Comprehensive Physiology Wiley Online Library

Pulmonary Circulation

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Historical Landmarks
1.1 Theories of Antiquity
1.2 Concepts of Circulation
1.3 Concepts of Respiration
1.4 Hemodynamic Measurements
2 Modern Views of Pulmonary Circulation
2.1 During Rest
2.2 During Exercise
3 Pulmonary Effects of Altitude
3.1 Species Variation
3.2 Individual Variation in Pressor Response
3.3 Pulmonary Arterial Pressure in Relation to Age
3.4 Pulmonary Vascular Reactivity
3.5 Exercise
3.6 Diffusing Capacity
3.7 Distribution of Pulmonary Blood Flow
3.8 Pulmonary Hypertension as Maladaptation
3.9 Summary
4 Circulatory Mechanisms to Optimize Blood Oxygenation
4.1 Matching Perfusion to Ventilation
4.2 Anatomical Site of Increased Resistance During Hypoxia
4.3 Hypoxic Pulmonary Vasoconstriction
4.4 Molecular Nature of Oxygen Sensor
4.5 Transduction Process
4.6 Modulators of Hypoxic Pulmonary Vasoconstriction
5 Current Perspective on Pulmonary Vascular Control
Figure 1. Figure 1.

Circulation according to Galen. Anatomy was generally correct except for postulated invisible pores across interventricular septum. Belief that blood ebbed and flowed rather than circulated was another serious error.

From Bradley
Figure 2. Figure 2.

Longitudinal distribution of local vascular resistance (Rx) plotted against vascular volume in lung at transpulmonary pressures of 0, 3, 8, and 16 cmH2O. After lung inflates, vascular resistance is relatively evenly distributed.

From Dawson et al.
Figure 3. Figure 3.

Pressure drop across lung from pulmonary artery to left atrium [P(PA − LA)] with increasing blood flow (cardiac index) during short‐term exercise. Pulmonary vascular resistance constant for each group except healthy old men.

Data from Bevegård et al. , Elkins and Milnor , Granath and Strandell , and Lockhart et al.
Figure 4. Figure 4.

With elevation of PLA, P(PA − LA) decreases.

Data from Hopkins et al.
Figure 5. Figure 5.

Pulmonary vascular resistance decreases during prolonged exercise in 4 individuals.

From Ekelund
Figure 6. Figure 6.

When blood flow is increased acutely (exercise) but not chronically [arteriovenous (A‐V) shunt], P(PA − LA) increases. Hence prolonged blood flow increase lowers pulmonary vascular resistance. Data from dogs.

From Elkins and Milnor , by permission of the American Heart Association, Inc
Figure 7. Figure 7.

Sympathetic nervous system (SNS) activated by hypothalamic stimulation in the anesthetized dog with right ventricular bypass. Blood flow to lungs (PA) is constant. Stimulation of SNS alters pulmonary arterial pressure (PPA) by increasing systolic pressure with minimal lowering of diastolic pressure and slight increase in upper lobe flow (UL), implying decrease in pulmonary vascular compliance with little resistance change.

From Szidon and Fishman
Figure 8. Figure 8.

Mean transit time of red blood cells in pulmonary capillaries shortens as blood flow increases. Solid line, hypothetical relationship for fixed capillary blood volume.

From Johnson et al.
Figure 9. Figure 9.

Pulmonary arterial pressor response to acute hypoxia is similar in most animal species.

From Reeves, Wagner, McMurtry, and Grover
Figure 10. Figure 10.

Species variability in severity of pulmonary hypertension during chronic hypoxia.

From Reeves, Wagner, McMurtry, and Grover
Figure 11. Figure 11.

Cattle exposed to chronic hypoxia at 3,048‐m altitude: 8 susceptible to severe pulmonary hypertension, 11 resistant.

From Reeves, Wagner, McMurtry, and Grover
Figure 12. Figure 12.

Postnatal regression of pulmonary hypertension at 4,540‐m altitude. Individual variability in pulmonary hypertension among adults is large. PA, pulmonary arterial.

From Reeves and Grover
Figure 13. Figure 13.

Pulmonary arterial pressure in residents of various altitudes. As altitude and hypoxia increase, arterial oxygen tension () decreases and individual variability in pulmonary hypertension increases.

Adapted from Reeves and Grover
Figure 14. Figure 14.

Postnatal decline in PA pressure at sea level. (Much faster than at high altitude: cf. Fig. ).

From Reeves and Grover
Figure 15. Figure 15.

Increase in total pulmonary vascular resistance (pulmonary arterial pressure/cardiac output) during progressive acute hypoxia (indicated by lowered ) is greater among residents at 3,100‐m altitude than at sea level

From Reeves and Grover
Figure 16. Figure 16.

Relative perfusion (R) of lung regions in upright humans from apex to base (scintillation detector positions 1–6). Flow distribution more uniform in altitude natives than normal sea‐level residents; nonnative altitude residents are intermediate.

From Dawson and Grover
Figure 17. Figure 17.

In intact anesthetized dog, progressive airway hypoxia causes pulmonary capillary recruitment measured as increase in capillary perfusion index.

From Wagner and Latham
Figure 18. Figure 18.

Increase in pulmonary capillary perfusion index raises lung diffusing capacity during acute hypoxia in 7 intact anesthetized dogs. Infusion of pulmonary vasodilator prostaglandin E1 (PGE1) during hypoxia causes derecruitment and lowers diffusing capacity.

From Capen, Latham, and Wagner
Figure 19. Figure 19.

Magnitude of diversion of pulmonary arterial flow in dog away from hypoxic lung segment as function of segment size. Test‐segment size (abscissa) is percent total pulmonary blood flow to segment during normoxia (%QSN). For example a value of 100% would indicate that the whole lung was the hypoxic test segment to be made hypoxic, whereas a value of N 20% indicates a test segment confined to left upper lobe. Flow diversion (ordinate) is percent reduction in flow to segment when alveolar PO2 is reduced from nonhypoxic value to 30 mmHg. Hypoxic vasoconstriction in small lung segments effectively redistributes intrapulmonary flow, but effectiveness diminishes as more lung becomes hypoxic.

Data from Benumof and colleagues
Figure 20. Figure 20.

Local perfusion is well matched to local ventilation in normal lung, giving ventilation‐perfusion ratio close to 1.0 with little dispersion.

From West
Figure 21. Figure 21.

In isolated rat lung perfused with blood at constant flow, airway hypoxia and angiotensin II increase perfusion pressure, implying pulmonary vasoconstriction (top). Verapamil, a calcium antagonist, selectively inhibits pressor response to hypoxia but not to angiotensin II (bottom).

From McMurtry, Davidson, Reeves, and Grover , by permission of the American Heart Association, Inc
Figure 22. Figure 22.

Transient pressor responses to 5 chemically different inhibitors of mitochondrial oxidative phosphorylation added to perfusate reservoir of blood‐perfused lungs. Note similarity of these responses to response to airway hypoxia (Fig. ). Adding inhibitor solvents (saline or mixture of alcohol and rat plasma) did not alter perfusion pressure.

From Rounds and McMurtry , by permission of the American Heart Association, Inc
Figure 23. Figure 23.

Distending main pulmonary artery with nonocclusive balloon stimulates stretch receptors, which elicit reflex pulmonary vasoconstriction and pulmonary hypertension with no significant change in cardiac output (CO) or aortic pressure (Ao). Systolic pressures in pulmonary artery (PA) distal to balloon and in right ventricle (RV) proximal to balloon rise together; no pressure gradient develops. EKG, electrocardiogram; HR, heart rate.

From Laks et al.
Figure 24. Figure 24.

Increase in pulmonary vascular resistance (PVR) during progressive acute airway hypoxia augmented by lowering pH.

From Rudolph and Yuan , by copyright permission from the American Society for Clinical Investigation
Figure 25. Figure 25.

When acute airway hypoxia increases vascular resistance in intact anesthetized dog, histamine infusion lowers resistance (vasodilator effect), which implies that histamine does not mediate hypoxic pulmonary vasoconstriction.

From Tucker, Weir, Reeves, and Grover
Figure 26. Figure 26.

Isolated rat lung perfused with blood at constant flow. Airway hypoxia causes pulmonary vasoconstriction indicated by rise in PA. A bolus injection of prostacyclin (PGI2), a potent pulmonary vasodilator, rapidly reverses this increased pulmonary vascular tone.

Figure 27. Figure 27.

Bolus injection of arachidonic acid during hypoxic pressor response in 10 blood‐perfused rat lungs. Early pressor response followed by vasodilation and inhibition of hypoxic vasoconstriction. Metabolites of arachidonic acid are therefore both potent vasoconstrictors and vasodilators.

From Voelkel, McMurtry, Reeves, et al. , by permission of the American Heart Association, Inc


Figure 1.

Circulation according to Galen. Anatomy was generally correct except for postulated invisible pores across interventricular septum. Belief that blood ebbed and flowed rather than circulated was another serious error.

From Bradley


Figure 2.

Longitudinal distribution of local vascular resistance (Rx) plotted against vascular volume in lung at transpulmonary pressures of 0, 3, 8, and 16 cmH2O. After lung inflates, vascular resistance is relatively evenly distributed.

From Dawson et al.


Figure 3.

Pressure drop across lung from pulmonary artery to left atrium [P(PA − LA)] with increasing blood flow (cardiac index) during short‐term exercise. Pulmonary vascular resistance constant for each group except healthy old men.

Data from Bevegård et al. , Elkins and Milnor , Granath and Strandell , and Lockhart et al.


Figure 4.

With elevation of PLA, P(PA − LA) decreases.

Data from Hopkins et al.


Figure 5.

Pulmonary vascular resistance decreases during prolonged exercise in 4 individuals.

From Ekelund


Figure 6.

When blood flow is increased acutely (exercise) but not chronically [arteriovenous (A‐V) shunt], P(PA − LA) increases. Hence prolonged blood flow increase lowers pulmonary vascular resistance. Data from dogs.

From Elkins and Milnor , by permission of the American Heart Association, Inc


Figure 7.

Sympathetic nervous system (SNS) activated by hypothalamic stimulation in the anesthetized dog with right ventricular bypass. Blood flow to lungs (PA) is constant. Stimulation of SNS alters pulmonary arterial pressure (PPA) by increasing systolic pressure with minimal lowering of diastolic pressure and slight increase in upper lobe flow (UL), implying decrease in pulmonary vascular compliance with little resistance change.

From Szidon and Fishman


Figure 8.

Mean transit time of red blood cells in pulmonary capillaries shortens as blood flow increases. Solid line, hypothetical relationship for fixed capillary blood volume.

From Johnson et al.


Figure 9.

Pulmonary arterial pressor response to acute hypoxia is similar in most animal species.

From Reeves, Wagner, McMurtry, and Grover


Figure 10.

Species variability in severity of pulmonary hypertension during chronic hypoxia.

From Reeves, Wagner, McMurtry, and Grover


Figure 11.

Cattle exposed to chronic hypoxia at 3,048‐m altitude: 8 susceptible to severe pulmonary hypertension, 11 resistant.

From Reeves, Wagner, McMurtry, and Grover


Figure 12.

Postnatal regression of pulmonary hypertension at 4,540‐m altitude. Individual variability in pulmonary hypertension among adults is large. PA, pulmonary arterial.

From Reeves and Grover


Figure 13.

Pulmonary arterial pressure in residents of various altitudes. As altitude and hypoxia increase, arterial oxygen tension () decreases and individual variability in pulmonary hypertension increases.

Adapted from Reeves and Grover


Figure 14.

Postnatal decline in PA pressure at sea level. (Much faster than at high altitude: cf. Fig. ).

From Reeves and Grover


Figure 15.

Increase in total pulmonary vascular resistance (pulmonary arterial pressure/cardiac output) during progressive acute hypoxia (indicated by lowered ) is greater among residents at 3,100‐m altitude than at sea level

From Reeves and Grover


Figure 16.

Relative perfusion (R) of lung regions in upright humans from apex to base (scintillation detector positions 1–6). Flow distribution more uniform in altitude natives than normal sea‐level residents; nonnative altitude residents are intermediate.

From Dawson and Grover


Figure 17.

In intact anesthetized dog, progressive airway hypoxia causes pulmonary capillary recruitment measured as increase in capillary perfusion index.

From Wagner and Latham


Figure 18.

Increase in pulmonary capillary perfusion index raises lung diffusing capacity during acute hypoxia in 7 intact anesthetized dogs. Infusion of pulmonary vasodilator prostaglandin E1 (PGE1) during hypoxia causes derecruitment and lowers diffusing capacity.

From Capen, Latham, and Wagner


Figure 19.

Magnitude of diversion of pulmonary arterial flow in dog away from hypoxic lung segment as function of segment size. Test‐segment size (abscissa) is percent total pulmonary blood flow to segment during normoxia (%QSN). For example a value of 100% would indicate that the whole lung was the hypoxic test segment to be made hypoxic, whereas a value of N 20% indicates a test segment confined to left upper lobe. Flow diversion (ordinate) is percent reduction in flow to segment when alveolar PO2 is reduced from nonhypoxic value to 30 mmHg. Hypoxic vasoconstriction in small lung segments effectively redistributes intrapulmonary flow, but effectiveness diminishes as more lung becomes hypoxic.

Data from Benumof and colleagues


Figure 20.

Local perfusion is well matched to local ventilation in normal lung, giving ventilation‐perfusion ratio close to 1.0 with little dispersion.

From West


Figure 21.

In isolated rat lung perfused with blood at constant flow, airway hypoxia and angiotensin II increase perfusion pressure, implying pulmonary vasoconstriction (top). Verapamil, a calcium antagonist, selectively inhibits pressor response to hypoxia but not to angiotensin II (bottom).

From McMurtry, Davidson, Reeves, and Grover , by permission of the American Heart Association, Inc


Figure 22.

Transient pressor responses to 5 chemically different inhibitors of mitochondrial oxidative phosphorylation added to perfusate reservoir of blood‐perfused lungs. Note similarity of these responses to response to airway hypoxia (Fig. ). Adding inhibitor solvents (saline or mixture of alcohol and rat plasma) did not alter perfusion pressure.

From Rounds and McMurtry , by permission of the American Heart Association, Inc


Figure 23.

Distending main pulmonary artery with nonocclusive balloon stimulates stretch receptors, which elicit reflex pulmonary vasoconstriction and pulmonary hypertension with no significant change in cardiac output (CO) or aortic pressure (Ao). Systolic pressures in pulmonary artery (PA) distal to balloon and in right ventricle (RV) proximal to balloon rise together; no pressure gradient develops. EKG, electrocardiogram; HR, heart rate.

From Laks et al.


Figure 24.

Increase in pulmonary vascular resistance (PVR) during progressive acute airway hypoxia augmented by lowering pH.

From Rudolph and Yuan , by copyright permission from the American Society for Clinical Investigation


Figure 25.

When acute airway hypoxia increases vascular resistance in intact anesthetized dog, histamine infusion lowers resistance (vasodilator effect), which implies that histamine does not mediate hypoxic pulmonary vasoconstriction.

From Tucker, Weir, Reeves, and Grover


Figure 26.

Isolated rat lung perfused with blood at constant flow. Airway hypoxia causes pulmonary vasoconstriction indicated by rise in PA. A bolus injection of prostacyclin (PGI2), a potent pulmonary vasodilator, rapidly reverses this increased pulmonary vascular tone.



Figure 27.

Bolus injection of arachidonic acid during hypoxic pressor response in 10 blood‐perfused rat lungs. Early pressor response followed by vasodilation and inhibition of hypoxic vasoconstriction. Metabolites of arachidonic acid are therefore both potent vasoconstrictors and vasodilators.

From Voelkel, McMurtry, Reeves, et al. , by permission of the American Heart Association, Inc
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Robert F. Grover, Wiltz W. Wagner, Ivan F. McMurtry, John T. Reeves. Pulmonary Circulation. Compr Physiol 2011, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow: 103-136. First published in print 1983. doi: 10.1002/cphy.cp020304