Rom J Leg Med [24] 71-77 [2016]
DOI: 10.4323/rjlm.2016.71
© 2016 Romanian Society of Legal Medicine Morphologic synergisms in the ortotaxy and heterotaxy of the subdiaphragmatic
digestive system viscera. Consequences in pathology and forensic medicine
Gheorghe S. Dragoi1,2,*, Ileana Marinescu3, Ileana Dinca4, Elena Patrascu4, Petru Razvan Melinte4
_________________________________________________________________________________________
Abstract: Spatial location of the subdiaphragmatic digestive system viscera fascinates through the manner in which
the 9-10 meters of tubular structures (gastroduodenal= approximate 50 cm; jejunal-ileal= approximate 7-8 meters; colorectal=
approximate 1.5 meters) wreathe together within the relatively narrow space of abdominal cavity. Authors proposed themselves
to perform an anatomic study regarding determinant factors of the combinatorial occupancy of abdominal-pelvic space by these
viscera, during the dynamic of their epigenesis. The study was conducted on human biologic material: 8 embryos aged between
6-8 weeks and 15 fetuses, aged between 12-28 weeks. Analysis of relations between digestive system primordia and mesenteric
mesenchyme derivates was achieved through macro- and microanatomic methods. Authors consider that the assessment of
ortotaxy and heterotaxy of subdiaphragmatic digestive system viscera, as effects of intestinal rotation and malrotation created
multiples confusions. The results of our observations, correlated with anatomic literature data, demonstrate that the location of
viscera from peritoneal cavity is determined by morphologic synergisms synchronization between ectoblastic and mesenteric
mesenchyme derivates. Intestinal rotations described by Fredet (1898), for the achievement of subdiaphragmatic digestive system
viscera ortotaxy and heterotaxy appear as effects of tubular digestive structures growth and elongation and not as causes of
these phenomenon. The asynchrony of morphologic synergisms generates heterotaxy, atresia, stenosis and abnormal peritoneal
recesses which may become sites for congenital internal hernias, highly important in surgical pathology and forensic examination
of peritoneal cavity.
Key Words: visceral ortotaxy, digestive system primordia, congenital internal hernia, intestinal rotation.
T
he issue of subdiaphragmatic digestive
system viscera location, in time and space,
determined the occurrence, in knowledge history, of
various researches and controversies, regarding relations
and reciprocal interactions between endoderm-derivate
and mesoderm-derivate structures, during their
morphologic differentiation dynamics. The assessment
of these variable relations represents a study hypothesis,
within the contradictions paradigm existing between
surgeons, anatomists and embryologists, regarding
the determinant factors of antepartum ortotaxy of
intraperitoneal and/or secondary retroperitoneal viscera.
The purpose of this paper is to analyze the anatomic
determinant factors for the abdominal location of
subdiaphragmatic digestive system viscera, in embryo
and fetus. The objectives of the study were imposed by
numerous theoretical and practical issues regarding the
epigenesis of subdiaphragmatic digestive system viscera. We mention:
1) The so-called “rotations of ansa umbilicalis”,
invoked by Fredet (1901) [1], during epigenesis of
subdiaphragmatic digestive system viscera may represent
1) Romanian Academy of Medical Sciences, Bucharest, Romania
2) University of Medicine and Pharmacy of Craiova, Doctoral School, Craiova, Romania
* Corresponding author: MD, PhD, Email: [email protected]
3) University of Medicine and Pharmacy of Craiova, 5th Department, Craiova, Romania
4) University of medicine and Pharmacy of Craiova, Department of anatomy, Craiova, Romania
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Dragoi G.S. et al.
Morphologic synergisms in the ortotaxy and heterotaxy of the subdiaphragmatic digestive system viscera
causes or effects of biostatics and biocinematics of
digestive system primordia? 2) In which way does the
abdominal cavity volume influence the biodinamics of
these primordia evolution? 3) Which are the anatomic
factors that allow the occurrence of intestinal ansa hernia,
their return into peritoneal cavity and their fixation onto
the posterior wall of abdominal cavity, in adult ortotaxy?
4) Which is the contention value of common dorsal meso
in the morphogenesis dynamics of subdiaphragmatic
digestive system? 5) Which are “the growth factors” for
the elongation of subdiaphragmatic digestive system
viscera primordia? 6) Which is the contribution of
vascular mesenchyme in angiogenesis, formation and
differentiation of subdiaphragmatic digestive system
viscera?
MATERIALS AND METHODS
The study was conducted on human biologic
material: 8 embryos aged between 6 and 8 weeks, 6
fetuses aged between 12 and 16 weeks and 9 fetuses
aged between 20 and 28 weeks. Embryos were fixed in
6% formaldehyde solution, at pH=7.4. After paraffin
inclusion of embryos, seriate sections were performed, in
transversal (4 embryos), sagittal (2 embryos), and frontal
(2 embryos) planes. Examination of seriate sections
stained with Hematoxylin-Eosin was performed with the
help of Nikon Eclipse 80i microscope, in order to assess
the relations between digestive system primordia and
mesenterial mesenchyme.
Fetuses were fixed in 10% formaldehyde
solution, at pH=7.4, by catheterization of umbilical vein.
Fetuses’ dissection included, after exposing abdominal
and peritoneal cavities, the visualization and analysis of
relations between medium intestine primordia derivates
and afferent mesos.
Microphotographs were taken with Nikon
Sight DS-Fi1 Hight Definition Color Camera Head
and processed by Software NIS-Elements Advanced
Research. Macrophotographs were taken with Canon
EOS-1ds Mark II Digital Camera with Macro Ultrasonic
Lens, 100mm, f/2,8.
RESULTS
A. Microanatomic analysis of relations between
subdiaphragmatic digestive system primordia and
mezenterial mesenchyme, in embryo
From the analysis of transversal seriate sections
through 7 and 8 weeks embryos, it was easily noticed the
presence of small intestine secondary loops, herniated
through umbilical ring (Anulus umbilicalis) (Fig. 1 A-D).
Common mesenteric pedicle (Truncus mesentericus
communis) is formed by the fusion of ansa umbilicalis
meso (common mesentery) to the duodenal meso.
After this merging, common mesentery divides into a
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superior portion, where the colon is attached and will
become mesocolon and an inferior portion, where the
small intestine is attached and will become the definitive
mesentery (mesojejunum and mesoileum) (Fig. 1C).
Intestinal loops, on seriate sections, have the shape of U, V
or A letters, their branches being reinforced by jejunoileal
mesentery (Fig. 1 B, C, D). Examination of supraumbilical
seriate sections reveals glandular derivates of duodenal
ansa: liver and pancreas, establishing contiguity relations
between them (Fig. 1A). Dorsal mesogastrum is
longitudinally sectioned and contains glandular elements
of pancreas and lymphoid spleen structures; between
them, relations are established through gastro-pancreatic
and pancreatic-spleen folds (Fig. 1B). Ventrally to these
structures, retrogastric space of omental bursa is visible
(Fig. 1 A, B); dorsally, relations of dorsal mesogastrum
derivates with suprarenal gland and genital crest are
easily identifiable (Fig. 1 A, B). Ventrally, gastric-spleen
fold becomes visible. The examination of infraumbilical
seriate sections allowed the visualization of mesonephros,
metanephros, terminal intestine (hindgut), connected to
the dorsal wall of celomic cavity through common dorsal
mesentery (mesocolon) (Fig. 1D).
B. Macroanatomic analysis of relations between
digestive system primordia derivates and mesenterial
mesenchyme in human fetus
Macroscopic examination of 10 weeks fetus’s
frontal and lateral parts of anterior abdominal wall,
allowed visualization of secondary intestinal ansa,
herniated through anulus umbilicalis (Fig. 2 A-C). It is
easily noticeable the spiral trajectory of intestinal ansa
(Fig. 2D). In 16 weeks fetus, after exposing abdominal
and peritoneal cavities, we identified, within the superior
level, a clew of tertiary jejunal-ileal intestinal loops,
which continues, caudally, with the primordial colon
(Fig. 2F). Intestinal ansa trajectory is determined by
helicoids spatial orientation of jejunal-ileal meso, the
loops describing curves with great curvatures, giving the
impression of merging during macroscopic examination
of these intestinal loops clew (Fig. 2 E, F, H). Primordial
colon is visible near the median plane, continuing
directly the jejunal-ileal loops clew, describing, within
its first portion, three curvatures, in a spiral trajectory
(Fig. 2 F, G). Jejunal-ileal loops clew tilting to the right
of medial-sagittal plane allows the visualization of two
major junctions: gastro-duodenal and duodenal-jejunal
(Fig. 2H). Examination of peritoneal cavity in 4 and 6
months old fetuses, allowed the visualization, within
supramesocolic space, of stomach and duodenum, till
the superior half of the descendent portion, and, within
inframesocolic space, the jejunal-ileal intestinal loops,
covered by greater omentum, attached by the greater
curvature of stomach and which, in its pathway, covers
the transverse colon (Fig. 2I). Jejunal-ileal loops have
a spiral trajectory and appear as suspended by the
Romanian Journal of Legal Medicine Vol. XXIV, No 1(2016)
Figure 1. Relations of primordia systematis digestorii to the derivates from mesenteria primordialia during the epigenesis of
subdiaphragmatic organs in human embryo. 1. Crista gonadalis; 2. Glandula suprarenalis; 3. Pars mesenteronica duodeni; 4.
Mesenterium dorsale primordiale – mesogastrium dorsale; 5. Pancreas ventrale; 6. Pancreas dorsale; 7. Pancreaticosplenic fold; 8.
Spleen; 9. Bursa omentalis; 10. Gastrosplenic fold; 11. Gaster; 12. Hepar; 13. Secondary intestinal loops herniated through anulus
umbilicalis; 14. Metanephros; 15. Pars mesenteronica coli primordialis; 16. Mesenterium dorsale commune; 17. Pancreaticocolic
fold; 18. Anulus umbilicalis; 19. Gastropancreatic fold; 20. Mesonephros; 21. Pars metenteronica coli primordialis; 22.
Mesenterium dorsale commune – mesocolon. Serried sections throug parrafin embedded specimens. Hematoxyline Eosine Stain.
Microphotographs taken with Nikon Sight DS-Fi1 Hight Definition Color Camera Head x 28.
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Dragoi G.S. et al.
Morphologic synergisms in the ortotaxy and heterotaxy of the subdiaphragmatic digestive system viscera
Figure 2. Relations of midgut loop (Ansa umbilicalis intestini) to the derivates of vascular mesenchyme and mesentery in human
fetus. 1. Hepar; 2. Hernia umbilicalis physiologica; 3. Tertiaty jejunum-ileal loops; 4. Pars mesenteronica coli primordialis; 5. Pars
metenteronica coli primordialis; 6. Gaster; 7. Pars praeenteronica duodeni; 8. Tertiary jejunal loops; 9. Pars mesenteronica coli
transversi; 10. Omentum majus; 11. Colon ascendens; 12. Colon descendens; 13. Nodi mesenterici superiores; 14. Mesoileum;
15. Ileum – pars terminalis; 16. Ileocecal jonction; 17. Caecum; 18. Apendix vermiformis; 19. Spleen; 20. Mesentery for transverse
colon; 21. Meso for descending colon containing branches of inferior mesenteric artery; 22. Colon sigmoideum; 23. Rectum; 24.
Pancreas.Macrophotographs taken with Canon EOS 1 ds Mark II Digital Camera. Macro Ultra Lens 100 mm, f/2,8.
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Romanian Journal of Legal Medicine Vol. XXIV, No 1(2016)
Diagram 1. International embryological terminology for the primordium of digestive system (Primordia systematis digestorii).
(Federative International Programme on Anatomical Terminologies, 2013).
mesentery, which present subperitoneal, lymphaticnodular conglomerates (Fig. 2 J, K). At the level of ilealcaecal junction, it is easily highlighted the ileal-caecal
meso, containg branches of superior mesenteric artery
(Fig. 2L). Caecum and ascendant colon are attached
to the posterior wall of abdominal cavity (Fig. 2L).
Examination of transverse mesocolon, after cranial tilting
of transverse colon, allowed the visualization, within the
meso thickness, of an arterial vascular network, formed
by inferior and superior mesenteric arteries branches
(Fig. 2M). Spatial distribution of inferior mesenteric
artery branches was visible after the excavation of left
mesenteric-celiac space. Sigmoid colon is easy to mobilize
through its meso (Fig. 2N).
DISCUSSION
Morphogenesis of subdiaphragmatic digestive
system viscera is multifactor dependent and yet widely
debated by anatomists, embryologists, surgeons and
pediatric doctors. Viscera primordia belong to those three
parts derivated from vitelin sack: foregut (Praenteroni),
midgut (Mesenteron) and hindgut (Metenteron).
Epigenesis of medium intestine led to intense researches
and controversies.
Two particular features were nominated within
midgut (mesenteron) evolution: hernia and rotation
of intestinal loops (Meckel 1817 [2]; Mall 1898 [3];
Fredet 1901 [1]). Intestinal organogenesis in the first
development weeks of embryo is presented in classical
works by the scheme of the surgeon Fredet (1901)[1], in
the work of human anatomy of Poirier-Charpi (1901)[1].
It is known as “intestinal rotation”.
The assessment of ortotaxy and heterotaxy of
subdiaphragmatic digestive system viscera, as effects
of intestinal rotation or malrotation, created many
confusions. Frazer and Robbins (1915)[5] remarked
that small intestine development occurs between two
landmarks of ansa umbilicalis: a proximal one, at the level
of duodenal-jejunal junction and another one, distally,
at the level of umbilical ansa colic angle. Later, Snyder
and Chaffin (1954)[6] considered that these landmarks
are more likely growth and differentiation areas of ansa
umbilicalis derivates.
Soffer et al. (2015)[7], resuming the idea of
Meckel (1817)[2], demonstrated that rapid longitudinal
growth process of midgut coincides with the one of
mesentery. Intestinal rotation process is classically
divided into three stages (Frazer and Robbins, 1915)[5]:
1) Temporal, physiologic, extracelomic hernia of intestine
through anulus umbilicalis; 2) Intracelomic return of the
herniated intestine and 3) Intestinal portions attachment
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Dragoi G.S. et al.
Morphologic synergisms in the ortotaxy and heterotaxy of the subdiaphragmatic digestive system viscera
to the abdominal posterior wall through mesentery, into
the adult position. During these stages, ansa umbilicalis
would suffer rotations up to 270 degress (Fredet, 1901)
[1].
There are, still, contradictory data regarding major
events synchronization: time of physiological umbilical
hernia onset (Frazer and Robbins,1915[5]; Estrada, 1958)
[8] Skandalakis and Eray, 1994[9]), hernia reduction
speed (Mall, 1898[3]; Snyder and Chaffin, 1952[6] Cyr et
al. 1986[10]); caecum location immediately after hernia
reduction (Frazer and Robbins, 1915[5]; Dott, 1923[11]);
Snyder and Chaffin, 1954; Fitzgerald et al. 1971[12]) and
not least, the temporal duration of rotation (Frazer and
Robbins, 1915[5]; Estrada, 1958[8]).
Repciuc (1964[13], 1971[14]), anatomist and
embryologist, observed that in the intervals between
ansa umbilicalis rotations, the intestine still grows and
folds, and thus, shadows the successive rotations effects.
Already in 1920 and 1926, Pernkopf [15;16], anatomist
and embryologist, noticed the inconsistence of a certain
part of Fredet’s rotations description (1901)[1]. It is
considered that, after umbilical ansa rotation, colon is
situated above and the small intestine, below. The root of
common meso is located inside “duodenal horseshoes”, so
that mesocolon is situated upper and the mesentery lower,
continuing to the right through common meso root,
being parallel and inside duodenal ansa. This situation
is impossible to explain by Fredet’s proposed rotation
theory. This fact led to a new series of researches. Repciuc
et al. (1964, 1971)[13, 14] contributed to the discrediting
of rotation theory, demonstrating that reality is different.
First, authors observed that digestive tract,
mostly ansa umbilicalis, were not located in the medialsagittal plane. Descendent portion is deviated to the right,
meanwhile, the ascendant part is situated in an almost
perfect transversal (horizontal) plane, directed from right
to left, crossing medial-sagittal plane and returning again
to the right till the median line, from where it continues
with terminal intestine, which descends vertically down.
Neither the following stage of development involves
rotations. Ansa umbilicalis meso, with the shape of a cone,
sectioned after its generator, is opened to the right and
merges with duodenal meso (mesoduodenum) which,
in this development stage, is almost horizontal. Still,
mesoduodenum already contains pancreas sketch and
has, consequently, a considerable thickness (Fig. 1B).
When common mesentery (ansa umbilicalis meso) merges
with mesoduodenum, they constitute an assembly which
Pernkopf (1922)[15] nominated as “common mesenteric
pedicle” (Truncus mesentericus communis).
After merging, common mesentery divides
into two mesos: a superior one, where colon is attached
(mesocolon) and an inferior one, where small intestine is
suspended (mesoenter) (Fig. 1C). Because the two mesos
derivate from common mesentery, they must continue
one to each other. If we take into account the geometrical
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shape of common mesentery, then the continuity line is
located to the right. Authors mention that mesocolon
remains short, while mesentery elongates considerably,
mostly because intestinal ansa grow vigorously and leave
the abdominal cavity through umbilical ring (Anulus
Umbilicalis), achieving the physiological umbilical
hernia. In this development stage, mesos remain for a
long period of time inside “duodenal horseshoe”.
During the last development stage, small intestine
mesentery merges with abdominal cavity posterior wall,
in the same time with mesoduodenum. In this manner,
the coalescence fascias apear: Treitz fascia, behind
mesoduodenum and Told fascia, behind mesentery. Still,
mesentery coalescence is only partial. It occupies the
triangular area situated between transverse colon meso,
ascendant colon and an oblique line that units duodenaljejunum flexure with the point where ileum makes the
junction with ascendant colon. To the left of this line,
called also tertiary mesentery root (Radix mesenterii),
the free, unattached mesentery portion is found.
Common mesenteric pedicle merges through
its right face (mainly superior in certain development
stages) to the trunk’s posterior wall and through its left
face (mainly inferior in certain development stages) to
the common mesentery (namely to the ansa umbilicalis
meso). So, we understand that common mesenteric
pedicle is a veritable structural plate in abdominal viscera
evolution.
Equally, the theory of stomach rotations was
discredited by researches of Meffert (1970; 2000)[17;18].
She demonstrated that stomach modifies its shape, but
does not pivot in its axis; the greater epiplon (Omentum
majus) is just a mesenchyme proliferation in the region
of stomach’s greater curvature and does not have any
connection with dorsal mesogastrum. All the beautiful
theories regarding the six layers of dorsal mesogastrum,
which the student must learn, in a shameful way, are
legends (Repciuc, 1971)[14].
The results of our observations, correlated with
anatomic literature data, demonstrate that ortotaxy of
subdiaphragmatic digestive system viscera is determined
by morphogenesis synergisms synchronism between
ectoblastic and mesenteric mesenchyme derivates.
Asynchronies of reciprocal interactions between digestive
system and mesenteric mesenchyme primordials generate,
on one side, heterotaxy, atresia and stenosis and on the
other side, through peritoneal relations, the formation
of abnormal peritoneal recesses. It is known the fact that
peritoneum achieves, frequently, in duodenal, caecal and
sigmoid portions, semilunar folds, under which, more or
less deeper depressions are found, nominated as recesses
(synonym with fossette in French Nomina). In pathology,
these recesses may become sites for hernia (congenital
internal): paraduodenal, pericaecal and intersigmoid,
widely explored in peritoneal cavity forensic examination.
It is regrettably the fact that International Embryology
Romanian Journal of Legal Medicine Terminology (2013) [2013] includes within the
group of small intestine malformations also the
malrotations, although the absence of rotations during
subdiaphragmatic digestive system viscera morphogenesis
was demonstrated. Moreover, types of malrotations are
nominated: incomplete rotations, hyperrotations, nonrotations and reverse rotations.
CONCLUSIONS
1. Ortotaxy of subdiaphragmatic digestive
system viscera is determined by synergic and synchronic
interactions, in time and space, between ectoblastic and
mesenteric mesenchyme derivates.
2. Morphologic differentiation synchronism
Vol. XXIV, No 1(2016)
of digestive system primordia, offers anatomic
arguments against rotation and malrotation concepts,
in order to explain the location and spatial relations
of subdiaphragmatic digestive system in normal and
pathological conditions.
3. Umbilical ansa rapid growth and fold shadow
the effects of its successive rotations.
4. Common mesenteric pedicle, through its
location inside “duodenal horseshoes” represents
a veritable structural plate in the evolution of
subdiaphragmatic digestive system viscera.
5. Peritoneal recesses within duodenal, caecal
and sigmoid regions become elective sites for congenital
internal hernias.
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