Download Premature Closure of the Mitral and Tricuspid Valves

Premature Closure of the Mitral
and Tricuspid Valves
By DONALD A. SPRING, M.D., JOHN D. FOLTS, B.S.E.E., PH.D.,
WILLIAM P. YOUNG, M.D., AND GEORGE G. RowE, M.D.
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
SUMMARY
Premature closure of an atrioventricular valve was observed in 80 of a group
of 519 subjects catheterized for aortic insufficiency (Al) or mitral insufficliency (MI),
or both. Sole premature mitral closure (PMC) was present in nine subjects, sole premature tricuspid closure (PTC) in 40, and combined PMC and PTC in 31. Clinically
PMC was associated with a first sound that was soft or absent in 75% and an atrial
contraction sound in 50% of the subjects with dominant aortic insufficiency. PMC or
PTC, or both, were verified at surgery in three subjects and were produced experimentally in intact dogs by acute AI. The presence of PMC and PTC appears related to the
severity and chronicity of valvular disease.
Additional Indexing Words:
Mitral insufficiency
Experimental aortic insufficiency
Bulging interventricular septum
Aortic insufficiency
Pericardial restriction
RECORDS from cardiac catheterization
frequently reveal premature mitral valve
closure' in subjects with severe aortic1 2 or
mitral3 insufficiency (fig. la) by demonstrating that left ventricular end-diastolic pressure
exceeds left atrial pressure. A similar reversal
of right atrial and ventricular end-diastolic
pressures suggests premature tricuspid valve
closure (fig. lb). The incidence of these
phenomena and their clinical and hemodynamic correlates was' studied in human
subjects and produced in dogs with acute
aortic insufficiency.
Methods
mitral valve disease were scrutinized for the
presence of premature mitral or tricuspid valve
closure as manifested by reversal of the usual enddiastolic atrioventricular pressure gradient. Two
hundred sixty-two subjects had aortic insufficiency and 257 had mitral insufficiency. If insufficiency of both valves was present, the subjects were
classed as having the more severe lesion.
All subjects were evaluated clinically and by
right as well as retrograde and transseptal left
heart catheterization. Via Statham P 23 Db strain
gauges, pressures were recorded on a Waters
Conley photographic recorder at a paper speed of
25 mm/sec. Simultaneous pressures were recorded by utilizing a Brockenbrough catheter in
the right atrium and a no. 6 Lehman catheter in
the right ventricle. We required the end-diastolic
pressure to be the same during recording with
both catheters in the ventricle and any observation which could not be confirmed from the
reversed catheter positions was rejected. Similar
technic was used for left-sided recordings. The
reverse end-diastolic mitral or tricuspid gradient
was accepted if it was 2 mm Hg or more.
Valvular insufficiency was graded as mild,
moderate, or severe, from the combined results of
angiographic and indicator-dilution studies.
In three subjects during aortic valve replacement, right- and left-sided intracardiac pressure
recordings were made before and after opening
the pericardium.
Clinical and Hemodynamic Investigation
The records of 519 consecutive subjects who
underwent cardiac catheterization for aortic or
From the Cardiovascular Research Laboratory,
Department of Medicine, University of Wisconsin
Medical School, Madison, Wisconsin.
Supported in part by grants from the U. S. Public
Health Service, National Heart Institute HE 5364, HE
5738, HE 14,928, and HE 07754.
Address for reprints: Dr. George G. Rowe, 420 N.
Charter Street, Rm. 523, Madison, Wisconsin 53706.
Received April 19, 1971; revision accepted for
publication October 5, 1971.
Circulation, Volume XLV, March 1972
663
SPRING ET AL.
664
mm
diagnostic studies reported here. Cardiac output
was obtained by indicator-dilution curves.
After control observations, aortic insufficiency
was produced as deselibed previously,5 and
repeat observations were made. One dog was
studied before and after acute aortic insufficiency
by means of simultaneous right and left cineven-
Hg
triculography.
Results
The Clinical and Hemodynamic Investigation
Evidence for premature closure of the
r
1
I\
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
mitral valve (PMC), tricuspid valve (PTC),
or both, was found in 80 subjects. Premature
closure was associated with at least moderate,
and usually severe, insufficiency of the aortic
(58 cases), mitral (12 cases), or both leftsided valves (10 cases). PMC was less
common (40 cases) than PTC (71 cases). Sole
PMC was present in nine subjects (group 1),
sole PTC in 40 (group 2) and combined
PMC and PTC in 31 (group 3). The clinical
and hemodynamic data are presented in table
1, and typical pressure tracings are given in
figures 1 and 2.
Intracardiac pressures were recorded in one
subject in each of these groups before and
after opening the pericardium during aortic
valve replacement. The pressure patterns
were
similar to those recorded at
catheterization (fig. 2). In one operative study
PTC was decreased (or abolished) after
opening the pericardium widely, while the left
ventricular end-diastolic pressure rose and
premature mitral valve closure occurred.
In the 40 subjects with PMC the left
ventricular diastolic flow period correlated
negatively with left ventricular end-diastolic
pressure (r = -0.3691; P <0.02) but not with
the cardiac index. Thus a shortened filling
time did not seriously limit mitral diastolic
inflow. The reversed end-diastolic pressure
gradient and end-diastolic pressure were
directly related (r 0.4555; P < 0.01) in
PMC. For the 71 subjects with PTC right
ventricular end-diastolic pressure correlated
negatively with right ventricular diastolic flow
period (r = -0.2486; P < 0.05). Left ventricular end-diastolic pressure correlated with the
right ventricular end-diastolic reversed pressure gradient (r= 0.3585; P < 0.01) and the
,
b
Figure 1
Combined premature mitral valve closure (PMC)
(panel a) and premature tricuspid valve closure (PTC)
(panel b) in a subject with severe aortic insufficiency.
Abbreviations: ECG electrocardiogram; FA =femoral artery; LA 'A' --left atrium a wave; LV =
left ventricle; LVEDP
pressure; RA = right
tricular end-diastolic
left ventricular end-diastolic
ven-
atrium; RVEDP = right
pressure.
Diastolic time intervals were measured in at
least five consecutive cycles for timing mitral and
tricuspid valve openings and closures. The
diastolic flow period was measured from the point
at which ventricular pressure fell below the atrial
pressure until premature closure occurred and
was expressed as a percentage of diastole.
Experimental Animal Investigation
Twelve mongrel dogs, average weight 25 kg,
anesthetized,* and cardiac catheters were
positioned in the pulmonary artery and in both
atria and ventricles. In six aniimals the pericardial
space was also catheterized by a modified
percutan-eous technic.4 The manometer systems
and recorder were those used in the human
were
'Morphine sulfate, 3 mg/kg im, followed in 1
hour by 0.25 ml/kg of a 50/50 solution of veterinary
pentobarbital and Dialurethane. Dialurethane contains
diallylbarbituric acid, 100 mg/ml; monoethylurea, 400
mg/mi; and urethane, 400 mg/ml. Veterinary
pentobarbital contains 60 mg/mi of pentobarbital.
Circulation, Volume XLV, March 1972
PREMATURE CLOSURE OF VALVES
right ventricular end-diastolic pressure (r =
0.7124; P < 0.001). There was no significant
relationship between cardiac index and tricuspid diastolic flow period for those having
PTC. In the group having PMC with aortic
insufficiency, mild or moderate mitral insufficiency was a common finding (28 of 29
cases); tricuspid insufficiency, however, was
present in only 14% of the combined group of
71 subjects with PTC.
The
Experimental Investigation
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
After the induction of aortic insufficiency in
the six animals in which the pericardial space
had been catheterized, PMC was persistent in
one animal and inconstant in two; no
changes were observed in two animals, and
one rapidly developed hypotension and died.
PTC was observed in none of these animals;
however, postmortem examination revealed
that the pericardium had been torn. After the
induction of aortic insufficiency in the six
animals with intact pericardiums, persistent
combined PMC and PTC were observed in
665
three, inconstant PMC was present in one,
no changes were observed in one animal,
and one developed hypotension and died.
The hemodynamic findings in the four
animals with persistent premature valve closure are summarized in table 2 and figure 3.
The induction of aortic insufficiency caused
the left ventricular end-diastolic pressure to
rise rapidly producing typical PMC and PTC.'
Simultaneous biventricular angiography before and after the induction of aortic insufficiency revealed marked dilatation of the left
ventricular chamber, with pronounced diastolic displacement6 of the ventricular septum to
the right (fig. 4).
Discussion
Premature mitral valve closure was postulated7 from results seen in simulated aortic
insufficiencys and after atrioventricular diastolic gradient reversal was demonstrated in
subjects with severe aortic insufficiency.9
Subsequent reports from many laboratories
have documented the occurrence of early mitral
Figure 2
Combined PMC and PTC at catheterization (panels a and b) and at operation (panels c
and d) for severe aortic insuficiency. Abbreviations: RV= right ventricle; others same as in
figure 1.
Circulation, Volume XLV, March 1972
SPRING ET AL.
666DU
Table 1
Clinical Findings and Hemodynamic Summary in Subjects with Premature Atrioventricular Valve Closure
Sex
and
no.
Group
Age (yr)*
Group 1:
9
Premature
mitral valve M
F
closure
=
=
40.3
9.86
8
1
Clinical
diagnosis,
etiology
Average duration
Murmur
Symptoms
(yr)
Al 3
AS & AI = 2
MI = 2
RHD=
(+SBE = 2)
ABE = 1
CMN - 1
CAVD = 1
1
Unknown
AI
12
AS & AI = 10
AS = 4
MI = 14
RHD = 34
3.4
(yr)
Palpable
enlarge-
NYHA
F. C.
13.6
(4 mo to
34 yr)
III-IV
12.3
(3 mo to
III-IV
ment
=
7
I-II = 2
LV
=
Decreased
or absent
first
sound
6
5
RV =2
=
Group 2:
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
Premature
tricuspid
valve
closure
40
M
F
=
=
42.3
13
26
14
=
(+SBE
3.7
50yr)
I-II
=
=
20
20
LV
=
22
IRV
=
10
11
2)
CAVD = 3
(+SBE
Group 3:
Premature
mitral and
tricuspid
valve
closure
31
M -27
F - 7
44.1
13
=
1)
TCT = 1
AI
17
AS & AI = 12
MI 2
RHI) 23
=
(+SBE
2.4
16.4
(1 wk to
38yr)
III-IV = 16
I-II = 15
LV
27
22
RIV -2
3)
1
ABE
ASHD - 1
1
CAVD
IHSS 1
Marfan= 1
Unknown - 1
*All values are mean - standard deviation.
tHemodynamic data for subjects with aortic insufficiency (AI) and subjects with mitral insufficiency (MI) presented
separately.
Abbreviations: ABE = acute bacterial endocarditis; AI = aortic insufficiency; AF = atrial fibrillation; AS = aortic
stenosis; ASHD = atherosclerotic heart disease; CAVD = congenital aortic valve disease; CMN = cystic medial necrosis
(Erdheim); IHSS - idiopathic hypertrophic subaortic stenosis; LVSP = left ventricular systolic pressure; LVEDP =
left ventricular end-diastolic pressure; MI = mitral insufficiency; NYHA F. C. = New York Heart Association functional
capacity; RHD = rheumatic heart disease; RSR = regular sinus rhythm; RV = right ventricle; SBE = subacute bacterial
endocarditis; S3 - left ventricular diastolic gallop; S4 = atrial contraction sound; TCT = torn chordae tendineae of
mitral valve; TI - tricuspid iinsufficiency; 10 Blk = first-degree heart block; VDI = ventricular diastolic interval.
valve closure.1 3 14), 11, 13 Although in most
cases premature mitral valve closure has been
found to occur with severe aortic insufficiency,
it also occurs with severe mitral insufficiency3
and is not a rare phenomenon." 2, 10 However
only four examples of PMC were found from
among our records of 257 subjects with
primarily mitral disease, and the number cited
in the literature is small.3
Premature tricuspid valve closure, with or
without accompanying PMC, was more common (13.6%) than PMC (7.7%) in this series.
It is presumed that this phenomenon has not
been described because the tricuspid valve is
studied less rigorously than the aortic and
mitral valves. Morphologically, the reversal of
right-sided end-diastolic pressures in PTC is
similar to the diastolic gradient reversal seen
Circulation, Volume XLV, March 1972
PREMATURE CLOSURE OF VALVES
Dominant
S3
S4
Rhythm
FIISR
0)
=
1° Blk = 2
AF = 1
6
8
RSR
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
1° Blk
AF
(liters/min/M2)
7
3.088 0.787
156
34
MII = 2
35) AI
32t
(3 with
'a' sev. MI)
2
MI = 8
(mnild TI
=
Pressure (mm Hg)
Left atrial
LVSP
mean
LVSP
LVEDP
pressture
Cardiac
Dominant
index
lesion
6 AI
667
=
3.382
1.364
163
23
15)
RtSR
24 AI = 29
(7 with
10 Blk = 6 sev. MI)
AF - 1
2
MI
=
3.602
48
11
18
8
(msec)
269
89
DFP/VDI
(% VDI)
Enddiastolic
gradient
(mm Hg)
72
6
13
-
3
(range,
.,57-81%)
8
283
118
l 11
ll71
5
2
4
2
5
2
(range,
8S
1.344
121
19
10- 6
16
3.425.- 1.397
172- 43
27 - 11
20 -1()
=
(mild TI -
.5/31)
in PMC. The presence of PTC in a large
number of diagnostic catheterization records
(fig. 1), its persistence at open-heart surgery
(fig. 2), and its reproduction in laboratory
animals (fig. 3) document its authenticity.
Both human and animal studies demonstrate
that valve closure on the right side of the
heart may be influenced by major insufficiency
of the aortic or mitral valve.
Contrary to previous reports'2 sudden,
severe aortic insufficiency was found to be
associated here with PMC infrequently (five
of 36 subjects). The average duration of
symptoms of about 2 to 4 years and known
presence of a heart murmur for many years
clearly indicate chronicity of the valvular
lesions in most of these subjects. Thus,
Circulation, Volume XLV, March 1972
23
periodflow
(DFP)
40-88%)
.)/40)
10
40
13
Diastolic
112
276
Tricuspid valve
68 14
(range,
40-94%)
255
-
95
Mitral Valve
71 14
(range,
40-90%)
premature valve closure seems more closely
related to the severity than to the duration of
aortic or mitral insufficiency. In those subjects
with dominant mitral insufficiency PTC was
more common (10 subjects) than PMC (four
subjects).
In 75% of our subjects with aortic insufficiency and PMC the first heart sound was soft
or absent.1 2, 10 Contrary to reports stressing
its relative frequency,'2' 13 first-degree heart
block was present in only six subjects (17%),
and in five of these there was clear-cut
pressure crossover during or before the atrial
contraction wave. Since in these instances the
atrium was contracting against a closed valve,
it is not surprising that 50% of the human
subjects with predominant aortic insufficiency
SPRING ET AL.
668
,
4i)
(_
os
-H
rm
0PP.u R
mcp'M
Cdc,
C:
.
1
.6]1
F._
4_
es
R
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
.o
0
SX;,
~~ 0-
-H
°032
.5
AS-;
a:J
c.
Q
-H
.e
-H
-4
t^:
I
-H-
M M
*n
x
1
M
z
rIC
-4
cq
m
--
1-4
X
'J20
1-
z
cc
cs
0i
.e.
-su S H
-e
-4.
'.t
41
0. .
Z
H-.
u
43
>
,;
m
-4
o
V-
L.C
'
0
0-
o
S
¢~
$.C.
c
had a late diastolic sound (fourth heart
sound). This forceable contraction is clearly
reflected in the marked elevation of the left
atrial "A" wave seen in figures 1 and 2.
It is interesting that the cardiac index was
relatively normal in spite of rather severe
valvular lesions and marked reduction in left
ventricular diastolic flow period. This implies
that ventricular filling from atrial systolic contraction was not important in the
maintenance of an effective stroke output at
these heart rates. Furthermore the modest
elevations in left atrial and pulmonary artery
pressures in both the human and experimental
studies support the concept that PMC protects
the pulmonary vascular bed from regurgitant
aortic flow, and consequent elevated pressures. In addition PMC increases left ventricular end-diastolic pressure so that the force of
the contraction is increased to compensate for
regurgitation.8
Although direct proof of PMC has not been
obtained, there is considerable deductive
evidence for its occurrence: (a) the pressure
curve morphology from man1-3, 9 10, 12, 13
(figs. 1 and 2) and experimental animals (fig.
3) having severe aortic insufficiency; (b)
longer diastolic cycles through prolonging
aortic regurgitation produce higher left
ventricular end-diastolic pressure and more
marked end-diastolic atrioventricular pressure
reversal; (c) a late diastolic sound that
coincides with left atrioventricular pressure
crossover during closure of natural2 and
prosthetic14 mitral valves; and (d) implanted
mitral electromagnetic flowmeters in calves
with acute aortic insufficiency15 that show
cessation of forward flow through the mitral
valve at atrioventricular pressure crossover (premature closure). In the present
investigation, the characteristic early pressure
reversal of PMC was attained by the induction
of aortic insufficiency in intact animals without alteration of the P-R interval. Since
atrioventricular valve closure frequently took
place before atrial contraction in the present
data, an atriogenic mechanism of pre-closure
must be uncommon. The presence of mild-tomoderate mitral insufficiency in 96% of the
Circulation, Volume XLV, March 1972
PREMATURE CLOSURE OF VALVES
669
CONTROL
ECG
mmHg
150-\
C--
100
O
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
5025 Z-
.
0_,
LR\A
.
_E
._
\
s~~~R
b
a
d
c
Figure 3
Combined PMC and PTC resuilting from the induction of
intact experimental animal. (Compare panels a and h with
in figures 1 and 2.
severe
c
aortic
insugiciency
and d). Abbreviations
in the
same as
C
b: :.:.
Figure 4
(a and b) Single frames taken from cineangiogram made after contrast material was injected simultaneously into the right and left v)entricles. (a) Before and (b) after induction of
severe aortic insufficiency. These show a rightward shift of the interventricular septum and
encrochment on the tright ventricular cavity. (c) Diagrammatic representation of the changes
caused by aortic insufficiency made by tracing and superimposing panels a and b. The solid
lines represent panel a and the dotted lines panel b. The change in the left ventrictular diastolic
shape and the septal displacement to the right are shown.
a
Circulation, Volume XLV, March 1972
SPRING ET AL.
670
subjects of this series with dominant aortic
insufficiency correlates well with experimental
observations'5 and angiocardiographic demonstrations of diastolic mitral incompetence in
human subjects with this condition.16-18
While the mechanism of PMC in aortic
insufficiency seems clear, the mechanism of
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
PMC in dominant mitral insufficiency3 is
much less clear. It is suggested that the
overdistended left atrium empties so rapidly
that when the ventricle reaches its capacity a
rebound wave occurs and closes the mitral
valve. The mechanisms causing PTC may
differ from those causing PMC. The pericardium may play an important role in PTC since
PTC was abolished or greatly reduced in one
subject by a wide incision of the pericardium.
This suggests that the pericardium distributed
the pressure created by aortic regurgitation
into all cardiac chambers including the right
ventricle and right atrium. Since blood could
flow freely out of the right atrium but not
from the right ventricle, premature tricuspid
closure would be expected to occur. When the
pericardium no longer caused this redistribution of pressure, only PMC occurred. PTC did
not occur in the series of experimental animals
in which the pericardium had been torn.
allowing the pericardial fluid to escape and
removing or ameliorating the pericardial
restrictive effect.19 Since PTC was seen to
increase markedly during the increased aortic
regurgitation of longer diastolic cycles and
since biventricular angiograms during experimentally induced aortic insufficiency revealed
that the septum appeared to encroach on the
right ventricle in diastole (fig. 4), it appears
likely that right ventricular compression is
produced by left ventricular dilatation. The
modest elevation in right ventricular enddiastolic pressures in these human and experimental subjects and the low incidence of right
ventricular hypertrophy among human subjects with PTC support the idea that the right
ventricle is only passively affected.
In conclusion, it appears that premature
atrioventricular valve closure may be found on
both sides of the heart. Furthermnore, a variety
of hemodynamic changes can alter the closure
timing of both semilunar valves20' 21 as well as
the atrioventricular valves.'-' 8---12 It is hoped
that an awareness of these possible variations
in valve closure and their causative mechanisms may lead to increased understanding of
the diseased heart.
References
1. MEADOWS WR, VAN PRAAGH S, INDREIKA
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
M,
SHARP JT: Premature mitral valve closure: A
hemodynamic explanation for absence of the
first sound in aortic insufficiency. Circulation
28: 251, 1963
WIGLE E, LABROSSE CJ: Sudden, severe aortic
insufficiency. Circulation 32: 708, 1965
AUGER P, WIGLE ED: Sudden, severe mitral
insufficiency. Canad Med Ass J 96: 1493,
1967
WOOD EH, NOLAN AC, DONALD DE, EDMUNDowIcz AC, MARSHALL HW: Technics for
measurements of intrapleural and pericardial
pressures in dogs studied without thoracotomy
and methods for their application to study of
intrathoracic pressure relationships during exposure to forward acceleration (+G,). Technical Documentary Report No. AMRL-TDR63-107. Pps 1-12, 1963
SPRING DA, RowE GG: A device for the
production of aortic insufficiency in intact
experimental animals. J Appl Physiol 29: 538,
1970
RUSHMER RF, THAL N: The mechanics of
ventricular contraction: A cinefluorographic
study. Circulation 4: 219, 1951
McKusicK VA: Cardiovascular Sound in Health
and Disease. Baltimore, Williams & Wilkins
Co., 1958, p 278
WELCH CH, BRAUNWALD E, SARNOFF SJ:
Hemodynamic effects of quantitatively varied
experimental aortic regurgitation. Circ Res
5: 546, 1957
WRIGHT JL, TOSCANO-BARBOZA E, BRANDENBURG
RO: Left ventricular and aortic pressure pulses
in aortic valvular disease. Proc Mayo Clin 31:
120, 1956
REES J, EPSTEIN J, CRILEY JM, Ross RS:
Haemodynamic effects of severe aortic regurgitation. Brit Heart J 26: 412, 1964
KELLY ER, MORROW AG, BRAUNWALD E:
Catheterization of the left side of the heart.
New Eng J Med 262: 162, 1960
COLVEZ P, ALHIOMME P, SAMSON M, GUEDON J:
La pression de remplissage du ventricule gauche
dans les grandes insuffisances aortiques: Ses
relations avec l'allongement de la conduction
auriculo-ventriculaire. Arch Mal Coeur 52:
1369, 1959
Circulation, Volume XLV, March 1972
PREMATURE CLOSURE OF VALVES
13. HERBERT WH: Atrial transport and aortic
insufficiency. Brit Heart J 29: 559, 1967
14. AGNEW TM, CARLISLE R: Premature valve
closure in patients with a mitral Starr-Edwards
prosthesis and aortic incompetence. Brit Heart
J 32: 436, 1970
15. NOLAN SP, FISHER RD, DIXON SH, WILLIAMS
WH, MORROW AC: Alterations in left atrial
transport and mitral valve blood flow resulting
from aortic regurgitation. Amer Heart J 79:
668, 1970
16. LOCHAYA S, IGARASHI M, SHAFFER A: Late
diastolic mitral regurgitation secondary to
aortic regurgitation: Its relationship to the
Austin Flint murmur. Amer Heart J 74: 161,
1967
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
Circulation, Volume XLV, March 1972
671
17. ALDIRIDGE HE, LANSDOWN EL, WIGLE ED: Diastolic mitral insufficiency. Circtulation 34: 42,
1966
18. WONG M: Diastolic mitral regurgitation: Haemodynamic and angiographic correlation. Brit
Heart J 32: 436, 1970
19. BERGLUND E, SARNOFF J, ISAACS JP: Role of the
pericardium in regulation of cardiovascular
hemodynamics. Circ Res 3: 133, 1955
20. BRIGDEN W, LEATHAM A: Mitral incomiipetence.
Brit Heart J 15: 55, 1953
21. SPRING DA, ROWE GC: Backward transmission
of the left atrial V wave and premature
pulmonary valve closure. Amer Heart j 81:
327, 1971
Premature Closure of the Mitral and Tricuspid Valves
DONALD A. SPRING, JOHN D. FOLTS, WILLIAM P. YOUNG and GEORGE G.
ROWE
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
Circulation. 1972;45:663-671
doi: 10.1161/01.CIR.45.3.663
Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX
75231
Copyright © 1972 American Heart Association, Inc. All rights reserved.
Print ISSN: 0009-7322. Online ISSN: 1524-4539
The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://circ.ahajournals.org/content/45/3/663
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles
originally published in Circulation can be obtained via RightsLink, a service of the Copyright
Clearance Center, not the Editorial Office. Once the online version of the published article for
which permission is being requested is located, click Request Permissions in the middle column
of the Web page under Services. Further information about this process is available in the
Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Circulation is online at:
http://circ.ahajournals.org//subscriptions/