Effect of coronary perfusion on the basal performance, volume loading and oxygen consumption in the isolated resistance-headed heart of the trout Oncorhynchus mykiss
1 Università degli studi di Napoli `Federico II', Dipartimento di
Fisiologia Generale ed Ambientale, via Mezzocannone 8, 80134-Napoli,
Italy
2 Institute of Biology, Odense University, Campusvej 55, DK-5230, Odense,
Denmark
* Author for correspondence (e-mail: agnisola{at}unina.it)
Accepted 22 July 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: heart, trout, Oncorhynchus mykiss, coronary circulation, volume loading, mechanical efficiency
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
As only part of the myocardial tissue is supplied by coronary arteries, it
is likely that the fish heart does not have an obligatory dependence on its
coronary blood flow (Farrell,
2002). Only the skipjack tuna heart, whose ventricle contains up
to 60% of compacta, is thought to be obligatorily dependent on its coronary
circulation (Farrell et al.,
1992
). On the other hand, there are several indications that
coronary circulation is essential under conditions of both hypoxia and intense
swimming activity. In trout, coronary flow can increase during exercise or
hypoxia (Gamperl et al.,
1994
), and coronary ligation resulted in a reduced proportion of
compact myocardium together with a decrease in a series of metabolic enzymes
(Farrell et al., 1990
;
Gamperl et al., 1994
).
Moreover, the long-term significance of coronary circulation was demonstrated
by the fact that arteries can grow around the ablation site in 14 days
(Farrell et al., 1990
). The
modulation of coronary flow under conditions of hypoxia or swimming suggests a
neurohumoral and/or local regulation of the coronary resistance and
consequently of the perfusion of the myocardium. Although the mechanism for
such regulation in vivo is not known, a number of studies in
vitro suggest that a complex interaction between various circulating and
paracrine factors is involved (Mustafa et
al., 1992
; Mustafa and
Agnisola, 1994
; Agnisola et
al., 1996
; Mustafa and
Agnisola, 1998
).
There is no direct evidence for the mechanical significance of compacta perfusion. Information on the interplay between coronary physiology and ventricle performance in teleosts is derived from in situ and in vitro work. One limitation of these studies is that in all the preparations used, the heart was working against a fixed pressure (pressure head) rather than against a resistance. In vivo, aortic pressure and flow result from the matching of vascular resistance and the capacity of the heart to produce force and then to move blood. This cannot be simulated under pressure-head in vitro conditions, where the heart is constrained by the need to produce a minimal constant pressure in order to get flow. Also, coronary flow can barely be synchronised with heart requirements, something that in vivo is self-accommodated via changes in the pressure generated by the heart and local, paracrine and/or metabolic mechanisms. The aim of the present study was to define the role played by a well supplied compacta in fish heart performance using a simple protocol (with or without coronary perfusion) in an in vitro preparation in which the isolated trout heart was working against a resistance, as in vivo, and with the coronary flow related to the ventricular function on a beat-to-beat basis. The results provided evidence for some self-regulating properties of the teleost heart.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Dissection and preparation of the isolated trout heart
Fish were injected with heparin (1 ml kg-1 of a 0.9% NaCl
solution containing 300 units heparin ml-1) in the caudal vein and
killed by a quick blow on the head. The thorax was cut open and after removing
the pericardium the entire heart was dissected out. The atrium, ventral aorta
and coronary artery were cannulated as previously described
(Mustafa et al., 1992
;
Agnisola et al., 1994
). The
isolated heart was pre-perfused with ice-cold saline solution during the
cannulation procedure to clear the blood from the lumen and coronary arteries.
The entire procedure from opening of thorax to coronary cannulation took
approximately 15 min. After cannulation the heart was mounted in the perfusion
chamber.
The experimental set-up
The perfusion chamber, a double-jacketed chamber similar to that previously
described (Houlihan et al.,
1988; Agnisola et al.,
1994
), was connected to a water bath (RM6 Lauda, DRR.WOBSER GMBH
& Co. KG, Lauda-Königshofen, Germany), which maintained a chamber
temperature of 10±0.5°C. The input and output reservoirs were at
the fixed heights of 7 cm and 10 cm from the level of saline in the chamber,
respectively, and were connected to each other via a small tube as
described by Agnisola et al.
(1998
)
(Fig. 1), which enabled
perfusion of the isolated heart with 50 ml of recirculating saline. The input
and output loadings on the heart were set through resistances according to
Agnisola et al. (1998
).
Briefly, the input loading on the heart was set by a variable resistance
(Ri) and the saline level difference between the input
reservoir and the heart. Output resistance was set by a fixed resistance
(Ro) in the output tube (a teflon tube 17.8 cm long, 0.5
mm i.d.). The input to the coronaries was via a side arm on the
output tube before Ro, and a constant resistance
(Rc, consisting of a nylon tube 10 cm long, 0.3 mm i.d.)
allowed the coronary input pressure to be directly related to the pressure
generated by the heart. The experimental set-up was placed in a refrigerated
cabinet set at 10°C. No detectable temperature changes occurred while
opening and closing the glass door of the cabinet.
|
Once mounted in the perfusion chamber, the heart was wrapped with a transparent plastic film. Although not properly simulating a pericardium (no negative preload was generated), this procedure avoided overstretching of the atrium during volume loading of the preparation.
The saline in the input and output reservoirs was gassed with 99.5%
O2 and 0.5% CO2 throughout the entire experiment, taking
care not to trap any air bubbles in the system. The perfusate was Cortland
saline (Wolf, 1963) as
modified by Farrell et al.
(1986
) and Farrell
(1987
), of composition (in g
l-1): NaCl, 7.25; KCl, 0.23,
MgSO4·7H2O, 0.23;
NaH2PO4·H2O, 0.016;
NaHPO4·2H2O, 0.28; glucose, 1.0;
polyvinylpyrrolidone (PVP) 10.0; CaCl2. 2H2O, 0.37; the
pH was adjusted to 7.9 at 10°C with NaHCO3 (approx. 1 g
l-1).
Measurements and calculations
Atrial pressure was measured through a small saline-filled rigid tube, the
side arm of the atrial-cannula support in the chamber wall, connected with the
pressure transducer (Baxter, USA). Aortic and coronary pressures were measured
through saline-filled side arms connected to the pressure transducer.
Pressures were acquired sequentially at 5 min intervals from chamber, atrium
and saline-filled tubes placed upstream and downstream of
Ro and downstream of Rc, via
a computer controlled set of valves (Fig.
1). The inset in Fig.
1 is a typical pressure trace recorded upstream of
Ro (aortic pressure), and shows that the pressure pulse
was very similar to that usually recorded in vivo
(Holeton and Randall, 1967;
Wood and Shelton, 1980
).
Pressures (kPa) was measured using the pressure in the perfusion chamber as
reference. Atrial preload (end-diastolic atrial pressure, Pa) and
ventricular preload (mean atrial pressure, PV) were
determined from the atrial pressure recordings. Corrections were made for
aortic and coronary cannulae resistances to obtain afterload (= mean aortic
pressure) and coronary input pressure (= mean pressure in the coronary artery,
PC), respectively. At the end of each experiment, the
ventricle was dissected, blotted dry and weighed. Heart rate
(fH; beats min-1) was determined from pressure
records. Cardiac output (
; ml
min-1 kg-1) and coronary flow (FC;
ml min-1 kg-1) were calculated from the fall of mean
pressure (calculated from the pressure data acquired over a period of 10 s)
through Ro and Rc, respectively.
Stroke volume (VS; ml kg-1) was determined by
the relationship:
/fH. The power
output (PO; mW g-1) of the heart was calculated as:
[(afterload - preload) (kPa) x
(
+FC) (ml
min-1 kg-1) x animal mass (MA)
/ ventricle mass (MV) / 60. Stroke work
(WS; mJ g-1) was calculated as:
POx60/fH. Coronary resistance
[RC; TPa s m-3 (note that
T=tera=1012)] was calculated as: PC
(kPa)x0.06/FC (ml min-1). The factor 0.06 is
necessary to convert coronary flow to ml s-1 and pressure to TPa
(Mustafa and Agnisola,
1998
).
Oxygen consumption of the heart was determined as follows:
,
where PiO2 is the input
PO2, PoO2 is the
output PO2,
w,O2
is the oxygen solubility of the saline (ml O2 l-1
g-1), and
is the cardiac
output in ml min-1 g-1. Oxygen partial pressure
(PO2) was measured using a 16-730 oxygen
electrode (Microelectrodes, Inc., Bedford, NH, USA) thermostatted at 10°C.
The sensor was calibrated with sodium sulphite/borax solution for zero
PO2, and with air-equilibrated saline for
20.94% oxygen. Linearity of the sensor response up to 100% oxygen was checked,
and the percentage properly converted to oxygen partial pressure (in mmHg).
Mechanical efficiency of the heart (i.e. the ratio between mechanical work and
energy consumption, expressed as %) was determined as: 100 x
(POx0.0498) x
O2, where
PO is the power output in mW and
O2 is the rate
of oxygen consumption in ml min-1 [assuming that 1 mW
s-1 (1 mJ) is equivalent to 0.0498 µl O2
min-1 (Davie and Franklin,
1992
)]. We also assumed that the heart mainly worked aerobically,
so that the energy source of the heart was considered proportional to the
oxygen consumption.
Experimental protocols
Basal conditions
After mounting the isolated cannulated trout heart in the chamber, and
putting an input load on the atrium, the heart started working against the
fixed resistance, recirculating the 50 ml saline solution. Any leaks in the
heart were discovered by a decrease in the saline level in the input reservoir
and these hearts were discarded. The isolated working heart was left for a
period of at least 30 min to stabilize, i.e. when the heart had settled into
regular beating. Hearts that did not stabilize were discarded. At the end of
the stabilization period, the cardiac output was adjusted to approximately 15
ml min-1 kg-1
(Houlihan et al., 1988;
Agnisola et al., 1994
) by
changing the variable input resistance (Ri). As soon as a
basal cardiac output was obtained, automatic recording of pressure at 5 min
intervals was begun; seven determinations were made for a total period of 30
min perfusion under basal conditions. At the end of this period, the oxygen
consumption of the heart was determined.
Volume loading
At the end of the 30 min period of perfusion under basal conditions, the
filling pressure was increased (by varying Ri) in seven
steps of 5 min each and the pressure measured at each step. When maximal
stroke work was reached, oxygen consumption was measured again.
Statistics
All values are means ± S.E.M. One-way analysis of
variance (ANOVA) was used to test the time course of the effect of different
parameters during basal perfusion. Two-way ANOVA was used to analyse the
changes in stroke work, ventricular preload and afterload during volume
loading. P<0.05 was taken to indicate statistical significance.
Statistics were performed with GraphPad Prism (GraphPad Software, Inc., San
Diego, CA, USA).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
In the -CF group, although the initial set of atrial preload was not significantly different from that of the +CF group, the atrium adjusted within 5 min to a significantly higher preload value (Fig. 2), which remained constant during the remaining perfusion period at the basal setting. As a consequence, mean atrial pressure also increased up to about 0.3 kPa. The increased preload in the -CF group of hearts was associated with a significant reduction in cardiac output and power output (Fig. 3A). Stroke volume and stroke work were consistently lower in the -CF hearts (Fig. 3B), although the difference was not statistically significant. There was no difference in afterload and heart rate between the two groups (Fig. 3C).
In the +CF group, coronary performance, as evaluated by coronary pressure, flow and resistance values, was constant throughout the 30 min perfusion period under basal conditions (Fig. 4).
|
Effect of coronary perfusion on the heart's response to volume
loading
At the end of the 30 min period of basal perfusion, hearts were challenged
with a stepwise increase in input pressure, with consequent increases in
atrial and ventricular preloads (volume loading). The stroke work-preload
curves determined in the two experimental groups are shown in
Fig. 5. Volume loading induced
a doubling of stroke work in both groups, although the overall response was
significantly affected by the perfusion of coronaries. In the +CF hearts the
curve was significantly shifted left: higher stroke work values were obtained
at lower preloads. Also, the maximal stroke work value observed was lower in
the -CF hearts (3.36±0.35 mJ g-1) than in the +CF hearts
(3.77±0.28 mJ g-1). The coronary flow in the +CF group of
hearts remained constant during volume loading
(Fig. 5, inset A), while there
was a significant enlargement in coronary resistance that increased from a
basal value of 0.30±0.09 TPa s m-3 up to 0.91±0.30
TPa s m-3 at maximal loading (significant change; repeated-measures
one-way ANOVA, P<0.05).
|
It is worth noting that in our resistance-headed preparation, volume loading induced increases in both stroke volume and aortic pressure. As can be seen in Fig. 5, inset B, coronary perfusion did not significantly affect pressure generation. In both the +CF and -CF hearts, there was a significant increase in afterload (about 40%). This increase was associated with a significant increase in both diastolic and systolic aortic pressure, with no significant differences between +CF and -CF hearts. In fact, in the +CF group, diastolic pressure increased from the basal level of 2.98±0.19 kPa up to 4.45±0.22 kPa at the maximal volume loading. The corresponding systolic pressure values were 6.14±0.34 kPa and 9.94±0.55 kPa, respectively. In the -CF group, diastolic pressure augmented from the basal level of 3.28±0.43 kPa up to 4.68±0.40 kPa at the maximal volume loading. The corresponding systolic pressure values were 6.25±0.59 kPa and 9.78±0.98 kPa, respectively. So, there was an approximately 70% increase in pulse pressure in both groups, associated with a corresponding significant increase in stroke volume, which then accounted for most of the increase in stroke work during volume loading. Pulse pressure and stroke volume were consistently lower in the -CF hearts (data not shown).
Effect of coronary perfusion on oxygen consumption and mechanical
efficiency of the trout heart.
The total oxygen consumption and the mechanical efficiency of the heart
measured under basal perfusion conditions and at maximal volume loading are
shown in Fig. 6. In both +CF
and -CF hearts, volume loading induced a significant increase in rate of
oxygen consumption, from a basal level of approximately 20 µl O2
min-1 g-1 to approx. 40 µl O2
min-1 g-1 at maximal volume loading. In both groups,
basal mechanical efficiency was about 17% and was not affected by volume
loading. Neither rate of oxygen consumption nor efficiency were affected by
coronary perfusion.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A main feature of the present study is the use of a resistance-headed
isolated heart preparation. In this preparation, the actual aortic pressure
and flow result from matching a fixed resistance (Ro),
simulating the peripheral resistance in vivo, and the intrinsic
capacity of the heart to produce force and then to move the perfusion saline
(Agnisola et al., 1998). The
resistance-headed condition, as occurs in vivo, was hereby
reproduced. More importantly, in this set-up the coronary flow was
continuously and automatically linked to the pressure generated by the heart.
In vivo, ventral aorta pressure and gill resistance determine the
driving force for coronary perfusion (the coronary pressure), a situation that
was reproduced in the perfusion set-up we used thanks to the fixed resistance
Rc. This allowed maintenance of the intrinsic and
reciprocal interactions between ventricle and coronaries on a beat-to-beat
basis, as occurs in vivo. While lacking the potential to dissect the
role of single specific features on heart performance (e.g. the effect of
pressure loading), the resistance-headed preparation that we used did allow
the isolated heart preparation to express some of the intrinsic
self-regulating mechanisms that determine the heart's global pump function
in vivo (Kresh and Armour,
1997
). Thus, this preparation is well suited for the study of the
relative significance of a well-perfused compacta on trout heart
performance.
The basal performance of the resistance-headed heart with the perfused
coronary vascular tree (+CF group) was close to that of a similar preparation
previously reported (Agnisola et al.,
1998), and similar to that of in situ or in
vitro pressure-headed preparations
(Farrell et al., 1986
;
Houlihan et al., 1988
;
Davie and Farrell, 1991
;
Davie et al., 1992
). As no
attempt was made to simulate the role of the pericardium in determining
absolute values of atrial preload (Farrell
et al., 1988
), the input pressure necessary to get basal cardiac
output was higher than the ambient pressure (approx. 0.1 kPa), and similar to
that reported previously for both pressure-headed
(Houlihan et al., 1988
) and
resistance-headed (Agnisola et al.,
1998
) isolated trout heart preparations. The pressure generated by
the heart was similar to that reported in vivo in the trout ventral
aorta (Kiceniuk and Jones,
1977
; Wood and Shelton,
1980
), while the coronary pressure was somewhat lower than the
in vivo dorsal aorta pressure
(Kiceniuk and Jones, 1977
;
Gamperl et al., 1995
). This
was probably a consequence of the lower coronary resistance in vitro
with respect to the value in vivo, due to the lower viscosity of
saline with respect to blood (by a factor of 2.5-3.5;
Farrell, 1987
). In agreement
with previously reported data in vitro
(Agnisola et al., 1998
;
Houlihan et al., 1988
),
coronary flow was 2-5% of cardiac output, and higher than the in vivo
values (1-2%, Axelsson and Farrell,
1993
; Gamperl et al.,
1994
), probably because both the viscosity and oxygen content of
saline were low compared with blood.
The absence of a coronary supply did not affect the heart rate and pressure generated by the heart, but significantly did affect the heart's capacity to maintain basal cardiac output, initially set at 15 ml min-1 kg-1, resulting in a significant reduction in the heart's power output. This result suggests that coronary perfusion was significantly affecting cardiac contractility. However, the consequences of this effect were apparently limited by self-regulating mechanisms, which led to a significant increase in preload which, via the Starling mechanism, would oppose the stroke volume reduction. This may explain the non-significant, although consistent, reduction in stroke volume and stroke work.
The dependence of cardiac contractility on a well-supplied compacta was
confirmed by the response of hearts to the volume-loading protocol. This was
accomplished by a stepwise increase in input pressure, with no attempt to
control other parameters. In particular, as the heart was working against a
fixed resistance, the increase in atrial preload caused a significant increase
in both stroke volume and afterload (Berne
and Levy, 1992). Thus the maximal stroke work thereby obtained was
the combination of an increase in both pressure and volume work. In the +CF
hearts, this effect was probably part of intrinsic adjustments that resulted
in a constant coronary flow despite the increased coronary resistance due to
the increased extravascular compression produced by the myocardium (systolic
strangulation of coronary perfusion;
Gamperl et al., 1995
). In the
absence of coronary perfusion, the shift of the stroke work-preload curve
towards the right, shown in Fig.
5, confirmed that a main effect of coronary perfusion and a main
role for the compacta were the increase in ventricular contractility, allowing
the heart to produce a greater stroke work at the same preload.
Several theoretical models based on the mammalian left ventricle have
suggested that the vascular and ventricular properties are matched to achieve
maximal transfer of mechanical energy or maximal ventricular metabolic
efficiency (Sunagawa et al.,
1983; Burkhoff and Sagawa,
1986
; Van den Horn et al.,
1985
; Toorop et al.,
1988
). De Tombe et al.
(1993
) have suggested that,
when confronted with variable vascular loading, these parameters are both kept
nearly maximal, although not precisely optimised. An interesting result of the
present study is the apparent independence of mechanical efficiency from
volume loading. This contrasts with previous data, obtained using
pressure-headed fish heart preparations
(Farrell and Steffensen, 1987
;
Davie and Franklin, 1992
),
showing lower efficiency at lower loads. It is possible that the combined
effects of the increased stroke volume (which should increase efficiency;
Shipke, 1994
) and afterload
(which may decrease efficiency; Shipke,
1994
) would help to maintain efficiency at a constant, nearly
optimal level. On the other hand, neither oxygen consumption nor efficiency
were affected by coronary perfusion. This result, which contrasts with the
reduction observed by Houlihan et al.,
(1988
) on a pressure-headed
preparation, may in part reflect the fact that coronary perfusion did not
affect afterload and heart rate, two major determinants of oxygen consumption
in fish (Farrell and Jones,
1992
). However, it may also indicate that the interplay and
integration of the different homeodynamic mechanisms operating in the heart,
help control its energetics under a wide range of variations of extrinsic and
intrinsic factors, including coronary perfusion.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Agnisola, C., Venzi, R., Houlihan, D. and Tota, B. (1994). Coronary flow-pressure relationship in the working isolated fish heart: trout (Oncorhynchus mykiss) versus torpedo (Torpedo marmorata). Phil. Trans. R. Soc. Lond. B 343,189 -198.
Agnisola, C., Mustafa, T. and Hansen, J. K. (1996). Autoregulatory index, adrenergic responses and interaction between adrenoreceptors and prostacyclin in the coronary system of rainbow trout. J. Exp. Zool. 275,239 -248.[CrossRef]
Agnisola, C. and Tota, B. (1994). Structure and function of the fish ventricle: flexibility and limitations. Cardiosci. 5,145 -154.
Agnisola, C., Jensen, F. B., Tota, B. and Mustafa, T. (1998). Performance of the isolated rainbow trout heart perfused under self-controlled coronary pressure conditions: effects of high and low oxygen tension, arachidonic acid and indomethacin. J. Comp. Physiol. B 168,96 -104.
Axelsson, M. and Farrell, A. P. (1993). Coronary blood flow in vivo in the coho salmon (Oncorhynchus kisutch). Am. J. Physiol. 264,R963 -R971.[Medline]
Berne, R. M. and Levy, M. N. (1992). Cardiovascular Physiology. St Louis: Mosby-Year Book.
Burkhoff, D. and Sagawa, K. (1986). Ventricular efficiency predicted by an analytical model. Am. J. Physiol. 250,R1021 -R1027.[Medline]
Davie, P. S. and Farrell, A. P. (1991). Cardiac performance of an isolated heart preparation from the dogfish (Squalus acanthias): the effects of hypoxia and coronary artery perfusion. Can. J. Zool. 69,1822 -1828.
Davie, P. S. and Franklin, G. E. (1992). Myocardial oxygen consumption and mechanical efficiency of a perfused dogfish heart preparation. J. Comp. Physiol. B 162,256 -262.[Medline]
Davie, P. S., Farrell, A. P. and Franklin, G. E. (1992). Cardiac performance of an isolated eel heart: Effects of hypoxia and responses to coronary artery perfusion. J. Exp. Zool. 262,113 -121.[Medline]
De Tombe, P. P., Jones, S., Burkhoff, D., Hunter, W. C. and Kass, D. A. (1993). Ventricular stroke work and efficiency both remain nearly optimal despite altered vascular loading. Am. J. Physiol. 264,H1817 -H1824.[Medline]
Ewart, H. S. and Driedzic, W. R. (1987). Enzymes of energy metabolism in salmonid hearts: spongy versus cortical myocardia. Can. J. Zool. 65,623 -627.
Ewart, H. S., Canty, A. A. and Driedzic, W. R. (1988). Scaling of cardiac oxygen consumption and enzyme activity levels in sea raven (Hemitripterus americanus). Physiol. Zool. 61,50 -56.
Farrell, A. P. (1987). Coronary flow in a perfused rainbow trout heart. J. Exp. Biol. 129,107 -203.[Abstract]
Farrell, A. P. (2002). Coronary arteriosclerosis in salmon: growing old or growing fast? Comp. Biochem. Physiol. 132A,723 -735.
Farrell, A. P. and Jones, D. R. (1992). The heart. In Fish Physiology, vol.XIIA (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 1-88. New York: Academic Press.
Farrell, A. P. and Steffensen, J. F. (1987). An analysis of the energetic cost of the branchial and cardiac pumps during sustained swimming in trout. Fish Physiol. Biochem. 4, 73-79.
Farrell, A. P., MacLeod, K. R. and Chancey, B. (1986). Intrinsic mechanical properties of the perfused rainbow trout heart and the effects of catecholamines and extracellular calcium under control and acidotic conditions. J. Exp. Biol. 125,319 -345.[Abstract]
Farrell, A. P., Johansen, J. A. and Graham, M. S. (1988). The role of the pericardium in cardiac performance of the trout (Salmo gairdneri). Physiol. Zool. 61,213 -221.
Farrell, A. P., Johansen, J. A., Steffensen, J. F., Moyes, C. D., West, T. G. and Suarez, R. K. (1990). Effects of exercise-training and coronary ablation on swimming performance, heart size and cardiac enzymes in rainbow trout (Oncorhynchus mykiss). Can. J. Zool. 68,1174 -1179.
Farrell, A. P., Davie, P. S., Franklin, C. E., Johansen, J. A. and Brill, R. W. (1992). Cardiac physiology in tunas: I. In vitro perfused heart preparations from yellowfin and skipjack tunas. Can. J. Zool. 70,1200 -1210.
Gamperl, A. K., Pinder, A. W. and Boutilier, R. G.
(1994). Effect of coronary ablation and adrenergic stimulation on
in vivo cardiac performance in trout (Oncorhynchus mykiss).
J. Exp. Biol. 186,127
-143.
Gamperl, A. K., Axelsson, M. and Farrell, A. P. (1995). Effects of swimming and environmental hypoxia on coronary blood flow in rainbow trout. Am. J. Physiol. 269,R1258 -R1266.[Medline]
Holeton, G. F. and Randall, D. J. (1967). The effect of hypoxia upon the partial pressure of gases in the blood and water afferent and efferent to the gills of rainbow trout. J. Exp. Biol. 46,317 -327.[Medline]
Houlihan, D. F., Agnisola, C., Lyndon, A. R., Gray, C. and Hamilton, N. M. (1988). Protein synthesis in a fish heart: responses to increased power output. J. Exp. Biol. 137,565 -587.[Abstract]
Kiceniuk, J. W. and Jones, D. R. (1977). The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. J. Exp. Biol. 69,247 -260.
Kresh, J. Y. and Armour, J. A. (1997). The heart as a self-regulating system: integration of hemodynamic mechanisms. Technol. Health Care 5,159 -169.[Medline]
Mustafa, T. and Agnisola, C. (1994). Vasoactivity of prostanoids in the trout (Oncorhynchus mykiss) coronary system: modification by noradrenaline. Fish Physiol. Biochem. 13,249 -261.
Mustafa, T. and Agnisola, C. (1998).
Vasoactivity of adenosine in the trout (Oncorhynchus mykiss) coronary
system: involvement of nitric oxide and interaction with noradrenaline.
J. Exp. Biol. 201,3075
-3083.
Mustafa, T., Agnisola, C. and Tota, B. (1992). Myocardial and coronary effects of exogenous arachidonic acid on the isolated and perfused heart preparation and its metabolism in the heart of trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 103C,163 -167.[CrossRef]
Rodnick, K. J. and Williams, S. R. (1999). Effects of body size on biochemical characteristics of trabecular cardiac muscle and plasma of rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 122A,407 -413.
Shipke, J. D. (1994). Cardiac efficiency. Basic Res. Cardiol. 89,207 -240.[Medline]
Sunagawa, K., Maughan, W. L., Burkhoff, D. and Sagawa, K. (1983). Left ventricular interaction with arterial load studied in isolated canine ventricle. Am. J. Physiol. 245,H773 -H780.[Medline]
Toorop, G. P., Van den Horn, G. J., Elzinga, G. and Westerhof, N. (1988). Matching between feline left ventricle and arterial load: optimal external power and efficiency. Am. J. Physiol. 254,H279 -H285.[Medline]
Tota, B. (1983). Vascular and metabolic zonation in the ventricular myocardium of mammals and fishes. Comp. Biochem. Physiol. 76A,423 -437.[CrossRef]
Van den Horn, G. J., Westerhof, N. and Elzinga, G. (1985). Optimal power generation by the left ventricle. A study in the anesthetized open thorax cat. Circ. Res. 56,252 -261.[Abstract]
Wolf, K. (1963). Physiological salines for fresh-water teleosts. Prog. Fish. Cult. 25,135 -140.
Wood, C. M. and Shelton, G. (1980). Cardiovascular dynamics and adrenergic responses of the rainbow trout in vivo. J. Exp. Biol. 87,247 -270.[Abstract]