Pulmonary vascular heterogeneity and the Starling hypothesis

Microvascular Research

Volumn 78, Issue 1, 2009, Pages 71-77

  Effros, Richard M ^a   Parker, James C ^b  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTH ALABAMA   (United States)

Author keywords

Endothelial permeability; Extra alveolar vessels; Hydrostatic pressure; Protein osmotic pressure; Pulmonary edema; Pulmonary interstitium; Reflection coefficient

Indexed keywords

ALBUMIN; PLASMA PROTEIN;

CAPILLARY PERMEABILITY; ELECTROLYTE TRANSPORT; FLUID TRANSPORT; HUMAN; HYDROSTATIC PRESSURE; HYPOTHESIS; LUNG BLOOD FLOW; LUNG CAPILLARY; LUNG CIRCULATION; LUNG EDEMA; LUNG ENDOTHELIUM; LUNG FLUID; LUNG PRESSURE; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PULMONARY ARTERY; PULMONARY VEIN; REVIEW; STARLING LAW; ULTRAFILTRATION; VASCULAR ENDOTHELIUM;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD VESSELS; CAPILLARY PERMEABILITY; HUMANS; HYDROSTATIC PRESSURE; LUNG; MICROCIRCULATION; MICROVESSELS; OSMOTIC PRESSURE; PROTEINS; PULMONARY ALVEOLI; PULMONARY ARTERY; PULMONARY CIRCULATION; PULMONARY EDEMA;

EID: 67349096094     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2009.03.004     Document Type: Review

References (90)

1. Adamson R.H., Lenz J.F., Zhang X., Adamson G.N., Weinbaum S., and Curry F.E. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J. Physiol. 557 (2004) 889-907
2. Albert R.K., Kirk W., Pitts C., and Butler J. Extra-alveolar vessel fluid filtration coefficients in excised and in situ canine lobes. J. Appl. Physiol. 59 (1985) 1555-1559
3. Barber B.J., and Nearing B.D. Spatial distribution of protein in interstitial matrix of rat mesenteric tissue. Am. J. Physiol, Heart Circ. Physiol. 258 (1990) H556-H564
4. Bhattacharya J. Hydraulic conductivity of lung venules determined by split-droplet technique. J. Appl. Physiol. 64 (1988) 2562-2567
5. Bhattacharya J., Gropper M.A., and Staub N.C. Interstitial fluid pressure gradient measured by micropuncture in excised dog lung. J. Appl. Physiol. 56 (1984) 271-277
6. Brigham K.L., Harris T.R., and Owen P.J. [14C]urea and [14C]sucrose as permeability indicators in histamine pulmonary edema. J. Appl. Physiol.: Respir., Environ. Exercise Physiol. 43 (1977) 99-101
7. Chang R.S.Y., Wright K., and Effros R.M. Role of albumin in prevention of edema in perfused rabbit lungs. J. Appl. Physiol. 50 (1981) 1065-1070
8. Charron P.D., Fawley J.P., and Maron M.B. Effect of epinephrine on alveolar liquid clearance in the rat. J. Appl. Physiol. 87 (1999) 611-618
9. Chinard F.P., and Enns T. Transcapillary pulmonary exchange of water in the dog. Am. J. Physiol. 178 (1954) 197-202
10. Chinard F.P., Vosburgh J., and Enns T. Transcapillary exchange of water and other substances in certain organs of the dog. Am. J. Physiol. 183 (1955) 221-234
11. Conhaim R.L., Gropper M.A., and Staub N.C. Effect of lung inflation on alveolar-airway barrier protein permeability in dog lung. J. Appl. Physiol.: Respir., Environ. Exercise Physiol. 55 (1983) 1249-1256
12. Crone C. The permeability of capillaries in various organs as determined by usse of the "indicator dilffusion" method. Acta Physiol. Scand. 58 (1963) 292-305
13. Curry F.R. Effect of albumin on the structure of the molecular filter at the capillary wall. Fed. Proc. 44 (1985) 2610-2613
14. Dammacco F., Miglietta A., D'Addabbo A., Fratello A., Moschetta R., and Bonomo L. Analbuminemia: report of a case and review of the literature. Vox Sang. 39 (1980) 153-161
15. Del Vecchio P.J., Siflinger-Birnboim A., Belloni P.N., Holleran L.A., Lum H., and Malik A.B. Culture and characterization of pulmonary microvascular endothelial cells. In Vitro Cell. Dev. Biol. 28A 11-12 (1992) 711-715
16. Dorhout E.J., Ross J.C., Boer P., Yoe O., and Simatupang T.A. Observations on edema formation in the nephrotic syndrome in adults with minimal lesions. Am. J. Med. 67 (1979) 378-384
17. Drake R.E., and Gabel J.C. Effect of histamine and alloxan on canine pulmonary vascular permeability. Am. J. Physiol. 239 (1980) H96-H100
18. Drake R.E., Dhother S., and Gabel J.C. Pulmonary microvascular reflection coefficients estimated with modified lymphatic washdown technique. Am. J. Physiol, Heart Circ. Physiol. 272 (1997) H382-H385
19. Drake R.E., Dhother S., Teague R.A., and Gabel J.C. Protein osmotic pressure gradients and microvascular reflection coefficients. Am. J. Physiol, Heart Circ. Physiol. 273 (1997) H997-H1002
20. Drake R.E., Smith J.H., and Gabel J.C. Estimation of the filtration coefficient in intact dog lungs. Am. J. Physiol. 238 (1980) H430-H438
21. Dreyfuss D., Soler P., and Saumon G. Spontaneous resolution of pulmonary edema caused by short periods of cyclic overinflation. J. Appl. Physiol. 72 (1992) 2081-2089
22. Effros R.M. Osmotic extraction of hypotonic fluid from the lungs. J. Clin. Invest. 54 (1974) 935-947
23. Effros R.M., and Chang R.S.Y. Distribution of water and proteins in the lungs in pulmonary edema. In: Fishman A.P., and Renkin E.M. (Eds). Pulmonary Edema (1979), American Physiological Society, Bethesda, Md 137-144
24. Effros R.M., Chang R., and Silverman P. The effect of single transit and equilibrium studies of 22Na+ distribution in the lung. Chest 71 (1977) 296S-298S
25. Effros R.M., Schapira R., Presberg K., Ozker K., and Jacobs E.R. Stop flow studies of solute uptake in rat lungs. J. Appl. Physiol. 85 (1998) 986-992
26. Effros R.M., Jacobs E.R., Schapira R.M., Lin W., and Presberg K. Increasing airway pressures can promote transvascular edema reabsorption. Chest 116 (1999) 30S-31S
27. Fukue M., Serikov V.B., and Jerome E.H. Recovery from increased pressure or increased leakiness edema in perfused sheep lungs. J. Appl. Physiol. 77 (1994) 184-189
28. Gaar Jr. K.A., Taylor A.E., Owens L.J., and Guyton A.C. Pulmonary capillary pressure and filtration coefficient in the isolated perfused lung. Am. J. Physiol. 213 (1967) 910-914
29. Gebb S., and Stevens T. On lung endothelial cell heterogeneity. Microvasc. Res. 68 (2004) 1-12
30. Gee M.S., Gee M.H., and Williams D.O. Effect of lung inflation on perivascular cuff fluid volume in isolated dog lung lobes. Microvasc. Res. 17 (1979) 192-201
31. Guyton A.C., and Lindsey A.W. Effect of elevated left atrial pressure and decreased plasma protein concentration on the development of pulmonary edema. Circ. Res. 7 (1959) 649-657
32. Harris P., and Heath D. The Human Pulmonary Circulation. (2nd ed.) (1977), Edinburgh:S Churhill Livingstone 22-136
33. Hislop A., and Reid L.M. Formation of the pulmonary vasculature. In: Hodson W.A. (Ed). Development of the Lung (1977), Dekker, New York 37-86
34. Iliff L.D. Extra-alveolar vessels and edema development in excised dog lungs. Circ. Res. 28 (1971) 524-532
35. Ishibashi M., Reed R.K., Townsley M.I., Parker J.C., and Taylor A.E. Albumin transport across pulmonary capillary-interstitial barrier in anesthetized dogs. J. Appl. Physiol. 70 (1991) 2104-2110
36. Kappagoda C.T., and Krishnan R.K. The rapidly adapting receptors in mammalian airways and their responses to changes in extravascular fluid volume. Exp. Physiol. 91 (2006) 647-654
37. Kelly J.J., Moore T.M., Babal P., Diwan A.H., Stevens T., and Thompson W.J. Pulmonary microvascular and macrovascular endothelial cells: differential regulation of Ca2+ and permeability. Am. J. Physiol. 274 5 Pt 1 (1998) L810-L819
38. Keys A. The apparent permeability of the capillary membrane in man. The Properties and Functions of Membranes, Natural and Artificial (1937), Trans. Faraday Soc, London 930-939
39. King J., Hamil T., Creighton J., Wu S., Bhat P., McDonald F., and Stevens T. Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes. Microvasc. Res. 67 (2004) 139-151
40. Kramer G.C., Harms B.A., Bodai B.I., Renkin E.M., and Demling R.H. Effects of hypoproteinemia and increased vascular pressure on lung fluid balance in sheep. J. Appl. Physiol. 55 (1983) 1514-1522
41. Lai-Fook S.J. Perivascular interstitial fluid pressure measured by micropipettes in isolated dog lung. J. Appl. Physiol. 52 (1982) 9-15
42. Lamm W.J., Luchtel D., and Albert R.K. Sites of leakage in three models of acute lung injury. J. Appl. Physiol. 64 (1988) 1079-1083
43. Levick J.R. Capillary filtration-absorption balance reconsidered in light of dynamic extravascular factors. Exp. Physiol. 76 (1991) 825-857
44. Levick J.R. Revision of the Starling principle: new views of tissue fluid balance. Physiologist 557 (2004) 704
45. Levine O.R., Mellins R.B., Senior R.M., and Fishman A.P. The application of Starling's law of capillary exchange to the lungs. J. Clin. Invest 40 (1967) 934-944
46. Lindert J., Perlman C.E., Parthasarathi K., and Bhattacharya J. Chloride-dependent secretion of alveolar wall liquid determined by optical-sectioning microscopy. Am. J. Respir. Cell Mol. Biol. 36 (2007) 688-696
47. Lowe K., Alvarez D., King J., and Stevens T. Phenotypic heterogeneity in lung capillary and extra-alveolar endothelial cells. Increased extra-alveolar endothelial permeability is sufficient to decrease compliance. J. Surg. Res. 143 (2007) 70-77
48. Macklin C.C. Evidences of increase in capacity of the pulmonary arteries and veins of dogs, cats and rabbits during inflation of the freshly excised lung. Rev. Can. Biol. 5 (1946) 199-233
49. Matthay M.A., Folkesson H.G., and Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Phys. Rev. 82 (2002) 569-600 10
50. Mazzone R.W., Durand C.M., and West J.B. Electron microscopy of lung rapidly frozen under controlled physiological conditions. J. Appl. Physiol.: Respir., Environ. Exercise Physiol. 45 (1978) 325-333
51. Mehta D., Bhattacharya J., Matthay M.A., and Malik A.B. Integrated control of lung fluid balance Am. J. Physiol., Lung Cell. Mol. Physiol. 287 (2004) 1081-1090
52. Michel C.C., and Curry F.E. Microvascular permeability. Physiol. Rev. 79 (1999) 703-761
53. Miserocchi G., Negrini D., and Gonano C. Direct measurement of interstitial pulmonary pressure in in situ lung with intact pleural space. J. Appl. Physiol. 69 (1990) 2168-2174
54. Miserocchi G., Negrini D., Passi A., and De Luca G. Development of lung edema: interstitial fluid dynamics and molecular structure. News Physiol. Sci. 16 (2001) 66-71
55. Mitzner W., and Robotham J.L. Distribution of interstitial compliance and filtration coefficient in canine lung. Lymphology 12 (1979) 140-148
56. Mutlu G.M., and Sznajder J.I. Mechanisms of pulmonary edema clearance. Am. J. Physiol. 289 (2005) L685-L695
57. Nagaishi C. Functional Anatomy and Histology of the Lung Baltimore (1972), University Park, MD
58. Ofori-Acquah S.F., King J., Voelkel N., Schaphorst K.L., and Stevens T. Heterogeneity of barrier function in the lung reflects diversity in endothelial cell junctions. Microvasc. Res. 75 (2008) 391-402
59. Oh P., Borgström P., Witkiewicz H., Li Y., Borgström B.J., Chrastina A., Iwata K., Zinn K.R., Baldwin R., Testa J.E., and Schnitzer J.E. Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung. Nat. Biotechnol. 25 (2007) 327-337
60. Parker J.C. Hydraulic conductance of lung endothelial phenotypes and Starling safety factors against edema. Am. J. Physiol., Lung Cell. Mol. Physiol. 292 (2006) 378-380
61. Parker, J.C. 2006b.Hydraulic conductance (Lp) of lung endothelial phenotypes and Starling safety factors against edema. Am J Physiol 2007, 36: L378-L380 12
62. Parker J.C., and Yoshikawa S. Vascular segmental permeabilities at high peak inflation pressure in isolated rat lungs. Am. J. Physiol. 283 (2002) L1203-L1209
63. Parker J.C., Crain M., Grimbert F., Rutili G., and Taylor A.E. Total lung lymph flow and fluid compartmentation in edematous dog lungs. J. Appl. Physiol.: Respir., Environ. Exercise Physiol. 51 (1981) 1268-1277
64. Parker J.C., Parker R.E., Granger D.N., and Taylor A.E. Vascular permeability and transvascular fluid and protein transport in the dog lung. Circ. Res. 48 (1981) 549-561
65. Parker J.C., Ryan J., and Taylor A.E. Plasma-lymph albumin kinetics, total lymph flow, and tissue hematocrit in normally hydrated dog lungs. Microvasc. Res. 28 (1984) 254-269
66. Parker J.C., Perry M.A., and Taylor A.E. Permeability of the microvascular barrier. In: Staub N.C., and Taylor A.E. (Eds). Edema (1984), Raven Press, New York 143-187
67. Parker J.C., Stevens T., Randall J., Weber D.S., and King J.A. Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers. Am. J. Physiol., Lung Cell. Mol. Physiol. 291 (2006) L30-L37
68. Perl W., Chowdhury P., and Chinard F.P. Reflection coefficients of dog lung endothelium to small hydrophilic solutes. Am. J. Physiol. 228 (1975) 797-809
69. Permutt S. Mechanical Influences on Water Accumulation in the Lungs in Pulmonary Edema (1979), APS
70. Rackow E.C., Janz T., Astiz M.E., and Weil M.H. Absence of lung edema in nephrotic rats. J. Lab. Clin. Med. 108 (1986) 349-353
71. Rippe B., Townsley M., Parker J.C., and Taylor A.E. Osmotic reflection coefficient for total plasma protein in lung microvessels. J. Appl. Physiol. 58 (1985) 436-442
72. Rutili G., Kvietys P., Martin D., Parker J.C., and Taylor A.E. Increased pulmonary microvasuclar permeability induced by alpha-naphthylthiourea. J. Appl. Physiol.: Respir., Environ. Exercise Physiol. 52 (1982) 1316-1323
73. Safdar Z., Wang P., Ichimura H., Issekutz A.C., Quadri S., and Bhattacharya J. Hyperosmolarity enhances the lung capillary barrier. J. Clin. Invest. 112 (2003) 1541-1549
74. Schnaper H.W., Robson A.M., Jeffrey B., and Kopp J.B. In: Schrier R.W. (Ed). Nephrotic Syndrome: Minimal Change Nephropathy, Focal Segmental Glomerulosclerosis, and Collapsing Glomerulopathy. Diseases of the Kidney & Urinary Tract Diseases of the Kidney & Urinary Tract. (8th Edition) (2007), Lippincott Williams & Wilkins 1602 Chapter 64
75. Schneeberger E.E., and Hamelin M. Interaction of serum proteins with lung endothelial glycocalyx: its effect on endothelial permeability. Am. J. Physiol, Heart Circ. Physiol. 247 (1984) H206-H217
76. Schnitzer J.E., Siflinger-Birnboim A., Del Vecchio P.J., and Malik A.B. Segmental differentiation of permeability, protein glycosylation, and morphology of cultured bovine lung vascular endothelium. Biochem. Biophys. Res. Commun. 199 (1994) 11-19
77. Selinger S.L., Bland R.D., Demling R.H., and Staub N.C. Distribution volumes of [131I]albumin, [14C]sucrose and 36Cl in sheep lung. J. Appl. Physiol. 39 (1975) 773-779
78. Snashall P.D. Mucopolysaccharide osmotic pressure in the measurement of interstitial pressure. Am. J. Physiol, Heart Circ. Physiol. 232 (1977) H608-H616
79. Snashall P.D., Lucas J., Guz A., and Floyer M.A. Measurement of interstitial 'flluid' pressure by means of a cotton wick in man and animals: an analysis of the origin of the pressure. Clin. Sci. 41 (1971) 35-53
80. Starling E.H. On the absorption of fluids from connective tissue spaces. J. Physiol. 19 (1896) 312-326
81. Starling, E.H., 1896b. The Arris and Gale lectures on the physiological factors involved in the causation of dropsy. Lancet i:1267-1270, 1331-1334,1407-1410.
82. Staub N.C., Gee M., and Vreim C. Mechanism of alveolar flooding in acute pulmonary edema in Lung Liquids. Ciba Symp. 38 (1976) 255-263
83. Stevens T., Phan S., Frid M.G., Alvarez D., Herzog E., and Stenmark K.R. Lung vascular cell heterogeneity endothelium, smooth muscle, and fibroblasts. Proc. Am. Thorac. Soc. 5 (2008) 783-791
84. Taylor A.E., and Parker J.C. The interstitial spaces and lymph flow. In: Fishman A.P., and Fisher A.B. (Eds). Handbook of Physiology: The Respiratory System. Circulation and Nonrespiratory Function (1985), Am. Physiol. Soc., Bethesda, MD 167-320
85. Townsley M.I., King J.A., and Alvarez D. Ca2+ channels and pulmonary endothelial permeability: insights from study of intact lung and chronic pulmonary hypertension. Microcirc. 13 (2006) 725-739
86. Vargas F.F., and Blackshear G.L. Secondary driving forces affecting transcapillary osmotic flows in perfused heart. Am. J. Physiol, Heart Circ. Physiol. 240 (1981) H457-H464
87. Ware L.B., and Matthay M.A. Clinical practice. Acute pulmonary edema. N. Engl. J. Med. 353 (2005) 2788-2796
88. Waterlow J.C. Kwashiorkor revisited: the pathogenesis of oedema in kwashiorkor and its significance. Trans. R. Soc. Trop. Med. Hyg. 78 (1984) 436-441
89. Watkins S., Madison J., Galliano M., Minchiotti L., and Putnam F.W. Analbuminemia: three cases resulting from different point mutations in the albumin gene. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 9417-9421
90. Wiederhielm C.A., Fox J.R., and Lee D.R. Ground substance mucopolysaccharides and plasma proteins: their role in capillary water balance. Am. J. Physiol. 230 (1976) 1121-1125