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Developmental morphology of vascular and lymphatic capillaries in the working myocardium and purkinje bundle of the sheep septomarginal band.

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Developmental Morphology of Vascular and
Lymphatic Capillaries in the Working Myocardium
and Purkinje Bundle of the Sheep
Septomarginal Band
Department of Anatomy, University of Melbourne, Parkville, 3052 (E.C., G.R.C) and Basic
Cardiology Laboratory, Baker Medical Research Institute, Prahran, 3181 (J.J.S.), Victoria,
Australia; Department of Anatomy, Medical College of Oita, Oita, 879-56 Japan (T.S.)
The normal development of vascular and lymphatic capillaries in
the right ventricular septomarginal band of the sheep heart was studied in 9
fetuses aged 60-143 days (term = 147 days), 14 lambs aged 1day to 16 weeks, and
3 adults. Tissue was fixed by perfusion and examined with light and transmission
electron microscopy.
The septomarginal band is composed of working myocardium and a well-defined
peripheral bundle of Purkinje cells. Vascular capillaries of the working myocardium were closely apposed to myocardial cells. By contrast, vascular capillaries of
the Purkinje bundle were situated within the connective tissue sheath and septa,
at variable distances from the Purkinje cells. After birth, the capillaries of the
Purkinje bundle were also found in grooves and tunnels within the Purkinje
strands. The ultrastructure of fetal vascular capillaries associated with myocardial
and Purkinje cells was initially similar, and characterized by a n abundance of
synthetic organelles in endothelial cells and pericytes. However, after 115 days in
utero, capillary endothelium with diaphragmed fenestrae, 40-60 nm in width,
were observed within the Purkinje bundle. The fenestrae attained a n average
frequency of 1 per 11 capillary cross sections just before term, and this was maintained in lambs and adults. The ultrastructure of lymphatic capillaries, which
were not observed in the septomarginal band until just before term, changed little
during development.
Adult mammalian cardiac ventricles contain both
vascular and lymphatic capillaries. The vascular capillaries of the working myocardium form a dense anastomosing network which is directed predominantly
along the long axis of myocytes (Anderson and Anderson, 1980; Shimada et al., 1985). By contrast, vascular
capillaries of the conduction system surround Purkinje
strands a s a relatively loose network situated in surface clefts (Shimada et al., 1985). The lymphatic capillaries comprise irregularly shaped channels which occur throughout the myocardium in connective tissue
septa and vascular bundles (Leak et al., 1978; Marchetti et al., 1985). Vascular capillaries of the working
myocardium (Bruns and Palade, 1968) and lymphatic
capillaries (Leak et al., 1978) are lined by a continuous,
nonfenestrated endothelium. However, the ultrastructure of capillaries associated with the ventricular conduction system has not been examined in detail. Moreover, very little is known about the developmental
morphology of vascular and lymphatic capillaries during fetal and postnatal growth of the cardiac ventricles.
Accordingly, the aim of this study was to examine
the comparative morphology of myocardial and conduction tissue vascular capillaries, and lymphatic capillar0 1990 ALAN R. LISS, INC
ies in the ventricular myocardium from early gestation
to adulthood. Studies were performed in the sheep because ventricular myocytes and Purkinje cells are easily distinguished in this species (Canale et al., 1986).
To avoid the potentially confounding effects of any regional variability during development, all tissue was
obtained from a constant location, the right ventricular
septomarginal (moderator) band, a well-defined structure composed of a discrete bundle of Purkinje cells
surrounded by ventricular myocytes (Truex and Copenhaver, 1947).
Tissue was obtained from 26 fetal, neonatal, and
adult Border-Leicester cross sheep. The gestation of the
sheep fetuses, in which term was 147 days, was 60 days
(n = 2), 90 days (n = l ) , 115 days (n = a), 128 days (n = 11,
and 143 days (n = 3). The lambs were studied a t 1 day
(n = 3), 3 days (n = 3), 8 days (n = 2 ) , 4 weeks (n = 31, and
Received September 23, 1988; accepted May 9, 1989.
Fig. 1. Light micrograph of cross section through the septomarginal band of a 90-day-old sheep fetus showing the central artery (A),
the working myocardium (M) partitioned by connective tissue septa,
and the peripheral Purkinje bundle (P). x 180 Inset: Light micrograph of Purkinje strands from a 60-day-old sheep fetus, separated by
loose connective tissue and interspersed with capillaries. x 580.
16 weeks of age (n = 3). The adults comprised non-pregnant ewes aged 2-3 years ( n = 3 ) .
chiocephalic trunk and the aortic arch to isolate the
coronary vasculature from the rest of the circulation
(Smolich et al., 1984). The coronary circulation was
cleared of blood at the previously measured mean arterial blood pressure with a compound sodium lactate
solution containing sodium heparin (50-100 IU/ml),
potassium chloride (50 mEq/L) and sodium bicarbonate
(to pH 7.4). The heart was then fixed a t the same pressure for 10-15 min by retrograde aortic perfusion of 2%
paraformaldehyde and 2% glutaraldehyde in either 0.1
M phosphate or 0.1 M sodium cacodylate buffer. At the
end of the perfusion fixation, the entire septomarginal
band was excised from the right ventricle and immersed in the primary fixative for a further 1-4 h.
Each septomarginal band was subsequently cut perpendicular to its long axis into segments 1-2 mm in
length. These were post-fixed in 1%Os04 in 0.1 M
phosphate or 0.1 M sodium cacodylate buffer for 1 hr,
dehydrated in a graded series of acetone and embedded
in Epon-Araldite.
Transverse semi-thin sections of the septomarginal
band were cut with glass knives, stained with 1%methylene blue, and examined with light microscopy. The
tissue blocks were then trimmed and silver-gold thin
Tissue Fixation and Preparation
The lambs and ewes (both pregnant and non-pregnant) were anesthetized with intravenous sodium thiopentone (30 mg/kg) and artificially ventilated with
room air through a tracheostomy. Anesthesia was
maintained by additional intravenous doses of alphachloralose (30 mg/kg), a s required. The head and thorax of the fetal sheep were exteriorized through a maternal midline abdominal incision.
After exposure of the heart through a median sternotomy, a catheter attached to a gravity-fed perfusion
apparatus was inserted into a n umbilical artery in the
60 day fetuses and into the brachiocephalic artery in
all other animals. Arterial blood pressure was measured through a side-arm of the same catheter with a
strain-gauge transducer connected to a physiological
recorder. At the beginning of the fixation procedure,
KC1 was injected into the left atrium to arrest the heart
in diastole. The right atrial appendage was incised to
provide a n outflow tract, and, in animals other than
the 60 day fetuses, snares were applied around the bra-
Fig. 2. Light micrograph of the boundary between the working myocardium and Purkinje bundle in
a 1-day-old lamb. Capillaries of the Purkinje bundle are embedded in dense, collagenous connective
tissue and occur at variable distances from the Purkinje strands. Note the lymphatic capillaries ( t ),
arteriole (A), and venule (V). X 500.
sections cut on a Cambridge Huxley ultramicrotome
with diamond knives. The thin sections were stained
with methanolic lead citrate followed by uranyl acetate
and examined in a Philips 400T transmission electron
Structure of the Septomarginal Band
The general architecture of the septomarginal band
was similar a t all ages examined (Fig. 1).The core of
the septomarginal band contained one, or sometimes
two, small to medium-sized arteries which were often
flanked by several small veins. Smaller arterial
branches and venous tributaries were present in connective tissue septa which radiated out from the central part of the septomarginal band. The bulk of the
septomarginal band was composed of myocytes interspersed with abundant capillaries. Purkinje cells were
situated in a well-defined peripheral bundle which was
usually located just beneath the endocardium or, less
frequently, within the substance of the working myocardium. Small arterioles and venules were often embedded within the connective tissue delimiting the periphery of the Purkinje bundle (Fig. 2).
Capillary Morphology
Purkinje bundle vascular capillaries
Throughout the period of development studied, most
vascular capillaries within the transversely sectioned
Purkinje bundle were circular in outline. In 60- and
90-day-old fetuses, the capillaries of the Purkinje bundle were situated within loose connective tissue which
enveloped the constituent Purkinje strands. The relationship between these capillaries and adjacent Purkinje cells was quite variable. Although some were
closely apposed to Purkinje cells, the majority were
separated from them by a distance which ranged between 1.5 and 6 pm (Fig. 1).By 115 days in utero,
however, collagen and elastin fibers were a prominent
feature of the connective sheath and septa of the Purkinje bundle. Despite this change in connective tissue
morphology within the Purkinje bundle, the variable
distances observed betweeen Purkinje cells and adjacent capillaries in young fetuses persisted in the nearterm fetuses and during postnatal growth. However,
with growth of Purkinje cells after birth, capillaries
also came to lie within thin connective tissue septa
separating closely apposed Purkinje strands (Figs. 2,
Fig. 3. Light micrograph of capillaries located in tunnels within
Purkinje strands (P)of a 16-week-old lamb. In an adjacent Purkinje
strand, a capillary is evident at the bottom of a groove containing a
minimal amount of connective tissue ( T ). ~ 5 0 0Inset: Light mi-
crograph of a capillary situated a t the bottom of a deep, connective
tissue-filled groove ( t 1 in a Purkinje strand (PI from an 8-day-old
lamb. x 680
3). As well, capillary profiles were occasionally observed at the bottom of grooves within individual Purkinje strands (Fig. 3). Still later in postnatal development, capillaries, accompanied by neural elements,
were commonly found in tunnels within Purkinje
strands (Fig. 3).
phatic capillaries were easily identified with light microscopy because, unlike vascular capillaries which
were circular and devoid of blood cells and plasma, they
had a n irregular outline and were filled with a palestaining material.
Myocardial vascular capillaries
In contrast to capillaries of the Purkinje bundle, capillaries within the working myocardium were closely
apposed to myocytes at all ages examined. However, a s
in the Purkinje bundle, capillaries situated between
transversely-sectioned myocytes were generally circular in outline (Figs. 1, 2).
Capillary Ultrastructure
Purkinje vascular capillaries
At 60 and 90 days in utero, the capillaries of the
Purkinje bundle were lined by a continuous, non-fenestrated endothelium, approximately 3 pm thick in the
nuclear region and 0.2-0.7 pm thick over the remainder of the cell (Fig. 4). At 60 days in utero, endothelial
cells had few projections. Endothelial cell junctions,
which usually consisted of a n end-to-end or oblique apLymphatic capillaries
position of cell margins, were of the occluding type.
Lymphatic capillaries were not observed within the Marginal flaps were commonly observed overlying the
septomarginal band of 60-, 90-, 1 1 5 , or 128-day-old junctional region. The endothelial cell cytoplasm confetuses, but were present in the 143-day-old fetuses, tained a n abundance of synthetic organelles including
neonatal lambs, and adults. The lymphatic capillaries a prominent Golgi apparatus, a n extensive network of
were situated in the subendocardial connective tissue, rough endoplasmic reticulum and many free ribowithin the connective tissue septa separating bundles somes. Pinocytotic vesicles were observed both within
of myocytes, and at the boundary between the Purkinje the cytoplasm and a t the plasmalemma. In occasional
bundle and the surrounding myocardium (Fig. 2). Lym- sections, endothelial cells displayed multivesicular
Purkinje strands. The average frequency of fenestrae
increased strikingly from 1per 100 capillary cross sections at 115 days in utero to 1 per 23 capillary cross
sections a t 128 days and 1 per 11 capillary cross-sections at 143 days gestation. However, the average frequency of fenestrae then stabilized to between 1 per 3
and 1per 13 capillary cross sections in the lambs, and
1 per 14 capillary cross sections in adult sheep.
Myocardial vascular capillaries
Myocardial capillaries were lined by a continuous,
nonfenestrated endothelium a t all ages studied. The
ultrastructure of myocardial capillaries, including the
pericytes, was identical to that of Purkinje bundles at
60 and 90 days in utero (Fig. 7). At later ages, myocardial capillaries also underwent the general developmental changes observed in capillaries of the Purkinje
bundles but without the formation of fenestrae (Fig. 8).
Rarely, a fenestrated capillary within the connective
tissue sheath of the Purkinje bundle was closely related to myocytes of the surrounding working myocardium (Fig. 9).
Lymphatic capillaries
Fig. 4. Electron micrograph of capillary within the Purkinje bundle of a 60-day-old sheep fetus. The endothelial cells and pericyte
contain mitochondria, pinocytotic vesicles and lamellae of rough endoplasmic reticulum. The junctions between endothelial cells have a
simple morphology. The capillary basement membrane ( T ) is thin but
continuous. x 7,000
bodies and a juxtanuclear centriole. The abluminal
surface of the capillary was enveloped by a continuous
basement membrane. The basement membrane also
enclosed peripheral pericytes which contained a prominent nucleus, as well a s numerous mitochondria and
profiles of rough endoplasmic reticulum. The ultrastructure of capillaries was similar at 90 days in utero,
except that the endothelial cells also displayed many
lumina1 projections.
With ongoing development, two general changes in
capillary ultrastructure were apparent within the
Purkinje bundle. Firstly, the endothelial cells (and pericytes) became thinner and their cytoplasmic organelles less prominent. Secondly, and more importantly,
fenestrae were a constant feature of capillaries within
the Purkinje bundle after their initial observation a t
115 days in utero. The fenestrae, which were spanned
by a diaphragm, ranged from 40 to 60 nm in width and
had a similar ultrastructure within the fetal (Fig. 5)
and postnatal periods (Fig. 6). Fenestrae were only
present in very attenuated portions of the endothelial
cell and occurred either singly or in clusters of up to
four fenestrations. Fenestrae were observed both in
capillaries lying within connective tissue between
Purkinje strands and within those a t the periphery of
the Purkinje bundle. Fenestrae were also present in
capillaries situated in grooves and tunnels within
The ultrastructure of lymphatic capillaries was similar throughout development (Fig. 10). The lumen contained a fine, f locculent precipitate. The endothelium
was thin, except over the usually bulging nucleus, and
contained numerous pinocytotic vesicles but few organelles. Endothelial junctions had a variable morphology, ranging from a simple apposition to a complex
interdigitation of the cell margins. The abluminal surface was characterized by the presence of anchoring
filaments and a discontinuous basement membrane.
This morphological study of vascular and lymphatic
capillaries within the septomarginal band of the developing sheep heart has produced two main new findings.
Firstly, vascular capillaries of the Purkinje bundle are
lined by a continuous endothelium during mid- to late
gestation, but a fenestrated endothelium near-term
and throughout postnatal development. Secondly, a
feature of the postnatal maturation of the Purkinje
bundle is the appearance of vascular capillaries situated in grooves and tunnels within Purkinje strands.
Endothelial fenestrae are characteristic of endocrine
glands and those structures, such as the renal glomerulus, intestine and exocrine glands, which are involved
in either fluid production or absorption (Majno, 1965).
However, fenestrae have also been reported as a n occasional feature of capillary endothelium in many
other locations including the diaphragm and hindlimb
musculature (Korneliussen, 1975) and the extraocular
muscles (Collin, 1969). In the heart, endothelial
fenestrae have been observed in capillaries of the atrioventricular node and bundle (Weihe and Kalmbach,
1978) and in relation to catecholamine-containing cells
in the interatrial septum (Van der Zypen, 1974). However, to our knowledge, this is the first time that endothelial fenestrae have been reported in capillaries of
the ventricular portion of the mammalian conduction
Within the Purkinje bundle of the septomarginal
band, the appearance of fenestrated vascular endothe-
Fig. 5. Electron micrograph of a capillary fenestration ( T in the
Purkinje bundle of a 143-day-old sheep fetus. Purkinje cell (P).
x 11,900. Inset: Higher magnification of fenestration. x 41,100.
Fig. 6. Electron micrograph of capillary fenestrae in the Purkinjebundle of a 16-week-old lamb. Note the sometimes abrupt thinning of
the endothelial cell in the vicinity of fenestrae ( t ). Purkinje cell (P).
x 11,400. Inset: Higher magnification of fenestrae. x 49,200.
lium coincided with a n increase in the density of the
connective tissue septa and sheath. From our study, it
is unclear whether a cause and effect relationship existed between these two morphological changes. However, observations from pathological conditions (Suzuki, 1969; Hirano and Zimmerman, 1972), transplant
experiments (Campbell and Uehara, 19721, and tissue
culture studies (Milici et al., 1985) suggest that the
formation of endothelial fenestrae is modulated by the
characteristics of the pericapillary tissue. A link between connective tissue elements and the occurrence of
endothelial fenestrae in capillaries of striated muscle is
also implied by two other observations. Firstly, in the
atrioventricular node and bundle, fenestrae were more
numerous in capillaries lying within conective tissue
than in those situated between conduction cells (Weihe
and Kalmbach, 1978). Secondly, in capillaries of skeletal muscle, endothelial fenestrae occurred in the perimysial and perineural connective tissue (Korneliussen,
The average frequency of fenestrae within the Purkinje bundle of the septomarginal band of adult hearts
(1per 14 capillary cross-sections) was considerably less
than found in intestinal (Casley-Smith, 1971; Simionescu, 1983) and pancreatic endothelium (Simionescu,
1983), but greater than the incidence of 1 fenestration
per 60 capillary cross-sections reported for skeletal
muscle (Korneliussen, 1975). Moreover, our findings
indicate that this adult level of endothelial fenestra-
tion within the Purkinje bundle of the septomarginal
band was attained in utero and then maintained
throughout postnatal development.
Chronologically, the appearance of capillaries lying
in grooves within the Purkinje strands (“groove capillaries’’) preceded those lying in tunnels (“tunnel capillaries’’). This suggests that the tunnels may have
formed from apposition of the sides of preexisting
grooves rather than a s a result of direct growth of capillaries into Purkinje strands. Groove and tunnel capillaries are a characteristic feature of cardiac hypertrophy in the spontaneously hypertensive rat (Imamura,
1978) and have also been observed with marked skeletal muscle hypertrophy arising from myotonic dystrophy (Wohlfart, 1951) and exercise (Reitsma, 1973).
There are, however, two important differences between
the groove and tunnel capillaries noted in our study
and those reported by previous investigators. Firstly,
groove and tunnel capillaries observed in the Purkinje
bundle were a normal feature of postnatal development. Secondly, while tunnel capillaries described in
cardiac (Imamura, 1978) and skeletal muscle hypertrophy (Reitsma, 1973) coursed through individual muscle
cells, the boundaries of capillary tunnels within Purkinje strands of the septomarginal band were formed
by several Purkinje cells.
What is the likely functional significance of groove
and tunnel capillaries? In a companion study (Canale,
1986), we have shown that the cross-sectional area of
Fig. 7. Electron micrograph of vascular capillary from working
myocardium of a 60-day-old fetus. The ultrastructure of the endothelial cell and pericyte is similar to that of the vascular capillary within
the Purkinje bundle in Figure 4. x 8,200.
Fig. 8. Electron micrograph of vascular capillary within working
myocardium of a 16-week-old lamb. Except in the nuclear region, the
capillary endothelium is quite thin compared t o Figure 7. x 14,400.
Purkinje strands within the Purkinje bundle of the sep- (Hudlicka, 1984), are still present in muscular capiltomarginal band increases tenfold between 60 days in laries of the r a t at this time (Majno, 1965).
Our observation that the appearance of endothelial
utero and adulthood in the sheep. As this corresponds to
a more than threefold increase in the average radius of fenestrae in the Purkinje bundle antedated the formaPurkinje strands, the inevitable consequence of this tion of lymphatic capillaries in the septomarginal band
developmental hypertrophy would be a n increase in complements a similar conclusion reached in a phylothe diffusion distance for oxygen and nutrients be- genetic study of the intestinal, renal, pancreatic and
tween the periphery and interior of the Purkinje ciliary body microcirculation in the shark (Casleystrands. The formation of groove and tunnel capillaries Smith and Mart, 1970). Both local and general factors
might thus minimize this increase in diffusion dis- are likely to be implicated in the formation of lymtance. Indeed, a similar role has been proposed by phatic capillaries within the Purkinje bundle of the
Imamura (1978) for the tunnel capillaries found within sheep septomarginal band. Casley-Smith (1976) has
proposed that, particularly with fenestrated vascular
hypertrophied cardiac myocytes.
Most previous studies of the development of vascular endothelium, the presence of lymphatic capillaries is
capillaries have been performed in rat (Donahue and necessary to prevent the development of tissue edema.
Pappas, 1961; Majno, 1965; Milici and Bankston, 1981; Furthermore, the progressive rise in fetal arterial
Van Diest and Kanan, 1979). A comparison of our find- blood pressure, especially in the last quarter of gestaings with these studies suggests that the general fea- tion in the sheep (Dawes, 19681, might result in a
tures of capillary development in r a t and sheep are greater movement of macromolecules and solutes into
similar. However, important species differences appear the perivascular space.
to exist at the level of maturation of capillary ultrastructure in the fetal and neonatal periods. In the
sheep, for example, occluding junctions without gaps
and a complete basement membrane were present twoWe thank John Cannata, Andrew Pearson, Julie Saffifths of the way through gestation. By contrast, the strom, and Simone Young for their technical assisbasement membrane in rat capillaries is only fully de- tance. We are also grateful t o Dr. Adrian Walker from
veloped a t birth (Hudlicka, 19841, while gaps between the Centre for Early Human Development, Monash
endothelial cells, a feature of embryonic capillaries University, for access to tissue specimens.
Fig. 9. Electron micrograph of a capillary, located adjacent to ventricular myocytes in a 16-week-old lamb, which contains endothelial
fenestrae ( T ). x 6,500 Inset: Higher magnification of fenestrated region. x 35,500.
Fig. 10. Electron micrograph of lymphatic capillary from adult
sheep showing the generally thin endothelium and flocculent contents within the lumen (L). x 5,700. Inset: Higher-power micrograph
of lymphatic capillary showing endothelial flap overlying a simple
junction, the discontinuous basement membrane ( t ), and anchoring
filaments (F). x 16,000.
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development, band, capillaries, working, morphology, vascular, purkinje, myocardial, septomarginal, sheet, lymphatic, bundles
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