© 2002 by The Society for Integrative and Comparative Biology
The Intracardiac Shunt as a Source of Myocardial Oxygen in a Turtle, Trachemys scripta1
1 University of California, Irvine, Irvine, California 92697
 |
SYNOPSIS |
|---|
TOP
 SYNOPSIS INTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
The functional significance of many features of the reptilian cardiopulmonary system remains unknown; particularly the importance of cardiac shunts. One hypothesis for a physiological function for shunts is that they play a role in myocardial oxygenation and are therefore important when cardiac work is elevated. In this study we examined cardiac function by monitoring electrocardiograms in red-eared slider turtles (Trachemys scripta) with a reduced myocardial oxygen supply. Exposing the animals to a hypoxic gas mixture reduced oxygen levels in the pulmonary venous return. When cardiac work was elevated during hypoxia, the electrocardiogram changed in a manner consistent with myocardial hypoxia, suggesting enrichment of the luminal blood with oxygen by the intracardiac shunt facilitates cardiac performance.
|
INTRODUCTION |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
Biologists have been interested in the vertebrate cardiovascular system for hundreds of years (Panizza, 1833
; Griel, 1903; Axelsson and Franklin, 1996; reviewed in Hicks, 1998); yet there remain numerous features of this system with obscure functions. This is particularly true of the complex cardiovascular system of reptiles. Because the ventricles of reptiles are not completely subdivided into two chambers (with the exception of crocodilians and birds), mixing of oxygen-rich and oxygen-poor blood can occur within the ventricle. When blood is shunted from the left side of the ventricle to the right side of the ventricle, oxygen-rich pulmonary venous blood bypasses the body and is returned to the lung. This blood flow pattern is known as a left-to-right (L-R) shunt (Fig. 1A). Conversely, a right-to-left (R-L) shunt occurs when oxygen-poor systemic venous blood bypasses the pulmonary circulation and is returned to the body. Both birds and mammals evolved a circulatory system that completely separates oxygen-rich and oxygen-poor blood.
|
Historically, the avian and mammalian cardiovascular systems were considered to be more efficient than the reptilian system (Foxon, 1955
). However, when it became clear that the type and degree of cardiac shunting varies with the physiological state of the animal, the idea that shunts are adaptive became credible. Shunts have been hypothesized to confer a number of physiological advantages (Table 1) but data supporting or refuting many of these hypotheses are scarce.
|
One hypothesis for the functional significance of the L-R intracardiac shunt is that it oxygenates the heart (Farmer, 1997
, 1999). In mammals and birds, the heart is oxygenated by a coronary circulation, an extensive network of arteries, capillaries, and veins. In contrast, the hearts of most fishes, amphibians, and reptiles are primarily avascular. The cardiac tissue is a mesh of intercommunicating spaces (lacunae) and numerous strands or beams (trabeculae) of heart muscle (myocytes) encased by connective tissue, the epicardium. As the heart beats, blood flows to and fro through the lacunae. This tissue resembles a sponge and is called "spongy myocardium." The exchange of respiratory gases and nutrients occurs directly across the plasma membranes of the myocytes with blood contained within the lacunae (reviewed in Farmer, 1999). When coronary supported myocardium is found in reptiles, it is generally a thin layer of more compact fibers that form a shell just proximal to the epicardium. For example, Brady and Dubkin (1964) report that in a turtle (Chrysemys elegans) a distal shell of muscle, making up about 10% of the mass of the ventricle, is supplied oxygen through a coronary circulation. The remaining myocytes receive oxygen from luminal blood.
The L-R intracardiac shunt carries oxygen-rich blood into regions of the heart that would otherwise be oxygen-poor (Hicks and Malvin, 1995; Hicks et al., 1996). Thus, this shunt may be important for myocardial oxygenation. This hypothesis predicts that the L-R shunt will occur when the cardiac workload is elevated, since myocardial oxygen demands are greater when the heart is working hard than when the heart is at rest (Bing et al., 1972; Farrell et al., 1994, but see Jackson et al., 1995). In reptiles, cardiac workloads are not only elevated during exercise and immediately during recovery from exercise but also during periods of ventilation. Reptiles generally are intermittent lung breathers that exhibit a pronounced cardiorespiratory synchrony (reviewed in Hicks, 1998). When at rest during periods of apnea, these animals generally exhibit bradycardia and reduced cardiac output. During ventilation, there is generally an increase in heart rate and an elevation in cardiac output (Burggren, 1975; Shelton and Burggren, 1976; reviewed in Hicks, 1998).
As predicted by the hypothesis that a L-R shunt provides oxygen to the heart, previous research indicates that a large L-R shunt develops during exercise and during periods of ventilation (Shelton and Burggren, 1976; West et al., 1992; Hicks and Krosniunas, 1996; Wang and Hicks, 1996; Wang et al., 1997; Hicks and Wang, 1998). Although consistent with the hypothesis, these data do not demonstrate that a L-R shunt is serving to oxygenate the heart. The shunt may occur at these times for different reasons. For example, it has been shown that development of a L-R shunt is often associated with a reduction in R-L shunt, thus improving systemic oxygen transport by increasing systemic arterial saturation (Hicks, 1994). Consequently, more data are needed to determine the importance of L-R shunting for myocardial oxygenation. The following study was undertaken to assess cardiac performance of red-eared slider turtles deprived of elevated oxygen levels in the heart during periods of increased oxygen demand.
|
MATERIALS AND METHODS |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
Experimental design
A direct test of our hypothesis would be to completely subdivide the ventricle, preventing a L-R intracardiac shunt. Thus, it would be possible to determine whether myocardial function is reduced during periods of increased oxygen demands when oxygen-rich blood is prevented from shunting into the right side of the ventricle. However, subdividing the reptilian heart is not feasible. An alternative approach would be to reduce the magnitude of the L-R shunt by manipulating the vascular resistance in the pulmonary and systemic circulation, either pharmacologically or mechanically (Hicks et al., 1996
). However, this approach may confound the results by affecting the afterload or contractility of the heart. Hence, we used an indirect approach to examine the hypothesis that L-R shunts provide oxygen necessary for cardiac function under elevated demands by addressing the following question: If the ventricle were only exposed to blood that had a partial pressure of oxygen (PO2) similar to that of mixed systemic venous return during exercise, would cardiac function be affected?
We chose to address this question in turtles because more is known about when and how they shunt than for other reptiles. However, at low workloads the hearts of turtles are well known for their tolerance of anoxia (Jackson, 1987; Wasser et al., 1990; Jackson et al., 1991, 1995) and it is possible that the myocardium could function normally without any enrichment of blood oxygen from L-R shunts. Hence we investigated cardiac performance by monitoring the electrocardiogram (ECG) when the vigorously working heart was subjected to blood with a reduced PO2.
All experiments were conducted at 23°C. Furthermore, we carried out the experiments in several steps. First, we determined the pH and PO2 in the mixed systemic venous return in resting and in swimming turtles while normoxic gas passed through the air-hole of the swimming chamber. Then we reduced the percentage of oxygen in gas of the air-hole and swam the turtles. We decreased the fraction of inspired oxygen (FIO2) so that the PO2 of pulmonary venous blood approached values that were similar to those measured in the systemic venous return of normoxic animals (Fig. 1B). We estimated the PO2 of pulmonary venous blood by measuring the PO2 of the blood in the carotid artery. During a L-R shunt, the PO2 of blood in these vessels is approximately the same (Ishimatsu et al., 1996). There is a slight decrease in the oxygen levels of blood in the carotid compared to the blood entering the heart from the pulmonary vein due to the fact that some oxygen has been consumed by the myocytes. Nevertheless, by decreasing the oxygen levels in pulmonary venous blood, we ensured that the myocardium was bathed with blood containing a level of oxygen similar to that normally occurring in the systemic venous blood during exercise, even though the magnitude of the L-R shunt increased during activity. The sensitivity of the myocardium to this range of PO2s was assessed with ECGs. These experiments are referred to as series 1: Blood gases and electrocardiograms.
We then investigated the relationship between the ECG patterns and cardiac performance by measuring cardiac output and ECGs simultaneously when subjecting turtles to the same experimental regime. In addition, we were able to obtain arterial pressure measurements from three of these animals to examine cardiac power. These experiments are referred to as series 2: Blood flow and electrocardiograms.
In summary, our experimental design aimed to examine the ECG of a vigorously working heart while the heart was supplied with oxygen by blood that had a partial pressure of oxygen similar to what is found in the mixed systemic venous return of exercising turtles.
Animals
Red-eared sliders, Trachemys scripta, of mixed sex weighing 1.2 ± 0.5 kg were obtained from a commercial dealer (Lemberger Inc., Oshkosh, Wisc., USA). The animals were housed in large aquariums equipped with dry basking areas and heat lamps. They were fed a diet of live goldfish and kept under a 12:12 L:D photoperiod.
Swimming chamber
The swimming chamber (61 x 27.7 x 15.2 cm) consisted of a rectangular box. Four sides were constructed of acrylic and two ends of plastic grid. This chamber was set in a water-filled flume. The top of the swimming chamber contained an elevated acrylic "air-hole" (2.5 x 15.0 x 2.5 cm). The air-hole had a port on each end that allowed gases to pass through the chamber.
Data acquisition
All electrical signals were converted from analog to digital by an MP100 AD converter (Biopack System, Goleta, Calif., USA) and recorded on a Macintosh computer using AcqKnowledge software (Biopack System, Goleta, Calif., USA).
|
SERIES 1: BLOOD GASES AND ELECTROCARDIOGRAMS |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
Turtles (n = 5) of mixed sex (0.9 ± 0.4 kg) underwent surgery for blood collection and electrode placement. However, not all of the catheters were patent during the experiments. ECGs were obtained from all five animals.
Surgery
Turtles were anesthetized with halothane and the neck injected with Lidocain. The carotid and jugular were catheterized (PE 50 tubing) and the jugular catheter was slid into the vena cava to obtain samples of the mixed systemic venous return. Placements of the catheters were confirmed post-mortem. Catheters were flushed twice daily with heparinized saline (200 iu). The surgeries required 20 min and the animals recovered for at least 24 hr prior to experiments. Post-surgical analgesics and antibiotics were administered.
Electrocardiogram lead placement
Stainless steel nuts and bolts secured an electrode wire in small holes (1.6 mm) that were drilled in the shell at the junction of the plastron and carapace over each leg. Silicone insulated the bolt and wire. The three standard limb leads were recorded in the following way: lead 1 between the right and left forelimbs; lead 2 between the right and left hindlimbs; lead 3 across the left fore and hindlimbs. A fourth signal between the left hindlimb and an electrode placed ventrally over the center of the heart (analogous to the original precordial lead used on humans and referred to in this paper as lead 4 or as P). Additionally, a non-standard lead was observed across the left forelimb and right hindlimb. The signals were filtered with a bandpass filter (1 Hz to 3 kHz FWHM) and a notch filter (60 Hz) and amplified 5,000 fold (Grass P5, Quincy, Mass., USA).
Experimental protocol
A turtle was placed in the flume and given one hour to relax. Then ECGs were recorded during a period of ventilation and mixed systemic venous blood was drawn into a chilled glass syringe and analyzed immediately for PO2 and pH (Radiometer BMs MK2 blood gas analysis system; Copenhagen, Denmark). To prevent excessive blood withdrawal, no arterial samples were taken at this time. Ventilation was monitored visually. The turtle was then forced to swim while normoxic gas (FIO2 = 0.20) flowed through the breathing chamber. Five minutes into a 10 min bout of exercise, both venous and arterial blood-samples were drawn and analyzed. The animal was given 20 min to recover. The chamber was then flushed with hypoxic gas, either FIO2 = 0.10 or 0.05. After one hour of resting in the hypoxic gas mixture, ECGs were recorded during ventilation and both venous and arterial blood samples taken. The animal then swam while exposed to the hypoxic gas and another set of blood samples was taken. The animals recovered from exercise for 8–10 min while the air-chamber remained hypoxic, then they recovered an additional 20 min while normoxic gas flowed through the chamber.
|
SERIES 2: BLOOD FLOW AND ELECTROCARDIOGRAMS |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
Surgery
Turtles (n = 5) were anesthesized by ventilating their lungs (SAR-830 ventilator, CWE Inc., Ardmore, Penn., USA) with a 4% halothane gas mixture. Upon reaching anesthesia (no response to pinching of the limbs) the halothane concentration was reduced to 1%.
A rectangular opening (4 x 5 cm) cut into the plastron exposed the cardiovascular system. Ultrasonic flow probes (2R Transonic Systems, Inc., Ithaca, N.Y., USA) were placed around the following vessels: the left pulmonary artery (LPA), the left aorta (LAo), and the branch of the right aorta (RRAo) distal to the subclavian and carotid branching. This last site was selected due to its accessibility. It was used to estimate blood flow in the entire right aorta (RAo) in the following manner: QRAo = 1.85 x QRRAo. This estimate has been found to be valid for different physiological states (Comeau and Hicks, 1994) and has been studied for anaesthetized and recovered animals during both apnea and during ventilation in room air, as well as with anoxic animals (Wang and Hicks, 1996).
A small vessel branching from the left subclavian was occlusively cannulated (PE 50 tubing) for arterial blood pressure measurements. Post mortem, the cardiac ventricles were removed and weighed wet.
Electrocardiogram lead placement
Short sections (2 mm) of electrode wires (As 765-40 Cooner Wire, Chatworth, Calif., USA) were cleared of insulation and placed with a 25 gauge needle into the pericardium over the left and right atria and over the apical ends of the left and right sides of the ventricle. An additional electrode was placed over the center of the ventricle. A small drop of Nexaband glue held the electrodes in place. The ECG wires were connected to shielded wire (5/30-4046SJ) and the electrical signals from these leads represented an Einthoven triangular arrangement. Lead 1 refers to the signal obtained when recording from the wires connected over the left and right atria, lead 2 from the right atrium and left apex, lead 3 across the left atrium and left apex, and lead 4 across the center of the ventricle and the left apex (analogous to the original precordial lead). The signals were processed as described previously. The excised piece of plastron was glued into place with epoxy. Antibiotics (Baytril 2.5 mg/kg, daily) and analgesic (0.5 mg/kg Flumeglumine, daily) were administered intramuscularly after the surgery. Animals were given seven to ten days to recover from the surgery.
Calculation of cardiac power
Ventricular systemic power output, VSPO (mW), was calculated per gram of wet ventricular mass during the last minute of the exercise period by multiplying the mean systemic blood pressure by the systemic blood flow (LAo + RAo flow).
Protocol
The same protocol was used and is described above in the section entitled "Blood gas and electrocardiogram."
|
RESULTS |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
Series 1: Blood gases
Blood PO2 and pH are summarized in Table 2. The ECGs recorded during the blood gas measurements were consistent with the ECGs obtained from animals studied during the blood flow measurements. Hence these results were pooled.
|
Series 2: Blood flow
To control for differences in the ECG that might be accounted for by respiratory state (Burggren, 1978
), periods of ventilation were examined in this study before and immediately after exercise. To reduce artifacts caused by swimming motions, ECGs were recorded immediately after exercise rather than during exercise. After exercising while breathing hypoxic gases, the ECGs were abnormal compared to those recorded before and after exercise with FIO2 = 0.20. Coincident with the onset of these electrical anomalies were signs of myocardial dysfunction, such as ventricular depolarizations that did not result in sufficient contraction to cause ejection, or resulted in reduced stroke volumes (Fig. 2). Post exercise function remained impaired and the ECG abnormal until FIO2 returned to normal (Fig. 3). At this time the ECG returned to a pattern similar to that observed before exercise. The top trace of Figure 3 shows an ECG recorded from lead 1 during ventilation (FIO2 = 0.20) before any exercise was undertaken. During ventilation after exercise with FIO2 = 0.05, the T wave was inverted and the PR interval increased. These electrical anomalies remained until FIO2 increased to approximately 0.12, at which time the T wave returned to an upright position and the PR interval shortened. Figure 4 illustrates inversion of the T wave on a different animal that is apparent on lead 2 and 3. The left side of the figure shows the ECG during ventilation before exercise and the right side shows the ECG during ventilation after exercise. FIO2 was 0.20 in the top traces and 0.05 in the bottom traces. Inversion of the T wave was seen after exercise with FIO2 = 0.05, but not on all the leads.
|
|
|
During and after exercise with FIO2 of 0.10 and 0.05, the hearts also became arrhythmic and the ECG exhibited a pattern consistent with atrial-ventricular (A-V) block. Figure 5A shows a continuous recording of blood flow in the RRAo that illustrates heart beats that occur in doublets and triplets. Furthermore, changes in the atrial ECG were observed. Figure 5B illustrates multiple P waves without corresponding QRS waves.
|
Cardiac power (N = 3) significantly (P = 0.048 one tailed paired t-test) declined from 3.1 ± 0.5 mW gm–1 ventricle (mean ± SE) during normoxic exercise to 1.0 ± 0.3 mW gm–1 ventricle (mean ± SE) during hypoxic exercise (FIO2 = 0.05) (Fig. 6).
|
0.05; one tailed paired t-test) |
DISCUSSION |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
In general, the demand for myocardial oxygen is a function of how vigorously the heart is working, consequently myocardial oxygen requirements increase during ventilation and during exercise in turtles. It is well established that a net L-R shunt develops during breathing and during activity, when myocardial workload is elevated (Shelton and Burggren, 1976
; West et al., 1992; Hicks and Krosniunas, 1996; Wang and Hicks, 1996; Wang et al., 1997). The development of a large L-R shunt can significantly increase the oxygen available to the right side of the heart. For example, a study on anesthetized turtles showed that during periods of L-R shunting, the PO2 of pulmonary arterial blood can be as much as 30 torr greater than the values found in the right atrium (Ishimatsu et al., 1996). Consequently it is possible that the L-R shunt provides oxygen to the myocardium.
To address the question of whether or not cardiac function is impaired without the L-R shunt is difficult. A direct test of this hypothesis would require surgically subdividing the ventricle, which is not feasible. Consequently the approach of the current study was indirect. Many reptiles, particularly turtles, are well known for their tolerance to hypoxia (Jackson, 1987; Wasser et al., 1990; Jackson et al., 1991, 1995); hence the levels of oxygen found in systemic venous blood may be adequate for sustaining normal cardiac function. Therefore, it was critical to determine the sensitivity of the turtles' hearts to low oxygen.
In resting turtles breathing room air, the PO2 of the mixed systemic venous blood was 29 ± 8.8 (SD) torr. This is similar to values measured in previous studies (Burggren and Shelton, 1979; Hicks and Wang, 1998). When swimming, the mixed venous PO2 decreased to 15 ± 4.7 (SD) torr (Fig. 2). During activity, with FIO2 = 0.05, mixed systemic venous blood PO2 was 12 ± 1.4 (SD) torr and the arterial blood was 21 ± 2.8 (SD) torr. During this period, the chambers of the heart contained an oxygen tension in the range of 12 to 21 torr, which encompasses the 15 torr measured in the systemic venous return of turtles swimming with access to normoxic air.
During periods of elevated cardiac work under hypoxic conditions we found several indicators of reduced cardiac performance: (1) electrical anomalies; (2) arrhythmia; (3) bradycardia; (4) decrease in systemic ventricular power.
The most sensitive indicator of myocardial hypoxia is electrical anomalies, which can often be detected before any gross malfunction occurs (Marriott, 1983). Although systematic analysis of ECGs during myocardial hypoxia has not been conducted in reptiles, our analysis of the ECG in this study indicated several changes that are consistent with myocardial hypoxia (Marriott, 1983). During the ventilatory period with FIO2 = 0.20, pre-exercise and post-exercise ECGs were similar. In contrast, reductions in FIO2 to 0.10 and 0.05 during exercise and immediately following exercise resulted in inversion of the T wave. Inversion of the T wave at FIO2 = 0.05 was seen for all the animals studied, but was not seen for all the turtles at FIO2 = 0.10. This inversion is illustrated in Figures 3 and 4 for two of the turtles. The T wave was not inverted on all of the leads examined (Fig. 4), suggesting that inversion was not due to pericarditis or effusion (Marriott, 1983). At low levels of inspired oxygen (FIO2 = 0.05) additional anomalies in the ECG occurred (e.g., appearance or increased prominence of Q waves, ST segment changes).
In addition to changes in ventricular depolarization and repolarization in the ECG, changes in the P-R interval were observed (Figs. 3, 5). In mammals, a gradual lengthening of the P-R interval can result from ischemic heart disease and produces a pattern of ventricular contractions that is characterized by groups of beats, especially pairs, trios, etc. These patterns are known as the "footprints of Wenckebach" and can be used to identify AV block, even when the P-wave is not seen in the ECG (Marriott, 1983). Patterns of pairs and trios that are similar to the footprints of Wenckebach observed in humans were found in turtles breathing hypoxic air (Fig. 5A) and have been observed in perfused turtle hearts subjected to a hypoxic solution (Farmer, personal observation). Furthermore, recordings from pericardial leads show a progressive lengthening in the P-R interval, as well as high grade (advanced) second degree AV block, where a series of P waves occurs without an ensuing T wave (Fig. 5B). This is consistent with an apparent A-V block observed in anoxic isolated turtle heart strips (Jackson, 1987). Finally, these findings in turtles are also consistent with atrial extra-systoles observed in hypoxic carp (Rantin, 1993).
The electrical changes we observed in turtles during hypoxia are consistent and similar to changes seen by other researchers in the ECG of reptiles. For example, T wave amplitude changes have been reported in the tuatara (Sphenodon punctuatus), carp (Cyprinus carpio), and a turtle (Trachemys scripta) (McDonald and Heath, 1971; Glass et al., 1991; Rantin, 1993; Altimiras, 1995). Glass et al. (1991) found an increased T wave during aquatic hypoxia in carp and Rantin (1993) reports inversion of the T wave with extreme hypoxia in carp. Changes in ventricular depolarization (the QRS complex) associated with ventilation (compared to apnea) have been observed in turtles (Burggren, 1978), although Altimiras (1995) did not detect a similar pattern, perhaps due to differences in methodology, but did detect on rare occasions inversion of the T wave.
Alternate explanations
The electrical changes observed in turtles after exercise while breathing hypoxic gas are similar to electrical changes observed in ischemic mammalian hearts and include inversion of the T-wave, heightened T-wave, elongation of the P-R interval, and multiple p waves without a corresponding QRS complex. However, electrocardiography does not always provide a clear-cut diagnosis because similar anomalies can occur for a variety or reasons. For example, massive pulmonary embolism can produce an electrical signature typical of myocardial infarction. Pericarditis, myxedema, hypokalemia, hyperkalemia, hypocalcemia can affect the hearts electrical signals (Marriott, 1983). Thus, our measurements of blood flow and cardiac power were important to verify that the electrical anomalies were indeed a result of the hypoxic treatment and that they were harbingers of impaired cardiac function.
We found that anomalies in the ECG corresponded to problems with ejection (Figs. 2, 5). We also found that hypoxia reduced systemic ventricular power output, which is consistent with reductions of ventricular power reported for anoxic and acidic turtle hearts during heavy workloads (Farrell et al., 1994; Shi and Jackson, 1997; Hicks and Wang, 1998).
In summary, the changes of the ECG that occurred in the turtles when the myocardium was hypoxic (the ventricle contained blood with a PO2 that ranged between 12 and 21 torr) suggest that maximum power and performance of the heart cannot be maintained on the oxygen available in the mixed systemic venous return of exercising animals. Therefore, the additional oxygen that is washed into the right side of the heart by the L-R shunt appears to contribute to myocardial oxygenation and to maintaining cardiac performance.
|
ACKNOWLEDGMENTS |
|---|
We thank Dr. Donald Jackson and Dr. Charles Kuhn III for comments on the manuscript. We are grateful to Dr. Tobias Wang for assistance collecting some of the preliminary blood gas data and to Everette Yee and Paul Lim for assistance training the turtles. This work was supported by NSF IBN-9423297 Doctoral Dissertation Improvement Grant to C. G. F. and NSF IBN-9982671 to J.W.H.
|
FOOTNOTES |
|---|
1 From the Symposium Molecules, Muscles, and Macroevolution: Integrative Functional Morphology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 Present address: Department of Biology, 257 S. 1400 E., University of Utah, Salt Lake City, UT 84112; E-mail: Farmer{at}biology.utah.edu
|
References |
|---|
|
TOP
SYNOPSISINTRODUCTIONMATERIALS AND METHODSSERIES 1: BLOOD GASES...SERIES 2: BLOOD FLOW...RESULTSDISCUSSIONReferences |
|---|
Ackerman, R. A., and F. N. White. 1979. Cyclic carbon dioxide exchange in the turtle, Pseudemys scripta. Physiol. Zool, 52:378-389.
Altimiras, J. 1995. Heart rate variability; its significance in lower vertebrates. Department de Bioquimica i Fisiologia. Barcelona, Universitat de Barcelona: 194.
Axelsson, M., and C. E. Franklin. 1996. From anatomy to angioscopy: 163 years of crocodilian cardiovascular research, recent advances and speculations. Comp. Biochem. Physiol, 118A:51-62.
Baker, L. A., and F. N. White. 1970. Redistribution of cardiac output in response to heating in Iguana iguana. J. Exp. Biol, 35:253-262.
Bing, O. H. L., W. W. Brooks, A. N. Inamdar, and J. V. Messer. 1972. Tolerance of isolated heart muscle to hypoxia: Turtle vs. rat. Am. J. Physiol, 223:1481-1485.
Brady, A. J., and C. Dubkin. 1964. Coronary circulation in the turtle ventricle. Biochem. Physiol, 13:119-128.[CrossRef]
Burggren, W. 1982. Pulmonary plasma filtration in the turtle: A wet vertebrate lung? Science, 215:77-78.
Burggren, W. 1987. Form and function in reptilian circulations. Amer. Zool, 27:5-19.
Burggren, W., and G. Shelton. 1979. Gas exchange and transport during intermittent breathing in chelonian reptiles. J. Exp. Biol, 82:75-92.
Burggren, W., A. Smits, and B. Evans. 1989. Arterial O2 homeostasis during diving in the turtle Chelodina longicollis. Physiol. Zool. 668–686.
Burggren, W. W. 1975. A quantitative analysis of ventilation tachycardia and its control in two chelonian reptiles Pseudemys scripta and Testudo graeca. J. Exp. Biol, 63:367-380.
Burggren, W. W. 1978. Influence of intermittent breathing on ventricular depolarization patterns. J. Physiol, 278:349-364.
Comeau, S. G., and J. W. Hicks. 1994. Regulation of central vascular blood flow in the turtle. Am. J. Physiol, 267: R569-R578.
Farmer, C. 1997. Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates? Paleobiology, 23:358-372.[Abstract]
Farmer, C. G. 1999. Evolution of the vertebrate cardio-pulmonary system. Ann. Rev. of Physiol, 61:573-592.[CrossRef][ISI][Medline]
Farmer, C. G. 2000. Evolution of the vertebrate cardio-pulmonary system: New insights. Comp. Biochem. and Physiol. Part B Biochem. & Mol. Biol, 126B: S33.
Farmer, C. G., and D. R. Carrier. 2000. Respiration and gas exchange during recovery from exercise in the American alligator. Resp. Physiol, 120:81-87.[CrossRef][ISI][Medline]
Farrell, A. P., C. E. Franklin, P. G. Arthur, H. Thorarensen, and K. L. Cousins. 1994. Mechanical performance of an in situ perfused heart from the turtle Chrysemys scripta during normoxia and anoxia at 5°C and 15°C. J. Exp. Biol, 191:207-229.[Abstract]
Foxon, G. E. H. 1955. Problems of the double circulation in vertebrates. Biol. Rev, 30:196-228.
Glass, M. L., F. T. Rantin, R. M. N. Verzola, M. N. Vernandes, and A. L. Kalinin. 1991. Cardio-respiratory synchronization and myocardial function in hypoxic carp, Cyprinus carpio. J. Fish Biol, 39:143-150.
Griel, A. 1903. Beitrage zur vergleichenden Anatomie und Entwicklungsgeschicte des Herzens und des Truncus arteriosis der Wirbelthiere. Morph. Jb, 31:123-310.
Grigg, G. C. 1989. The heart and flow patterns of cardiac outflow in the crocodilia. Proc. Aust. Physiol. Pharmac. Soc, 20:43-57.
Hicks, J. W. 1994. Adrenergic and cholinergic regulation of intracardiac shunting. Physiol. Zool, 67:1325-1346.
Hicks, J. W. 1998. Cardiac shunting in reptiles: Mechanisms, regulation and physiological functions. In C. Gans and A. S. Gaunt (eds.), Biology of the Reptilia, Society for the Study of Amphibians and Reptiles, Ithaca, New York.
Hicks, J. W., A. Ishimatsu, S. Malloi, A. Erskin, and N. Heisler. 1996. The mechanism of cardiac shunting in reptiles: A new synthesis. J. Exp. Biol, 199:1435-1446.[Abstract]
Hicks, J. W., and E. Krosniunas. 1996. Physiological states and intracardiac shunting in non-crocodilian reptiles. Exper. Biol. on Line:1–12.
Hicks, J. W., and G. M. Malvin. 1995. Mechanisms of intracardiac shunting in reptiles: Pressure vs washout shunting. In Advances in comparative and environmental physiology, Vol. 21, pp. 137–157. Springer-Verlag, Berlin.
Hicks, J. W., and T. Wang. 1998. Cardiovascular regulation during anoxia in the turtle: An in vivo study. Physiol. Zool, 71:1-14.[Medline]
Hicks, J. W., and T. Wang. 1999. Hypoxic hypometabolism in the anesthetized turtle: An in vivo study. Am. J. Physiol, 277: R18-R23.
Ishimatsu, A., J. W. Hicks, and N. Heisler. 1996. Analysis of cardiac shunting in the turtle Trachemys (Pseudemys) scripta: Application of the three outflow vessel model. J. Exp. Biol, 199:2667-2677.
Jackson, D. C. 1987. Cardiovascular function in turtles during anoxia and acidosis: In vivo and in vitro studies. Amer. Zool, 27:49-58.
Jackson, D. C., E. A. Arendt, K. C. Inman, R. G. Lawler, G. Panol, and J. S. Wasser. 1991. 31P-NMR study of normoxic and anoxic perfused turtle heart during graded CO2 and lactic acidosis. Am. J. Physiol, 260: R1130-R1136.
Jackson, D. C., H. Shi, J. H. Singer, P. H. Hamm, and R. G. Lawler. 1995. Effects of input pressure on in vitro turtle heart during anoxia and acidosis: A 31P-NMR study. Am. J. Physiol, 268: R683-R689.
Jones, D. R., and G. Shelton. 1993. The physiology of the alligator heart: Left aortic flow patterns and right-to-left shunts. J. Exp. Biol, 176:247-269.[Abstract]
Marriott, H. J. L. 1983. Practical electrocardiography. Williams and Wilkins, Baltimore.
McDonald, H. S., and J. E. Heath. 1971. Electrocardiographic observations on the tuatara, Sphenodon punctatus. Comp. Biochem. Physiol, 40A:881-892.[Medline]
Panizza, B. 1833. Sulla struttura del cuore e sulla circolazione del sangue del Crocodilus lucius. Bibl. Ital, 70:87-89.
Rantin, F. T. 1993. Effects of environmental oxygen changes on cardio-respiratory function in fish. In J. Eduardo and P. N. Bicudo (eds.), The vertebrate gas cascade, adaptations to environment and mode of life, pp. 233–241. CRC Press, Boca Raton.
Shelton, G., and W. W. Burggren. 1976. Cardiovascular dynamics of the chelonia during apnea and lung ventilation. J. Exp. Biol, 64:323-343.
Shi, H., and D. C. Jackson. 1997. Effects of anoxia, acidosis and temperature on the contractile properties of turtle cardiac muscle strips. J. Exp. Biol, 200:1965-1973.[Abstract]
Tucker, V. A. 1966. Oxygen transport by the circulatory system of the green iguana (Iguana iguana) at different body temperatures. J. Exp. Biol, 44:77-92.
Wang, T., and J. W. Hicks. 1996. Cardiorespiratory synchrony in turtles. J. Exp. Biol, 199:1791-1800.[Abstract]
Wang, T., E. H. Krosniunas, and J. W. Hicks. 1997. The role of cardiac shunts in the regulation of arterial blood gases. Amer. Zool, 37:12-22.
Wasser, J. S., K. C. Inman, E. A. Arendt, R. G. Lawler, and D. C. Jackson. 1990. 31P-NMR measurements of pHi and high-energy phosphates in isolated turtle hearts during anoxia acidosis. Am. J. Physiol, 259: R521-R539.
Webb, G. 1979. Comparative cardiac anatomy of the Reptilia. III. The heart of crocodilians and an hypothesis on the completion of the interventricular septum of cocodilians and birds. J. Morphol, 161:221-240.[CrossRef]
West, N. H., P. J. Butler, and R. M. Bevan. 1992. Pulmonary blood flow at rest and during swimming in the green turtle, Chelonia mydas. Physiol. Zool, 65:287-310.
White, F. N. 1985. Role of intracardiac shunts in pulmonary gas exchange in chelonian reptiles. In K. Johansen and W. Burggren (eds.), Cardiovascular shunts: Phylogenetic, ontogenetic and clinical aspects, pp. 296–309. Munksgaard, Copenhagen.
Wood, S. C. 1984. Cardiovascular shunts and oxygen transport in lower vertebrates. Am. J. Physiol, 247: R240-R247.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||