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Morphological Study on Microvasculature of Left Ventricular Wall in Infant and Adult Yaks.

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THE ANATOMICAL RECORD 293:1519–1526 (2010)
Morphological Study on
Microvasculature of Left Ventricular
Wall in Infant and Adult Yaks
Y.Y. HE,1 S.J. YU,2 Y. CUI,2* AND P. DU2
Instrumental Research and Analysis Center, Gansu Agricultural
University, Gansu, China
2
College of Veterinary Medicine, Gansu Agricultural University, Gansu, China
1
ABSTRACT
Observations on the microvasculature in the left ventricular wall of
infant and adult yaks under light and scanning electron microscope (SEM)
were presented. Moreover, the diameter of different microvasculature and
the density of the capillaries in three layers of the ventricular myocardium
were measured using Image Pro-Plus 5.0. The results showed that the average luminal diameter of arterioles and precapillary arterioles in adult
yak’s hearts were, in most cases, larger than those in infant yaks. On the
contrary, the diameters of the capillary in infant yak’s hearts were larger
than those in adult yaks. The density of capillary in the myocardium of
adult yak’s heart had significantly higher values (P<0.01) than those in
infant yaks. Arterioles of yak’s hearts were characterized by the bark-like
structure and the impressions of endothelial cell nuclei, and it always gave
rise to capillary after three to four grades of embranchment. The outer surface of capillaries cast in infant yak’s hearts was smooth, and no constrictions were found. This was different from adult yak that always had some
constrictions. The capillary anastomosis of ‘‘H’’ and ‘‘Y’’ usually existed in
the myocardium of both adult and infant yaks; however, those in infant
yaks were not typical as in adult yaks in their shape. The peculiar arrangement of the venules in infant yak was a ‘‘baggy’’ or ‘‘bulgy’’ arrangement,
while in the adult yak, they had a root-like pattern. Our findings suggest
that the patterns of microvasculature in yak’s heart could be propitious to
adapt better in their environment following their increase of age. Anat
C 2010 Wiley-Liss, Inc.
Rec, 293:1519–1526, 2010. V
Key words: yak; left ventricle; microvasculature; diameter;
density
In previous studies, the characteristics of microvasculature in many kinds of domestic mammals have been
demonstrated (Bayer et al., 2002; Grabherr et al., 2008).
Some used microangiography (Speck, 2003; Djonov and
Makanya, 2005; Suo et al., 2007), and some used the
method of vascular corrosion casting (Krucker et al.,
2006; Lametschwandtner et al., 2006). As Meyer et al.
(2008) said, the combination of scanning electron microscope (SEM) and vascular corrosion casting is a powerful
and best method for studying vascular morphology and
architecture. Although there is a long-lasting interest in
the microvasculature of heart, the fine distribution and
the three-dimensional arrangement of the entire microvasculature bed of heart still remain to be elucidated in
C 2010 WILEY-LISS, INC.
V
more detail. What is more, there are no studies done
where the heart’s microvasculature of the infant yak is
compared with that of the adult animal.
Grant sponsor: Nature Science Foundation of China; Grant
number: 30960270.
*Correspondence to: Y. Cui, College of Veterinary Medicine,
Gansu Agricultural University, Lanzhou, Gansu 730070, China.
E-mail: cuiyan369@sina.com
Received 13 October 2008; Accepted 30 March 2010
DOI 10.1002/ar.21201
Published online 24 July 2010 in Wiley Online Library
(wileyonlinelibrary.com).
1520
HE ET AL.
Yak is one of the most important breed living in high
mountain grassland at an extreme cool temperature and
low oxygen content. Therefore, yak’s heart must have
the stronger function to fit the special environment. As
in high altitude, the amount of oxygen available for animals decreases and the number of red blood cells tends
to increase making the blood more viscous. It would be
interesting to know whether the heart of yak that has to
pump blood against a then increased resistance copes
with this situation by adaption of the microvasculature
of its muscular layers to keep the energy costs for its
perfusion low. The present study was undertaken to
observe the microvascular in ventricular wall of infant
and adult yaks. Although it is reasonable to suppose
that the basic pattern is likely to be similar in infant
and adult yak’s hearts, there must have a maturation of
the microvasculature bed from juvenile to the adult in
terms of the diameter, arrangement, and configuration
of the microvasculature and the density of capillary.
Otherwise, there are certain important age differences
that must be appreciated before the results of any experimental work can be evaluated. Such information would
also be useful in exploring the relationship between
heart microvasculature and ambient oxygen partial
pressure.
MATERIALS AND METHODS
Yak
Twelve yaks of infant and adult ages were included in
the investigation. They were purchased from small holders in Datong County of Qinghai Province. Infant yaks
varied from 120 to 180 days of age and 30–50 kg of
weight, and those of adult yaks were 5–8 years and 100–
200 kg, respectively. No apparent diseases were found
before they were sampled.
Sampling
Yaks were exsanguinated, and the vascular system
was injected via coronary artery. In some cases, perfusions of glutaraldehyde were made initially, followed by
injection of the solution of ABS in butanone to make
microcorrosion casts, and the solution of formalin (40%,
p.A.) blended with black Chinese ink (vþv ¼ 1þ6) to
make tissue sections, either under controlled pressure
(150–200 mmHg) or hand pressure. We used three kinds
of concentration of ABS solution (5% ABS in butanone,
10% ABS in butanone, 15% ABS in butanone) when we
injected the heart of yak via both right and left coronary
artery at the same time. At the first stage of injection,
we used 5% ABS, then 10% ABS, and last, 15% ABS.
The heart that was injected with three kinds of concentration of ABS solution was kept in cold water for about
48–72 hr for complete fixation, frozen fast and then the
specimen was cut to 1 cm3 with a razor blade in epicardium, myocardium, and endocardium of left ventricular
wall from anterior, posterior, and apex, respectively.
These small specimens were placed in a solution of 30%
HCl to remove the soft tissue. The specimens remained
in this solution for a period of 3–6 days and were then
flushed with tap water to remove the residue from the
cast. For a final cleaning and removal of the residue,
specimens were placed in an ultrasonic cleaner for 3
min. After complete tissue corrosion and cleaning, the
casts were frozen in water, cut with a razor blade, air
dried, coated with gold, and observed in an SEM.
The heart injected with formaldehyde in black Chinese
ink via both the right and left coronary artery, at the
same time, was immersed in 5% neutral aqueous formalin for 72 hr for further fixation, then sampled, dehydrated by an ascending series of alcohol, and embedded
in paraffin wax. The tissue sections were cut from
sampled blocks at 20 and 40 lm in thickness. The microvasculature was apparent when the entire microvasculature was completely injected with the solution of
formaldehyde in black Chinese Ink.
Measurements
For quantification of the diameter of the microvasculature, the stereopaired images were taken with SEM
(Hitachi S-3400N) and were measured with its incidential software at an accelerating voltage of 20 kV and
magnifications ranging from 75 to 1,500 times. For
quantification of the density of capillary, the images of
transverse tissue sections of the epicardium, myocardium, and endocardium, to whom the solution of formaldehyde in carbon black ink were injected, were taken
with the Olympus DP-controller 70. Five different areas
(two anterior, two posterior, and one apex) in each steps
of left ventricular wall from anterior, posterior, and apex
were selected. In each area, 20 photos with the magnification of 100 times were taken. Finally, the number of
capillary in each photos were counted with the Imageproplus 5.0. Data were subjected to one-way analysis of
variance (ANOVA) between steps (endocardium, myocardium, enpicardium) and ages (adult and infant).
RESULTS
The Diameter and Characteristic of Arteriole
The arterioles of adult yak’s hearts were characterized
by the bark-like structure and impressions of endothelial
cell nuclei (Fig. 1A). At this level, it was found that a
single layer of plastic ‘‘strips’’ was wrapped around the
outer surface of the cast (Fig. 1B). With the decrease of
diameter, the number of circular strips became fewer,
and in some cases, they were observed as partially torn
away from the cast. Arterioles decreased in size by
branching in a dichotomous or pectinate manner to form
capillaries, with always two daughter vessels of equal
sizes. In general, the terminal arteriole divided into two
daughter capillaries, and these capillaries could pursue
the same direction but often ran in opposite directions
(Fig. 1C). Arterioles frequently had a distinctive and
characteristic arrangement, which might be described
variously as helical, bellows-like or undulating (Fig.
1D,E). In most cases, the earlier features were similar in
an infant yak’s heart. The average luminal diameter of
the arterioles in infant and adult yak’s hearts were
73.50 8.64 and 78.50 9.72 lm, respectively, with the
ranges of 11.53–100 lm and 12.5–100 lm, respectively.
The arterioles of yak’s hearts gave rise to capillary after
three to four grades of embranchments (Fig. 1F). The average luminal diameter of the different grades of
embranchment from the first to fourth in the infant
yaks were 85.66 4.53, 63.69 6.21, 44.38 5.90, and
35.45 6.17 lm, respectively; and those in the adults
were 87.64 4.87, 69.46 6.67, 48.52 5.77, and
MICROVASCULATURE OF LEFT VENTRICULAR WALL IN YAK
1521
Fig. 1. The arterioles of heart in infant and adult yaks. A: The barklike structure (quadrate-boxed area) and impressions of endothelial
cell nuclei (circular boxed area). The asterisk marks a transversely cut
vessels. B: Single layer of ‘‘plastic strip’’ wrapped around the surface
of the cast (asterisk). C: Arterioles decreased in size by branching in a
dichotomous or pectinate manner to form capillaries. A, arteriole; C,
capillary. D,E: Arterioles were described variously as helical, bellow-
like, or undulating under both light and scanning electron microscope
(arrow). Boxed areas mark blind ending vessels with rounded endings.
F: The arterioles of yak’s hearts common give rise to capillary after
three to four grades of embranchment. A, arteriole; A1,2,3,4, the first-,
second-, third- and fourth-grade arteriole; Pa, precapillary arteriole; C,
capillary.
30.45 5.44 lm, respectively. According to those measurements, the average luminal diameter of arterioles in
adult yak’s hearts were, in most cases, larger than those
in infant yaks, except that in the fourth grade of
embranchment.
16.24 2.27 lm, respectively, with the ranges of 11.53–
15.49 and 12.50–19.99 lm, respectively. At the level of
the precapillary arteriole, the most striking feature in
the precapillary arteriole was a long series of constrictions, which were evident at all of the site sampled both
in infant and adult yaks. In general, the constrictions
completely encircled the luminal cast; however, they
were occasionally irregular or semicircular in their
appearance. In an adult yak, there was a marked change
in luminal diameter of precapillary arteriole, giving it a
distinctive cone-shaped appearance (Fig. 2A). The
Diameters and Characteristics of
Precapillary Arterioles
The average luminal diameters of precapillary arterioles in infant and adult yak’s hearts are 13.20 2.35 and
1522
HE ET AL.
the capillaries usually had some constrictions (Fig. 3F).
The density of capillary in epicardium, myocardium, and
endocardium in infant yak’s hearts were 1,674 243/
mm2, 2,407 328/mm2, and 1,489 337/mm2 and those
in adult yaks’ hearts were 1,864 179/mm2, 2,528 263/mm2, and 1,636 235/mm2, respectively. The density of capillary in myocardium were significantly higher
than those in epicardium and endocardium either in
infant or adult yak’s hearts (P<0.01), and the density of
capillary in myocardium of adult yak’s heart had significantly higher values (P<0.01) than those in infant yak.
Venules
The peculiar arrangement of the venules was a striking feature of the microvasculature. A collecting venule
looked quite different from a terminal arteriole. The venous capillaries were gathered from the capillary sheets
into venule that was commonly oriented in a direction
perpendicular to that of the capillaries (Fig. 4A). The
capillaries came from all directions along the muscle
fibers, made a sweeping curve to join with each other,
and rapidly formed a venule (Fig. 4B). The capillaries
frequently were spaced at regular intervals when entering the venules and did so only on the axis parallel to
the muscle fiber. This unusual appearance of the venules
and small veins had been called the ginger or turniproot arrangement and sometimes was quite spectacular
in adult yak (Fig. 4C,D). But in infant yak, it looked like
a pockety arrangement (Fig. 4E,F).
DISCUSSION
Fig. 2. The precapillary arterioles of heart in infant and adult yaks.
A: A long series of constrictions (arrowheads) and a distinctive coneshaped appearance in the cast of precapillary arteriole in an adult yak
(boxed area). Asterisks mark blind-ending incompletely filled vessels.
A, arteriole; Pa, precapillary arteriole; B: Long series of constrictions
(arrowheads) with no distinct decrease in the diameter of the precapillary arteriole of the infant yak.
capillary in each case of adult yaks was considered to
begin at a point where the luminal diameter became uniform, while that was not evident in infant yak (Fig. 2B).
Capillary
The average diameter of capillary in infant and adult
yak’s hearts were 8.57 1.29 and 6.57 2.28 lm,
respectively, with the ranges of 5.75–11.53 and 6.25–
12.50 lm, respectively. The diameters of the capillary in
infant yak’s hearts were larger than those of adult yaks.
Generally, the precapillary arterioles gave rise to a number of capillary, but occasionally, a capillary would originated from an arteriole. Capillaries were in parallel
with each other in myocardium (Fig. 3A,B), while their
arrangement were irregular in endocardium and epicardium (Fig. 3C). It was clearly found that the capillaries
lay within the fascicles and did not cross between their
layers. The capillary anastomosis of ‘‘H’’ and ‘‘Y’’ usually
existed in the myocardium of both adult and infant yaks
(Fig. 3A,B,D); however, those in infant yaks were not
typical as in adult yaks in their shape (Fig. 3E). In addition, the outer surface of capillaries casts in infant yaks
were smooth, and no constrictions were found in the
plastic cast of capillaries (Fig. 3D), while in adult yaks,
To examine the sequential morphological changes of
the microvasculature, heart’s samples from different age
group should be included. However, the fetus heart was
too small to inject the solution into the whole microvascular system successfully, so only the samples from
infant and adult yaks were chosen in this investigation.
Several methods for injections of the microvasculature
of the heart with various materials were employed in
previous studies by many scientists. Filling vessels with
special materials is an established procedure and many
different compounds have been reported so far. Besides
the well-known polymerized methyl methacrylate resin
(Anderson and Anderson, 1978; Gannon, 1981; Ohtani
and Gannon, 1982), mostly PU4ii (Krucker et al., 2006)
and Mercox-Cl-2B (Kachlik et al., 2002, 2007; Lametschwandtner et al., 2004, 2006; Minnich et al., 2007) have
been historically used. In the present study, we found
that the combination of the method using the solution of
ABS in butanone for microcopists with the method using
the solution of formaldehyde in black Chinese ink for tissue sections would provide a satisfactory way for both
planar and three-dimensional observations.
ABS is an amorphous thermoplastic blend, with the
recipe of 15%–35% acrylnitrile, 5%–30% butadiene, and
40%–60% styrene. Generally, ABS has satisfactory stiffness and dimensional stability, glossy surface, and is
easy to machine. The molding minification of this kind
of ABS is 0.4%–0.7%, and the same blend properties has
the same shrinkage behavior. Therefore, we ignored the
molding minification when the diameter of the microvasculature cast was measured in this study. According that
different concentrations of ABS have different viscosity
MICROVASCULATURE OF LEFT VENTRICULAR WALL IN YAK
1523
Fig. 3. The capillaries of heart in infant and adult yaks. A,B: Capillaries in myocardium are in parallel with each other. C: Irregular arrangement of capillaries in the endocardium. D: ‘‘H’’ (white arrow) and ‘‘Y’’
(black arrow) capillary anastomoses are found frequently in the myocardium of adult yak. E: ‘‘H’’ (white arrow) and ‘‘Y’’ (black arrow) capil-
lary anastomoses in infant yak. Note that diameters of capillaries are
not uniform, and anastomoses differ from that in adult yak. Boxed
areas mark blind ending vessels with rounded endings. F: Capillaries
of the heart in adult yaks with characteristic constrictions
(arrowheads).
and fluidity, and different vasculature in the heart has
different diameter, we used three kinds of concentration
of ABS solution when we injected the heart of yak, they
were 5% ABS in butanone, 10% ABS in butanone, and
15% ABS in butanone, respectively, and their injection
order was 5% first, 10%, and 15% last. Because the diameter of capillary is the smallest in all of the vasculature of heart, so we used 5% ABS first, which could
easily pass through the capillary and cast the whole capillary bed. And for the same reason, because of the high
viscosity and low fluidity of 15% ABS, we used it at the
last stage of injection, which could fill the coronary artery completely and prevent outflow of the solution that
we had injected in the heart like a stopper. In addition,
we injected the heart of yak via both right and left coronary artery at the same time. This method was propitious to keep the balance of injection pressure in the
vasculature, avoid the rupture of blood vessel availably,
and get the perfect effect of microvasculature injection
at last. Also, we found that the hand pressure that can
offer a sensitive pressure and gave the best results were
better than controlled pressure, in spite of there being
no manometric control of injection pressure, and it was
the same as the method of Ohtani and Gannon (1982).
Impressions into the plastic compound produced by
nuclei of endothelial cells have been described previously
1524
HE ET AL.
Fig. 4. The venules of heart in infant and adult yaks. A: Orientation
of venules. Note that venules (arrows) run perpendicularly to capillaries. B: The capillaries made a sweeping curve to join with each other
and rapidly form venules. Asterisks mark blind-ending incompletely
filled vessels. V, venules; C, capillary. C,D: Spectacular ginger or turnip-root patterns of venules in adult yak (boxed area). V, venule. E,F:
The arrangement of venules in infant yak looks like a pocket (boxed
area). V, venule.
in the hypophyseal vessels of the toad and in the cochlear vessels of the rat even throughout the capillary network (Lametschwandtner et al., 1976; Hodde et al.,
1977). Similar nuclear impression was found in the
arteries and arterioles of both the canine abdominal vessels and the canine and equine intracranial vessels
(Anderson and Anderson, 1978, Bayer et al., 2002).
Lametschwandtner et al. (2004) also found the long endothelial cell nuclei imprints, orientated parallel with
the vessel axis, and considered it as a characteristic that
differentiated from venous. In this study, we still found
that the nuclear impression in the cast of arterioles either in infant or adult yak’s hearts. But it was not evi-
dent in the capillary portions of the casts due to the
absence of the smooth muscle in the vessel walls, which,
presumably, permitted relatively greater distension of
the capillary.
It has been suggested that the innermost layer of
smooth muscle of the walls of small arterioles is
arranged circularly in some areas (Anderson and Anderson, 1978), helically in others (Rhodin, 1967), and both
circularly and spirally in others (Rhodin, 1978; He and
Cui, 2007). We found that the same spirally arrangement in arterioles of both infant and adult yak’s hearts,
with the characteristic appearance of the arteriolar casts
of the heart in contracted states. We would suggest that
MICROVASCULATURE OF LEFT VENTRICULAR WALL IN YAK
the contraction of the smooth muscle of the vessels may
produce a spring-like action of the arteriole by which
blood flow is effectively reduced in contraction and
restored in relaxation. On the other hand, this arrangement most likely resulted from the lack of intraluminal
pressure during the casting procedure. More morphological evidence is required to support this spring-action
concept.
The occurrence of the plastic strips overlaid around
the lumen is rather a peculiar phenomenon. It has been
observed in both experimental models and humans
(Anderson and Anderson, 1978; Hodde 1981; Lametschwandtner et al., 2004). A considerable number of authors
have related the presence of plastic strips to a corrosion
defect (Schraufnagel, 1987; Christofferson and Nilsson,
1988). However, Wolff (1977) noted that localized regions
of the arterioles were highly permeable to large tracer
molecules such as ferritin, lanthanum, and alcian blue.
It is possible that the perfusion pressure opened the
tight junctions of the endothelial cells. With the lack of
an internal elastic lamina, an open extracellular communication exists between the vessel lumen and the tunica
media, which allows for the passage of large molecules,
such as ABS in this study. Thus, the wrapping of the
plastic around the filled lumen is not considered to be a
replication of the smooth muscle cells but rather represents the spaces between compressed cells, and this idea
is in accordance with Castenholz et al. (1982). Possibly,
the frequent lack of plastic strips on vessel replicas due
to the difference in pressure required to achieve the passage of material to the muscle layer.
The precapillary arterioles in adult yak’s hearts were
readily distinguished by the prominent long series of
constrictions left by the smooth muscle cell or by the abrupt decrease in luminal diameter that gave a cone-like
shape to the arteriole. These vessels correspond closely
to the precapillary sphincter area and were suddenly
altered drastically to that of a capillary, producing a
‘‘bottle-neck’’ effect at the level of the sphincter. The
authors agree with the interpretation of Nicoll (1971)
that the precapillary sphincter area is composed of a series of constrictions along the terminal twigs of the arterioles system, which may modify the flow and pressure
in the capillary network. The precapillary arterioles in
infant yak’s hearts, however, were not found to show
obvious constrictions and cone-like shape, and they could
be only determined according to the diameter of their
luminal cast and the context of vein.
The morphological pattern of venules in infant and
adult yak’s hearts was similar to those in dog (Reynolds
et al., 1958) and in the work of Brown (1965) on the six
domestic species. In addition, we have found the pockety
arrangement in infant yak’s hearts. Compared with the
arrangement of arterioles, we support a quickly reflux
function of these microvasculature, which can better
control blood pressure.
Makanya et al. (2007) found that there were blind
endings in the capillary corrosion cast of the developing
chicken embryo lung and considered it as sprouting
angiogenesis, which was responsible for the formation of
the basic vascular pattern. Joachim et al. (2002)
observed the presence of blind endings vessels in the primary tumors. In this study, we also observed the blind
endings vessels in the heart of yak. Given the structural
similarities with branching trees, it has been suggested
1525
that the growth of the cardiovascular system follows a
mode in which tiny tubules in the size range of capillaries "sprout" from existing "mother" vessels. These
sprouts, which form new vascular branches, then grow
in length until they meet another vessel to which they
connect. This process allows for the establishment of
flow between both preexisting vessels. It is, however,
still not clear how the growth of sprouts is directed toward one another so that their fusion is possible.
The present study made a serial investigation on the
density of capillary in three layers of hearts in infant
and adult yaks. We found that arterioles of yak’s hearts
always give rise to capillary after three to four grades of
embranchments, and so we did the classification to arterioles according their arrangement and diameter of each
grade arterioles. Also, we agree the idea of Gössl et al.
(2003) that the arterioles have a distributing function.
The distributing function of arterioles is indicated by a
significant decrease of microvasculature diameter at
each bifurcation level. Moreover, it was found that the
density of capillary in myocardium of adult yak’s heart
had significantly higher values than those in infant yak,
while the diameter of capillary in infant yaks were
larger than those in adult yaks. We assumed that there
was a maturation of the capillary bed from infant to
adult yaks in terms of decreasing capillary diameter
with increasing age, thus making it possible to increase
capillary densities in adult yaks.
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