Cardiac plasticity in fishes: environmental influences and intraspecific differences
1 Ocean Sciences Center, Memorial University of Newfoundland, St John's,
Newfoundland, Canada A1C 5S7
2 Department of Biological Sciences, 8888 University Drive, Simon Fraser
University, Burnaby, British Columbia, Canada V5A 1S6
* Author for correspondence (e-mail: kgamperl{at}mun.ca)
Accepted 27 April 2004
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Summary |
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Key words: intraspecific cardiac plasticity, fish, environment, heart, myocardium, hyperplasia, hypertrophy, preconditioning, hypoxia, temperature, maturation, food deprivation
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Introduction |
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In this review, we focus primarily on temperature effects, which are
relatively well studied, and on the effects of other environmental and
biological factors that modify cardiac anatomy and physiology, including food
deprivation, sexual maturation, exercise training and rearing under
aquaculture conditions. Further, we summarize recent work on cardiac
preconditioning and myocardial hypoxia tolerance in fishes, and discuss the
potential implications of this work. Preconditioning is a short-term form of
cardiac plasticity that has the potential to protect the heart from insults
that might normally lead to cardiac damage, dysfunction or death.
Preconditioning has been the focus of several thousand mammalian studies (e.g.
see review by Yellon and Downey,
2003), and so the handful of recent studies in fish, which already
point to important intraspecific differences, may find application outside the
piscine world. Similarly, researchers who wish to stimulate cardiac growth to
replace damaged myocardial tissue in mammals, may be heartened to discover
that fish cardiac tissue, unlike the mammalian heart, does not lose its
ability for hyperplastic growth with age. In fact, we suspect that the high
degree of intraspecific plasticity that we describe below is partly related to
the fact that fish hearts grow through hyperplasia as well as hypertrophy.
The heart powers an internal convection system for the whole animal, and in this context, global comparisons of cardiac function (e.g. cardiac output, stroke volume) are best represented in units of ml min1 kg1 body mass. However, relative ventricular mass (RVM) can vary considerably (e.g. by 50% intraspecifically, see below), and thus of units of ml min1 g1 ventricular mass or cardiac power output (mW g1 ventricular mass) allow us to interpret whether differences in cardiac function are due to changes in heart size, and/or plasticity in cellular physiology. We utilize both measurements of cardiac function in this review, because as a more mechanistic understanding of cellular plasticity emerges, elucidating the roles of these cellular changes will require increasingly refined comparators of cardiac performance.
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Temperature |
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Salmonids have adapted to exploit the cold water habitats created by
retreating glaciers, despite the fact that optimum temperatures for maximum
cardiac performance, aerobic scope and swimming ability are commonly around
1518°C and preferred temperatures typically range from 12 to
18°C (McCauley and Huggins,
1979; Jobling,
1981
). Thus, it is perhaps not surprising to find that cardiac
function in rainbow trout has a rather low sensitivity to temperature change.
Indeed, temperature acclimation between 5 and 18°C results in
Q10 values in the range 1.21.4 for maximum cardiac output
(
max) and maximum power
output (POmax) for rainbow trout
(Graham and Farrell, 1989
;
Keen and Farrell, 1994
),
rather than Q10 values of around 2 if there had been no
compensation.
The ability to almost maintain
max and
POmax across a broad temperature range clearly involves
cardiac plasticity that provides advantages to fish that inhabit an
environment with fluctuating temperatures. The mechanisms behind this cardiac
plasticity in response to temperature are partially understood. For example,
exposure to a 10°C decrease in temperature for 34 weeks increases
relative ventricular mass by 2040%, but decreases the proportion of
compact myocardium by 1530%
(Farrell et al., 1988
;
Graham and Farrell, 1989
). A
larger ventricular muscle mass compensates for a cold-temperature-induced
decrease in contractility, thereby helping maintain stroke volume
(VS),
and
pressure development. Implicit in this argument is that a decrease in
contractility negatively affects end-systolic volume of the ventricle, which
in trout is normally very small. At warmer temperatures, ventricular mass
could be relatively smaller while maintaining the same
because, in addition to improved
force of contraction, rates of ventricular contraction and relaxation are
faster. These latter effects would increase the time available for cardiac
filling, and may compensate for the effect of increased heart rate on
end-diastolic volume. Cardiac enlargement, however, is apparently dependent on
other factors beside temperature, because rainbow trout held on a 12 h:12 h
light:dark photoperiod show either no or a smaller degree of cardiac
enlargement (<15%) when acclimated to different temperatures
(Keen et al., 1993
;
Keen and Farrell, 1994
;
Sephton and Driedzic, 1995
;
Aho and Vornanen, 2001
).
Although we know little about what these environmental and physiological
factors might be, recent work by Tiitu and Vornanen
(2003
) suggests that
cold/seasonal cardiac enlargement may be partially related to thyroid state.
Thyroid hormones affect many physiological functions in fishes (e.g.
osmoregulation, nitrogen excretion, morphological changes associated with
smoltification, muscle growth etc.), and these authors found that
hypothyroidism was associated with increases in heart size and heart rate in
rainbow trout. The involvement of hypertrophic or hyperplastic myocardial
growth in cold/seasonal cardiac enlargement is presently unresolved
(Driedzic et al., 1996
),
although hypertrophy is a well-documented compensatory response to cold
temperature in tissues such as the liver
(Kent and Prosser, 1985
).
The intrinsic cardiac pacemaker rate is also reset with cold acclimation,
with heart rate (fH) being higher than it would be
following an acute decrease in temperature. This elevation in
fH, which is obviously important in maintaining
, involves alterations to membrane ion
channel function and density, the details of which have been recently
discovered and reviewed (Vornanen et al.,
2002a
,b
).
For example, the repolarizing K+ currents (Ik), which
affect the shape and duration of the action potential (AP), are altered in
cold-acclimated rainbow trout and this partially compensates for a
cold-induced prolongation of the AP. Specifically, the density of the inward
rectifier potassium current, Iki, is depressed in the ventricle,
while that of the delayed rectifier current, Ikr, is strongly
increased: the net effect is that AP duration and presumably the
refractoriness of the heart are shortened.
Similarly, the delivery of calcium to troponin C, which initiates the
contractile event and regulates the strength of cardiac contraction, is
clearly plastic in fish and responds to temperature. Calcium entry into
cardiomyocytes via the L-type Ca2+ channel
(ICa) plays an important role in cardiac contractility, including
triggering the release of intracellular Ca2+ from the sarcoplasmic
reticulum (SR) and directly activating the myofilaments. Ion flow through
cardiac L-type Ca2+ channels in mammals, and
surprisingly also rainbow trout, is extremely temperature sensitive, with peak
current having a Q10 of 1.82.1 for acute temperature changes
(Kim et al., 2000;
Shiels et al., 2000
). However,
in rainbow trout, a slowing of channel inactivation and a prolongation of the
AP counteracts the depressive effect of cold temperature on peak
ICa such that the net calcium charge transfer is essentially
independent of an acute temperature change
(Shiels et al., 2000
). With
cold-acclimation the AP is shortened through the plasticity of the sarcolemmal
K+ channels (noted above), and although the density of
ICa when measured at room temperature is the same for cold- and
warm-acclimated rainbow trout and carp, the rate of ICa
inactivation is greater for the cold-acclimated fish
(Vornanen, 1998
). Given the
temperature dependent decrease in myofilament Ca2+ sensitivity, it
seems likely that a compensatory increase in Ca2+ from another
source is needed to maintain the same force of contraction at low temperature
(see Vornanen et al.,
2002a
,b
).
In this regard, cold-induced proliferation of SR (another source of activator
Ca2+ for contraction) has been observed and cold-acclimated fish
respond more robustly to ryanodine (an SR Ca2+ release agonist),
especially when the tissue is acutely warmed (see
Shiels et al., 2002
). Thus, to
activate muscle contraction, a larger SR capacity could compensate for a
smaller SL Ca2+ trigger. However, the possibility that cold-induced
hyperplastic cardiac growth could enhance the myocyte to surface area to
volume ratio, and thus augment sarcolemmal-dependent processes, has not been
thoroughly explored.
Extrinsic modulation of the heart is also altered by temperature
acclimation, and in this regard certain cellular transduction mechanisms are
known to show temperature-dependent plasticity. Wood et al.
(1979) showed that cholinergic
inhibitory tonus in rainbow trout is more important in setting routine heart
rate at cold temperatures, while adrenergic excitatory tonus is relatively
more important at high temperature. However, temperature effects on the
adrenergic signal transduction pathway that controls ventricular contractility
appear to be opposite to those seen for heart rate. In particular, the rainbow
trout myocardium becomes more responsive to ß-adrenergic stimulation with
cold acclimation. This is due to an increase in the density of SL
ß-adrenoceptors (Keen et al.,
1993
) and an upregulation of the secondary messenger cascade
(Keen, 1992
), and the former
response clearly needs further study to determine whether receptors are being
sequestered and cycled to the membrane, or whether genes are being turned on
to make more receptors. ß-adrenergic stimulation shortens the AP and
stimulates ICa (Shiels et al.,
2002
). In fact, the possibility exists that tonic adrenergic
stimulation may be critical for adequate L-type Ca2+
channel function at cold temperatures in rainbow trout
(Shiels et al., 2004
), as well
as proper atrioventricular coordination
(Graham and Farrell,
1989
).
While much has been learned about the mechanistic basis for cardiac
plasticity in rainbow trout, limited studies with other fish species clearly
point to alternative patterns of cardiac plasticity. For example, the hearts
of Arctic charr Salvelinus alpinus reared at 15°C are
1530% larger, not smaller, than the hearts of fish reared at 5°C
(Ruiz and Thorarensen, 2001).
Carp are an extremely eurythermal family, and winter dormancy in Cyprinus
carpio is associated with a suppression of routine cardiac power output
(Q10
4) through intrinsic mechanisms rather than cholinergic
suppression of cardiac activity (J. A. W. Stecyk and A. P. Farrell,
unpublished data). Conversely, Carassius carassius, which survives
winter anoxic conditions by fermenting glucose to alcohol, maintains cardiac
activity (J. A. W. Stecyk et al., unpublished data) despite increased cardiac
refractoriness (Tiitu and Vornanen,
2001
). The ability of the Pacific bluefin tuna Thunnus
orientalis heart to maintain cardiac pumping at cold temperatures that
are refractory to hearts from other tuna species appears to be directly
related to a high SR Ca2+ ATPase activity, and this cardiac feature
may be a primary adaptation that allows this species to forage to deeper and
colder depths (Blank et al.,
2004
). Similarly, the burbot Lota lota, which also
remains active in deep lakes during winter, has an unusually high SR
Ca2+-release at 1°C, which is reduced at warmer acclimation
temperatures (Tiitu and Vornanen,
2002
). The idea that the pattern of cardiac plasticity for
cold-active fishes differs from cold-inactive fishes is also supported by data
on thermal compensation of heart rate and twitch kinetics in yellow perch
Perca flavescens vs sea raven Hemitripterus americanus
(Driedzic et al., 1996
), and
by data on the cardiac responses of sympatric bass species with differences in
winter activity (Cooke et al.,
2003
).
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Sexual maturation |
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The trout heart has a significant population of androgen receptors
(Pottinger, 1988;
Fitzpatrick et al., 1994
),
which probably mediate the increased protein synthesis needed for
maturation-induced cardiac enlargement in response to elevated levels of
circulating androgens. However, Clark and Rodnick
(1999
) provide evidence for
two scenarios where changes in haemodynamics with maturation may also promote
ventricular hypertrophy. For example, an androgen-dependent expansion of blood
volume could increase both venous pressure and VS (through
the Starling response), and cause stretch-induced remodeling. Similarly,
work-induced remodeling could occur if androgens increase blood pressure
through alterations in vascular tone and resistance.
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Feeding, exercise and inactivity |
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Exercise training
Aerobic training alters various components of the salmonid cardiovascular
system, inducing cardiac growth
(Hochachka, 1961;
Farrell et al., 1990
), and
increasing
max, certain
cardiac enzymes, haematocrit, arterial O2 content, skeletal muscle
capillarity and tissue O2 extraction (Hochahcka, 1961;
Davie et al., 1986
;
Farrell et al., 1991
;
Gallaugher et al., 2001
).
These exercise-induced changes, however, are often small and variable
(Davison, 1989
), and even the
25% increase in
O2max brought
about by a 3 month intense training regime
(Fig. 1) is small relative to
the twofold variability in
O2max that often
exists among individual fish. Thus, although many individual components
responsible for internal arterial O2 convection show plasticity,
the sum of the changes in individual components produce, at best, about a 25%
improvement in metabolic capacity.
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Because tissue O2 extraction can increase with training, and the
O2 supply to the heart's spongy myocardium comes from
oxygen-depleted venous blood (Davie and
Farrell, 1991; Farrell and
Clutterham, 2003
), the possibility exists that training-induced
cardiac growth occurs predominantly in the compact myocardium, which receives
oxygen-rich coronary arterial blood. This pattern of cardiac growth would be
consistent with that seen in sexually maturing male trout (see above);
however, this possibility remains to be studied.
Aquaculture
Aquaculture conditions contrast with food deprivation and exercise-training
studies in that fish become less active and are often overfed, and cardiac
morphology certainly changes in salmonids raised for aquaculture. The normally
distinct pyramidal structure of the ventricle
(Fig. 2A) becomes more rounded
(Fig. 2B,D), resembling the
morphology of sedentary fish species (see
Santer et al., 1983). Fat
deposition can increase around the heart
(Fig. 2B,C) and cardiac
deformities may develop (Fig. 2E
vs F). Further, studies show that the enhanced growth
rates associated with aquaculture increase the rate of development of coronary
arteriosclerosis (Saunders et al.,
1992
; Farrell,
2002
), and that cultured salmonids have a decreased swimming
capacity compared to wild fish (Duthie,
1987
; Brauner, 1994; MacDonald
et al., 1998
). While these observations all point to diminished
cardiac performance, direct measurements of cardiac performance in fish
displaying the above morphological changes have not been performed. Moreover,
two recent studies indicate that maximum cardiac function may not be different
between wild and hatchery-reared salmonids. Dunmall and Schreer
(2003
) examined whether there
is a genetic component to domestication by measuring swimming performance and
in vivo maximum cardiac function in genetically distinct adult farmed
and wild Atlantic salmon raised in identical conditions, and found no
difference between the two groups. Further, maximum in situ cardiac
function for two groups of pond-reared (domesticated) rainbow trout was found
to be no different from either wild or sea-ranched (fish from wild stock,
raised in hatcheries until smolts and then released into the wild) steelhead
trout (Table 3; A. K. Gamperl
et al., unpublished data).
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|
While a definitive answer as to whether aquaculture/domestication affects
maximum cardiac function requires more refined/controlled studies, aquaculture
practices such as triploidy certainly alter cardiac physiology. Cardiomyocytes
are 60% larger in triploid brown trout than in diploid rainbow trout, and they
have an increased sensitivity to ryanodine (a blocker of SR Ca2+
release; Mercier et al.,
2002). Perhaps the enhanced role for SR calcium release in the
contraction of triploid cardiac muscle reflects the decrease in cellular
surface to volume ratio associated with cell enlargement and a concomitant
limitation to ICa via L-type Ca2+
channels.
When growth rate is further enhanced using growth hormone (GH) transgenic
fish, swimming performance and
O2max can be
either reduced (Farrell et al.,
1997
; Lee et al.,
2003a
) or no different
(Stevens et al., 1998
;
McKenzie et al., 2000
). With
respect to the potential for cardiac changes in GH transgenic fish, we are
only aware of one study. Pitkänen et al.
(2001
) found that the relative
ventricular mass (RVM) of GH transgenic animals was enhanced by 60%
vs size-matched controls, and suggested, based on non-significant
differences in myocardial DNA contents (2.54 mg g1 in
transgenics vs 2.69 mg g1 in size-matched
controls), that this difference was due to hypertrophy alone.
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Hypoxia |
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Whether such adaptations are found in more active, hypoxia-sensitive,
species is unclear. Bushnell et al.
(1984) reported that 3 weeks
of hypoxic acclimation (PO2
40 mmHg) failed
to enhance the swimming performance or oxygen consumption of rainbow trout
when swum at this O2 level, which argues against significant
hypoxia-induced compensation in trout heart function. In contrast, recent
experiments (Faust et al.,
2004
; vs Gamperl et
al., 2001
; Gesser,
1977
; Fig. 3) show
cardiac differences among rainbow trout obtained from different hatcheries,
and report an unusual degree of myocardial hypoxia tolerance for fish reared
at a facility where oxygen and other water quality parameters are sub-optimal.
Clearly, further experiments are required to determine whether these
differences in myocardial hypoxia tolerance are a result of acclimation to
poor water quality (e.g. low O2 saturation) or of genetic selection
by hatchery operators.
|
Preconditioning
So far, this review has focused on cardiac alterations following long-term
environmental change. However, recent research shows that fish can also
respond rapidly to acute hypoxic exposure. Zebrafish Danio rerio
exposed to just 48 h of non-lethal hypoxia
(PO2=15 mmHg) have a significantly increased
survival time (by 9x in males and 3x in females) when subsequently
exposed to more severe hypoxia (PO2=8 mm Hg)
(Rees et al., 2001). Further,
Gamperl et al. (2001
)
demonstrated a cardioprotective response, in that pre-exposure to only 5 min
of hypoxia (PO2=510 mmHg) completely
eliminated the loss of in situ maximum cardiac function that normally
follows 15 min of exposure to hypoxia in rainbow trout
(Fig. 4A). This
cardioprotective response, termed preconditioning, is broadly defined as the
ability of brief periods of stress (e.g. hypoxia, ischaemia, stretch, heat
shock) or biochemical/pharmacological substances to make tissues resistant to
damage caused by a subsequent period of ischaemia or hypoxia. Gamperl et al.
(2001
) provided the first
evidence (using hypoxia-sensitive trout) that preconditioning exists in
fishes, and thus that preconditioning is a mechanism of cardioprotection that
appeared early in the evolution of vertebrates. In mammals, numerous cellular
pathways and end-effectors are involved in preconditioning
(Okubo et al., 1999
;
Nakano et al., 2000
;
Yellon and Downey, 2003
). No
experiments have directly investigated the cellular mechanisms that mediate
myocardial preconditioning in fishes, although recent studies suggest that
sarcolemmal (Cameron et al.,
2003
) and mitochondrial
(MacCormack and Driedzic,
2002
) ATP-sensitive K+ channels, and MAPK signaling
pathways (ERK, JNKs and p38-MAPK;
Gaitanaki et al., 2003
) may be
involved.
|
The importance and indeed existence of preconditioning in hypoxia-tolerant
vertebrate hearts has been questioned in recent years. For example, ischaemic
preconditioning failed to improve contractile function following 40 min of
global ischemia in hypoxia-tolerant neonatal rat hearts (1 or 4 days post
partum), only slightly (by 7%) improved contractile function in relatively
hypoxia-sensitive rat hearts tested 7 days post partum
(Ostadalova et al., 1998), and
Baker et al. (1999
) showed that
hearts from 710 day old rats that were reared in a hypoxic environment
(12% oxygen) no longer experienced increased functional recovery in response
to preconditioning. In contrast, both Tajima et al.
(1994
) and
Nechá
et al. (2002) demonstrated that although hearts from
chronically hypoxic adult rats had increased resistance to ischaemia-related
damage, preconditioning conferred an additional amount of protection. Thus, to
examine whether hearts from hypoxia-tolerant trout can be preconditioned, we
recently conducted in situ studies on two different
populations of rainbow trout that display an unusual degree of myocardial
hypoxia tolerance. Gamperl et al.
(2004
) performed in
situ experiments using trout with hearts that Faust et al.
(2004
;
Fig. 3) previously identified
as hypoxia-tolerant (again using 5 min of hypoxia as the preconditioning
stimulus), while Overgaard et al.
(2004
) used a population of
trout from British Columbia (Canada) and 2x 5 min cycles of hypoxia or
exposure to high adrenaline (250 nmol l1) as preconditioning
stimuli. Both studies (e.g. Fig.
4B) showed that hypoxia-tolerant trout hearts could not be
preconditioned, and thus that the protection afforded by inherent myocardial
hypoxia tolerance and preconditioning was not additive. These data suggest
that the relationship between hypoxic adaptation and preconditioning in the
trout heart resembles that of the neonatal/immature, not adult, mammalian
heart.
It is tempting to associate myocardial preconditioning with myocardium that
is supplied with blood from the coronary circulation because the rat heart
becomes increasingly dependent on its coronary circulation as it ages, and
rainbow trout possess a coronary circulation
(Tota et al., 1983) that
supplies blood to the compact myocardium, which comprises the outer one-third
of the heart (Fig. 5). However,
the hypoxia-sensitive heart of Atlantic cod Gadus morhua, which lacks
a coronary circulation and is composed entirely of spongy myocardium, can be
preconditioned (A. G. Genge and A. K. Gamperl, unpublished;
Fig. 6) in much the same way as
rainbow trout (Gamperl et al.,
2001
). Why cod hearts that have only spongy myocardium and display
a moderate degree of hypoxia tolerance, but not trout hearts that have
developed a high degree of hypoxia tolerance
(Gamperl et al., 2004
;
Overgaard et al., 2004
), can
be preconditioned is not known. However, investigations into the cellular
mechanisms that mediate these differences are likely to provide valuable
information on how the hearts of fish and other lower vertebrates deal with
oxygen deprivation.
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Cardiac variability among fish stocks |
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Summary and perspective |
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Recently, we have shown that a preconditioning-like phenomenon exists in
fishes, that there is a significant degree of intraspecific variation in
myocardial hypoxia tolerance and the ability to be preconditioned among
rainbow trout, and that the spongy myocardium of cod can be preconditioned.
These findings strongly suggest that protective pathways can still be
stimulated in myocardium that is normally perfused by blood of low oxygen
partial pressure, and that preconditioning and acquired hypoxia tolerance in
trout are mediated by the same or similar cellular mechanisms. Further, we
provide substantial indirect evidence that trout myocytes are not permanently
damaged by exposure to prolonged periods (15 min to 4 h) of severe hypoxia,
even though contractile function is diminished
(Gamperl et al., 2004;
Overgaard et al., 2004
; J.
Overgaard and J. A. W. Stecyk, unpublished). While this enhanced ability of
rainbow trout hearts to tolerate long periods of severe hypoxia as compared
with mammals is likely to be related in part to temperatures
(1015°C vs 37°C) and absolute workload, we suspect
that there are also mechanistic reasons for this difference.
In this review we have demonstrated that the fish heart has tremendous capacity to respond to both short-term and long-term perturbations, and hint at mechanistic explanations of how this is accomplished. However, it is apparent that we have little understanding of the molecular and biochemical signaling pathways that mediate much of this plasticity. Important and obvious questions include: What cellular events are responsible for stimulating hyperplastic vs hypertrophic growth of the fish heart? Which signal transduction pathways and end-effectors mediate preconditioning and inherent hypoxia tolerance of the fish myocardium, and how do they compare with those in mammals? Why does the trout heart not experience permanent damage (necrosis) when exposed to severe hypoxia or anoxia for periods up to 4 h? Our challenge, therefore, is to design experiments that will provide insights into the novel control mechanisms that mediate myocardial plasticity and adaptation in fish.
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Acknowledgments |
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