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Pulmonary Interstitial Spaces and Lymphatics

Aubrey E. Taylor, James C. Parker

10.1002/cphy.cp030104

Source: Supplement 10: Handbook of Physiology, The Respiratory System, Circulation and Nonrespiratory Functions

Originally published: 1985

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Structure and Composition of Pulmonary Interstitium
1.1 Pulmonary Interstitial Connective Tissues
1.2 Physicochemical Properties of Interstitial Matrix
1.3 Vascular and Extravascular Fluid Compartments in the Lung
1.4 Effect of Increased Hydration on Tissue Fluid Compartments
2 Starling Forces and Lymph Flow
2.1 Theoretical Considerations
2.2 Endothelial Pathways
2.3 Filtration Coefficient
2.4 Capillary Pressure
2.5 Tissue Fluid Pressure
2.6 Estimation of Intra‐Alveolar Fluid Pressure by Analysis of Structure
2.7 Interstitial Compliance
2.8 Interstitial Fluid Pressure Gradients
2.9 Colloid Osmotic Pressure Gradient
2.10 Lymph Flow
2.11 Analyses of Force Changes During Formation of Alveolar Edema: Edema Safety Factor
3 Abnormal Capillary Permeability to Plasma Proteins (Leaky Lung Syndromes)
3.1 α‐Naphthylthiourea
3.2 Hydrochloric Acid Aspiration
3.3 Hemorrhagic Shock
3.4 Septic Shock
3.5 Histamine
3.6 High‐Altitude Pulmonary Edema
3.7 Neurogenic Pulmonary Edema
3.8 Microemboli Vascular Damage
3.9 Oxygen Toxicity
3.10 Other Compounds
3.11 Possible Mechanisms: Superoxide System
4 Sequence and Pathways for Pulmonary Edema Formation
5 Conclusions
Figure 1.

Intra‐alveolar interstitium (IS) showing filaments of proteoglycans throughout the slightly edematous interstitium. CO, bundle of collagen fibers; EP, epithelial barrier. × 6,100.

Micrograph courtesy of J. Gil
Figure 2.

Diagram of the extracellular matrix showing a collagen mesh with interspersed proteoglycans and glycosaminoglycans. Effect of increased hydration on matrix density and intragel dispersion of proteins and small solutes is also shown.

From Parker, Taylor, et al. , by permission of the American Heart Association, Inc
Figure 3.

Effect of increased hydration on hydraulic conductivity of umbilical interstitial matrix. Normal hydration, ∼9 ml H2O/g dry wt.

Adapted from Granger
Figure 4.

Schematic representation of lung fluid compartments. BDW, blood dry weight; BFDW, blood‐free dry weight; Qw, extravascular lung water; VA, albumin interstitial volume; VBW, blood water volume; Vcell, cell volume; VE, albumin‐excluded volume; VI, interstitial volume.
Figure 5.

A: effect of volume expansion on extravascular water (Qw) and diethylenetriamine pentaacetic acid (DTPA) interstitial volume (VI) in dog lung. BFDW, blood‐free dry weight. B: effect of increased pulmonary capillary pressure (Pc) on interstitial volume (ordinate) available to albumin (VAV) and excluded albumin volume (VE) in dog lungs. C: effect of increasing extravascular 99mTc‐DTPA VI on albumin‐excluded volume fraction (FE). Increasing left atrial pressure produced interstitial pulmonary edema.

A from Parker, Taylor, et al. , by permission of the American Heart Association, Inc.; B and C from Parker, Taylor, et al. , by permission of the American Heart Association, Inc
Figure 6.

Schematic representation of continuous and fenestrated capillary walls. 1, Plasmalemmal vesicles; 2, endothelial junctions; 3, transendothelial channels; 4, fenestrations. Diameters of structures are given. Top right, schematic of a transendothelial channel with its related structure and dimensions.

Adapted from Taylor and Granger
Figure 7.

Rate of pulmonary edema formation as a function of left atrial pressure.

From Guyton and Lindsey , by permission of the American Heart Association, Inc
Figure 8.

Lung weight gain curve after elevation of capillary pressure in isolated dog lung (top panel). Slopes were plotted as functions of time with a semilogarithmic plot (bottom panel). Two distinct components are always observed: a rapid blood volume component and a slower capillary filtration component.

From Drake
Figure 9.

A: estimation of capillary pressures (Pc) with alveolar absorptive measurements. Capillary pressure is shown as a function of vertical height. Distance between pulmonary arterial pressure (Ppa) and Pc represents precapillary resistance. Distance between left atrial pressure (Pla) and Pc represents postcapillary resistance. Arrow, transition from zone III to zone II perfusing conditions. Zone III, regions of the lung in which venous pressures exceed alveolar pressures. Zone II, areas in which alveolar pressures exceed venous pressures but not pulmonary arterial pressures. B: regional blood flow and resistances as a function of vertical height. Ra, precapillary resistance; Rt, total vascular resistance; Rv, postcapillary resistance. IV, III, and II: zonal conditions within the lung. Arrows, distance from bottom of the lung at which zonal conditions change. Zone IV, height at which vascular resistance increases after zone III condition.

From Parker, Taylor, et al.
Figure 10.

Schematic representation of balance of forces surrounding an extra‐alveolar vessel. Fo, outward acting stress exerted by alveolar wall attachments; Palv, alveolar gas pressure; Pv, vascular pressure; Pel,w, elastic vessel wall tension; Px, interstitial pressure.
Figure 11.

Calculated perivascular interstitial pressures (Px) relative to pleural pressure (Ppl) as a function of transpulmonary pressure at different vascular pressures (Pv).

From Smith and Mitzner
Figure 12.

Septal fluid pressures (Psf) measured by direct micro‐puncture and calculated from critical pressures for alveolar flooding. Palv alveolar pressure; Ptp, transpulmonary pressure.

Replotted data from Bhattacharya et al. , Lai‐Fook and Beck , and Lai‐Fook and Toporoff
Figure 13.

Rabbit lung alveolar septum preserved by vascular perfusion. A, alveolar space; A‐TI, air‐tissue interface, which appears very smooth; C, capillary; IA‐F, intra‐alveolar cusp fluid; LL, lipid lining layer; TIC, type I alveolar cell; TM, tubular myelin (surfactant), × 6,100.

Micrograph courtesy of J. Gil
Figure 14.

Hilar perivascular pressure [Px(f) ‐ Ppl] as a function of transpulmonary pressure (Ptp). Decreased values of K′ indicate a decreased radial traction exerted on the perivascular interstitial space as edema forms in the lung.

Data from Inoue et al.
Figure 15.

Lung interstitial volume as a function of calculated interstitial fluid pressure (PT). Slope of curve represents total interstitial compliance.

From Drake
Figure 16.

Wick‐catheter measurements of hilar perivascular fluid pressures as a function of lobe weight gain. Lobe A: vascular pressure, 25 cmH2O; transpulmonary pressure, 20 cmH2O. Lobe B: vascular pressure, 20 cmH2O; transpulmonary pressure, 25 cmH2O. Larger changes occur in perivascular fluid pressure during interstitial filling than alveolar flooding.

From Lai‐Fook and Toporoff
Figure 17.

A: schematic representation of fluid pathways (→) and pressure vectors (→) in septa and septal corner regions. B: fluid pathways in whole lung.
Figure 18.

Effect of steady‐state increases in capillary pressure on pressure gradients between septal and extra‐alveolar interstitial fluid, hydraulic conductivity of the septal interstitium, lymph flow, lymph protein concentration, and edema fluid accumulation in both the septal and perivascular interstitium.

From Guyton, Taylor, Drake, and Parker
Figure 19.

Plot of lymph‐to‐plasma concentration ratios (CL/CP) for plasma protein fractions (○, •, □, Δ) and povidone (×). ○, □, ×: CL/CP values obtained from sheep lymphatics by Brigham et al. , Parker et al. , and Boyd et al. , respectively, Δ, CL/CP values obtained from dog lung lymphatics by Parker, Taylor, et al. .

From Taylor and Granger
Figure 20.

A: lymph‐to‐plasma concentration ratios (CL/CP) as a function of lymph flow (JL) for 4 different osmotic reflection coefficient (σ) values. Ps, calculated permeability coefficient‐surface area product. B: CL/CP as a function of JL for 2 different osmotic reflection coefficient values (a) and surface areas (S).

From Taylor, Parker, et al.
Figure 21.

A: 1 − σ as a function of molecular radii for 6 protein fractions. Renkin's method was used to fit points to pore distributions. •, Data points, ×, Differences between data points not falling on 200‐Å curve and the predicted 200‐Å curve; these points (×) were best fitted with an 80‐Å curve. B: lymph‐to‐plasma concentration ratios (CL/CP) as a function of lymph flow from data obtained in sheep lymph by Parker .

A from Parker, Taylor, et al. , by permission of the American Heart Association, Inc.; B from Taylor and Granger
Figure 22.

Concentration ratios of lactate dehydrogenase in lymph and plasma (CL/CP) as a function of the isoelectric point (P1) of the particular isoenzyme of lactate dehydrogenase. The more positive lactate dehydrogenase is more restricted than its more negative isomer.

Adapted from Taylor and Granger
Figure 23.

A: change in plasma‐lymph colloid osmotic pressure gradient in isolated dog lung lymph as a function of change in capillary pressure (ΔPc). B: change in plasma‐lymph colloid osmotic pressure gradient in sheep lungs as a function of change in capillary pressure.

A adapted from Drake ; B from Erdmann et al. , by permission of the American Heart Association, Inc
Figure 24.

Difference in colloid osmotic pressure gradient between plasma and lymph (ΠP — ΠL) when only left atrial pressures were elevated (↑LAP) and when the lung circulation of the sheep was exposed to Pseudomonas aeruginosa, histamine, and endotoxin in the studies of Brigham et al. .

From Taylor, Parker, et al.
Figure 25.

Effect of protein exclusion on tissue colloid osmotic pressure (ΠT) when interstitial volume (V1) is expanded. _____, Decrease in ΠT if no exclusion is present; —-, ΠT when protein is excluded from a portion of the interstitial space. Note that for the same interstitial value, ΠT is lower when exclusion is present.

From Taylor, Parker, et al.
Figure 26.

Lung lymph flow as a function of capillary pressure for controls (○-○) and lungs challenged with Pseudomonas aeruginosa (□—□) and endotoxin (•-•).

Adapted from Brigham
Figure 27.

Lymphatic safety factor as a function of the filtration coefficient (Kf,c). Shaded area, range of Kf,c values determined with weight analyses.

Adapted from Taylor and Drake
Figure 28.

A: pressure gradients for fluid filtration and blood flow as a function of alveolar gas pressure (Palv) when pulmonary perfusing pressure is constant. Pc, capillary pressure; Ppa, pulmonary arterial pressure; Pla, left atrial pressure. Ppa — Palv is considered to be the perfusing gradient; Pc — Palv is the capillary filtration gradient. Flow would cease before pulmonary arterial pressure equaled alveolar gas pressure if all alveolar gas pressure was reflected to the capillary. B: pulmonary artery pressure as a function of time at 4 different levels of positive end‐expiratory pressure (PEEP) in a dog lung perfused at constant blood flow .

B from Permutt
Figure 29.

Starling force analyses in sheep and dog lungs. Change (%) in lymph flow (LF), in colloid osmotic pressure gradient between plasma and tissues (ΠP — ΠT), and in tissue pressure (PT) relative to change in capillary pressures. Numbers below each histogram are maximum change in each tissue force when capillary pressure was increased by 18 mmHg.

Adapted from Taylor
Figure 30.

Lymph‐to‐plasma concentration ratios (CL/CP) for total protein as a function of lymph flow relative to control .

Adapted from Rutili, Parker, Taylor, et al.
Figure 31.

Lymphatic protein clearances ( × CL/CP) after acid aspiration in intact dog lungs. Histograms, protein clearance when capillary pressures were elevated in controls and after acid. Effects of albumin and furosemide on acid‐induced clearance are also shown.

Data from Grimbert, Parker, and Taylor
Figure 32.

Flow diagram of superoxide system showing tissue damage (blocks 8-10), pretreatments to increase free‐radical scavengers (blocks 11-13), tissue hypoxic generation of superoxides (blocks 14-15), direct generation of O2 radicals with hyperoxia (block 7), and generation of arachidonic acid metabolites and subsequent generation of superoxides (blocks 5-6). Circled numbers, proposed sites of actions of different compounds on the generation of superoxides, peroxides, and hydroxyl radicals. Ibuprofen would act at the entry to block 5. Far right, free radicals generated either by tissues or leukocytes are summed and ability of tissues to scavenge free radicals is subtracted. Interplay between generation and scavenging determines whether capillary damage results.

From Taylor and Martin
Figure 33.

Alveolar fluid volume and minimum radius of curvature at air‐liquid interface at different steady‐state interstitial fluid pressures. At a critical fluid pressure of −2 mmHg a stable fluid volume could not be maintained and the alveolus completely filled with fluid.

From Guyton, Taylor, Drake, and Parker


Figure 1.

Intra‐alveolar interstitium (IS) showing filaments of proteoglycans throughout the slightly edematous interstitium. CO, bundle of collagen fibers; EP, epithelial barrier. × 6,100.

Micrograph courtesy of J. Gil


Figure 2.

Diagram of the extracellular matrix showing a collagen mesh with interspersed proteoglycans and glycosaminoglycans. Effect of increased hydration on matrix density and intragel dispersion of proteins and small solutes is also shown.

From Parker, Taylor, et al. , by permission of the American Heart Association, Inc


Figure 3.

Effect of increased hydration on hydraulic conductivity of umbilical interstitial matrix. Normal hydration, ∼9 ml H2O/g dry wt.

Adapted from Granger


Figure 4.

Schematic representation of lung fluid compartments. BDW, blood dry weight; BFDW, blood‐free dry weight; Qw, extravascular lung water; VA, albumin interstitial volume; VBW, blood water volume; Vcell, cell volume; VE, albumin‐excluded volume; VI, interstitial volume.



Figure 5.

A: effect of volume expansion on extravascular water (Qw) and diethylenetriamine pentaacetic acid (DTPA) interstitial volume (VI) in dog lung. BFDW, blood‐free dry weight. B: effect of increased pulmonary capillary pressure (Pc) on interstitial volume (ordinate) available to albumin (VAV) and excluded albumin volume (VE) in dog lungs. C: effect of increasing extravascular 99mTc‐DTPA VI on albumin‐excluded volume fraction (FE). Increasing left atrial pressure produced interstitial pulmonary edema.

A from Parker, Taylor, et al. , by permission of the American Heart Association, Inc.; B and C from Parker, Taylor, et al. , by permission of the American Heart Association, Inc


Figure 6.

Schematic representation of continuous and fenestrated capillary walls. 1, Plasmalemmal vesicles; 2, endothelial junctions; 3, transendothelial channels; 4, fenestrations. Diameters of structures are given. Top right, schematic of a transendothelial channel with its related structure and dimensions.

Adapted from Taylor and Granger


Figure 7.

Rate of pulmonary edema formation as a function of left atrial pressure.

From Guyton and Lindsey , by permission of the American Heart Association, Inc


Figure 8.

Lung weight gain curve after elevation of capillary pressure in isolated dog lung (top panel). Slopes were plotted as functions of time with a semilogarithmic plot (bottom panel). Two distinct components are always observed: a rapid blood volume component and a slower capillary filtration component.

From Drake


Figure 9.

A: estimation of capillary pressures (Pc) with alveolar absorptive measurements. Capillary pressure is shown as a function of vertical height. Distance between pulmonary arterial pressure (Ppa) and Pc represents precapillary resistance. Distance between left atrial pressure (Pla) and Pc represents postcapillary resistance. Arrow, transition from zone III to zone II perfusing conditions. Zone III, regions of the lung in which venous pressures exceed alveolar pressures. Zone II, areas in which alveolar pressures exceed venous pressures but not pulmonary arterial pressures. B: regional blood flow and resistances as a function of vertical height. Ra, precapillary resistance; Rt, total vascular resistance; Rv, postcapillary resistance. IV, III, and II: zonal conditions within the lung. Arrows, distance from bottom of the lung at which zonal conditions change. Zone IV, height at which vascular resistance increases after zone III condition.

From Parker, Taylor, et al.


Figure 10.

Schematic representation of balance of forces surrounding an extra‐alveolar vessel. Fo, outward acting stress exerted by alveolar wall attachments; Palv, alveolar gas pressure; Pv, vascular pressure; Pel,w, elastic vessel wall tension; Px, interstitial pressure.



Figure 11.

Calculated perivascular interstitial pressures (Px) relative to pleural pressure (Ppl) as a function of transpulmonary pressure at different vascular pressures (Pv).

From Smith and Mitzner


Figure 12.

Septal fluid pressures (Psf) measured by direct micro‐puncture and calculated from critical pressures for alveolar flooding. Palv alveolar pressure; Ptp, transpulmonary pressure.

Replotted data from Bhattacharya et al. , Lai‐Fook and Beck , and Lai‐Fook and Toporoff


Figure 13.

Rabbit lung alveolar septum preserved by vascular perfusion. A, alveolar space; A‐TI, air‐tissue interface, which appears very smooth; C, capillary; IA‐F, intra‐alveolar cusp fluid; LL, lipid lining layer; TIC, type I alveolar cell; TM, tubular myelin (surfactant), × 6,100.

Micrograph courtesy of J. Gil


Figure 14.

Hilar perivascular pressure [Px(f) ‐ Ppl] as a function of transpulmonary pressure (Ptp). Decreased values of K′ indicate a decreased radial traction exerted on the perivascular interstitial space as edema forms in the lung.

Data from Inoue et al.


Figure 15.

Lung interstitial volume as a function of calculated interstitial fluid pressure (PT). Slope of curve represents total interstitial compliance.

From Drake


Figure 16.

Wick‐catheter measurements of hilar perivascular fluid pressures as a function of lobe weight gain. Lobe A: vascular pressure, 25 cmH2O; transpulmonary pressure, 20 cmH2O. Lobe B: vascular pressure, 20 cmH2O; transpulmonary pressure, 25 cmH2O. Larger changes occur in perivascular fluid pressure during interstitial filling than alveolar flooding.

From Lai‐Fook and Toporoff


Figure 17.

A: schematic representation of fluid pathways (→) and pressure vectors (→) in septa and septal corner regions. B: fluid pathways in whole lung.



Figure 18.

Effect of steady‐state increases in capillary pressure on pressure gradients between septal and extra‐alveolar interstitial fluid, hydraulic conductivity of the septal interstitium, lymph flow, lymph protein concentration, and edema fluid accumulation in both the septal and perivascular interstitium.

From Guyton, Taylor, Drake, and Parker


Figure 19.

Plot of lymph‐to‐plasma concentration ratios (CL/CP) for plasma protein fractions (○, •, □, Δ) and povidone (×). ○, □, ×: CL/CP values obtained from sheep lymphatics by Brigham et al. , Parker et al. , and Boyd et al. , respectively, Δ, CL/CP values obtained from dog lung lymphatics by Parker, Taylor, et al. .

From Taylor and Granger


Figure 20.

A: lymph‐to‐plasma concentration ratios (CL/CP) as a function of lymph flow (JL) for 4 different osmotic reflection coefficient (σ) values. Ps, calculated permeability coefficient‐surface area product. B: CL/CP as a function of JL for 2 different osmotic reflection coefficient values (a) and surface areas (S).

From Taylor, Parker, et al.


Figure 21.

A: 1 − σ as a function of molecular radii for 6 protein fractions. Renkin's method was used to fit points to pore distributions. •, Data points, ×, Differences between data points not falling on 200‐Å curve and the predicted 200‐Å curve; these points (×) were best fitted with an 80‐Å curve. B: lymph‐to‐plasma concentration ratios (CL/CP) as a function of lymph flow from data obtained in sheep lymph by Parker .

A from Parker, Taylor, et al. , by permission of the American Heart Association, Inc.; B from Taylor and Granger


Figure 22.

Concentration ratios of lactate dehydrogenase in lymph and plasma (CL/CP) as a function of the isoelectric point (P1) of the particular isoenzyme of lactate dehydrogenase. The more positive lactate dehydrogenase is more restricted than its more negative isomer.

Adapted from Taylor and Granger


Figure 23.

A: change in plasma‐lymph colloid osmotic pressure gradient in isolated dog lung lymph as a function of change in capillary pressure (ΔPc). B: change in plasma‐lymph colloid osmotic pressure gradient in sheep lungs as a function of change in capillary pressure.

A adapted from Drake ; B from Erdmann et al. , by permission of the American Heart Association, Inc


Figure 24.

Difference in colloid osmotic pressure gradient between plasma and lymph (ΠP — ΠL) when only left atrial pressures were elevated (↑LAP) and when the lung circulation of the sheep was exposed to Pseudomonas aeruginosa, histamine, and endotoxin in the studies of Brigham et al. .

From Taylor, Parker, et al.


Figure 25.

Effect of protein exclusion on tissue colloid osmotic pressure (ΠT) when interstitial volume (V1) is expanded. _____, Decrease in ΠT if no exclusion is present; —-, ΠT when protein is excluded from a portion of the interstitial space. Note that for the same interstitial value, ΠT is lower when exclusion is present.

From Taylor, Parker, et al.


Figure 26.

Lung lymph flow as a function of capillary pressure for controls (○-○) and lungs challenged with Pseudomonas aeruginosa (□—□) and endotoxin (•-•).

Adapted from Brigham


Figure 27.

Lymphatic safety factor as a function of the filtration coefficient (Kf,c). Shaded area, range of Kf,c values determined with weight analyses.

Adapted from Taylor and Drake


Figure 28.

A: pressure gradients for fluid filtration and blood flow as a function of alveolar gas pressure (Palv) when pulmonary perfusing pressure is constant. Pc, capillary pressure; Ppa, pulmonary arterial pressure; Pla, left atrial pressure. Ppa — Palv is considered to be the perfusing gradient; Pc — Palv is the capillary filtration gradient. Flow would cease before pulmonary arterial pressure equaled alveolar gas pressure if all alveolar gas pressure was reflected to the capillary. B: pulmonary artery pressure as a function of time at 4 different levels of positive end‐expiratory pressure (PEEP) in a dog lung perfused at constant blood flow .

B from Permutt


Figure 29.

Starling force analyses in sheep and dog lungs. Change (%) in lymph flow (LF), in colloid osmotic pressure gradient between plasma and tissues (ΠP — ΠT), and in tissue pressure (PT) relative to change in capillary pressures. Numbers below each histogram are maximum change in each tissue force when capillary pressure was increased by 18 mmHg.

Adapted from Taylor


Figure 30.

Lymph‐to‐plasma concentration ratios (CL/CP) for total protein as a function of lymph flow relative to control .

Adapted from Rutili, Parker, Taylor, et al.


Figure 31.

Lymphatic protein clearances ( × CL/CP) after acid aspiration in intact dog lungs. Histograms, protein clearance when capillary pressures were elevated in controls and after acid. Effects of albumin and furosemide on acid‐induced clearance are also shown.

Data from Grimbert, Parker, and Taylor


Figure 32.

Flow diagram of superoxide system showing tissue damage (blocks 8-10), pretreatments to increase free‐radical scavengers (blocks 11-13), tissue hypoxic generation of superoxides (blocks 14-15), direct generation of O2 radicals with hyperoxia (block 7), and generation of arachidonic acid metabolites and subsequent generation of superoxides (blocks 5-6). Circled numbers, proposed sites of actions of different compounds on the generation of superoxides, peroxides, and hydroxyl radicals. Ibuprofen would act at the entry to block 5. Far right, free radicals generated either by tissues or leukocytes are summed and ability of tissues to scavenge free radicals is subtracted. Interplay between generation and scavenging determines whether capillary damage results.

From Taylor and Martin


Figure 33.

Alveolar fluid volume and minimum radius of curvature at air‐liquid interface at different steady‐state interstitial fluid pressures. At a critical fluid pressure of −2 mmHg a stable fluid volume could not be maintained and the alveolus completely filled with fluid.

From Guyton, Taylor, Drake, and Parker
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Article Title: Pulmonary Interstitial Spaces and Lymphatics
 

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Aubrey E. Taylor, James C. Parker. Pulmonary Interstitial Spaces and Lymphatics. Compr Physiol 2011, Supplement 10: Handbook of Physiology, The Respiratory System, Circulation and Nonrespiratory Functions: 167-230. First published in print 1985. doi: 10.1002/cphy.cp030104