Download Functional Morphology of the Heart in Mammals

A M . ZOOLOGIST, 8:221-229 (1968).
Functional Morphology of the Heart in Mammals
Ursula Rowlatt
Chicago Zoological Park, Brookfield, Illinois, 60513, and
Lincoln Park Zoological Gardens, Chicago, Illinois
SYNOPSIS. The heart in all mammals is composed of four separate chambers and in broad
outline is very similar in monotremes, marsupials, and placenta! mammals. The functional
anatomy of the chambers and valves of the dog's heart has been investigated by Rushmer (1961)
and others. They concluded that the atria serve as reservoirs and the ventricles as reciprocating
pumps, the right ventricle being a volume pump and the left ventricle a pressure pump. Similar
investigations in man, horses, cattle, sheep, and goats suggest that other mammalian hearts act in
the same way.
However, there is a wide range of variation in heart weight relative to body weight, in heart
shape, and in minor points of internal anatomy. The general contention in this paper is that
these differences should be considered functionally significant unless proven otherwise. Certain
morphological structures such as the valves of the posterior vena cava, Lower's tubercle, the atrial
appendages, and the more extreme forms of double ventricular apex may not have functional
significance. Verbal descriptive anatomy has probably reached the end of its usefulness and
should be replaced with measurements. A correlation of quantitative anatomy and hemodynamics
would seem to be the most promising line of future research.
The heart of any mammal is composed of
four separate chambers arranged in parallel and is very similar in construction in
monotremes, marsupials, and placental
mammals. A functional explanation can be
given in general terms for the gross morphology of each chamber. Such an explanation probably holds good for mammals
as a whole and will be given first. However,
there are many differences in structural
detail between genera, species, and individuals and, if these are to be explained in
functional terms, certain evolutionary and
morphogenetic processes must be taken
into consideration. These will be discussed
in the second part of the paper.
Most of the following observations are
based on the work of Rushmer and coworkers using several different techniques
in dogs (Rushmer, 1961). The dynamics of
the heart in horses, cattle, sheep, and goats
are similar (Sporri, 1965). The atria and
contiguous systemic and pulmonary veins
act as expanding reservoirs for blood returning from the body and lungs. Semilunar
valves preventing backflow are present in
the major systemic veins proximal to their
entry into the thoracic cavity. There is no
valve at the mouth of the anterior vena
cava and only in some species is there a
valve at the mouth of the posterior vena
cava (Eustachian valve) or coronary sinus
(Thebesian valve). The muscle fibers of the
atria are arranged in two groups: (1) those
that are common to both atria, and (2)
those that belong to each atrium. The
common fibers are superficial (Robb, 1965).
Constriction of the muscle bands around
the orifices of the systemic veins may reduce if not prevent backflow during atrial
systole (Keith, 1904). There are no valves in
the pulmonary veins, but a muscular valvular mechanism was postulated by Keith
and has been demonstrated in the living
dog by Little (1960).
Much of the atrial transport of blood is
brought about by elastic recoil of the wall.
Blood will move either forwards through
the atrioventricular valves or backwards
along the veins depending on which direction provides the least resistance to flow.
Only a small part of the expulsive force of
the atria is by active muscular contraction
and this occurs at the very end of ventricular diastole.
The ventricular myocardium is composed of two thin layers of spiral muscle
bundles running more or less at right
angles to each other and an intervening
constrictor layer. The superficial spiral
221
222
URSULA ROWLATT
muscles arise from the atrioventricular
rings, run towards the apex, reverse their
direction forming a vortex, and return to
the base of the heart as the deep spiral
layer. This layer forms the trabeculae carneae and papillary muscles. The constrictor bands lying between the spiral layers
encircle the basal two-thirds of the ventricles and constitute a much greater proportion of the total thickness of the wall in the
left than in the right ventricle.
Emptying of the right ventricle is
brought about by three mechanisms occurring at about the same time: (1) contraction
of the spiral muscles shortens the long axis
of the ventricle, pulling the right atrioventricular ring towards the apex, which remains stationary; (2) contraction of the
constrictor muscle layer moves the free wall
towards the septum in a bellows-like action
(the surface area of the ventricle is large
compared to its volume so that a small
excursion of the free wall will displace a
large volume of blood); (3) contraction of
the constrictor fibers of the left ventricle
will augment the bellows action by pulling
on the free wall of the right ventricle at the
interventricular groove. This last mechanism has been shown to be capable of
adequate ventricular emptying when the
free wall has been destroyed by cautery in
dogs or by coronary occlusion in man.
Presumably it is of even greater significance in animals such as bats, in which the
septum bulges well into the right ventricle
at all times.
The conus of the right ventricle has been
shown to behave as a separate chamber.
Conal diastole is still occurring when the
sinus has begun to contract, and conal
systole overlaps sinus relaxation (March,
Ross, and Lower, 1962). This dissociation is
in keeping with the ontogenetic and phylogenetic history of the conus, which represents the bulbus cordis of lower forms
(Keith, 1924).
Left ventricular emptying is brought
about mainly by a squeezing action caused,
by contraction of the constrictor layer.
This action reduces the diameter of the
chamber and is responsible for the power
of ejection. The power of thrust is augmented by the elastic recoil of the aorta
after closure of the aortic valve. The spiral
muscles shorten the long axis of the chamber, pulling the left atrioventricular ring
towards the apex.
Rushmer (1961) concluded that the right
ventricle is a volume pump ideally suited
to the disposal of large and varying
amounts of blood against a low peripheral
resistance. The left ventricle acts as a
pressure pump, capable of forceful contraction against a much higher peripheral
resistance. This difference in function is
related to the different disposition of musclefibersin each ventricle.
The functional anatomy of the atrioventricular valves was demonstrated in real
and simulated heart valves by Henderson
and Johnson in 1912. They showed that two
theoretical actions are possible. There is (1)
retrograde flow of blood towards the atria
at the beginning of ventricular contraction.
This action lifts the valve leaflets from
below, bringing them together, but inevitably results in leakage of blood through
the center of the closing orifice. However
this is prevented by (2) the occurrence at
the same time of a suction effect caused by
the momentum of the column of blood as
it is forced through the valve at the end of
atrial contraction. The degree of excursion
of the valve leaflets has been studied in
intact dogs by placing small metal clips on
the atrial side of the leaflets and by
recording their movement by cinecardiography. It was seen that the metal clips
moved only very short distances during the
cardiac cycle presumably due to continuous
restraint by the chordae tendineae (Rushmer, 1961).
Because both sets of atrioventricular
valves look superficially the same in general construction, it has been inferred that
their action is similar. However, the morphology of the left atrioventricular apparatus is much more uniform among mammals
than is that of the right atrioventricular
valve. The number of valve leaflets, the arrangement of trabeculae carneae at the valve
ring, and the attachment of the papillary
MORTHOLOGY OF THE HEART IN MAMMALS
muscles varies greatly from species to species and between individuals of the same
species. That each valve is constructed
specifically for its own position in the heart
is suggested by the course of events in a
human congenital anomaly called ventricular inversion. In this abnormality, the heart
is normal in all respects except that the
ventricle on the right side of the heart is a
morphological left ventricle and that on
the left a morphological right ventricle, as
judged by the appearance of the ventricular
septum (Lev, 1954). Since the configuration
of the valvular apparatus depends on the
arrangement of the papillary muscles,
which are in themselves part of the morphology of the ventricle from which they
arise, the right atrioventricular valve is a
morphological mitral valve and the left
atrioventricular valve is a tricuspid valve.
Such a heart may function properly for
many years, but the limiting factor is the
developmemt of tricuspid (left atrioventricular) incompetence and final heart failure
from the accumulated effects of regurgitation of blood through this orifice. From
this one can infer that the exact morphology of the mitral valve is required for
proper control of the left atrioventricular
orifice and that another apparently similar
valve is less efficient. Ventricular inversion
is in effect a translocation of morphological
units within the heart, and its consideration at this point illustrates the usefulness
of studying the abnormal alongside the
normal for the better understanding of
both.
The semilunar valves at the pulmonary
and aortic orifices are mechanically much
simpler. Each consists of three symmetrical
cusps. It has been shown that two cusps
would close equally well but would require
more elastic stretch to open adequately
(Rushmer, 1961). Closure is brought about
partly by suction following the initial rush
of blood through the orifice during ventricular systole and partly by lateral pressure
from eddy currents in the sinuses of Valsalva.
Usually two coronary arteries arise from
the base of the aorta, but the larger branches
223
of either may have an independent origin
as indicated by supernumerary ostia. The
coronary arteries and their main branches
lie either on the surface of the heart
beneath the epicardium or deep to the
superficial layer of the myocardium where
they lie parallel to the muscle fibers. Further subdivisions arise at right angles to the
main branches and run between the muscle
fibers to supply all layers of the myocardium. In some mammals, the ventricular
septum is supplied by a special septal
artery arising from the left coronary artery
close to its origin and running on the low
pressure side of the septum beneath the
endocardium of the right ventricle (see
Robb, 1965, for references). The resistance
to blood flow in the coronary arteries varies
enormously during the cardiac cycle because of the squeezing effect of the surrounding myocardial fibers. Flow is greatest
in diastole. Large animals and athletes
have a slow heart beat and a long diastole
which allows the heart muscle to recover
between contractions. Venous drainage is
by way of the coronary veins which enter
the right atrium by various routes. The
Thebesian veins probably play an arterial
role and supply the deeper parts of the
myocardium when the arteries are closed
during ventricular systole (Burton, 1965).
However, within this general morphological framework mammalian hearts differ in
several important respects. There is a wide
range of heart weight relative to body
weight. The shape of the heart differs
markedly from mammal to mammal. Various points of external and internal anatomy make it possible to identify hearts from
distant and closely related genera with a
fair degree of confidence. However, it must
be emphasized that the intraspecific variation is great and that any morphological
detail should be examined in many individuals before it can be considered to be a
constant entity. Extra caution should be
taken in animals that have been bred
selectively such as domestic animals and
pets.
The ratio of heart weight to body weight
(heart ratio) is independent of body weight
224
URSULA ROWLATT
within a wide range of body size. Stahl
(1965) plotted heart weight against body
weight on a log-log scale for figures given
by Brody for animals ranging in size from
mice (25 g) to steers (500 to 1000 kg). He
also obtained an allometric line, indistinguishable statistically from that obtained
from Brody's data, using measurements for
321 primates of body weight from 10 g to
100 kg.
For many years it has been assumed that
animals with a higher ratio of heart
weight/body weight have more efficient
hearts and possess, therefore, a physiological or environmental advantage over animals of similar body weight but lower
heart ratio. Clark (1927) noticed that animals capable of continuous and severe
muscular exertion had heart ratios greater
than 0.6 and those incapable of such exertion had heart ratios of less than 0.6.
Furthermore, the heart ratio of a wild
animal such as a rabbit was greater than
that of a tame one, and dogs bred for speed
had a higher heart ratio than mongrels.
Increased heart weight is due to increased left ventricular weight which is
itself related to stroke volume. The physiological responses to exercise are complex
and variable under different conditions,
but, in general, increased cardiac output in
response to increased venous return is
brought about more significantly by a rise
in heart rate than by increased stroke
volume. A large heart in a continuously
active animal probably merely reflects an
increase in general muscle bulk and a large
capillary network. Animals that run fast
over small distances are not exceptionally
muscular and do not possess proportionately large hearts. Clark's observations are
correct but the interpretation is misleading.
The variation in heart shape in mammals (Fig. 1), although striking, has received
no adequate explanation. Casual observation suggests that the shape of the heart
follows the shape of the chest. The whale's
heart is broad and flat and lies in a broad
thoracic cage with an obliquely slanting
diaphragm (Slijper, 1962). The ungulate
heart is long and narrow as is the thorax.
The peculiar shape of the mole's heart is
typical of the marked modification of the
common mammalian plan in the animal as
a whole. In man, the cardiothoracic ratio,
as seen radiologically, is sufficiently constant over a large range of body size to be
used as an index of cardiac normality
(Oberman, Myers, Karunas, and Epstein,
1967). The same general relationship is
seen in dogs, but ratios relating cardiac
silhouette to chest dimensions have not
been found reliable for diagnosis (D. K.
Detweiler, personal communication).
The most extreme view relating chest to
heart size is that of Davis (1964). He studied
the hearts of 14 bears, 3 procyonid carnivores, 4 canids, and 7 telids. He found
that the right ventricle was broader in
bears, procyonids, and dogs than in cats.
He observed (p. 567) that:
"the heart is part of a regional growth
area that includes the entire thorax. Accelerated transverse growth in this area in
bears and procyonids affects that part of
the heart (the venous portion of the right
ventricle) that is undergoing rapid differentiation and growth at the moment when
the acceleration manifests itself."
"The differences between the right ventricle of bears and procyonids and the right
ventricle of other carnivores are an accident of ontogenetic timing. They do not
represent functional adaptations."
Although ingenious, this explanation is
purely speculative. It is based on examination of very few specimens, and thoracic
measurements fundamental to the argument are lacking. Cardiac morphology has
been evolved in the vertebrates as a whole
in response to physiological demands and
might reasonably be supposed to be doing
so within the mammalian class. In my
opinion, a functional explanation for heart
shape should be expected until proved to
be false.
The next important step is to collect
numerous data on dimensions of the heart
and chest of living and dead mammals to
establish if chest and heart size are interdependent or not. Internal as well as external
225
MORPHOLOGY OF THE HEART IN MAMMALS
measurements of a dead heart will only be
meaningful if fixation is standardized (Glagov, Eckner, and Lev, 1963). The old belief
that a slender, pointed heart is character-
DOG
istic of fast-moving animals could then be
tested (Lechner, 1942). By applying Laplace's law, which relates intraluminal pressure, intramural tension, and radius of a
GIBBON
BAT
HEDGEHOG
FIG. 1. The hearts of the dog (Cants familiaris),
gibbon (Hylobates lar), deer (Dama dama), bat
(Eidolon helvum), rat (Rattus ratlu.s), rabbit (Oryctolagus cunicuhis), hedgehog (Erinacem europaea),
RAT
MOLE
DEER
RABBIT
SLOTH
mole (Talpa europaea), and sloth (Choloepas didactylus), to show the variation in the shape o£
mammalian hearts.
226
URSULA ROWLATT
chamber, it is likely that a long narrow left
ventricle with a low diastolic volume would
require less myocardial tension to develop
an adequate intraventricular pressure than
would a more rounded chamber. Such a
heart would be more suitable for sustaining
chronic pressure loads as in long-distance
running. Many hypotheses such as this can
be tested by correlating physiological and
anatomical data.
Examination of the mammalian heart
outside the body shows that there is considerable structural variation in the component parts. The basic supposition is that
these features are useful to the animal and
are important to the efficient working of
the heart. However, the development of
the mammalian heart has a long and
complicated evolutionary history, and
several non-functional influences must be
taken into account in interpreting structural variation.
Various anatomical features have been
identified as being primitive. Benninghoff
(1933) recognized that concentration of
parts of the heart is a fundamental process
in vertebrate cardiac evolution and that
this process continues in mammals. The
sinus venosus has been absorbed into the
right atrium in most mammals, but in
monotremes and the armadillo, Dasypus, it
remains as a small, shallow chamber at the
confluence of the three venae cavae. In
these animals it is separated from the right
atrium by a competent semilunar valve.
Two pulmonary veins enter the left atrium
by way of a separate vestibule in monotremes and marsupials but open directly
into the wall of the atrium in placental
mammals. The vestibule is still present in
the developing embryo of placental mammals. Often the main tributaries of the
pulmonary veins drain independently into
the roof of the left atrium, but much
variation occurs. The bulbus cordis is always incorporated into the right ventricle,
but, as the conus, may be more prominent
in some species than others. Even when
absorption of the developmental components of the heart is complete, evidence
of their former relations is given by the
coronary arteries, the main branches of
which overlie the primitive subdivisions of
the heart.
A coarse trabecular pattern in the free
wall of the right ventricle is the primitive
condition in phylogeny and ontogeny. Intraspecific variation must be taken into
consideration as always, but it seems that
the wall of the right ventricle of some
mammals is strikingly smooth. Other patterns are found fairly consistently in other
mammals (Fig. 2) Any functional explanation of the trabeculation should be directed at the smooth rather than the coarse
pattern.
The right atrioventricular valve in monotremes is mainly muscular as in birds
and crocodilians. In marsupial and placental mammals, an occasional chorda tendinea may be muscular, indicating its
origin from the muscular wall of the ventricle, but in general the right atrioventricular valve is formed of connective tissue
only.
Modern mammals are subdivided into
three infraclasses on the basis of their
prenatal development and by inference on
the course and duration of the embryonic
circulation. It follows that intra-uterine
circulatory requirements determine the
morphology of the right atrium and atrial
septum. This should be the easiest area of
the heart to understand in functional terms
but in practice it is the most difficult. The
functions of the residual valves of the
embryonic sinus venosus and the muscle
bands in the wall of the atrium have
mystified anatomists since Eustachius described his valve in 1563 and Lower his
tubercle in 1669. The copious literature on
the comparative anatomy of these structures has been reviewed by Franklin (1948).
No clear interpretation of their function
has been given to this day, nor has it been
established except in rare cases, if these
structures are of importance in postnatal
life. The sinus valve leaflets in bats and in
the mole have migrated into the mouth of
the posterior vena cava where they form a
semilunar valve that has been shown by
227
MORPHOLOGY OF THE HEART IN MAMMALS
YELLOW FRUIT BAT
AMERICAN BISON
FIG. 2. Different degrees of trabeculation in the
wall of the right ventricles of the yellow fruit bat
cine-angiography to be competent during
adult life.
It is important to remember that the
heart is beating throughout its transformation from a simple, coiled tube to a complicated, double-circulatory organ. The view,
originally suggested by Spitzer in 1923, that
the passage of blood through the developing heart is an important factor in
moulding the embryonic tissues into the
adult shape has received ample recent
confirmation (see Jaffee, 1967, for references). Possibly, both the Eustachian valve
(Franklin, 1948) and Lower's tubercle may
be produced by such hemodynamic forces.
The varying prominence of Lower's tubercle in the animals shown in Figure 3 may
be related to the angle at which the right
anterior and posterior venae cavae enter
the heart. A myoendocardial ridge tends to
form between two converging streams of
blood in the developing heart and this
process may continue in postnatal life.
The existence of atrial appendages may
be an example of the influence of early
LAR GIBBON
(Eidolon helvum), the American bison
bison), and the lar gibbon (Hylobates lar).
MAN
(Bison
WOLF
DEER
SEA LION
FIG. 3. Position and prominence of Lower's Tubercle (shaded) in man (Homo sapiens), the wolf
(Canis lupus), the deer (Dama dama), and the sea
lion (Zalophus californianus).
228
URSULA ROWLATT
certain physical proportions within the
heart. Quantitation is needed to verify this
point. Lastly, consideration of the events of
cardiac phylogeny and ontogeny may help
to separate morphological features that are
probably ancestral from those that may
have functional significance. The greatest
need is for correlation of in vivo physiological observations, such as those provided by
angiocardiography and telemetry, with the
presence of structures that seem to suggest,
on theoretical grounds, a functional rather
than a non-functional origin.
PLACENTAL MAMMAL
MARSUPIAL
FIG. 4. Position of the right atrial appendage relative to the root of the aorta.
events in the development of the heart on
adult morphology. No function has been
ascribed convincingly to these structures,
and they may be removed without ill effect
during cardiac surgery. Probably they are
formed by pressure on the developing atrium by the truncus arteriosus as the heart
tube bends to accommodate itself within the
pericardium. The presence of a double right
atrial appendage in marsupials may be a refinement of this process. In these animals,
the aorta lies farther to the right of the pulmonary trunk than in placental mammals,
allowing a further compression of atrial
tissue between the roots of the great vessels
(Fig. 4). The markedly bifid apex of the
manatee heart may be caused by asynchronous development of the two aneurysmal out-pouches of the ventricle which are
destined to be the definitive ventricles
(Robb, 1965). A similar explanation may be
given for less marked degrees of duplication of the apex of the heart.
In summary, mammalian hearts are
more similar than they are dissimilar. However, variations in relative size, shape, and
details of anatomy exist between species.
Differences in heart shape are probably
related to the extent of the capillary bed
and in particular to that of the total
skeletal muscle mass. Differences in shape
may be related directly or indirectly to the
shape of the chest or may better be correlated with exercise potential by virtue of
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