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The extent of cardiac muscle in the great veins of the dog.

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The Extent of Cardiac Muscle in the
Great Veins of the Dog
REXFORD CARROW AND M. LOIS CALHOUN
Department of Anatomy, College of Veterinary Medicine,
Michigan State University, East Lansing
ABSTRACT
The extent and arrangement of cardiac muscle in the great veins of
adult dogs of both sexes was investigated. Cardiac muscle was found for varying
distances in the venae cavae and pulmonary and azygos veins in all animals. The
average distances which the muscle extended into these vessels in the beagles were:
1.88, 0.859, 0.525, and 0.622cm. Similar measurements in the poodle were: 1.35,
0.705, 0.764,and 0.690 cm and in the shepherd: 3.05, 1.36, 1.22, and 0.926 cm. Both
the venae cavae and pulmonary veins contained circular, spiral and longitudinal
muscle bundles. The cardiac muscle was continuous from the superior venae cavae
into the wall of the azygos vein and appeared to occupy the medial layer of the wall
in all instances. Elastic and white fibrous connective tissue extended between the
muscle bundles and appeared to invest the tapered muscle fibers in some places.
In the past many investigators have
noted the presence of cardiac muscle in
the great vessels of the heart. Textbooks
of histology (Trautmann and Fiebiger,
'57; Krolling and Grau, '60; Copenhaver
and Johnson, '58; Bloom and Fawcett,
'62; Arey, '63) indicate that near the heart
the walls of large veins contain varying
amounts of cardiac muscle. Several excellent manuscripts on the heart (Keith, '03;
Glomset and Glomset, '40; Robb, '34; Keith
and Flack, '07; Flack, '10; Thomas, '59;
Papez, '20) have reported that atrial muscle extends along the venae cavae and pulmonary veins for varying distances. Takino ('33) and Takino and Ezaki, ('34) noted
that the invasion of "striated muscle into
the pulmonary veins was greater in the
mouse and rat than in the cat and dog.
It has been pointed out by Thomas ('59)
and Papez ('20) that cardiac muscle extends along the pre-cava to the last tributary of that vessel, the azygos vein. Recent
studies with the electron microscope (Heppleston, '61; Karrer, '59; Karrer and Cox,
'60) have provided new information on
the morphology of striated muscle of the
cardiac type in the great veins.
The possibility that the presence of cardiac muscle in these vessels may be important in pulmonary hemodynamics is
reflected in several reports. (Heppleston,
'61; Karrer, '59; Karrer and Cox, '60; Best
and Heath, '61; Burch and Romney, '54).
ANAT. REC., 150: 249-256.
Since cardiopulmonary problems are of
prime importance in human subjects, it
follows that in order to carry out physiological studies directed toward these problems we must know what animal most
resembles the human being in this respect.
It is with these objectives in mind that the
present report on the histology of the
great veins in the dog is presented.
METHOD
The hearts and lungs of freshly killed
dogs were obtained at necropsy within one
hour after death and fixed in mercuryformol-saline solution (Dawson and Friedgood, '38). All of the animals (table 1)
were beagles except C-7 which was a purebred toy poodle and C-8 which was a german shepherd.
The heart and great vessels were removed intact. This allowed for obtaining
strips of the vessels extending from their
severed ends well into the atria. These
strips represented longitudinal segments
of the lungs, veins and atria, including
the junctional area.
The strips were dehydrated in dioxane,
embedded in paraffin and sectioned at 6 cr.
Measurements were made with a calibrated ocular micrometer and are shown
in table 1. Hematoxylin and eosin, Weigert
and Van Gieson's, and Crossmon's modification of Mallory's connective tissue stain
aided the study of muscle and connective
tissue.
249
250
REXFORD CARROW AND M . LOIS CALHOUN
TABLE 1
Cardiac muscle measurements in the great veins
Superior
vena cava
length 2
Animal 1
mm
c-1
23.81
18.52
15.87
16.02
18.55
16.46
16.90
17.93
21.16
22.93
19.08
13.52
30.57
20.43
d
C-4 d
c-9 d
c-11d
Average
c-2 0
c-3 0
c-5 0
C-6 0
c-10 0
Average
c-7 d
C-8 0
Total average
Inferior
vena cava
length 2
mm
8.70
7.68
8.23
8.54
8.29
9.55
8.65
9.71
7.35
9.26
8.90
7.05
13.67
9.48
Pulmonary
vein
length 2
Azygos
vein
length 3
mm
mm
4.23
3.41
6.23
8.08
5.48
5.10
3.82
6.17
6.32
7.64
5.81
7.64
12.20
7.78
7.64
6.17
6.46
6.32
6.65
5.63
6.05
4.70
6.76
7.49
6.12
6.90
9.26
7.23
' A l l animals were medium sized, mongrel type dogs except C-8 which was larger (shepherd
type) and C-7 which was a pure bred poodle.
%Distance(mm) that carhac muscle extends from the heart.
3 Distance (mm) that cardiac muscle extends from its junction with the superior venae cava.
RESULTS
General considerations
All blood vessels were comprised of the
three tunics described in textbooks of histology. The endothelial layer of the intima
was continuous with that of the atria. The
adventitia contained an admixture of collagenous and elastic fibers while the media
was composed of a compact layer of cardiac muscle.
Superior vena cava
The atrial myocardium passed uninterrupted into the wall of the superior vena
cava. The cardiac muscle constituted the
tunica media for distances ranging from
13.52 to 30.57mm. The extension of the
muscle varied directly with the size of the
dog and, therefore, was greater in the
larger animal than in the smaller one.
Measurements on the medium sized beagle
type dog fell between the two extremes.
Near the heart the cardiac muscle was
arranged in three layers (fig. 1). The inner
and outer layers were predominately circular although some were spiral and appeared oblique in sections. The middle
layer was oriented longitudinally and
dwindled out in the first few millimeters
from the heart. In many instances the
muscle ended abruptly in fibrous tissue.
Elastic and white fibrous connective tissue
extended between the muscle bundles and
appeared to invest them in some places
(fig. 2).
Azygos vein
Cardiac type muscle continued into the
azygos vein from the superior vena cava
(fig. 3 ) and measurements of the muscle
layer were taken from the point of its
junction with that vessel. The range of
length in this vessel was from 4.70 to
9.26mm. These figures did not vary directly with the size of the animal as they
did in the superior vena cava and, therefore, the muscle was often less extensive
in the medium sized dogs than in the toy
poodle.
Near the superior vena cava the muscle
layer was heavy and oriented in a circular or oblique pattern (fig. 3). As it continued distally in the vena azygos it
terminated by dwindling out (fig. 4).
Inferior Vena Cava
A heavy layer of cardiac muscle continued uninterrupted from the heart into
the caval wall (fig. 6 ) and constituted the
tunica media (fig. 5) of that vessel for
distances ranging from 7.05 to 13.67 mm.
Its terminal point varied directly with the
size of the animal as in the superior vena
cava. Elastic and white fibrous connective
tissue fibers were present at the termination of cardiac muscle (fig. 7) and were
concentrated around the ends of the mus-
CARDIAC MUSCLE IN THE GREAT VEINS
cle as in the other vessels. In many places
there seemed to be a connection between
the investing elastic fibers and the muscle
bundles.
Pulmonary veins
Fascicles of cardiac muscle were present
in the pulmonary veins, but did not extend
as far as the lung in any of the dogs observed (fig. 8). Close to the heart the muscle fibers coursed spirally and circularly
with a few middle longitudinal bundles
(fig. 9). This was similar to the arrangement seen in the superior vena cava. The
muscle extended for distances ranging
from 3.41 mm to 8.08 mm in the mongreltype dogs, while it had maximum measurements of 7.64 mm and 12.20 mm in the
poodle and shepherd, respectively. Elastic
fibers closely invested the tips of muscle
fascicles and white fibrous tissue was in
greater proportion to elastic tissue than in
the other vessels (fig. 10).
(DOG)
251
It is possible that the ends of these fibers
were not seen because of the level at which
the sections were cut. However, it is also
reasonable to believe some of them encircle the vein and return to be inserted in
the heart as described by Thomas (’59).
By observing the axiom that structure
and function go hand in hand, it is interesting to speculate what effect these findings might contribute to the function of the
pulmonary veins. What relation this arrangement could have to cardiopulmonary
problems is of still greater importance.
If the excitatory wave spreads from the
atria into the pulmonary veins, the flow
of oxygen rich blood from the lungs would
be impeded due to constriction of the vessels. This would account for the “throttle”
or “sphincter” mechanisms mentioned
earlier.
Since the muscle fibers course in a circular manner from the atria into the veins
DISCUSSION
and back to the heart again, an equally atIt has been suggested that cardiac mus- tractive hypothesis is possible. By followcle in the pulmonary veins may have some ing the pathway established by the muscle,
special functional significance. Takino the conducting impulse in the veins would
(’33) and Takino and Ezaki, (’34) stated create a peristaltic or milking action
that the veins could contract and “throttle toward the heart. Under these conditions
the blood stream,” while others (Amano, venous return and atrial filling would be
’33; Otterbach, ’38; Bucciante, ’40) pro- enhanced. It is possible that both of these
posed a “sphincter action” to these vessels. actions take place. In any case, the histoBurch and Romney (’54) pointed out that logic arrangement of the pulmonary veins
therapeutic measures in such cases as pul- would promote the transmission of immonary edema are directed at the heart pulses toward as well as away from the
when in reality the actual cause may be heart.
The pulmonary veins of the dog are
dysfunction of the pul-monary veins.
A gross anatomical study of the heart composed primarily of fibrous tissue from
and great veins of the dog was carried out the terminal point of the cardiac muscle
by Thomas (’59). The author mentioned into the lungs, while the same area in man
that tracts of cardiac muscle extended is characterized by a layer of smooth
from the left atrium into the pulmonary muscle. These two muscle types overveins. It was further determined that most lap to some extent and the significance
of the tracts ended in the wall of the vein; of this has been discussed by Burch
however, some return to insert in the heart. and Romney (’54).
In the present histologic investigation, each
In addition, it should be noted that carof the vessels studied contained fascicles diac muscle in both man and dog is conof cardiac muscle which ended in the ves- fined to the veins and does not extend into
sel wall. The ends of the fibers were in- the lungs. In animals such as the rat and
vested by fibrous tissue and seemed to be mouse, cardiac muscle is present in the inanchored at that point (figs. 2, 4, 7, 8, 9). trapulmonary vessels and some authors
In contrast, some bundles were arranged (Karrer, ’59; Arnstein, 1877) have indiin a circular or oblique manner and their cated that it may have an important relaterminal points were not demonstrated tionship to the high metabolic rate of these
(figs. 2, 5, 10).
animals.
252
REXFORD CARROW AND M. LOIS CALHOUN
It is realized that the function of the Best, P. V., and D. Heath 1961 Interpretation
of the appearances of the small pulmonary vesgreat veins cannot be determined solely
sels in animals. Circulation Research, 9: 288from an anatomical basis. It is important,
294.
however, to be aware of the differences Bloom, W., and D. W. Fawcett 1962 A Textbook of Histology. W. B. Saunders Co., Philathat exist between the human species and
delphia, London. Chapt. X, p. 281.
other animals in this special region so the Bucciante,
L. 1940 Architettura e struttura
best suited animal can be selected for dedella guaina miocardia della vena cave, pulmonari, e del sen0 caronario dell ‘uomo. Med.
tailed physiological studies. This investisper. Arch. Ital., 6: 273-279.
gation, which compared the significant hisBurch, G. E., and R. B. Romney 1954 Functologic features of the great vessels in dog
tional anatomy and “throttle valve” action of
and man, was carried out with these points
the pulmonary veins. Am. Heart J., 47: 58-66.
Copenhaver, W. M., and D. D. Johnson 1958
in mind.
SUMMARY
Cardiac muscle was demonstrated in
the venae cavae, azygos and pulmonary
veins. Near the heart most of the muscle
bundles coursed in a spiral or circular
manner. Some of the fascicles terminated
in the walls of the vessels and were securely anchored by fibrous tissue. Many
bundles encircled the veins and therefore
no terminal point could be seen. Although
these bundles might end at some other
point in the wall of the vessel, it is also
possible that they could return to insert
into the heart. This arrangement of muscle fibers would provide the pathways for
transmission of impulses toward as well as
away from the heart.
Certain histologic features of the pulmonary veins of the dog are similar to
those of man while others are quite different. In this regard, it was emphasized
that cardiac muscle was present in the
extrapulmonary vessels of both the dog
and human but did not extend as far as the
lung in either case. The pulmonary veins
of the dog are fibrous from the terminal
point of cardiac muscle into the lungs
while these same vessels in man contain
smooth muscle. The knowledge of differences and similarities in man and dog
may be important to investigators of cardio-pulmonary problems.
LITERATURE CITED
Amano, S. 1933 Beitrag zur funktionellen
Struktur der Lungenvenen. Tr. SOC.path. Jap.,
23: 842-851.
Arey, L. B. 1963 Human Histology. A Textbook in Outline Form. W. B. Saunders Co.,
Philadelphia, London. Chapt. XIII, p. 130.
Amstein, C. 1877 Zur Kenntniss der quergestreifen Muskulatur in der Lungenvenen. Centralbl. f. d. med. Wissenschl. Berl., 15: 692-696.
Bailey’s Textbook of Histology. The Williams
and Wilkins Company, Baltimore. Chapt. XII,
p. 235.
Dawson, A. B., and H. B. Friedgood 1938 Differentiation of two classes of acidophils in the
anterior pituitary of the female rabbit and rat.
Stain Tech., 13: 17-21.
Flack, M. 1910 An investigation of the sinoauricular node of the mammalian heart. J.
Phys., 41: 64-77.
Glomset, D. J., and A. T. A. Glomset 1940 A
morphologic study of the cardiac conduction
system in ungulates, dog and man. Am. Heart
J., 20: 389-398.
Heppleston, A. G. 1961 The musculature of the
aging mouse lung. J. Gerontology, 16: 106109.
Hooker, C. W., H. A. McAllister, Jr. and F. W.
Wells 1964 Active contractions of the large
thoracic veins in certain mammals. (Abst.)
Anat. Rec., 148: 292.
Karrer, H. E. 1959 The striated musculature
of blood vessels. I. General cell morphology.
J. Biophysic. and Biochem. Cytol., 6: 383-392.
Karrer, H. E.,and J. Cox 1960 The striated
musculature of blood vessels. 11. Cell interconnections and cell surface. J. Biophysic. and
Biochem. Cytol., 8: 135-150.
Keith, A. 1903 The anatomy of the valvular
mechanisms around the venous orifices of the
right and left auricles, with some observations
on the morpholgy of the heart. J. Anat. Phys.,
37: 221-236.
Keith, A., and M. Flack 1907 The form and
nature of the muscular connections between the
primary divisions of the vertebrate heart. J.
Anat. Phys., 41: 172-189.
Krolling, O., and H. Grau 1960 Lehrbuch der
Histologie und Vergleichende Mikroscopischen
Anatomie der Haustiere. 10th German Edition.
Paul Parey, Berlin, p. 135.
McAllister, H. A., Jr., C. W. Hooker and F. R.
Weedon 1963 Occurrence of cardiac muscle
in the azygos vein of mammals. (Abst.) Anat.
Rec., 145: 258.
Otterbach, K. 1938 Beitrage zur Kenntnis des
Lungenkreislaufes; die Genese des Myokardiiberzuges der Mundungsteiles der Vena pulmonalis. Morphol. Jahrb., 81: 547-561.
Papez, J. W. 1920 Heart musculature of the
atria. J. Anat., 27: 255-285.
Robb, J. S. 1934 The structure of the mammalian auricles. Med. Woman’s J., 41: 143.
CARDIAC MUSCLE IN THE GREAT VEINS (DOG)
Takino, M. 1933 Vergleichende Studien uber
die histologische Struktur der Arteriae und
Venae pulmon&s, die Blutgefassnerven der
Lunge und die Nerven der Bronchien bei verschiedenen Tierarten, besonders uber die Beziehung der BlutgefPssnerven zu den glatten
Muskeln der Blutgefasse. Acts Schol. Med.
Univ. in Kioto, 15: 321-334.
Takino, M., and Y. Ezaki 1934 Uber die Besonderheiten der Arteriae und Vena pulmonales
bei verschiedenen Tieren, besonders beim Men-
253
schen. Acta Schol. Med. Univ. in Kioto, 17: 113.
Thomas, C. E. 1959 The muscular architecture
of the atria of hog and dog hearts. Am. J.
Anat*,Io4: 207-236.
Trautmann, A., and J. Fiebiger 1957 Fundsmentals of the Histology of Domestic Animals.
Translated and revised from the 8th and 9th
German edition, 1949, by Robert E. Habel and
Emst L. Biberstein. Comstock Publishing Associates, A division of Cornell University Press,
Ithaca, New York. Chapt. VIII, p. 112.
PLATE 1
EXPLANATION OF FIGURES
1 Longitudinal section of superior vena cava showing cardiac muscle
arranged in three layers near the heart. H & E; X 80.
2 Longitudinal section of superior vena cava. The tapering ends of
cardiac muscle fibers ( a ) seem to be anchored by fibrous tissue
(arrows). Some fibers ( b ) have changed directions as if to encircle
the vessel. They may end at a different level in the vessel wall or
return to insert into the heart. Weigert and Van Giesen; X 500.
3 Junction of azygos vein and superior vena cava. Note the continuation of cardiac muscle from the vena cava ( a ) into the azygos vein
(b). H & E; X 70.
4
Cardiac muscle fibers ( a ) in the wall of the azygos vein are closely
associated with fibrous tissue (arrows). Weigert and Van Giesen;
X 490.
5 Longitudinal section showing the termination of cardiac muscle fibers in the inferior vena cava. Some fibers ( a ) seem to be anchored
in the wall while others appear free (b). H & E; X 114.
6
254
Longitudinal section of the junction of heart and inferior vena cava.
Cardiac muscle fibers continue uninterrupted from the heart ( a ) into
the caval wall (b). H & E; x 80.
CARDIAC MUSCLE IN THE GREAT VEINS (DOG)
Rexford Carrow and M. Lois Calhoun
PLATE 1
255
CARDIAC MUSCLE IN THE GREAT VEINS (DOG)
Rexford Carrow and M. Lois Calhoun
PLATE 2
7
Section of inferior vena cava showing the attachment of connective tissue fibers ( a ) to the terminal bundles of cardiac muscle ( b ) . Weigert and Van Giesen; X 390.
8
Longitudinal section of pulmonary vein. The cardiac muscle ( a ) ends abruptly i n the vein and
does not extend into the lung ( b ) . Weigert and Van Giesen; x 24.
9
Section of pulmonary vein taken near the heart.
Tunica intima (arrow). H & E; X 160.
Cardiac muscle comprises the tunica media.
10 Pulmonary vein. In places elastic tissue fibers appear to be continuous with the investing coat of
cardiac muscle ( a ) . Some fascicles ( b ) are in the process of turning. These muscle fiber tracts
may encircle the vessel and return t3 insert in the heart as mentioned by Thomas ('59). Weigert
and Van Giesen; X 450.
256
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