in intimate relationship with the terminations of fibers from the splanchnic and right vagus nerves. It is possible, under high magnification, to observe the nerve fibers penetrating into the interior of such masses.

There are two large inter-renal masses which represent the future aortic bodies. These are elongate and irregularly lobed; they interconnect, ventral to the aorta, by two prominent bridges of tissue. A similar, smaller mass is displaced down

QUARTERLY BULLETIN, N.U.M.S.

fig. 4.

Photomicrograph through a human embryo of 9 mm. at the level indicated in fig. 1. :1: 59. (1) Aorta; (2) posterior cardinal vein; (3) mesonephros; (4) gonad; (5) liver; (6) juxtaaortic body; (7) body of vertebra.

fig. 5. Photomicrograph through a human embryo of 14 mm. at the lower level indicated in figure 2. 1: 47. (1) Metanephros; (2) juxtaaortic body; (3) sympathetic cord; (4) aorta; (5) mesanephros; (6) body of vertebra.

fig. 6. Photomicrograph through a human fetus of 40 mm. at the middle level indicated in fig. 3. ac 15. (1) Suprarenal gland; (2) aorta; (3) body of vertebra; (4) duodenum; (5) metanephros; (6) crus of diaphragm; (7) sympathetic cord; (8) right splanchnic nerve; (9) masses of sympathoblasts; (10) paraganglia; (11 ) renal vein; (12) inferior vena cava. JIMENEZ-CASTELLANOS—JUXTA—AORTIC TISSUES 431

the middle sacral artery. All three bodies stain more weakly than do the smaller masses at higher levels, already mentioned. Their paler color with hematoxylin is like that observed in the most central part of the suprarenal gland.

Intermediate between the two levels already mentioned is a zone containing small masses that have a double structure (fig. 6). The main material of such a complex consists of the larger, pale type of cell; at the periphery are aggregations of the smaller, dark type of cell.

DISCUSSION

This study sheds no light on the origin of the juxta-aortic tissue since at 9 mm. it is already present as paired, continuous masses. At this period this common substance is not visibly differentiated in its definitive directions: ganglion tissue of the coeliac plexus; suprarenal medulla; and the chromaffin tissue of the aortic paraganglia. This lack of differentiation is in accord with the observations of other investigators and is not only shown by routine methods of staining but also by the application of specific methods for chromaflin tissue and by silver procedures.

The 14 mm. stage likewise fails to provide information concerning divergent differentiation in the common juxtaaortic tissue. It does, nevertheless, illustrate the subdivision of the common primordia into multiple small masses superiorly and two large inter- renal masses (aortic bodies of Zuckerkandl) that lie at a more caudal level. Likewise, the invasion of some smaller masses (future suprarenal medulla) into the cortical primordium has begun.

At 40 mm. some specialization, as indicated by staining differences with hematoxylin, can be detected readily; Zuckerkandl (6) was the first to notice this divergent stainability. The sympathoblasts of the small, cranial masses are larger, paler elements. These are coming into relationship with nerve fibers, all of which are preganglionic elements (Hollins head, 4). The small masses at an intermediate level between the ganglionic primordia and the aortic bodies tend to show representations of both cell types, as do also the later paraganglia.

SUMMARY

Planographic reconstructions have been made of the sympatho-chromaffin tissue in human embryos of 9, 14 and 40 mm. The two older stages were also modelled in wax.

The 9 mm. stage possesses two elongate, interconnecting juxta-aortic masses which consist of small, dark-staining cells.

At 14 mm. the suprarenal glands are beginning to be invaded by some of this tissue which also has subdivided into many small masses cranially and into two large masses located caudally between the metanephroi.

At 40 mm. the differentiation has taken three directions: (1) suprarenal medulla; (2) sympathetic ganglia; (3) paraganglia; (including the aortic bodies of Zuckerkandl). The cells of the future suprarenal medulla and paraganglia are large and stain palely. The small masses, located cranially (between the suprarenal glands), consist of small, dark-staining cells that are becoming similar to the sympathoblasts. In a location intermediate between these two extremes are compound, small masses containing both kinds of cells.

Raferences

1.Kohn, S.: Die Paraganglien, Arch. f. mikrAnat., Bd. 62, S. 263-365, 1903.

2. Zuckerkandl, E.: The Development of the Chromaffin Organs and the Suprarenal Bodies. In Keibel and Mall: Manual of Human Embryology, 2:157-179, 1912.

3.Iwanow, G.: Das Chromafline and Interrenales System des Menschen, Ergeb. d. Anat., Bd. 29, S. 87-280, 1932.

4. Hollinshead, W. H.: Chromaflin Tissues and faigganglia, Quart. Rev. Biol., 152156-171,

5. Wrete, M.: Beitrag zur Kenntnis von der Entwicklung des Chromaffinen Gewebes der Bauchregion beim Menschen, Zeitschr. f. mikr.-anat. Forsch., Bd. 9, S. 79-98, 1927.

6. Zuckerkandl, E.: Ueber Nebensorgane des Sympathicus in Retroperitonealraum des Menschen, Anat. Anz. (Ergéinzrheft), Bd. 19, S. 95107, 1901.


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