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The vascular architecture of the small intestinal mucosa of the monkey (Macaca mulatta).

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The Vascular Architecture of the Small Intestinal
Mucosa of the Monkey (Mcrcaccr mulatta)
DAVID G . REYNOLDS, .TACK BRIM AND THOMAS W. SHEEHY
Drpartment of Gastroenterology, Division of Medicine, Walter Rred Army
Institute of Research, Walter Reed Army Medical Crnter, Washington,
D . C., and Department of Medicine, Walter Reed Generul Hospital,
Walter Keed Army Medical Center, Washington, D. C.
ABSTRACT
Silicone rubber microvascular injection compounds have been used to
describe the mucosal vascular architecture of thc monkey’s small intestine. The
mucosal vascular patterns of this animal differ from the classical description. Instead
of the villus blood supply being delivered via a central villus arteriole, the arterioles
ramify to the undersurface o l the mucosa where they terminate i n the capillary plexus
surrounding the crypts of Lieberkuhn. The villus capillary net is derived directly from
the cryptic capillary plexus and is drained by a single, central villus vein. There is
a secondary venous return system that directly drains the cryptic plexus. These secondary venous channels might represent a mechanism that regulates the proportional
distribution of blood iii the cryptic and villus capillary beds.
This report is intended to describe the vascular patterns only as they occur in the
monkey. Observations of rat and rabbit mucosa prepared by the same technique
reveal arterial and venous channels extending the length of the villi. These animals,
therefore, more closely resemble the classical description.
BIoom and Fawcett’s (’62) description
of the vascular architecture of the intestinal mucosa which we shall call the classical description contains a dual arterial supply. One set of arterioles supplies the
capillary network surrounding the crypts
of Lieberkuhn while the second passes directly to the villi. These latter arterioles
pass axially through the bases of the villi
to the apices where they bifurcate, with
one branch supplying the dense capilIary
network underlying the surface epithelium,
and the other anastomosing with a vein.
Venous return is accomplished through a
pair of marginal villus veins. This concept of villus vasculature stems from
Mall‘s foulztak configuration (1887) and
incorporates Spanner’s (’31) modification
of the apical arteriovenous anastomosis.
There are, however, reports of villus vascular architecture that are inconsistent
with the classical description. Jacobson
and Noer (’52) studied the villus vasculature in rabbit, dog, opossum, and man
concluding that : ( 1 ) The villus capillary
net is derived from both the villus artery
and submucosal plexus; ( 2 ) ‘The axial
vessel i s venous in nature;” and ( 3 )
“Arterial supply and venous drainage exist throughout the villus from tip to base.”
AXAT. REC., 159: 211-218.
The vascular pattern of rat villi as recently
reported by Mohiuddin (’66) is compatible
with the findings of Jacobson and Koer.
Sobin et al. (’62, ’63) introduced and
described a silicone rubber injection medium (RTV-201) ’ that is ideally suited for
microvascular studies in that it thoroughly
fills all vessels, including the smallest
capillary channels. The use of these materials in microvascular studies has been
validated and their physical properties described (Sobin, ’65). In addition, this
material has been used successfully by
other workers in microvascular studies,
Demis and Brim (’65) and IIase (’66).
This material was used in the present
study of elucidate the microcirculatory pattern of the intwtinal mucosa of the monkey. With this technique, the vascular
structure of the jejunal and ileal mucosa
of Macaca mulatta was found to differ
markedly from that of the classical description.
METHODS
The specimens described in this report
were taken from seven animals in which
the entire gastrointestinal tract had been
. .~ 1 Silicone Products Department, General Electric
Company, Waterford, New York.
211
212
DAVID G. REYNOLDS, JACK BRIM AND THOMAS W. SHEEHY
prepared. The principles of laboratory animal care as promulgated by the National
Society for Medical Research were observed.
The animals were anesthetized with
nembutal, and heparinized. In order to
achieve complete filling of all vascular
channels of the gastrointestinal tract, the
visceral vascular bed was perfused
thoroughly with saline prior to infusing the
silicone rubber. Saline perfusion and rubber infusion were carried out through a
polyethylene cannula placed in the thoracic
aorta and advanced distally until its tip extended just below the diaphragm. The
right atrium was opened to serve as a
drain vent. Following saline perfusion, the
silicone rubber injection mass was infused
by hand with a syringe. The infusion was
Fig. 1
continued until, at completion, the rubber
flowed freely from the atrial vent and all
organs were thoroughly filled as evidenced
by their uniform coloration. The arterial
cannula and atrium were then clamped
and the animal refrigerated overnight, during which time the rubber polymerized.
Specimens were then removed and processed through a glycerin clearing procedure. Initially the tissues were placed in
50% glycerin and water for 24 hours. The
glycerin concentration of the mixture was
raised by increments of 10% every 24
hours untiI the solution was composed of
100% glycerin. At this stage, the tissue
water had been replaced by glycerin sufficiently to reduce the optical density of the
tissue appreciably and thus permit 3-dimensional microscopic examination of the
Jejunal Villi as viewed from the lumenal surface. x 40.
213
VASCULAR ARCHITECTURE O F INTESTINAL MUCOSA
vascular beds by using reflected, surface
lighting. The tissues can be stored in
100% glycerin for extended periods.
The recent introduction of silicone rubber compounds of different colors, (Microvascular Injection Compounds) ,2 has made
it possible to prepare %color specimens
and thus facilitate microscopic examination arid interpretation of the vascular
patterns. In three animals, 2-color preparations were made by first completely filling the vascular bed with red RTV-201
material and then ovcrinjecting a small
volume of yellow MV-122 into the arterial
system. The abundant submucosal arteriovenous anastomoses permitted an extensive intermixing of the yellow rubber in
the red. However, the yellow tag allowed us
to identify readily the submucosal vessels
and to make more precise microscopic
identification.
RESULTS
The normal appearance of thc luminal
surface of the monkey’s jejunal mucosa is
shown in figure 1. The compIex and extensive nature of the capillary bed underlying the surface epithelium of the villi can
readily be appreciated from this figure.
The villus capillary bed forms a network
of interconnected vessels in the upper half
of the villus. The lower half of the bed is
composed of vessels that essentially run
parallel to each other and appear to be
continuous with a plexus of capillary channels ramifying between the bases of the
villi. The resulting subnillus plexus characteristically presents a honeycomb pattern and consists of capillary rings surrounding the luminal openings of the
crypts of Lieberkuhn. The subvillus plexus
extends through the cryptic layer of the
mucosa as a rich plexus of capillaries surrounding the crypts themselves.
The 2-color injection procedure was helpful in distinguishing between small mucosal and submucosal arterial and venous
-
~
Canton Bio-Medical Products,
Street, Canton, ~Massachnsetts.
J See footnote 2.
3
1803 Washington
Pig. 2 Jejunal submucosal vascular plexus viewed from the serosal aspect. The serosa
and muscularis have been dissected away. A vein and parallel artery are easily identified.
X 50.
214
DAVID G . REYNOLDS, JACK BRIM AND THOMAS W . SHEEHY
channels (figs. 2, 3, 4 ) . In the specimen
shown in figure 2 , the submucosal vascular plexus has been exposed by dissecting
away the serosa and muscularis. Small
arterial branches ( a ) bifurcate to form
precapillary arteriolar twigs (arrows) that
are distributed to the undersurface of the
mucosa and run uninterruptedly into the
capillary plexus of the mucosal cryptic
layer. Venous channels are also in communication with the cryptic plexus but do
not terminate at this level. Instead, the
terminal branches penetrate the cryptic
layer of the mucosa and a single, centrally
located vein enters the base of each villus
and extends to the apex (arrows in fig. 1).
Details of the vascular architecture of
several villi are shown in figure 3. In this
photograph of a thick section of the intestinal wall, a branch of a large submucosal
vein (v) can be seen entering the cryptic
layer of the mucosa where it is continuous
with venous branches running along the
base of the villi. These latter branches receive the central veins (arrows) from the
villi. It is also clear in this figure that the
Fig. 3
villus capillary net is continuous with the
cryptic plexus. The venous nature of the
central villus vessels is also shown in figure 4. In this thin cross section, the submucosal vasculature is distorted due to &€ficulty in sectioning this thin-walled tissue.
However, the uninterrupted course of the
central villus vessel (arrow) to submucosal
veins (v) remains obvious.
Figure 5 illustrates a specimen in which
the mucosa has been dissected free and
folded back to expose the underlying venous drainage system. The venous channels
are highly branched and characterized by
venovenous anastomoses. In addition,
there are vessels that extend directly from
the under surface of the cryptic plexus to
the larger venous channels (arrows).
These vessels constitute a second avenue
for venous drainage of the mucosa.
The major features of the mucosal vascular architecture of the monkey are consolidated in schematic form in figure 6 .
The arterial supply is distributed to the
undersurface of the mucosa with the
terminal arteriolar twigs running continu-
Thick cross-section of jejunum, 2-3 mm. X 50.
VASCULAR ARCHITECTURE O F I N T E S T I N A L M U C O S A
215
Fig. 4 Thin cross-section of jejunum, 100--150 p. The central vein of the indiyidud
villus is continuous with the mucosal venous system. X 30.
ously into the capillary plexus surrounding the crypts of Lieberkuhn. The capillary nets of the villi are derived directly
from the cryptic plexus via a series of parallel capillary channels that extend from
the lumenal surface of the cryptic plexus
to approximately midlevel of the villi
where they break into a mesh of capillaries. These vessels converge near the
apex of each villus on a single, axially located villus vein. The central vein passes
into the cryptic layer of the mucosa where
it joins other venous channels which lead
to the submucosal venous return system.
In addition, there is an alternative venous
return route in the form of a second set of
venous channels that arise from the cryptic
capillary plexus and cxtend to the venous
channels leading to the submucosa.
DISCUSSION
In the classical description of the mucosal vascular architecture, the arterial
supply to the villi is via a central villus
arteriole while venous drainage is by a
pair of marginal villus veins. The version
presented here differs from the classical on
two major points. Extensive fine dissection and microscopic examination of the
intestinal mucosa has consistently failed
to reveal an arterial route extending directly from the submucosa to the villi.
The submucosal arterial distribution at all
times was observed to terminate in the
cryptic capillary plexus on the undersurface of the mucosa. In like manner, examination of the venous return system at
all times showed jejunal and ileal villi to
possess only a single, centrally located vein.
216
DAVID G .
REYNOLDS,
JACK BRIM AND THOMAS W. SIIEEHY
Fig. 5 Jejunal nimosa dissected Bree along the subniucosal plane axd folded over to
expose mucosal veins ( v ) which are bridged by veiiovcnous an?stomoses. At the bottom of
the figure four mucosal veins join to form a large subinucosal vcnous channel. x 50.
These observations suggest the vascular
architecture of monkey intestinal mucosa
to be closer in pattern to the tuft arrangement reported by Stohr ('01) and Szymonwicz ('02) than to Mall's fountain concept.
Stohr and Szyrnonwiu describe the villus
artery as giving rise to a tuft of capillaries
at the base of each villus which, in turn,
converge at the apex on an efferent vein.
The mucosal vascular pattern presented
here is intended only to describe the intestinal mucosa of the monkey. Sobin
('66) has shown that the circulatory patterns of individual organs or systems often
differ between species. This observation
is valid for the intestinal mucosa in that
the circulatory patterns of the villi of the
rat and rabbit, as well as gross villus morphology, differ markedly from that seen
in the monkey. Instead of the cylindrical,
finger-like shape of monkey villi, rat villi
are broad, leaf-like structures and those in
the rabbit vary from pyramidal structures
in the upper intestine to slender, long,
blade-like structures in the lower intestine.
The vascular patterns of rat and rabbit
villi resemble the classical version in that
they possess both arterial and venous channels. Eat intestine. prepared in the manner
described here, presents a picture that
precisely supports Mohiuddin's description
('66). One or two arterial channels pass
paraxially to the tip of each villus where
one forms a large marginal capillary. The
villus capillary network originates from
this vessel and is drained through a large
central vein. The width of rat and rabbit
villi is quite variable within the different
levels of the intestine. The broader structures commonly possess multiple arterial
and venous channels. In addition, neither
the cryptic layer is as thick nor the plexus
as dense in the rat and rabbit a s they are
in the monkey.
Regional diffcrcnccs also exist within the
monkey small intestinal mucosa. The description presented here is applicable only
to jejunal and ileal mucosa. Duodenal villi
VASCULAR ARCHITECTURS O F INTESTINAL MUCOSA
217
Fig. 6 Schematic of mucosal vascular architecture. A. Suhmucosal artcry; €3. cryptic
capillary plexus; C . villus capillary net; D. central villus vein; E. secondary veins.
of the monkey are broader than those from
more distant areas of the small intestine
and are often invested with two, and
occasionally three, venous channels. In
addition, the capillary nct of duodenal
villi is of finer mesh than that of the lower
regions. One subtle difference was observed
between jejunal and ileal mucosae. The
thickness and complexity of the cryptic
plexus was greater in the jejunum than it
was in the ileum.
Fine dissection of the 2-color specimens
often revealed a few channels of capillary
nature that passed through the cryptic
plexus with relatively few anastomoses.
These vessels could often be followed
directly into the villus capillary network
as figure 3 demonstrates. Several lighter
colored capillary channels can be seen to
pass directly through the cryptic plexus
and into the villus. This observation, plus
the existance of the secondary venous return vessels, suggests the possibility of a
regulatory mechanism that controls the
distribution of blood in the mucosae. Such
a mechanism would operate most efficiently in this system if the site of its
action were at the secondary venous channels. If the secondary venous system were
subjected to a constrictor influence, either
neural or humornl in origin, the resistance
to venous drainage of the mucosa would
218
DAVID G . REYNOLDS, JACK BRIM AND THOMAS W. SHEEHY
increase. If this venous constriction were
to occur without a reduction of arterial
volume rate of flow, a balanced mucuosal
flow could only be maintained if the volume of flow were to increase into the villus
capillary nets. The overall result would
be a passive shunting of blood into the
villus capillary bed and ultimately an increase in venous return through the central
villus vein. On the other hand, dilatation
of the secondary veins would result in a
drop in resistance through those channels
and the bulk of the blood would be diverted
through the cryptic plexus.
A mechanism such as this might produce a separation of mucosal blood flow
under different functional conditions.
During active digestion and absorption,
constriction of the secondary venous system would effectively increase blood flow
through the villus capillaries. In a postabsorptive condition, the drop in resistance
accompanying dilatation of these vessels
would rcduce flow through the v d u s net
by shunting it to the cryptic plexus.
ACKNOWLEDGMENTS
The authors would like to thank Lt.
Jay H. Karsch for drawing the schematic
diagram used in this report, Mr. John E.
McClain for his microscopic photography
and Mr. Dennis Townsend for technical
assistance.
LITERATURE CITED
Bloom, W., and D. W. Fawcett 1962 Histology.
W. B. Saunders, Philadelphia, pp. 454-456.
Dcmis, D. J., and J. Brim 1965 A method of
preparing thrce dimensional casts of the microcirculation of the skin. J. Invest. Derm., 45:
324-328.
Hase, T. 1966 Heptaic microcirculatory changes
i n acute and chronic carbon tetrachloride
poisoning i n rats. Amer. J. Path., 49: 10691086.
Jacobson, L. F., and R. J. Noer 1952 The vascular pattern of the intestinal villi i n various
laboratory animals and man. Anat. Rcc., 114.
85-93.
Mall, F. P. 1887 Die blut und lymphwege im
dunndarm des hundes. Abh. d. Mat-phys. el.
d. Kijnig. sachs. Gesell. d. Wiss., 1 4 : 153-200.
Mohiuddin, A. 1966 Blood and lymph vessels
in the jejunal villi of the white rat. Anat. Rec.,
356: 83-90.
Sobin, S. S., W. G . Frasher Jr. and H. M. Tremer
1962 Vasa vasorum of the pulmonary artery
of the rabbit. Circ. Res., 11: 257-263.
Sobin, S. S., W. G. Frasher Jr., H. M. Trcmer
and G . G . Hadley 1963 The microcirculation
of the tracheal mucosa. Angiology, 14: 165170.
Sobin. S. S. 1965 Vascular inicction methods.
1n:’Meth. in Mcd. Rcs., edited by R. F. Rushmer, 11: 233-238.
Sobin, S. S., and H. M. Tremer 1966 Functional geometry of the microcirculation. Fed.
Proc., 25: 1741-1752.
Spanncr, R. 1932 Neue hefunde uber die
hlutwege der darmwand und ihre functionelle
bedeutung. Morph. Jahrb., 69: 394-454.
Stohr, P. 1901 Textbook of Histology. Translated by E 1,. Rilstein, Blakiston, Philadelphia,
pp. 245-246.
Szymonwicz, L. 1902 Textbook and Microscopic Anatomy of the Human Body. J. B.
MacCallum, ed. Lea Brothers, Philadelphia.
p. 191.
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