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SHORT COMMUNICATION
Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery
Christian Lind Malte, Hans Malte, Lærke Rønlev Reinholdt, Anders Findsen, James W. Hicks, Tobias Wang
Journal of Experimental Biology 2017 220: 531-536; doi: 10.1242/jeb.149625
Christian Lind Malte
1Zoophysiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark
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  • ORCID record for Christian Lind Malte
  • For correspondence: christian.malte@bios.au.dk
Hans Malte
1Zoophysiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark
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Lærke Rønlev Reinholdt
1Zoophysiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark
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Anders Findsen
1Zoophysiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark
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James W. Hicks
2Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
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Tobias Wang
1Zoophysiology, Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark
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ABSTRACT

By virtue of their cardiovascular anatomy, reptiles and amphibians can shunt blood away from the pulmonary or systemic circuits, but the functional role of this characteristic trait remains unclear. It has been suggested that right-to-left (R–L) shunt (recirculation of systemic blood within the body) fuels the gastric mucosa with acidified and CO2-rich blood to facilitate gastric acid secretion during digestion. However, in addition to elevating PCO2, R–L shunt also reduces arterial O2 levels and would compromise O2 delivery during the increased metabolic state of digestion. Conversely, arterial PCO2 can also be elevated by lowering ventilation relative to metabolism (i.e. reducing the air convection requirement, ACR). Based on a mathematical analysis of the relative roles of ACR and R–L shunt on O2 and CO2 levels, we predict that ventilatory modifications are much more effective for gastric CO2 supply with only modest effects on O2 delivery. Conversely, elevating CO2 levels by means of R–L shunt would come at a cost of significant reductions in O2 levels. The different effects of altering ACR and R–L shunt on O2 and CO2 levels are explained by the differences in the effective blood capacitance coefficients.

INTRODUCTION

The ability to shunt blood away from the pulmonary or systemic circulations is a defining character of the reptilian and amphibian cardiovascular systems (Hicks, 1998). However, whilst much is known about the anatomical basis for central vascular shunts and their autonomic regulation, the functional role of bypassing one or the other circulation remains as mysterious as it is debated (Hicks and Wang, 2012). Thus, it remains uncertain as to whether this cardiovascular design is an exquisite adaptation to low ectothermic metabolism and intermittent pulmonary ventilation, or merely an atavistic relict with no particular functional benefits (Hicks and Wang, 2012).

In several species of reptiles and amphibians, the right-to-left (R–L) shunts (i.e. the direct recirculation of systemic venous blood into the arterial systemic circulation) decrease whenever oxygen demands are elevated (Hicks and Wang, 2012). However, in crocodilians, an elevated oxygen consumption associated with digestion may be an exception. A combination of unique anatomical features of the crocodilian cardiovascular system (Hicks, 1998) combined with physiological measurements fostered the idea that increased R–L shunts serve to fuel the gastric mucosa with acidic proton-rich blood during digestion in alligators (Farmer et al., 2008; Gardner et al., 2011; Jones and Shelton, 1993). Central to this proposal is the observation that the crocodilian coeliac artery appears as a continuation of the left aortic arch, which indicates that the stomach is preferentially perfused with CO2-rich blood from the right ventricle (e.g. Jones, 1996; Webb, 1979). In support for elevated (systemic) arterial partial pressure of CO2 (PCO2) governing acid secretion, Farmer et al. (2008) reported slower digestion after surgical removal of the left aorta in alligators. However, a number of other studies show that growth is not affected by similar procedures (Eme et al., 2009, 2010), and it is possible that the slower digestion stems from reduced perfusion of the gastrointestinal organs after occlusion of the left aortic arch (Hicks and Wang, 2012).

Although the cardiovascular system must simultaneously provide for O2 delivery and CO2 removal, the proposition that R–L shunts assist gastric acid secretion has not included considerations of the inexorable reduction in O2 delivery. R–L shunts cause large reduction in arterial O2 levels – whether expressed as partial pressure, O2 concentration or haemoglobin saturation (Wang and Hicks, 1996) – while the effects on arterial PCO2 are predicted to be considerably smaller given the high capacitance coefficient for CO2 in blood. An increased R–L shunt during digestion would therefore also compromise O2 delivery, which seems undesirable given the fourfold elevation in O2 demands during digestion (Busk et al., 2000). In this context, it may be more prudent to elevate arterial PCO2 by means of ventilation [i.e. a lowering of the air convection requirement (ACR) for CO2], a response that has been suggested to compensate for the rise in plasma bicarbonate during digestion (the so-called ‘alkaline tide’; Hicks et al., 2000; Hicks and White, 1992; Wang et al., 2001b). However, decreasing the ACR to elevate CO2 levels will simultaneously lower the lung PO2 and could negatively impact O2 delivery.

To address the compromise between adequate O2 delivery and arterial acid–base status, we developed an integrated numerical model that can be applied to amphibians and reptiles, to provide a quantitative comparison of the effects of R–L shunting and altered ventilation on blood O2 and CO2 levels.

List of symbols and abbreviations
ACR
air convection requirement
CPaCO2, CPaO2
concentration of CO2 or O2 in the pulmonary artery
CPvCO2, CPvO2
concentration of CO2 or O2 in pulmonary venous return (i.e. left atrium)
CSaCO2, CSaO2
concentration of CO2 or O2 in the systemic arterial blood
CSvCO2, CSvO2
concentration of CO2 or O2 in systemic venous return (i.e. right atrium)
Hb
haemoglobin
Lshunt
gas exchange limitation imposed by shunts
p
number of Bohr-groups of haemoglobin
PACO2, PAO2
partial pressure of CO2 or O2 in the lung gas
PCO2, PO2
partial pressure of CO2 or O2 in a given compartment
PICO2, PIO2
inspired partial pressure of CO2 or O2
Q̇LR
left-to-right shunt flow
Embedded Image
pulmonary blood flow
Embedded Image
right-to-left shunt flow
Embedded Image
systemic blood flow
Embedded Image
total cardiac output
R–L
right-to-left shunt
Rperf
blood convective/perfusive resistance
RQ
respiratory quotient
Rtot
total resistance imposed to transport between tissues and the environment
Rvent
air convective/ventilatory resistance
SH
fractional saturation of haemoglobin with protons
SO2
HbO2 saturation
λ
blood/gas partitioning coefficient

MATERIALS AND METHODS

Fig. 1A illustrates the model of gas exchange for O2 and CO2 based on mass balances and relationships that express electro-neutrality in blood compartments. The model does not include diffusion limitations or spatial heterogeneities at tissues or lungs, and incorporates a thermodynamically correct description of the Bohr–Haldane effect.

Fig. 1.
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Fig. 1.

Model illustration and 3D plots showing the effects of alveolar ventilation (and hence ACR) and FRL on PCO2, PO2 and SO2. (A) Illustration of the compartment model with abbreviations as follows: A, lung; Pa, pulmonary arterial blood; Pv, pulmonary venous blood; Sa, systemic arterial blood; Sv, systemic venous blood; T, tissues. For other definitions, see the List of symbols and abbreviations and Table 1. (B–D) 3D plots illustrate how (systemic) arterial PCO2 (B), PO2 (C) and HbO2 saturation (SO2; D) change as a function of the alveolar ventilation (and hence air convection requirement, ACR) and the right-to-left shunt fraction (FRL).

Mass balances

For O2: Embedded Image (1) Embedded Image (2) Embedded Image (3) Embedded Image (4)

For CO2: Embedded Image (5) Embedded Image (6) Embedded Image (7) Embedded Image (8)

See Table 1 and the list of symbols and abbreviations for parameter definitions.

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Table 1.

Parameter values used in simulations

Concentrations and partial pressures in blood

The concentration of O2 in each blood compartment (CbO2) is the sum of haemoglobin (Hb)-bound O2 [product of blood Hb concentration (CHb), number of O2 binding sites (q=4) and saturation (SO2)] and the physically dissolved O2 [product of physical solubility (αO2) and PO2]: Embedded Image (9)

To quantify the saturation of Hb with O2 and protons, the Monod–Wyman–Changeux two-state model (Monod et al., 1965) was incorporated where saturation is a function of both PO2 and proton concentration to include the Bohr–Haldane effect.

The total concentration of CO2 in blood (CbCO2) is the sum of the physically dissolved CO2 (αCO2PCO2) and the bicarbonate and carbonate concentration, as quantified by the equilibrium constants of CO2 hydration (K1 and K2) and the proton concentration ([H+], which is related to SO2): Embedded Image (10)

Electro-neutrality in blood

Equations that express electro-neutrality were derived by conservation of charge, where electro-neutrality in a given blood compartment (subscript i) is given below: Embedded Image (11)

where SID is the strong-ion difference (Stewart, 1978), Kw is the ionic product of water, βNB is the non-bicarbonate buffer capacity, pHiso is the pH of zero net charge of the buffer groups, SH is the fractional saturation of haemoglobin with protons and p is the number of Bohr-groups of haemoglobin.

Shunt fractions and blood flows

Total cardiac output (Embedded Image) is the sum of pulmonary and systemic flows (Embedded Image and Embedded Image, respectively) and the shunt flows (Embedded Imageand Embedded Image) are given by total blood flow and the shunt fractions (Embedded Image and Embedded Image). Given the desired general applicability of the model to reptiles with (both R–L and L–R) intra-cardiac shunts, and not just crocodilians with central vascular (R–L) shunts, we derived the following expressions by mass balance, assuming uniformly well-stirred compartments with constant volume where bi-directional shunts can occur independently: Embedded Image (12) Embedded Image (13)

However, given the present purpose we only considered unidirectional R–L shunts.

Numerical and analytical solutions

Owing to the simplifying assumptions of the model, at steady-state the pulmonary venous partial pressures of O2 and CO2 (PPvO2 and PPvCO2) are equal to the partial pressures in the lung (PAO2 and PACO2). The total system of 12 equations that express mass balance and electro-neutrality with 12 dependent variables (i.e. partial pressures and proton concentrations in the systemic and pulmonary arterial and venous system for O2 and CO2) was solved numerically in Mathematica (v.10.3, Wolfram Research).

When blood capacitances of O2 and CO2 are assumed constant (approximately true for CO2 and applicable to O2 during hypoxia), the system of equations can be solved analytically, leading to the following solutions: Embedded Image (14) Embedded Image (15)

where Rtot is the total resistance imposed to transport from the blood/tissues to the environment equal to the sum of the resistances associated with blood convective/perfusive transport (Rperf) and ventilation (Rvent): Embedded Image (16)

When only considering unidirectional R–L shunts, the total resistance simplifies to: Embedded Image (17)

where βb is the blood capacitance coefficient for O2 or CO2. The left part on the right-hand side of Eqn 17 corresponds to Rperf and simplifies to the normal perfusive resistance [Embedded Image] when there are no shunts, whereas the right part is Rvent. The perfusive resistance (Rperf) can be expressed as the normal resistance without shunts (Rperf,FRL=0) multiplied by a function of the shunt fraction [i.e. f(FRL)=½(2−FRL)/(1−FRL)]: Embedded Image (18)

While Rvent is the same for O2 and CO2, Rperf and hence Rtot differ given different βb. The gas exchange limitation (Piiper and Scheid, 1972, 1981) imposed by R–L shunts (Lshunt) is given by 1 minus the total resistance without shunts (Rtot, where FRL=0) divided by the total resistance with shunts (i.e. Rtot): Embedded Image (19)

This can also be expressed by the dimensionless ratio of the normal perfusive to ventilatory resistance without shunts (Embedded Image): Embedded Image (20)

where Embedded Image is given by the ventilation to perfusion ratio and the blood gas partitioning coefficient (λ=βb/βg) as follows: Embedded Image (21)

From Eqn 20 it is given that the transport limitation imposed by shunts approaches zero when Embedded Image approaches zero (i.e. infinitely high blood flow and partitioning coefficient relative to ventilation). Conversely, the limitation approaches FRL/(2−FRL) when Embedded Image approaches infinity (i.e. infinitely high ventilation and low partitioning coefficient relative to blood flow).

RESULTS AND DISCUSSION

The isolated and combined effects of R–L shunts and ACR are illustrated in 3D plots in Fig. 1B–D, where arterial PCO2, PO2 and HbO2 saturation (SO2) are shown as functions of both R–L shunt fraction (FRL) and alveolar ventilation. It is immediately clear that arterial PCO2 increases most steeply when alveolar ventilation is reduced (i.e. reduced ACR), but only moderately when FRL is increased (Fig. 1B). Conversely, both arterial PO2 and SO2 are markedly reduced as the R–L shunt increases, whilst reductions in alveolar ventilation only moderately reduce SO2 (Fig. 1C,D). Thus, our theoretical analysis reveals substantial differences on the influence of R–L shunt and ACR on arterial blood gases, and predicts that ventilatory compensations are much more effective in altering arterial PCO2 than cardiac shunt patterns.

The differences in the behaviours of O2 and CO2 upon changing shunt pattern or ACR are also illustrated in Fig. 2A–D, which shows PO2–PCO2 diagrams and similar plots that relate PCO2 and SO2. In Fig. 2B, the dashed line describes steady-state solutions for lung gases and hence also the arterial blood gases in the absence of cardiac shunts (i.e. the mammalian condition). In this case, reductions in ACR cause similar, but reciprocal changes in arterial PO2 and PCO2 as predicted by the respiratory quotient (RQ; set to 1 in the simulations). Conversely, an introduction of R–L shunt at a given ACR causes large reductions in arterial PO2 while arterial PCO2 only increases moderately (full green curve in Fig. 2B). Thus, to produce the same elevation in arterial PCO2 by means of a R–L shunt as by a moderate reduction in ACR (e.g. a reduction from 28 to 20 ml air ml–1 CO2; Fig. 2B), the shunt fraction would have to increase to 0.8, meaning that 80% of the systemic venous return bypasses the lungs (Fig. 2B). Such a large shunt fraction would concomitantly reduce arterial PO2 from more than 120 mmHg to less than 30 mmHg (Fig. 2B) and reduce SO2 from approximately 1.0 to less than 0.5 (Fig. 2A).

Fig. 2.
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Fig. 2.

PO2–PCO2 diagrams of the solutions comparing the effects of altering ACR and FRL on PCO2, PO2 and SO2. (A–D) Arterial PCO2 as a function of either HbO2 saturation (SO2) (A,C) or PO2 (B,D). In B and D, the dashed black line is the air-line with a slope given by a respiratory quotient (RQ) that describes how PCO2 and PO2 change when altering ACR without shunts, and similarly in A and C, where the ‘air-line’ becomes a curve. In B, the thick green curve originating at the dashed air-line/curve shows solutions when the right-to-left shunt fraction (FRL) is increased at a constant ACR. Note that to produce the same elevation in arterial PCO2 by means of R–L shunt as by a moderate reduction in ACR (e.g. a reduction from 28 to 20 ml air ml–1 CO2), the shunt fraction would have to increase to 0.8 with a concomitant large reduction in arterial PO2 and SO2 (A). (C,D) Solutions for different combinations of FRL (varied 0–0.8) and ACR (varied 12.5–50 ml air ml–1 CO2), where the colour coding indicates increasing PCO2. Here, the thicker curves originating from the air-line/curve show the effects of altering FRL at a given constant ACR. Conversely, the thinner curves originating from the thicker curves show the effects of altering ACR at a given FRL. (E) 3D plot summarizing the effects of altering FRL (thicker curves) and ACR (thinner curves) on both (systemic) venous and arterial blood. The plot is a combination of C and D, where PCO2 is on the vertical z-axis and SO2 and PO2 are on the horizontal x- and y-axes, and therefore also illustrates the effective O2 equilibrium curve. Note that when increasing FRL at a given ACR, the arterial and venous points move down the O2 equilibrium curve with only small elevations in PCO2. Conversely, reducing ACR at a given shunt leads to pronounced elevations of PCO2 but only moderate reductions in SO2.

The complete solutions for different combinations of FRL (varied 0–0.8) and ACR (varied 12.5–50) for arterial blood are given in Fig. 2C,D. The colour coding indicates increasing PCO2 and the thicker lines originating from the air-line (the black dashed line/curve) depict how PO2, PCO2 and SO2 change as FRL is altered at several constant levels of ACR. The thinner curves, originating from the thicker blood curves, represent solutions when ACR is altered at a given constant FRL. By combining the horizontal axes of Fig. 2C,D, the possible solutions are summarized as a 3D diagram with PCO2 on the vertical z-axis and SO2 and PO2 on the horizontal x- and y-axes (Fig. 2E). In this representation, the horizontal x–y plane reflects the effective O2 equilibrium curve. Fig. 2E illustrates that increasing FRL causes large reductions in PO2 of the arterial and venous blood along the O2 equilibrium curve, leading to pronounced SO2 reduction with only moderate elevation of PCO2. Conversely, reducing ACR at a given FRL leads to a large elevation of PCO2 with only moderate reductions in SO2 (thinner upwards-bending curves in Fig. 2E).

The different effects of altering ACR and R–L shunt on O2 and CO2 is explained by the differences in blood capacitance coefficients (βb) (alternatively expressed as differences in blood gas partitioning coefficients, λ). This is illustrated in Fig. 3, showing the limitation imposed on gas exchange by FRL (Eqn 21). Here, the ratio of the normal perfusive to ventilatory resistance without shunts (Embedded Image) is varied from a physiologically relevant range for O2 and CO2 (colour coded), and the asymptotic relationship between the limitation and FRL for Embedded Image approaching infinity and Embedded Image=0 is given by the black curve and the horizontal axis. Fig. 3 emphasizes that at a given shunt fraction, the gas species mostly limited by the shunt is the one with the highest blood to air convective resistance (Embedded Image) and hence the lowest λ (i.e. lowest βb). Therefore, owing to the high βb, CO2 is less limited by shunts than O2, although the differences may become less distinct in deep hypoxia where the effective βb for O2 increases. The same conclusion was made by Wagner (1979) when considering the effects of lung shunts on O2 versus CO2 exchange. Besides the differences in effects of shunts on O2 and CO2, Fig. 3 also illustrates that the limitation in general is predicted to increase when overall Embedded Image is high and vice versa.

Fig. 3.
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Fig. 3.

Simplified analytic solution of the model that illustrates the limitation imposed on gas exchange by shunts (Lshunt, Eqn 21) as a function of the right-to-left shunt fraction (FRL) for different values of the ratio of the perfusive to ventilatory resistance without shunts (Embedded Image, Eqn 22, colour coded). The asymptotic limitations when Embedded Image approaches infinity or zero are plotted. As a consequence of higher blood capacitance coefficient (βb) and hence blood/gas partitioning coefficient (λ), Embedded Image for O2 is higher than for CO2 and hence O2 uptake will be more limited by a given shunt.

If digestion is facilitated by supplying the gut with blood with higher CO2 levels, our model predicts that this is best mediated by reducing ACR instead of increasing R­–L shunt. Elevating CO2 levels by increasing R–L shunt would come at the cost of pronounced reductions in O2 levels, producing hypoxemia at a time at which O2 demand may be elevated fourfold above resting (e.g. Busk et al., 2000). Conversely, reductions of ACR entail much smaller reductions in O2 delivery, but provide for an effective elevation of PCO2 that compensates for the alkaline tide during digestion (Wang et al., 2001a). Furthermore, these postprandial reductions in ACR are well known in reptiles (Hicks et al., 2000; Overgaard et al., 1999; Secor et al., 2000) and PO2 remains high during digestion in all animals studied, including alligators (Busk et al., 2000; Hartzler et al., 2006; Overgaard et al., 1999).

For many reptiles and amphibians, digestion is associated with large elevations in oxygen demands and an increased need to secrete gastric acid with resulting challenges to blood acid–base balance. Our theoretical approach clearly demonstrates that reliance on R–L shunting to meet the digestive demands conflicts significantly with increased metabolic demands of the digestive organs, and cannot provide adequate compensation for the alkaline tide. In contrast, ventilatory regulation, through reductions in ACR, addresses all the physiological challenges simultaneously, i.e. blood acid–base regulation, increased CO2 delivery to the gastric mucosa without sacrificing O2 delivery. Thus, while our theoretical model obviously does not provide information on the actual physiological responses of living animals, it would certainly seem that natural selection should favour efficient ventilatory regulation on arterial PCO2 rather than the ineffective mean of regulation by central vascular shunts.

FOOTNOTES

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    This analysis results from numerous discussions over the past decade involving all the authors. C.L.M. constructed the model used in the manuscript on the basis of previous simpler attempts. The manuscript was written by H.M. and T.W. with continuous input and final approval of all co-authors.

  • Funding

    This study was funded by the Danish Research Council (Natur og Univers, Det Frie Forskningsråd).

  • Received September 12, 2016.
  • Accepted December 6, 2016.
  • © 2017. Published by The Company of Biologists Ltd
http://www.biologists.com/user-licence-1-1/

References

  1. ↵
    1. Busk, M.,
    2. Overgaard, J.,
    3. Hicks, J. W.,
    4. Bennett, A. F. and
    5. Wang, T.
    (2000). Effects of feeding on arterial blood gases in the American alligator Alligator mississippiensis. J. Exp. Biol. 203, 3117-3124.
    OpenUrlAbstract
    1. Christoforides, C. and
    2. Hedley-Whyte, J.
    (1969). Effect of temperature and hemoglobin concentration on solubility of O2 in blood. J. Appl. Physiol. 27, 592-596.
    OpenUrlFREE Full Text
  2. ↵
    1. Eme, J.,
    2. Gwalthney, J.,
    3. Blank, J. M.,
    4. Owerkowicz, T.,
    5. Barron, G. and
    6. Hicks, J. W.
    (2009). Surgical removal of right-to-left cardiac shunt in the American alligator (Alligator mississippiensis) causes ventricular enlargement but does not alter apnoea or metabolism during diving. J. Exp. Biol. 212, 3553-3563. doi:10.1242/jeb.034595
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Eme, J.,
    2. Gwalthney, J.,
    3. Owerkowicz, T.,
    4. Blank, J. M. and
    5. Hicks, J. W.
    (2010). Turning crocodilian hearts into bird hearts: growth rates are similar for alligators with and without right-to-left cardiac shunt. J. Exp. Biol. 213, 2673-2680. doi:10.1242/jeb.042051
    OpenUrlAbstract/FREE Full Text
  4. ↵
    1. Farmer, C. G.,
    2. Uriona, T. J.,
    3. Olsen, D. B.,
    4. Steenblik, M. and
    5. Sanders, K.
    (2008). The right-to-left shunt of crocodilians serves digestion. Physiol. Biochem. Zool. 81, 125-137. doi:10.1086/524150
    OpenUrlCrossRefPubMedWeb of Science
  5. ↵
    1. Gardner, M. N.,
    2. Sterba-Boatwright, B. and
    3. Jones, D. R.
    (2011). Ligation of the left aorta in alligators affects acid–base balance: a role for the R→ L shunt. Respir. Physiol. Neurobiol. 178, 315-322. doi:10.1016/j.resp.2011.07.001
    OpenUrlCrossRefPubMed
  6. ↵
    1. Hartzler, L. K.,
    2. Munns, S. L.,
    3. Bennett, A. F. and
    4. Hicks, J. W.
    (2006). Metabolic and blood gas dependence on digestive state in the Savannah monitor lizard Varanus exanthematicus: an assessment of the alkaline tide. J. Exp. Biol. 209, 1052-1057. doi:10.1242/jeb.02121
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. Hicks, J. W.
    (1998). Cardiac shunting in reptiles: mechanisms, regulation and physiological functions. Biol. Reptilia 19, 425-483.
    OpenUrl
  8. ↵
    1. Hicks, J. W. and
    2. Wang, T.
    (2012). The functional significance of the reptilian heart: new insights into an old question. In Ontogeny and Phylogeny of the Vertebrate Heart (ed. T.Wang and D.Sedmera), pp. 207-227. New York: Springer-Verlag.
  9. ↵
    1. Hicks, J. W. and
    2. White, F. N.
    (1992). Pulmonary gas exchange during intermittent ventilation in the American alligator. Respir. Physiol. 88, 23-36. doi:10.1016/0034-5687(92)90026-S
    OpenUrlCrossRefPubMedWeb of Science
  10. ↵
    1. Hicks, J. W.,
    2. Wang, T. and
    3. Bennett, A. F.
    (2000). Patterns of cardiovascular and ventilatory response to elevated metabolic states in the lizard Varanus exanthematicus. J. Exp. Biol. 203, 2437-2445.
    OpenUrlAbstract
  11. ↵
    1. Jones, D.
    (1996). The crocodilian central circulation: reptilian or avian? Verh. Dtsch. Zool. Ges. 89, 209-218.
    OpenUrl
  12. ↵
    1. Jones, D. R. and
    2. Shelton, G.
    (1993). The physiology of the alligator heart: left aortic flow patterns and right-to-left shunts. J. Exp. Biol. 176, 247-270.
    OpenUrlAbstract/FREE Full Text
  13. ↵
    1. Monod, J.,
    2. Wyman, J. and
    3. Changeux, J.-P.
    (1965). On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118. doi:10.1016/S0022-2836(65)80285-6
    OpenUrlCrossRefPubMedWeb of Science
  14. ↵
    1. Overgaard, J.,
    2. Busk, M.,
    3. Hicks, J. W.,
    4. Jensen, F. B. and
    5. Wang, T.
    (1999). Respiratory consequences of feeding in the snake Python molorus. J. Comp. Physiol. A 124, 359-365. doi:10.1016/s1095-6433(99)00127-0
    OpenUrlCrossRef
  15. ↵
    1. Piiper, J. and
    2. Scheid, P.
    (1972). Maximum gas transfer efficacy of models for fish gills, avian lungs and mammalian lungs. Respir. Physiol. 14, 115-124. doi:10.1016/0034-5687(72)90022-9
    OpenUrlCrossRefPubMedWeb of Science
  16. ↵
    1. Piiper, J. and
    2. Scheid, P.
    (1981). Model for capillary-alveolar equilibration with special reference to O2 uptake in hypoxia. Respir. Physiol. 46, 193-208. doi:10.1016/0034-5687(81)90121-3
    OpenUrlCrossRefPubMedWeb of Science
    1. Reeves, R. B.
    (1976). Temperature-induced changes in blood acid-base status: pH and PCO2 in a binary buffer. J. Appl. Physiol. 40, 752-761.
    OpenUrlAbstract/FREE Full Text
  17. ↵
    1. Secor, S. M.,
    2. Hicks, J. W. and
    3. Bennett, A. F.
    (2000). Ventilatory and cardiovascular responses of a python (Python molurus) to exercise and digestion. J. Exp. Biol. 203, 2447-2454.
    OpenUrlAbstract
  18. ↵
    1. Stewart, P. A.
    (1978). Independent and dependent variables of acid-base control. Respir. Physiol. 33, 9-26. doi:10.1016/0034-5687(78)90079-8
    OpenUrlCrossRefPubMedWeb of Science
  19. ↵
    1. Wagner, P.
    (1979). Susceptibility of different gases to ventilation–perfusion inequality. J. Appl. Physiol. 46, 372-386.
    OpenUrlAbstract/FREE Full Text
  20. ↵
    1. Wang, T. and
    2. Hicks, J. W.
    (1996). The interaction of pulmonary ventilation and the right–left shunt on arterial oxygen levels. J. Exp. Biol. 199, 2121-2129.
    OpenUrlAbstract/FREE Full Text
  21. ↵
    1. Wang, T.,
    2. Busk, M. and
    3. Overgaard, J.
    (2001a). The respiratory consequences of feeding in amphibians and reptiles. J. Comp. Physiol. A 128, 533-547. doi:10.1016/s1095-6433(00)00334-2
    OpenUrlCrossRef
  22. ↵
    1. Wang, T.,
    2. Warburton, S.,
    3. Abe, A. and
    4. Taylor, T.
    (2001b). Vagal control of heart rate and cardiac shunts in reptiles: relation to metabolic state. Exp. Physiol. 86, 777-784. doi:10.1111/j.1469-445X.2001.tb00044.x
    OpenUrlCrossRefPubMedWeb of Science
  23. ↵
    1. Webb, G. J.
    (1979). Comparative cardiac anatomy of the Reptilia. III. The heart of crocodilians and an hypothesis on the completion of the interventricular septum of crocodilians and birds. J. Morphol. 161, 221-240. doi:10.1002/jmor.1051610209
    OpenUrlCrossRefWeb of Science
    1. Weinstein, Y.,
    2. Ackerman, R. A. and
    3. White, F. N.
    (1986). Influence of temperature on the CO2 dissociation curve of the turtle Pseudemys scripta. Respir. Physiol. 63, 53-63. doi:10.1016/0034-5687(86)90030-7
    OpenUrlCrossRefPubMed
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Keywords

  • Gas exchange
  • Heart
  • Mathematical model
  • Reptile
  • Shunting

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Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery
Christian Lind Malte, Hans Malte, Lærke Rønlev Reinholdt, Anders Findsen, James W. Hicks, Tobias Wang
Journal of Experimental Biology 2017 220: 531-536; doi: 10.1242/jeb.149625
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SHORT COMMUNICATION
Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery
Christian Lind Malte, Hans Malte, Lærke Rønlev Reinholdt, Anders Findsen, James W. Hicks, Tobias Wang
Journal of Experimental Biology 2017 220: 531-536; doi: 10.1242/jeb.149625

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