Circulatory Structure

Pulmonary Circulation

The pulmonary arteries lie near and branch in unison with the airways in the bronchovascular bundle. They are much thinner than systemic arteries and have proportionately more elastic tissue in their walls. The walls of the arterioles, with a diameter less than 100 µm, are so thin relative to those of their systemic counterparts that fluid and gas can move across them. Within the gas-exchanging zone, the arterioles give rise to a network of pulmonary capillaries in the alveolar walls that is continuous throughout the lungs. They are so numerous that, when distended, blood flows almost as an unbroken sheet between the air spaces (Figure 4-1). “Sheet flow” reduces vascular resistance and optimizes gas exchange by creating a very large surface area, estimated at over 100 m². When the transmural pressure difference between the inside and outside of the vessels is low, many of the capillary segments are closed, but flow switches among segments frequently as some open and others close. Nonflowing segments are rapidly recruited into the pulmonary vascular bed as needed to accommodate increased flow and may be further distended by an increase in transmural pressure. Both recruitment and distention of the pulmonary capillary bed reduce resistance to blood flow and help to maintain a low pressure in the face of increased blood flow. This low pressure allows the capillary-alveolar membrane to be very thin (approximately 1 µm), facilitating diffusion of respiratory gases between blood and alveoli. A red cell that follows a capillary path from the pulmonary artery to a vein may cross several alveoli, with the average transit time through the vessels engaged in gas exchange calculated to be approximately 0.75 second. The capillaries unite to form larger alveolar microvessels, which become venules and then veins that run between the lobules toward the hila, where upper and lower pulmonary veins from each lung empty into the left atrium.

Figure 4-1 Alveolar capillaries. The normal cardiac output requires only a portion of the sheet of capillaries; any remaining vessels can be recruited when cardiac output rises during exercise.

(Modified with permission from Butler J: The circulation of the lung. In Culver BH, editor: The respiratory system, Seattle, 2006, University of Washington Publication Services, p 8.2.)

Bronchial Circulation

The bronchial arteries arise directly from the aorta or from intercostal arteries to supply the walls of the trachea and bronchi and also to nourish the major pulmonary vessels, nerves, interstitium, and pleura. Extensive small-vessel anastomoses occur between these (systemic) vessels and both the precapillary and postcapillary pulmonary vasculature. The bronchial veins from the larger airways and hilar region drain through the systemic veins (particularly the azygos system) into the right atrium. However, bronchial flow to the intrapulmonary structures connects to the pulmonary circulation and drains through the pulmonary veins into the left atrium. This small aliquot of desaturated blood contributes to the normal (2% to 5%) right-to-left shunt, which may increase when the bronchial circulation hypertrophies to supply inflammatory or neoplastic lesions. The bronchial circulation has a role in the regulation of temperature and humidity in the airways and supplies the fluid for secretion through the airway mucosa.

Lymphatic Circulation

Pulmonary lymphatics are not found in alveolar walls but originate in interstitial spaces at the level of the respiratory bronchioles and at the pleural surface, then follow the bronchovascular bundles to the hila. The lymph flows through the right lymphatic duct and the thoracic duct into the right and left brachiocephalic veins. The total flow from the lungs is quite low under normal conditions (less than 0.5 mL/minute in experimental animals) but can increase many-fold with pulmonary edema. The lymphatics have valves to prevent backflow and can generate sufficient pressures to maintain flow when systemic venous pressure is as high as 20 cm H₂O.

Circulatory Physiology

The pulmonary circulation conducts the entire cardiac output with a remarkably low driving pressure from the pulmonary artery (mean Ppa of 15 to 20 mm Hg) to the left atrium (Pla of 7 to 12 mm Hg). As in the airways, the branching pattern of vessels leads to an increase in total cross-sectional area as the alveolar vessels are approached, but unlike in the airways, this increase is not associated with a decrease in resistance. Total cross-sectional area increases at a branching point if the number of daughter branches (n) is greater than the ratio of the parent to daughter radii squared, (a/b)², but resistance decreases only if n is greater than (a/b)⁴. The latter case occurs in the peripheral airways but not in the vessels, so although small peripheral airways contribute little to normal airflow resistance, pulmonary microvessels make up a substantial portion of vascular resistance. Efforts to partition the pressure drop longitudinally suggest that approximately 20% to 30% is in the arterial portion (including arterioles), 40% to 60% in the microvascular portion, and the remainder in the veins. With increases in flow, recruitment occurs mainly at the level of microvascular vessels, so their relative contribution to resistance becomes less.

The pulmonary circulation is a network of segmental resistors that share common upstream (i.e., Ppa) and downstream (i.e., Pla) pressures. Flow is distributed to the various segments in proportion to the reciprocal of the total serial resistance through any segment. The benefit of having the highest resistance at the microvascular level is that the control of blood flow distribution can occur at a finer level, allowing active mechanisms of flow regulation (see further on) to adjust blood flow to relatively small lung regions.

The pulmonary vascular resistance, PVR, is calculated as transvascular driving pressure, ΔP (mean upstream Ppa minus mean downstream Pla), divided by the flow: PVR = ΔP/Q. The calculated resistance must be interpreted in the context of flow, because the relationship of driving pressure to flow usually is not linear and its plotted curve does not pass through zero. As shown in Figure 4-2, pulmonary vascular resistance decreases as flow and pressure increase with the attendant recruitment and distention of vessels.

Figure 4-2 Driving pressure across the pulmonary circulation. Mean pulmonary artery pressure (Ppa) minus mean left atrial pressure (Pla) increases nonlinearly with cardiac output. Resistance, represented by the slope from the origin to any point on the line, decreases with increased pulmonary blood flow, which reflects recruitment and distention of vessels.

The resistance to flow through a vessel increases with its length, with the viscosity of the fluid, and, most important, with the inverse of the radius to the fourth power. In addition to muscle activity in the wall, the caliber of a distensible vessel depends passively on the transmural pressure difference between intravascular and extravascular pressures. This mechanism is particularly important in the lungs, where the vessels are embedded in expandable parenchyma. It is convenient to consider separately the effect of lung expansion on the extraalveolar arterial and venous vessels, which differs from the effect on the microvessels of the alveolar zone. With lung volume increase, extraalveolar vessels are distended as the pressure is lowered in the expanding perivascular space around them (Figure 4-3), and they are elongated as the lung expands.

Figure 4-3 Lung volume affects alveolar and extraalveolar vessels differently. At high lung volumes, alveolar microvessels are stretched and compressed as vascular pressures fall relative to alveolar pressure. Extraalveolar vessels, however, tend to be expanded as the pressure surrounding them decreases.

(Modified with permission from Butler J: The circulation of the lung. In Culver BH, editor: The respiratory system, Seattle, 2006, University of Washington Publication Services, p 8.4.)

By contrast, the alveolar microvessels in the alveolar walls are elongated but partially collapsed by lung inflation, because the alveolar pressure that surrounds them tends to increase relative to the intravascular pressure. This effect is easy to recognize with positive-pressure ventilation, but it also occurs with spontaneous inspiration, because intravascular pressures fall relative to atmospheric and alveolar pressure. The sheets of capillaries in the alveolar walls are protected from the full compressive force of the alveolar pressure by the surface tension of the fluid that lines curved portions of the alveolar surface. Microvessels in the “corners” where alveolar walls meet are more fully protected from compression by the sharper curvature of the surface film and perhaps by local distending forces, analogous to the situation with extraalveolar vessels (Figure 4-4). The pulmonary vascular resistance is the sum of that through alveolar and extraalveolar vessels and thus has a complex relationship with lung volume. It is lowest at approximately the normal resting lung volume (functional residual capacity) but increases at higher and lower volumes.

Figure 4-4 Alveolar “corner” at the junction of three alveolar walls. Surface tension (depicted by “springs”) holds vessels open, particularly in corners, and promotes fluid transudation by lowering the pressure around vessels.

(Modified with permission from Butler J: The circulation of the lung. In Culver BH, editor: The respiratory system, Seattle, 2006, University of Washington Publication Services, p 8.5.)

Blood Flow Distribution

Both vascular geometry and gravity influence the distribution of blood flow within the lung. If the upright lung is viewed as a stacked series of slices, a vertical gradient occurs in which the average flow per slice rises progressively down the lung, consistent with the influence of gravity. Within each slice, however, a marked variability of blood flow is found among regions, with high-flow areas distributed dorsally. The tendency of blood flow to be higher in dorsal and basal regions is largely preserved even when the gravitational direction is reversed, which indicates that anatomic branching patterns are a major determinant of flow distribution.

The gravitational effect has been conceptualized by dividing the lung into four zones, one above another, on the basis of the relationship of vascular and alveolar pressures (Figure 4-5). Intravascular pressures are higher at the bottom of the lung than at the top by an amount equal to a vertical hydrostatic column as high as the lung. Near the lung apex, zone I, the pressure in the alveoli (PA) exceeds that in both the pulmonary arteries (Ppa) and pulmonary vein (Ppv) and collapses the alveolar vessels, except those in the alveolar corners, which remain patent and allow some flow to continue. Below this, in zone II, Ppa exceeds PA, but PA is greater than Ppv, so flow depends on the pressure difference between Ppa and PA. The vessels remain open but are critically narrowed at the downstream end, where venous pressure is lower than alveolar pressure. This condition creates independence of flow from the downstream venous pressure, analogous to a waterfall in which a stream that flows over a precipice is unaffected by a rising level in the pool below until it rises above the level of the lip. In the middle to lower portion of the lung, zone III, both Ppa and Ppv exceed PA, the vessels are distended, and blood flow is the highest. Zone IV is restricted to a small area in the most dependent region, where flow diminishes. It has been postulated that this reduction is the result of increased vascular resistance secondary to low lung volume or perivascular edema in this area.

Figure 4-5 Perfusion in the lungs is influenced by the relationship of pulmonary arterial and venous pressures (Ppa and Ppv) to alveolar pressure (PA). In this example, the alveolar pressure is 10 cm H₂O, as might be found in a patient who receives positive-pressure ventilation.

(Modified with permission from Culver BH: Hemodynamic monitoring: physiologic problems in interpretation. In Fallat RJ, Luce JM, editors: Cardiopulmonary critical care, Edinburgh, 1988, Churchill Livingstone.)

Although the gravitational effect expressed in the vertical zone concept contributes to the average increase in flow down the lung, it does not explain the observed large variability in flow within an isogravitational slice, which implies that other anatomic or vasoregulatory factors are important at this level. More recent studies have determined that the heterogeneous distribution of blood flow within horizontal (isogravitational) planes is due to asymmetric branching geometries (and hence resistances) of the vascular tree. Because the vascular tree is largely a dichotomous branching structure, differences in resistances between daughter branches cause flow to be distributed unevenly between the branches. With differences in resistances occurring at every bifurcation in the vascular tree, blood flow becomes progressively more heterogeneous, resulting in a broad distribution of flows at the terminal branches. Owing to the shared heritage up the vascular tree, neighboring lung regions have similar magnitudes of flow, with high-flow regions near other high-flow regions and low-flow regions neighboring other low-flow regions. Hence, the spatial distribution of pulmonary blood flow is not random but rather exhibits a clear pattern of high and low flows (Figure 4-6). Studies have demonstrated that the pattern of perfusion distribution is very stable over time and with growth, and that the pattern is genetically determined. These insights provide a new perspective on blood flow distribution in the lung. The traditional model of vertically stacked zones needs to be replaced by one in which the multiple zones can exist within horizontal planes. In addition, the large degree of heterogeneity within isogravitational planes suggests that mechanisms other than gravity must be responsible for the tight matching between regional ventilation and blood flow.