(Circulation. 1995;91:1790-1798.)
© 1995 American Heart Association, Inc.
Articles |
Capillary Distribution in the Ventricles of Hearts With Pulmonary Atresia and Intact Ventricular Septum
From the Department of Anatomy and Embryology, University of Leiden, The Netherlands (P.W.O., A.C.G.); the Department of Anatomy and Embryology, University of Amsterdam, The Netherlands (P.W.O., A.F.M.M.); and the Klinik für Herz und Kreislauferkrankungen, Deutsches Herzzentrum München, Germany (U.S.).
Correspondence to Prof Dr A.C. Gittenberger-de Groot, Department of Anatomy and Embryology, PO Box 9602, 2300 RC Leiden, The Netherlands.
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Abstract |
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Background Pulmonary atresia and intact ventricular septum (PA-IVS) can be complicated by the presence of a severely hypoplastic thick-walled right ventricle with or without ventriculo–coronary arterial communications. A variable amount of myocardial pathology has been described in these hearts, probably the result of ischemic conditions and a high pressure in the right ventricle. We studied whether the capillary network is still intact, allowing a sufficient perfusion of the myocardium, which will be important for the success of palliative surgery.
Methods and Results We studied the distribution of capillaries in the myocardium of hearts with PA-IVS and compared the results with normal hearts. The capillaries were detected by immunohistochemistry using a monoclonal antibody (408) against endothelium. Remarkable abnormalities in capillary distribution were found in the right ventricle of hearts with PA-IVS and reflect the arrangement of the myocytes. Thus, disorganization of capillaries, which is found to be the most common pattern, always paralleled the myocardial disarray. A low density of capillaries is always found in areas with a low density of myocytes, ie, with hypertrophied myocytes, compact fibrotic tissue, or diffuse fibrosis. Disarray and other disturbances in orientation of capillaries and myocytes are present in hearts with PA-IVS, a hypoplastic right ventricle, and ventriculo–coronary arterial communications. These disturbances are more extensive when interruptions of the coronary arteries are also present. In hearts with PA-IVS and a hypoplastic right ventricle only, extensive regions with low capillary densities and severe myocyte pathology are observed. On the contrary, hearts with PA-IVS and a normal-size right ventricle show minor abnormalities in capillary and myocyte organization.
Conclusions In hearts with PA-IVS, various abnormal capillary distribution patterns are found. Our findings correlate well with clinical data that reported the best surgical results in hearts in which the major part of the myocardium showed a normal capillary distribution and myocyte morphology. This suggests that the capillary distribution may be an important parameter for the function of the heart. Because the distribution of the capillaries is found to be a good reflection of the arrangement of the myocytes, antibody 408 is also a useful tool in detecting abnormalities of the myocardium in a fast and easy way.
Key Words: pulmonary heart disease • capillaries • myocardium
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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Myocardial pathology has been demonstrated in the right ventricle of hearts with pulmonary atresia and intact ventricular septum (PA-IVS) by use of histological staining methods and light microscopy.1 2 3 4 5 6 Gittenberger-de Groot et al5 studied the pathology of the myocardium by classic histology in hearts with PA-IVS. By cineangiocardiography, these hearts were divided into three groups: (1) hearts with a hypoplastic right ventricle and large ventriculo–coronary arterial communications (VCACs); (2) hearts with a hypoplastic right ventricle, VCACs, and interrupted epicardial coronary arteries; and (3) hearts with a hypoplastic right ventricle only. In this third group of hearts, myocardial sinusoids are present, defined as intramyocardial vascular spaces continuous with the right ventricular lumen and connected via a capillary bed in the myocardium with the epicardial coronary arteries.5 Myocardial pathology was most obvious in hearts with a hypoplastic right ventricle only and less severe in hearts with a hypoplastic right ventricle and VCACs.5
The surgical outcome of hearts with PA-IVS is variable. In hearts with PA-IVS and VCACs, the outcome is determined by the dependency of myocardial blood supply on these communications.7 8 9 When obstructions of the coronary arteries or severe hypoplasia of the right ventricle is present, more problems are to be expected.10 11 12 13 14 15 16 17
To gain more insight into the factors that might be involved in the survival of patients, we extended our study on the histology of the myocardium. In the present article, we describe the distribution of capillaries in the hearts used in the above-mentioned study5 by immunohistochemical techniques that are now often used in pathology.18 However, the antibodies against endothelium thus far described18 do not react in hearts from pathology collections, ie, after various fixation procedures and long storage times. To identify the capillaries in malformed hearts, we developed a novel monoclonal antibody specific for endothelium of the capillaries, to be used on tissue sections of freshly obtained human hearts and hearts from pathology collections as well.
In addition, we studied the myocardium and the capillary distribution in hearts with PA-IVS having only a slightly hypoplastic right ventricle. Present-day surgical techniques are sufficient for a successful repair of the hearts of this group, and we wondered whether capillary and myocardial pathology is less obvious in these hearts.
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Methods |
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Heart Specimens
Twelve hearts with PA-IVS were selected from the collection of the Department of Anatomy and Embryology, University of Leiden, The Netherlands, and the Deutsches Herzzentrum, Munich, Germany, for immunohistochemical study of the capillaries. A number of these hearts were previously described,4 5 and we used the same specimen numbers (Table 1
).
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On the basis of
cineangiocardiography and histology, the hearts were
distinguished into four groups (Table 2 and Fig
1): (1) hearts with a hypoplastic right ventricle and
VCACs (cases 1 through 5); (2) hearts with a hypoplastic right
ventricle, VCACs, and interrupted coronary arteries (cases 7 and 8);
(3) hearts with a hypoplastic right ventricle only (cases 14 and 15);
and (4) a group composed of hearts with PA-IVS and an approximately
normal-size right ventricle (cases 17 through 19). Furthermore, an
age-matched set of seven normal human hearts was studied.
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Tissue blocks
of the myocardium, including the endocardium and the
epicardium, were taken from the right ventricular free wall, the left
ventricular free wall, and the ventricular septum (Fig 1
). In
an
initial morphological study (Gittenberger-de Groot et
al5 ), tissue blocks were sampled at expected sites of
fistulas on the basis of clinical angiographic data. For the
present research, adjoining blocks were taken. Because of the small
size of the right ventricle of some hearts, there were limitations to
the material taken, and the entire right ventricle was serially
sectioned. The left ventricular wall samples were taken from the free
left ventricular wall in the heart. The blocks were rinsed and
dehydrated in alcohol, embedded in paraffin, and sectioned at 5 µm
perpendicular to the long axis of the heart.
Immunohistochemistry
For visualization of the capillaries, we
used an
anti-endothelial mouse monoclonal antibody (408) especially produced
for use on human hearts that had been extensively fixed and stored for
a long time.
In some hearts, immunoreactivity of antibody 408 was enhanced by pretreatment of the sections for 10 minutes in water at 100°C in a microwave (Biorad)19 or for 15 minutes with proteinase K (1 mg/mL PBS, pH 7.4, 20°C), according to Christensen and Strange.20 Overnight incubation with antibody 408 was followed by incubation with rabbit anti-mouse immunoglobulin (noncommercial) and goat anti-rabbit immunoglobulin (noncommercial). Binding of the antibodies was visualized by incubation with a rabbit peroxidase-antiperoxidase complex (Nordic), with 3,3'-diaminobenzidine as a substrate. After each incubation step, the sections were washed in PBS, pH 7.4. This method is based on Sternberger21 and described in detail by Wessels et al.22
Serial sections were stained with hematoxylin-eosin tissue stain or a modified van Gieson elastic tissue stain.
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Results |
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Capillary Distribution in Normal Neonatal Hearts
In both the left and the right ventricles of normal neonatal human hearts, a homogeneous distribution of capillaries and myocytes in the myocardial wall was observed, reflecting a regular stacking pattern and a parallel arrangement of capillaries and myocytes (Fig 2
).
In line with a study in the adult
heart,23 24 we observed layers of myocyte orientation
in
the neonatal heart. Because the myocytes and capillaries are aligned in
parallel, the orientation of the myocytes could now be nicely
demonstrated by the immunohistochemical staining of the capillaries. In
the subendocardial and subepicardial layers, the capillaries and
myocytes were oriented parallel to the long axis of the heart. Between
them, a layer of capillaries and myocytes oriented concentric to the
ventricular lumen was present. In the right ventricular free wall
of some hearts, only two layers of capillary and myocyte orientation
were observed, the subepicardial layer being composed of capillaries
and myocytes oriented concentric to the right ventricular lumen (Fig
3a).
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Capillary Patterns in Hearts With Pulmonary Atresia and Intact
Ventricular Septum
The capillary and myocyte distribution in the left
ventricle of
hearts with PA-IVS was comparable to that in the normal hearts (not
shown). Also, in the hearts of cases 7 and 8 (with interrupted coronary
arteries), we did not observe abnormalities in the left ventricle. The
distribution in the subepicardial layer of the right ventricle could be
compared with that in normal hearts. However, in the subendocardial
part of both the right ventricular free wall and the right ventricular
septum, abnormal capillary and myocyte distribution patterns were found
with variable extensions toward the midmyocardial layer (Fig
3b). The
right ventricular septum and the right ventricular free wall were not
always equally affected within one heart. (See Table 2.)
The abnormal patterns were localized in distinct regions, often sharply bordered. Thus, normal and various abnormal capillary distribution patterns were present within one tissue section, allowing a good comparison of the various patterns. Abnormalities in capillary distribution were found only in regions in which the distribution of myocytes was also abnormal. A correlation was present between the distributions of myocytes and capillaries, eg, the intercapillary distance and myocyte diameter were correlated, and the orientation of capillaries was parallel to that of the myocytes. Thus, by use of the immunohistochemical staining method for capillaries, the pathology of the myocytes could also be easily detected. Five basically different abnormal patterns were distinguished, which could be defined as follows.
Disarrayed capillaries. Capillaries bending in
all
directions and making many cross-bridges formed the most frequently
found abnormal distribution pattern (Fig 4a). The
capillaries had the same orientation as the disarrayed myocytes (Fig
4b). In accordance with this, the distribution of capillaries
was
called disarrayed.
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Large intercapillary distances, myocyte hypertrophy.
Large
intercapillary distances were present between hypertrophied
myocytes. In these regions, the distribution of capillaries was
somewhat less homogeneous than in the normal myocardium (Fig 5a
and 5b). Hypertrophied myocytes were found primarily next to
regions of compact fibrosis or diffuse fibrosis (Fig 5c through
5f).
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Large intercapillary distances, fibrosis. Only few
capillaries were found in regions of fibrosis with compact connective
tissue encircling myocytes with a normal morphology. When only few or
even no myocytes were present, capillaries were completely lacking.
Fibrosis was found mainly subendocardially, which is called endocardial
fibroelastosis (EFE). It could also be found around VCACs (Fig
3b, 3c, and 3d) or around
myocardial sinusoids (Fig 5a through 5d).
Large intercapillary distances, diffuse fibrosis. In
some
areas, a diffuse fibrotic network was observed superimposed on
degenerating myocytes. In these areas, few capillaries with an
irregular distribution were present. Furthermore, isolated
endothelial cells and swollen, wide-open vessels were observed. This
pattern was found only deep in the myocardial wall (Fig 5e and
5f).
Small blood sinuses. In the
endocardial layer of some
hearts, small blood sinuses were found aligned by one layer of
endothelial cells (Fig 6). The small blood sinuses
surrounded the individual or clustered, hypertrophied myocytes and gave
the myocardium a spongelike appearance (Fig 6b). The difference
between
a myocardial sinusoid and small blood sinus is visible in Fig
7a, as demonstrated by the aid of antibody 408.
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Hypoplastic Right Ventricle With VCACs Present
Disturbances
in capillary and myocyte distribution were found in
the subendocardial layer of the right ventricle of these hearts of
group 1 (Table 2). In the heart of case 4, the capillary
pattern was
more seriously affected compared with the other hearts of this group
(Fig 3b through 3d).
Hypoplastic Right Ventricle With VCACs and Interrupted Coronary
Arteries Present
In this group of hearts (group 2), disturbances in
capillary and
myocyte orientation were found in the subendocardial and midmyocardial
layers of the right ventricle. Thus, the abnormal regions were more
extensive compared with group 1 (Table 2).
Hypoplastic Right Ventricle Without VCACs
In the hearts of
this group (group 3), the endocardial and
midmyocardial layers of the right ventricle contained abnormal
capillary patterns. Not only disturbances in orientation but also low
capillary densities and degenerating myocytes were obvious (Table
2,
Figs 5 and 7).
Normal-Size to Slightly Hypoplastic Right Ventricle
In these
hearts (group 4), only some disturbances in orientation
of the capillaries were observed to be present in the
subendocardial layer of the right ventricle. In all these hearts, minor
to serious EFE was present (Table 2 and Fig 8).
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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This study demonstrated that various abnormal capillary patterns are present in hearts with pulmonary atresia and intact ventricular septum that are not, or only occasionally, found in normal hearts. The extent of the regions with abnormal capillary arrangements varies between hearts with different complications in right ventricular or coronary vessel morphology.
Abnormal capillary patterns are found exclusively in areas that show pathology of the myocytes, while the morphology of the individual capillaries might still be intact. Moreover, ultrastructural studies have demonstrated that damage of the capillaries is always preceded by damage of the myocytes.25 We presume that in pathological myocardium, the distribution of the capillaries is determined by the distribution of the myocytes: the intercapillary distance is dependent on the diameter of the myocytes, and the capillary orientation parallels that of the myocytes. Thus, the capillary distribution, which can be detected by use of antibody 408, is a perfect reflection of the arrangement of the myocytes. Therefore, antibody 408 will be very useful in studies on the microarchitecture of the myocardium to detect pathology of the myocardium.
Abnormalities in capillary distribution and myocardial pathology are observed only in the endocardial part of the right ventricular myocardium, in line with the observations of O'Connor et al,6 who described myocardial pathology in these regions. We did not find abnormalities in the left ventricle, in agreement with A.E. Becker (personal communication; see "Note Added in Proof"), who observed no remarkable abnormalities in the amount of connective tissue in the left ventricles of hearts with PA-IVS. These results suggest that, although the coronary blood supply to the left ventricle might be changed, it is functionally not disturbed.
In the right ventricle, large areas of myocardial pathology and abnormal capillary distribution patterns are observed. These abnormal areas are already present shortly after birth, suggesting that the pathology must have developed before birth. Presumably, the abnormalities are the result of the high blood pressure in the right ventricular lumen that develops as a result of the atretic pulmonary trunk. It is known that small blood sinuses and hypertrophy26 can develop as a result of high blood pressure. In hearts with VCACs, the blood pressure never reaches levels that are seen in hearts without communications.5 However, both patterns are found in hearts with or without VCACs. Human fetal studies suggest that pulmonary stenosis may progress to complete atresia at various times.27 The stage of development of the heart at the moment of complete atresia may affect the degree of myocardial pathology as well as the capillary distribution pattern. PA-IVS with a competent tricuspid valve will result in high blood pressure in the right ventricle. The high blood pressure will result in myocardial sinusoids and subsequent EFE formation. This mechanism is also described for the hypoplastic left heart syndrome.28 It is not known whether some myocardial sinusoids can develop into VCACs, thus relieving the high right ventricular blood pressure. The mechanism of VCAC formation in the embryo is not understood. However, it is not very likely that the VCACs are persistent embryonic structures, since these structures were not found in the developing heart.29
Hypertrophied myocytes and large intercapillary distances are found next to areas of diffuse fibrosis in the hearts with PA-IVS and might be a kind of compensatory hypertrophy to replace the degenerating myocardium30 as well as a result of the high blood pressure. The myocyte hypertrophy cannot be related only to normal growth of the heart, since a normal regular distribution of capillaries and enlarged intercapillary distances are found within one tissue section.
EFE might also be the result of high blood pressure in the right
ventricle.31 EFE was observed in the right ventricles of
all hearts without VCACs and in some hearts with VCACs, in line with
Gittenberger-de Groot et al.5 This proves that the
presence of EFE is not restricted to hearts with a hypoplastic left
heart, as was previously suggested.28 The presence of EFE
on the left ventricular surface of the septum of case 18 with an
adequate-size right ventricle and no right ventricular coronary
arterial communications is remarkable (Table 2).
The most normal capillary patterns are present in hearts with PA-IVS without further abnormalities of the right ventricle or the coronary arteries. In these hearts, the pulmonary trunk obstruction probably developed late during fetal life, at least after development of the semilunar valve leaflets, since these were fully developed but fused to each other. This might explain the fact that the right ventricle is more adequate in size and that myocardial pathology is not obvious. Because of the availability of prostaglandins and improved surgical techniques, these hearts can now be successfully operated on,8 indicating at least that slight abnormalities in capillary pattern are not lethal.
Our previous clinical experience has demonstrated a correlation between the degree of pathology of the subepicardial coronary arteries and the extent of right ventricular pathology.4 5 This present study demonstrates a similar correlation between the degree of microvascular abnormalities and the underlying right ventricular and coronary artery pathology. Comparison with literature data indicates that the capillary distribution is most disturbed in hearts with a bad prognosis after surgery, ie, hearts with serious right ventricular and coronary artery pathology.4 5 7 8 12 14 15 However, it is not quite certain which factor determines survival after surgery. Because all the patients died during or shortly after surgery, the operation itself, as well as the capillary distribution pattern or the right ventricular and coronary artery pathology, might have contributed to this fatal outcome. A careful study of the capillary pattern in fetal hearts as well as in those initially surviving surgery would provide important information on the relation between capillary distribution and function of the heart.
Physiological experiments in animals have demonstrated that the capillary pattern, also present in the normal human heart, is essential for optimal tissue oxygenation. Important parameters are the intercapillary distance and the parallel alignment of capillaries and myocytes.32 33 34 Studies in rats showed that enlarged intercapillary distances between hypertrophied myocytes result in a decrease of the capillary reserve,35 36 37 and thus, an increased chance of hypoxia in case of high oxygen demand is present in these hearts.38 However, physiological data for the human heart are not available, and although it can also be presumed that in human hearts with PA-IVS, tissue oxygenation will be disturbed in case of enlarged intercapillary distances or other abnormal capillary patterns, more research is essential.
It would be very useful if in vivo detection methods were to be developed for functional studies of the microvascularization in the myocardium that can be coupled to the descriptions of the various capillary distribution patterns. Animal models can be developed to study the various capillary patterns, as has already been done for the hypertrophied myocardium.35 36 37 The advances made with the technique of positron emission tomography in adult human hearts39 40 might be a promising diagnostic tool for future use in pediatric cardiac disease in humans. Information on tissue oxygenation in relation to the capillary distribution pattern as well as on regeneration or restoration of the capillary bed after right ventricular decompression might help in predicting whether the right ventricle is likely to grow to a normal size and function.
Note Added in Proof
Observations of Dr Becker have been
published since this article
was written.41
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Acknowledgments |
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This work was financially supported by research grant 88.093 from The Netherlands Heart Foundation. We would like to thank Carol Verhoek and Leonie Pronk for their technical assistance. Cars Gravemeijer and Jan Lens are acknowledged for their excellent photography.
Received July 21, 1994; revision received October 6, 1994; accepted October 30, 1994.
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