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From the Institut National de la Santé et de la Recherche
Médicale, IFR "Circulation Lariboisière," INSERM U
141 (Z.M., A.T.) and INSERM U 348 (M.L., J.M.), Hôpital
Lariboisière, Paris, and Service de Chirurgie Cardiovasculaire (I.P.,
D.C.), Hôpital Bichat, Paris, France. Correspondence to Alain Tedgui,
PhD, INSERM U 141, 41 boulevard de la Chapelle, 75475 Paris Cedex 10, France.
Methods and Results—To evaluate oxidant stress in the heart, we
measured pericardial fluid levels of 8-iso-prostaglandin
F2
Conclusions—Pericardial levels of 8-iso-PGF2
Oxidative modification of arachidonic acid leads to the
formation of free radical–catalyzed products called
F2-isoprostanes.5 One of
these compounds, 8-iso-prostaglandin
F2
The functional severity of heart failure was assessed before surgery by
use of the NYHA classification, and the patients were classified by an
independent investigator as asymptomatic (NYHA 1, n=10) or
symptomatic (NYHA 2, n=21; NYHA 3, n=20). When possible,
echocardiographic evaluation was performed by
independent cardiologists in the hospital just before cardiac surgery.
The NYHA status and the echocardiographic indices
(LVEDD, LVESD, and the derived left ventricular fractional
shortening) were subsequently correlated with pericardial fluid levels
of 8-iso-PGF2
Measurement of 8-iso-PGF2
Statistical Analysis
Correlation Between Pericardial Levels of 8-iso-PGF2
F2-isoprostanes are a family of
prostaglandin F2
Apart from being an index of oxidant stress,
8-iso-PGF2
Another interesting finding in the present study points to a
potential effect of oxidant stress on ventricular
remodeling. Pericardial fluid levels of
8-iso-PGF2
Little is known about the relation between oxidant stress and
ventricular remodeling. In our patients, acute
ischemia or ischemia-reperfusion are not likely to
explain the persistent increase in 8-iso-PGF2
Study Limitations
Conclusions
Received January 12, 1998;
revision received February 24, 1998;
accepted February 27, 1998.
2.
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Evidence of oxidative stress in chronic heart failure in humans.
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© 1998 American Heart Association, Inc.
Brief Rapid Communications
Elevated Levels of 8-iso-Prostaglandin F2
in Pericardial Fluid of Patients With Heart Failure
A Potential Role for In Vivo Oxidant Stress in Ventricular Dilatation and Progression to Heart Failure
Abstract
Top
Abstract
Introduction
Methods
Results
Discussion
References
Background—It has been suggested
that oxidant stress may play a role in the pathophysiology of heart
failure. However, no definitive information is available because most
previous approaches used to measure oxidant stress are nonspecific,
inaccurate, and unreliable. (8-iso-PGF2), a specific and
quantitative marker of oxidant stress in vivo, in a series of 51
consecutive patients with ischemic and/or valvular
heart disease referred for cardiac surgery. Pericardial levels of
8-iso-PGF2 were correlated with the functional severity
of heart failure (NYHA classification) and with
echocardiographic indices of ventricular
dilatation measured by independent physicians. Pericardial levels of
8-iso-PGF2 were significantly increased in patients with
symptomatic heart failure compared with
asymptomatic patients and gradually increased with the
functional severity of heart failure (P=.0003). In
addition, pericardial levels of 8-iso-PGF2 were
significantly correlated with left ventricular
end-diastolic and end-systolic diameters
(P=.008 and .026, respectively).
increase with the functional severity of heart failure and are
associated with ventricular dilatation. These data suggest
an important role for in vivo oxidant stress on ventricular
remodeling and the progression to heart failure.
Key Words: heart failure • free radicals • pericardium
Introduction
Top
Abstract
Introduction
Methods
Results
Discussion
References
Heart failure is a
serious health problem.1 Identification of
pathophysiological pathways that lead to heart
failure is necessary to design specific therapeutic strategies that
will hinder the progression of the disease. Oxidant stress, an
imbalance between oxidant production and antioxidant defenses
in favor of the former, leads to tissue injury and is thought to
contribute to the pathophysiology of heart failure in humans,
particularly heart failure due to coronary artery
disease.2 3 However, no definitive information is
available as to the importance of this process in vivo given that most
traditional methods previously used to assess oxidant stress are
nonspecific, inaccurate, and unreliable.4 (8-iso-PGF2), has
recently been shown to be a specific, chemically stable, quantitative
marker of oxidant stress in vivo.6 Therefore, to
assess the importance of oxidant stress in the progression to heart
failure, we measured, using a specific validated
immunoassay,7 pericardial fluid levels of
8-iso-PGF2 in a series of consecutive patients
with ischemic and/or valvular heart disease referred
for cardiac surgery.
Methods
Top
Abstract
Introduction
Methods
Results
Discussion
References
Patient Selection and Characteristics
This study included 51 consecutive patients (36 men and 15
women; age range, 39 to 78 years) with ischemic heart disease
(n=19), valvular heart disease (n=27), or both (n=5).
Valvular heart disease comprised 17 cases of mitral
regurgitation, 7 mitral stenosis, 13 aortic
stenosis, 9 aortic insufficiency, and 1 tricuspid
regurgitation. Ten patients had an association of two
or several types of valvular disease. There were no symptoms,
signs, or history of pericardial disease. No patient had undergone
previous cardiac surgery. The patients were addressed for
coronary artery bypass surgery, valve replacement, or valve
repair. Among other parameters, age, smoking status,
diabetes, aspirin treatment, use of antioxidants, and episodes of
ischemia-reperfusion were documented in each patient because
these parameters have previously been reported to influence
plasma or urinary 8-iso-PGF2
levels.6 7 8 9 10 11 Eight patients presented
with recent acute coronary syndromes (6 had unstable angina and
2 had myocardial infarction) at least 4 days before surgery. Eighteen
patients were taking aspirin. Nine patients had diabetes mellitus. Only
3 patients were current smokers. The remaining patients were nonsmokers
(n=16) or had abstained from cigarette smoking for periods ranging from
7 months to 32 years (n=31). Only 2 patients were taking allopurinol, a
medication with potential antioxidant properties. No patient received
antioxidants for cardiac protection. .
Undiluted samples of pericardial fluid were collected
immediately after incision in tubes containing 1 mmol/L
4-hydroxy-TEMPO. Time from incision to collection of pericardial fluid
varied from 22 minutes to 130 minutes. Samples were immediately
centrifuged at 3000g for 10 minutes and stored at
-80°C. We analyzed the samples for their
8-iso-PGF2 content by direct assay using a
validated enzyme immunoassay.7 In brief, the
standard or the biological sample, 8-iso-PGF2,
coupled to acetylcholine esterase from the electric eel, and specific
antiserums were added (50 µL each) at appropriate dilutions. All
measurements were done in duplicate.
Values are expressed as mean±SEM. Data were compared by use of
a one-way ANOVA. Simple regression analysis was performed to
analyze the relation between
8-iso-PGF2 and
echocardiographic indices of ventricular
dilatation and function. A value of P<.05 was considered to
be statistically significant.
Results
Top
Abstract
Introduction
Methods
Results
Discussion
References
Elevated Pericardial Levels of 8-iso-PGF2 in
Symptomatic Heart Failure
All patients had detectable pericardial fluid levels of
8-iso-PGF2 (ranging from 2 to 70 pg/mL). Time
from incision to collection of pericardial fluid (52.2±5.6 minutes)
had no influence on 8-iso-PGF2 levels. Levels
of 8-iso-PGF2 in symptomatic
patients (NYHA class 2 and 3, n=41) were significantly higher than
those in asymptomatic patients (NYHA 1, n=10) (27.0±2.5
versus 11.1±1.6 pg/mL, respectively; P=.0037). Pericardial
levels of 8-iso-PGF2 significantly increased
with the functional severity of heart failure (11.1±1.6 pg/mL in NYHA
1 patients, 20.8±2.9 pg/mL in NYHA 2 patients, and 33.4±3.7 pg/mL in
NYHA 3 patients; P=.0003) (Fig 1
). Patients treated with aspirin also
presented with elevated levels of
8-iso-PGF2 that correlated with NYHA status.
These values were not different from those of patients not taking
aspirin. Pericardial levels of 8-iso-PGF2 were
not influenced by age, sex, smoking status, diabetes, medical
treatment, or recent history of acute coronary syndromes.
View larger version (18K):
[in a new window]
Figure 1. Pericardial levels of 8-iso-PGF2 in
patients with ischemic and/or valvular heart disease
referred for cardiac surgery. Pericardial levels of
8-iso-PGF2 significantly increased with the functional
severity of heart failure assessed using the NYHA classification.
and Ventricular Dilatation
Echocardiographic evaluation was performed by
independent cardiologists just before surgery in 27 unselected
patients. Data on LVEDD were available for all these patients. Data on
LVESD and left ventricular fractional shortening were
available for 23 of these patients. Pericardial levels of
8-iso-PGF2 were significantly correlated with
LVEDD (r=.5, P=.008) (Fig 2, top) and LVESD (r=.46,
P=.026) (Fig 2, bottom). There was no correlation between
pericardial levels of 8-iso-PGF2 and left
ventricular fractional shortening (P=.45).
View larger version (23K):
[in a new window]
Figure 2. Top, Relation between pericardial levels of
8-iso-PGF2 and LVEDD. Pericardial levels of
8-iso-PGF2 correlated significantly with LVEDD
(y=0.304x+45.2, n=27, r=.5, P=.008).
Bottom, Relation between pericardial levels of
8-iso-PGF2 and LVESD. Pericardial levels of
8-iso-PGF2 correlated significantly with LVESD
(y=0.188x+28.2, n=23, r=.46,
P=.026).
Discussion
Top
Abstract
Introduction
Methods
Results
Discussion
References
It has been suggested that oxidant stress may play a role in the
pathophysiology of heart failure in animals and
humans.2 3 12 However, traditional approaches
used to evaluate the importance of oxidant stress in vivo, including
the analysis of reactive aldehydes, lipid hydroperoxides,
conjugated dienes, and exhaled pentane, suffer from major limitations
due to the inaccuracy of these methods in estimating the actual rate of
lipid peroxidation in vivo.4 13 The most widely
used index of lipid peroxidation is the measurement of malondialdehyde
by the thiobarbituric acid–reacting substances assay. When this assay
was used as an index of lipid peroxidation in vivo, conflicting results
were obtained. Indeed, this assay suffers from lack of specificity and
overestimates actual malondialdehyde levels by
>10-fold,14 rendering the assay inaccurate as an
indicator of oxidant stress in vivo. -isomers formed in
situ on phospholipids by the peroxidation of
arachidonic acid, catalyzed by free
radicals.5 7 11 15 16 They are presumably
released into biological fluids through a phospholipase-mediated
mechanism and are excreted in the urine.7 17 One
of these compounds, 8-iso-PGF2, has recently
been shown to be a specific, quantitative index of oxidant stress in
vivo.6 In this study, we found a significant
increase in pericardial fluid levels of
8-iso-PGF2 in patients with
symptomatic heart failure. Although we did not identify the
cell type(s) responsible for this increased production,
virtually all cell types present in the heart, including myocardial
and pericardial cells, might be implicated. Consistent with
studies showing that PGF2-isomers are formed
from mainly noncyclooxygenase oxidative
transformation of arachidonic
acid,5 7 11 15 16 the subgroup of patients
treated with aspirin also presented with elevated levels of
8-iso-PGF2. Although elevations in plasma or
urinary F2-isoprostane levels have been reported
in association with several cardiovascular risk
factors,6 7 8 9 10 11 no individual subgroup with
elevations in pericardial 8-iso-PGF2 levels
could be identified in our patient population, considering sex, age,
smoking status, or diabetes. However, the increased formation of
pericardial 8-iso-PGF2 was associated with
increased functional severity of heart failure as assessed by NYHA
status. Therefore, our findings suggest that oxidant stress in the
heart may play a significant role in the progression from
asymptomatic to symptomatic heart failure and
in the progressive deterioration of functional capacity. generated during this process may
exert potent vasoconstrictor activity in
vivo.18 19 20 21 We propose that this mechanism,
acting locally, may be responsible, at least in part, for the limited
functional capacity in patients with increased
8-iso-PGF2 levels. This may occur through a
decrease in subendocardial blood flow and an alteration in
diastolic function, for example. This hypothesis should be
verified in future studies. were significantly correlated with
echocardiographic indices of ventricular
enlargement, LVEDD, and LVESD. This observation is important because
several studies have shown that these and other
echocardiographic parameters of
ventricular dilatation are strong determinants of prognosis
in symptomatic or asymptomatic patients with or
without overt cardiovascular
disease.22 23 24 25 26 27
several days after the clinical syndrome, although the clearance of
this compound in pericardial fluid is totally unknown. A more likely
hypothesis involves the role of mechanical factors. It has recently
been shown that overstretching of the myocardium leads to
enhanced generation of reactive oxygen species, with increased
expression of Fas and induction of
apoptosis.28 This in turn would lead to
rarefaction and slippage of myocytes, resulting in an even more
pronounced ventricular dilatation. This
pathophysiological mechanism might account for the
significant correlation between pericardial
8-iso-PGF2 and ventricular
dilatation observed in the present study and in part for the
occurrence of apoptosis in the dilated human
heart.29 30 31 However, it cannot be ruled out that
8-iso-PGF2 is solely a marker for increased
myocardial damage in our patients with heart failure.
This study included patients with ischemic or
valvular heart diseases in NYHA classes 1 to 3. Whether our
findings will extend to patients with other types of heart disease
(hypertensive or dilated cardiomyopathy, for
example) or to patients with more severe heart failure (NYHA class 4)
merits further investigation.
In conclusion, this is the first study showing that
ventricular dilatation and symptomatic heart
failure are associated with an increase in pericardial fluid levels of
8-iso-PGF2, which is likely to reflect oxidant
stress in the heart. Our data open the way for dose finding with
antioxidant drugs and evaluation of their potential therapeutic effects
on both ventricular remodeling and the progression to heart
failure.
Acknowledgments
This work was supported by grant CNAMTS/INSERM No. 4API12. Dr
Mallat was supported by Assistance Publique, Hôpitaux de
Paris.
References
Top
Abstract
Introduction
Methods
Results
Discussion
References
1.
Cowie MR, Mosterd A, Wood DA, Deckers JW,
Poole-Wilson PA, Sutton GC, Grobbee DE. The
epidemiology of heart failure. Eur
Heart J. 1997;18:208–225. generation during coronary
reperfusion: a potential quantitative marker of oxidant stress in vivo.
Circulation. 1997;95:2492–2499.
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