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Normal variations in the relationship of the tricuspid valve to the membranous septum in the human heart.

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THE ANATOMICAL RECORD 226~258-263(1990)
Normal Variations in the Relationship of the
Tricuspid Valve to the Membranous Septum in the
Human Heart
ANGEL0 RESTIVO, AUDREY SMITH, JAMES L. WILKINSON, AND
ROBERT H. ANDERSON
Institute of Child Health, University of Liverpool, Royal Liverpool Children’s Hospital
Alder Hey, Liverpool (A.R., A S . , J.L.W.) and Department of Paediatric Cardiac
Morphology, Cardiothoracic Institute, Brompton Hospital,
London SW3 6HP (R.H.A.), England
ABSTRACT
The anatomy of the antero-septal commissure of the tricuspid
valve and its relationship to the membranous part of the septum are described in
72 normal hearts from subjects ranging in age from 25 weeks gestation to 13
months. Three major patterns were found. According to whether the contiguous
leaflets were fused at the commissure, joined at the circumference of the orifice, or
left a gap at the commissural site, the varieties are described as undivided, annular, or gap commissure, respectively. Commissures of annular type showed further
morphological varieties, as did the patterns of division of the membranous septum
into its atrioventricular and interventricular components. Dominance of the atrioventricular component andtor absence of the interventricular membranous septum
were encountered in 38 cases out of 72 (52%). This finding demonstrates that
dominance of the atrioventricular membranous septum during fetal life and infancy is not universal. The variability noted in the morphology and position of the
antero-septal commissure was not associated with other positional variations of
the tricuspid valve.
The morphology of the membranous septum of the
heart is well described, particularly its division into
atrioventricular and interventricular components by
the attachment of the septal leaflet of the tricuspid
valve (Walmsley, 1930; Odgers, 1938). The relationship of the commissure between the septal and anterosuperior leaflets and the membranous septum has also
been investigated in the normal heart (Rosenquist and
Sweeney, 1975). No correlation was produced in this
report, however, between the individual arrangements
of the antero-septal commissure and the various divisions of the membranous septum into its atrioventricular and interventricular components. This is significant because it has been suggested (Allwork and
Anderson, 1979) that the greater number of infant
hearts possess only a n atrioventricular component to
the membranous septum, formation of the interventricular part (if, indeed, it is formed a t all) being a postnatal event. To cast further light on these relationships, we have investigated this area in a large number
of fetal and infant hearts.
MATERIALS AND METHODS
Seventy-two hearts from the anatomy collection of
the Institute of Child Health, Royal Liverpool Children’s Hospital Alder Hey, University of Liverpool,
were studied in order to investigate the normal variations in the relationship of the tricuspid valve and the
membranous septum. This series of specimens covered
ages ranging from the 25th week of gestational life to
the 13th month of postnatal life. The most common
0 1990 WILEY-LISS, INC
causes of death amongst live-born infants were bronchopneumonia, brain haemorrhage, hyaline membrane disease, pulmonary haemorrhage, and septicaemia. The specimens had been fixed in 10% formalin,
and the hearts had been opened in the conventional
way. After a preliminary investigation of the intact
tension apparatus of the tricuspid valve, the tendinous
cords were cut in order to facilitate examination of the
area of the membranous septum. Transillumination
was obtained when necessary by a fibre optic light.
DEFINITION OF TERMS
Anfero-Septal Commissure
A commissure, in literal terms, is simply the junction
between two leaflets. In the case of the atrioventricular
valves, this meeting point is conventionally considered
at the level of the atrioventricular junction. The concept of a valve commissure in functional terms, however, can be expanded to include the proximal portions
of the apposing free edges of the leaflets. The most
proximal portions of adjacent leaflets usually share
common support (Goor and Lillehei, 1975). Some have
identified this common support as a fan-shaped cord
(Silver et al., 1971). They have used the feature for the
Received July 20, 1988; accepted April 28, 1989.
Address reprint requests to Dr. Audrey Smith, Institute of Child
Health, University of Liverpool, Royal Liverpool Children’s Hospital
Alder Hey, Eaton Road, Liverpool, L12 2AP England.
TRICUSPID V A L V E AND M E M B R A N O U S SEPTUM
septal
t
259
parietal
Membranous Septum
5
I
septai
I
//(
TV
-
I
or inferior I/
Undivided commlssure ( 4 5 )
Annular commlssure ( 2 5 )
Commiruural Gap ( 2 )
Fig. 1. Diagrammatic representation of the three main patterns (undivided, annular, and gap) of the
antero-septal commissure of the tricuspid valve. Compare with Figure 2a-c.
identification of a commissure. They also found, however, that fan-shaped cords are not universally present
in commissures of the tricuspid valve. Then other landmarks need to be used. Our study demonstrated three
distinct patterns at the antero-septal commissure of the
tricuspid valve (Fig. I), none of which was supported by
a discrete fan-shaped cord. The first is represented by
circumferential continuity together with variable fusion of the free edges of the septal and the antero-superior leaflets toward the centre of the valve orifice. We
have called this an “undivided commissure,” its most
distinctive feature being the fusion of the free edges of
the apposing leaflets. The second pattern (Fig. 1)shows
continuity of the leaflets only at the circumference of
the orifice without anatomic fusion oftheir adjacent free
edges. We have described this arrangement as an “annular commissure.” The third pattern is characterised
by discontinuity between the septal and the anterosuperior leaflets at the atrioventricular junction and is
described as a “commissural gap.”
In the latter (12 hearts), the commissural apex was
located a t the inferior aspect of the membranous septum. The septal leaflet had no attachment to the membranous septum but was attached exclusively to the
inlet septum, the antero-superior leaflet bisecting the
membranous septum. This arrangement produced a
small anterior interventricular and a large atrioventricular portion to the membranous septum (Fig. 2d).
In 20 hearts (28%),the membranous septum was divided almost equally into atrioventricular and interventricular components. The commissure was undivided in 17 of these hearts, being of the annular variety
in the remainder. In those hearts with an undivided
commissure, its apex (the junctional point a t annular
level between the antero-superior and the septal leaflets) was located centrally in the membranous septum
(Fig. 3a). When the commissure was of the annular
type, its apex lay anteriorly at the corner between the
posterior edge of the supraventricular crest and the
right atrial wall (Fig. 3b).
Dominance of the interventricular membranous sepRESULTS
tum was seen in eight hearts (11%).
The commissure
The results are summarised in Table 1,which shows was undivided in all cases (Fig. 4a). The atrioventricthe relationships between five arrangements of the ular component of the membranous septum was lackmembranous septum and the three patterns for the an- ing in six specimens (8%).In all of these, the commistero-septal commissure of the tricuspid valve. There sure was again undivided, the attachment of the
was no apparent correlation between these morpholog- leaflets of the tricuspid valve roofing the superior edge
of the membranous septum (Fig. 4b).
ical findings and age.
In 14 hearts (19%)no interventricular membranous
Among the 45 specimens showing an “undivided’
septum was identified. In two of these, the commissure commissure, 32 (71%) had a flap of fibrous tissue exwas undivided (Fig. 2a). In a further ten cases, the tending from the ventricular aspect of the conjoined
commissure was of the annular type, the antero-supe- leaflets along the interventricular membranous seprior and the septal leaflets meeting at the caudal end of tum to the border of the inlet septum (Fig. 3a). A raphe
the membranous septum (Fig. 2b). A commissural gap was occasionally identified on the atrial aspect of the
valvar tissue. This raphe extended from the point of
was present in the other two hearts (Fig. 2c).
Cases in which the atrioventricular membranous junction of the leaflets to the circumference of the
septum was dominant (24 hearts, 34%) were associated valve orifice and corresponded with the line of inserwith commissures of the undivided and annular types. tion of the flap seen on the ventricular aspect.
260
A. RESTIVO ET AL
TABLE 1. Anatomy of the membranous septum related to anatomy of antero-septal commissure
of the tricuspid valve (72 cases)'
Division
of MS
AV
AV > IV
AV = IV
IV > AV
IV
Total
Undivided
Cases
Age range
2
12
17
8
6
45
29140 -311 2
28140-12112
26140-4112
34140-3112
291'40-6112
Antero-septal commissure
Annular
Cases
Age range
10
12
3
0
0
25
Cases
27140-10112
25140-12/12
26140-35140
'MS = membranous septum; AV = atrioventricular; IV = interventricular; > = dominance; 40
in months.
2
0
0
0
0
2
=
Gap
Age range
33140-15 days
Total
14
24
20
8
6
72
ovulation age in weeks; 12 = postnatal age
Fig. 2. a-c: Show, respectively, the presence of a n exclusively atriventricular membranous septum with (a) undivided, (bj annular
(arrow),and (c) gap (arrow)commissures. The arrow in a indicates the
membranous septum. d: Shows atrioventricular dominance of the
membranous septum with a small anterior interventricular component (superior arrow) and an annular commissure (inferior arrow).
The important feature in these photographs of tiny foetal and neonatal hearts is the anatomy ofthe membranous septum. This has been
demonstrated by using a strong light source behind the specimen. In
experimenting with the lighting, it was found that stronger overhead
lighting, which enhanced the details of the surrounding anatomical
features, only served to reduce the impact of the transilluminated
light. The position of the surrounding anatomical structures has been
indicated thus for the purposes of orientation only. a, anterosuperior
leaflet; AV, atrioventricular; I, inlet septum; ra, right atrium; rv,
right ventricle; s, septal leaflet; TV, tricuspid valve.
A standard chi squared test for contingency tables
was performed on data (presented in Table l), which
related the anatomy of the membranous septum to that
of the antero-septal commissure of the tricuspid valve.
The results were significant (chi squared = 32.15 compared with chi squared on eight degrees of freedom =
TRICUSPID VALVE AND MEMBRANOUS SEPTUM
261
Fig. 3. a: Shows a balanced membranous septum with an undivided commissure. The arrow indicates
the fibrous flap on the interventricular aspect of the membranous septum. b Shows another balanced
membranous septum with an annular commissure (arrow) located anteriorly. ra, right atrium; rv, right
ventricle; TV, tricuspid valve.
Fig. 4. a: Shows interventricular dominance of the membranous septum with undivided commissure.
b Represents the situation where only an interventricular membranous septum (arrow) is present. ra,
right atrium; rv, right ventricle; TV, tricuspid valve.
15.51) in that the annular type of commissure tended to
be more common when the atrioventricular component
of the membranous septum predominated. The absolute numbers, however, show six nil values, indicating
that the usual chi squared test must be regarded as
conservative in claiming the significant association.
structure. Figure 5 illustrates diagrammatically the
five arrangements of the membranous septum as we
encountered them demonstrating both of these extreme
situations and the spectrum in between. These differences are self-evidently related to the point of attachment of the leaflets of the tricuspid valve across the
fibrous part of the septum. It is important to emphaDISCUSSION
sise, therefore, that our study was performed only on
It is well recognised (Walmsley, 1930; Odgers, 1938) hearts from fetuses and infants. In this respect, it conthat, in most human hearts, the membranous portion firms to some extent the previous study of Allwork and
of the septum is divided into atrioventricular and in- Anderson (19791, since it shows that the septum is preterventricular components. Our study has shown, how- dominantly an atrioventricular structure at that phase
ever, that this is not universally the case. In some in- of growth. Unlike the material of Allwork and Anderstances (10% out of our series), the membranous son (1979), however, some of our specimens had an exseptum was exclusively atrioventricular in position, clusively interventricular septum even at these stages.
while in others (8%)it only formed an interventricular It remains the case that existence of the interventric-
A. RESTIVO ET AL.
262
(8)
(24)
Domlnant lnterventrlcular
A
A
Excluslvely atrloventrlcular
(14)
Balanced
Exclusively lnterventrlcular
(20)
(6)
Fig. 5. Diagrammatic illustration of the anatomic divisions of the membranous septurn (exclusively
and dominant atrioventricular, balanced, and dominant and exclusively interventricular).
ular component is dependent upon the relationship of
the attachment of the leaflets of the tricuspid valve to
the fibrous skeleton. The precise mechanism determining this event and its timing during development cannot be answered by our investigation.
Our study has also shown marked variability in the
structure and position of the antero-septal commissure
of the tricuspid valve. Statistical analysis demonstrated significant correlation between the anatomy of
the commissure and the status of the membranous septum. Although this significance must be regarded conservatively, the values obtained show that the annular
type of commissure tends to be more common when the
atrioventricular component is predominant.
The commissural variant described by us in terms of
undivided and annular commissures along with the
commissural gap had been previously recognised by
Rosenquist and Sweeney (1975), although they did not
comment on their significance. In this respect, it should
be noted that, previously, our group has defined the
antero-septal commissure of the tricuspid valve as being “round the corner” from (or anterior to) the membranous septum (Smith et al., 1986),this being proportionately the greater area of valve supported directly by
the medial papillary muscle (of Lancisi) and a significant portion of the antero-septal commissure in systole.
Our present study suggests that this is not always true.
The antero-septal commissure is directly related to the
membranous septum, a s has been stated by the Toronto
group (Silver et al., 19711,but our present findings show
t h a t its precise position is variable. Whilst the anteroseptal commissure may lie anteriorly to the membranous septum (“aroundthe corner”), it may also lie either
caudally or inferiorly to it. In part, our earlier mistake
stemmed from a desire to follow the lead of the Toronto
group and to define a commissure according to its sup-
port by a fan-shaped cord. In the light of our present
findings, such endeavours were misguided. Commissures can only be defined realistically in terms of the
areas of junction between adjacent segments of the skirt
of the leaflet tissue forming the major component of any
valve, be i t atrioventricular or arterial. Within this
concept, it is then clear that the structure of the commissure will vary markedly depending upon whether it
is considered in terms of ventricular systole or diastole.
During ventricular systole, the leaflets of the atrioventricular valves will be closed, and their meeting edges
will extend from the circumferential periphery to the
centre of the valve orifice. During diastole, however, the
leaflets are open. Their junction is then seen related to
the circumferential margin of the valve orifice, in other
words, to the atrioventricular junction or “annulus”.
Only this latter meeting point is constant during systole
and diastole. Furthermore, it is rare for the morphologist to see the atrioventricular valve other than in its
diastolic state. For this reason, we have defined the
antero-septal commissure in the open position of the
valve. In this state, we have observed the three patterns
described above. None are supported by a discrete fanshaped cord. They remain, nonetheless, the unequivocal
site of junction (or non-junction in presence of a gap)
between the septal and the antero-superior leaflets of
the tricuspid valve. I t is for this reason that we submit
that this area is best considered as the valvar commissure. The variation observed depends upon whether the
adjacent septal and antero-superior leaflets meet perfectly at the atrioventricular junction (designated a s
annular commissure), whether they form a common
leaflet extending some way from the periphery of the
valve orifice (undivided commissure), or whether they
are attached to the atrioventricular junction so as to
leave a gap between the leaflets.
TRICUSPID VALVE AND MEMBRANOUS SEPTUM
The mode of variable formation of the undivided
commissure, along with the relationship noted to the
morphology of the membranous septum, is suggestive
that formation of the commissure occurs along with
and at similar times to that of the membranous septum. It seems possible that commissural architecture is
intimately related to whatever mechanism dictates liberation of the leaflets from the membranous septum.
The presence of the “gap variant” in the normal heart
is relevant to the type of congenital septal defect that
produces shunting from the left ventricle to the right
atrium. Although often thought of in terms of deficiency of the atrioventricular membranous septum,
this lesion is much more frequently due to a combination of a ventricular septal defect in the environ of the
membranous septum (perimembranous defect) and a
deficiency of leaflet tissue adjacent to the defect. A gap
commissure co-existing with a perimembranous defect
will provide exactly this combination.
ACKNOWLEDGMENTS
We thank Professor F. Harris for providing the facilities for this work. We are indebted to Mrs. Sandra
Longworth for typing the text and Mrs. Susan Dutton
for her help with the statistical analysis. Mr. Kenneth
Walters and Miss Ann Pownall produced the photographs and drew the diagrams.
263
A.R. received a grant from the British Heart Foundation, and the study was derived from his M.Sc thesis.
R.H.A. is also supported by the British Heart Foundation together with the Joseph Levy Foundation, while
A.S. is supported by the Endowment Fund of the Royal
Liverpool Children’s Hospitals.
LITERATURE CITED
Allwork, S.P.,and R.H. Anderson 1979 Developmental anatomy of the
membranous part of the ventricular septum in the human heart.
Br. Heart J., 41: 275-280.
Goor, D.A., and W.C. Lillehei 1975 Congenital Malformations of the
Heart: Embryological, Anatomical and Operative Considerations. Grune and Stratton Inc., New York, San Francisco and
London. pp. 1-37.
Odgers, P.N.B. 1938 The development of the membranacea septi in
the human heart. J . Anat., 72:247-259.
Rosenquist G.C., and L.J. Sweeney 1975 Normal variations in tricupsid valve attachments to the membranous ventricular septum: A
clue to the etiology of left ventricle-to-right atrial communication. Am. Heart J., 89:186-188.
Silver, M.D., J.H.C. Lam, N. Ranganathan, and E.D. Wigle 1971 Morphology of the human tricuspid valve. Circulation, 43:333-348.
Smith, A., J.L. Wilkinson, R.H. Anderson, R. Arnold, and D.F. Dickinson 1986 Architecture of the ventricular mass and atrioventricular valves in complete transposition with intact septum compared with the normal: 11.The right ventricle and tricuspid valve.
Pediatr. Cardiol., 6.299-305.
Walmsley, T. 1930 Transposition of the ventricles and arterial stems.
J . Anat., 65528-540.
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