Capillary filtration‐absorption balance reconsidered in light of dynamic extravascular factors

The evidence for the functional importance of extravascular Starling pressures now seems overwhelming, and when these terms are taken into account it is difficult to uphold the traditional conception that upstream microvascular filtration is largely matched by a sustained downstream reabsorption. Transient absorption can occur, however, during spontaneous vasomotion cycles, during sympathetic‐induced vasoconstriction and during hypovolaemic hypotension. Sustained absorption is possible in specialized tissues where the interstitium is ‘flushed’ by an independent stream (intestinal mucosa, renal cortex, lymph nodes). Both theory and experiment show, however, that absorption cannot be maintained across most low‐pressure exchange segments due to the finite permeability of microvessels to plasma protein, which leads to a rise in pericapillary interstitial oncotic pressure with time around absorbing microvascular segments. Extravascular hydraulic resistance may be a further determinant of net fluid transfer rate in situations where capillary wall resistance is low.

[1]  E. M. Renkin,et al.  Mechanics and thermodynamics of transcapillary exchange , 1984 .

[2]  L. Zachariae,et al.  The contributions from hyaluronic acid and from protein to the colloid osmotic pressure of human synovial fluid. , 1959, Acta rheumatologica Scandinavica.

[3]  A C Guyton,et al.  Interstitial Fluid Pressure , 1968, Circulation research.

[4]  C. Michel,et al.  Steady‐state fluid filtration at different capillary pressures in perfused frog mesenteric capillaries. , 1987, The Journal of physiology.

[5]  S. Weinbaum,et al.  A NEW MODEL FOR CAPILLARY FILTRATION BASED ON RECENT ELECTRON MICROSCOPIC STUDIES OF ENDOTHELIAL JUNCTIONS , 1989 .

[6]  C. Wiederhielm,et al.  Microvascular, lymphatic, and tissue pressures in the unanesthetized mammal. , 1973, The American journal of physiology.

[7]  P. Knox,et al.  The effect of the canine popliteal node on the composition of lymph. , 1983, The Journal of physiology.

[8]  Timothy W. Secomb,et al.  Effect of extravascular pressure gradients on capillary fluid exchange , 1986 .

[9]  P. Lund-johansen,et al.  Interstitial colloid osmotic and hydrostatic pressures in human subcutaneous tissue during early stages of heart failure. , 1984, Clinical physiology.

[10]  J. Levick,et al.  Synovial fluid--its mass, macromolecular content and pressure in major limb joints of the rabbit. , 1988, Quarterly journal of experimental physiology.

[11]  M. Intaglietta,et al.  Experimental and quantitative analysis of microcirculatory water exchange. , 1979, Acta physiologica Scandinavica. Supplementum.

[12]  J. Levick,et al.  Effect of fluid pressure on the hydraulic conductance of interstitium and fenestrated endothelium in the rabbit knee. , 1985, The Journal of physiology.

[13]  E. Landis,et al.  Micro-injection studies of capillary blood pressure in human skin , 1930 .

[14]  J. Levick,et al.  Synovial capillary distribution in relation to altered pressure and permeability in knees of anaesthetized rabbits. , 1989, The Journal of physiology.

[15]  S. Jacobsson,et al.  FLOW AND PROTEIN CONTENT OF LYMPH IN RESTING AND EXERCISING SKELETAL MUSCLE. , 1964, Acta physiologica Scandinavica.

[16]  J. Tooke,et al.  Effect of postural change and thermoregulatory stress on the capillary microcirculation of the human toe. , 1989, Clinical science.

[17]  H. Granger,et al.  Permeability of Connective Tissue Linings Isolated from Implanted Capsules: IMPLICATIONS FOR INTERSTITIAL PRESSURE MEASUREMENTS , 1975, Circulation research.

[18]  B. Zweifach,et al.  Micropressures and capillary filtration coefficients in single vessels of the cremaster muscle of the rat. , 1970, Microvascular research.

[19]  A. Taylor,et al.  Vascular Permeability and Transvascular Fluid and Protein Transport in the Dog Lung , 1981, Circulation research.

[20]  R. W. Gore Fluid exchange across single capillaries in rat intestinal muscle. , 1982, The American journal of physiology.

[21]  L. W. Eichna,et al.  CAPILLARY BLOOD PRESSURE IN MAN. DIRECT MEASUREMENTS IN THE DIGITS OF NORMAL AND HYPERTENSIVE SUBJECTS DURING VASOCONSTRICTION AND VASODILATATION VARIOUSLY INDUCED. , 1942, The Journal of clinical investigation.

[22]  C. Michel,et al.  The ultrastructure of frog microvessels following perfusion with the ionophore A23187. , 1988, Quarterly journal of experimental physiology.

[23]  M. Gordon The renal circulation. , 1951, Canadian journal of medical technology.

[24]  A. Taylor,et al.  The Effect of Increased Vascular Pressure on Albumin‐Excluded Volume and Lymph Flow in the Dog Lung , 1980, Circulation research.

[25]  J. Pappenheimer,et al.  Effective osmotic pressure of the plasma proteins and other quantities associated with the capillary circulation in the hindlimbs of cats and dogs. , 1948, The American journal of physiology.

[26]  R. D. Hogan,et al.  Interspecific comparison of subcutaneous tissue fluid pressure in the bat wing. , 1985, Microvascular research.

[27]  K. Arfors,et al.  Protein concentration in interstitial and lymphatic fluids from the subcutaneous tissue. , 1977, Acta physiologica Scandinavica.

[28]  C. Michel,et al.  Inflammatory changes in permeability and ultrastructure of single vessels in the frog mesenteric microcirculation. , 1988, The Journal of physiology.

[29]  C. Michel Capillary permeability and how it may change. , 1988, The Journal of physiology.

[30]  P. F. Scholander,et al.  Negative pressure in the interstitial fluid of animals. Fluid tensions are spectacular in plants; in animals they are elusively small, but just as vital. , 1968, Science.

[31]  B. Oberg,et al.  VASCULAR ADJUSTMENTS TO INCREASED TRANSMURAL PRESSURE IN CAT AND MAN WITH SPECIAL REFERENCE TO SHIFTS IN CAPILLARY FLUID TRANSFER. , 1964, Acta physiologica Scandinavica.

[32]  J. L. D'silva,et al.  Interfibre fluid from guinea-pig muscle. , 1962, The Journal of physiology.

[33]  R K Jain,et al.  Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. , 1989, Microvascular research.

[34]  J. H. Dial,et al.  Influence of flow variations on capillary hematocrit in mesentery. , 1971, The American journal of physiology.

[35]  A. Guz,et al.  Measurement of interstitial 'fluid' pressure by means of a cotton wick in man and animals: an analysis of the origin of the pressure. , 1971, Clinical science.

[36]  G. Kramer,et al.  Wick sampling of interstitial fluid in rat skin: further analysis and modifications of the method. , 1986, Microvascular research.

[37]  C. Wiederhielm,et al.  Dynamics of capillary fluid exchange: a nonlinear computer simulation. , 1979, Microvascular research.

[38]  W. Durán,et al.  Mathematical modeling of mass transfer in microvascular wall and interstitial space. , 1990, Microvascular research.

[39]  J. Levick,et al.  Ultrastructure of transport pathways in stressed synovium of the knee in anaesthetized rabbits. , 1989, The Journal of physiology.

[40]  E. M. Renkin,et al.  Influence of saline infusion on blood-tissue albumin transport. , 1989, The American journal of physiology.

[41]  A. C. Guyton,et al.  Modification of lymph by lymph nodes. II. Effect of increased lymph node venous blood pressure. , 1983, The American journal of physiology.

[42]  E. M. Renkin Some consequences of capillary permeability to macromolecules: Starling's hypothesis reconsidered. , 1986, The American journal of physiology.

[43]  K. Aukland,et al.  A colloid osmometer for small fluid samples. , 1974, Acta physiologica Scandinavica.

[44]  J. M. Yoffey,et al.  Lymphatics, lymph and the lymphomyeloid complex , 1970 .

[45]  O. Sejersted,et al.  Intramuscular fluid pressure during isometric contraction of human skeletal muscle. , 1984, Journal of applied physiology: respiratory, environmental and exercise physiology.

[46]  C. Wiederhielm,et al.  Effects of oncotic gradients and enzymes on negative pressures in implanted capsules. , 1970, The American journal of physiology.

[47]  J. Levick,et al.  Pressure‐volume relationships above and below atmospheric pressure in the synovial cavity of the rabbit knee. , 1982, The Journal of physiology.

[48]  D. Slaaf,et al.  Pressure regulation in muscle of unanesthetized bats. , 1987, Microvascular research.

[49]  R. K. Reed An implantable colloid osmometer. Measurements in subcutis and skeletal muscle of rats. , 1979, Microvascular research.

[50]  P. Simkin,et al.  Hydrostatic and oncotic determinants of microvascular fluid balance in normal canine joints. , 1990, Arthritis and rheumatism.

[51]  J. Levick,et al.  Interaction of plasma colloid osmotic pressure and joint fluid pressure across the endothelium-synovium layer: significance of extravascular resistance. , 1988, Microvascular research.

[52]  E. Landis MICRO-INJECTION STUDIES OF CAPILLARY PERMEABILITY , 1927 .

[53]  K. Brigham,et al.  Effect of Increased Vascular Pressure on Lung Fluid Balance in Unanesthetized Sheep , 1975, Circulation research.

[54]  D. Moffatt,et al.  Quantitation of changes in lymph protein concentration during lymph node transit. , 1982, The American journal of physiology.

[55]  C. Wiederhielm,et al.  Interstitial fluid oncotic pressures in rabbit subcutaneous tissue. , 1976, American Journal of Physiology.

[56]  S. Mellander,et al.  Relation between capillary pressure and vascular tone over the range from maximum dilatation to maximum constriction in cat skeletal muscle. , 1990, Acta physiologica Scandinavica.

[57]  A. C. Guyton,et al.  Modification of lymph by lymph nodes. III. Effect of increased lymph hydrostatic pressure. , 1985, The American journal of physiology.

[58]  R. Reed,et al.  Interstitial fluid pressure in rats measured with a modified wick technique. , 1977, Microvascular research.

[59]  P. Fraser,et al.  Microvascular pressures and filtration coefficients in the cat mesentery. , 1978, The Journal of physiology.

[60]  A. Lindsey,et al.  Effect of Elevated Left Atrial Pressure and Decreased Plasma Protein Concentration on the Development of Pulmonary Edema , 1959, Circulation research.

[61]  M. Mulvany,et al.  Structure and function of small arteries. , 1990, Physiological reviews.

[62]  G. Kramer,et al.  Protein concentration of lymph and interstitial fluid in the rat tail. , 1984, The American journal of physiology.

[63]  W. Akeson,et al.  Tissue fluid states in compartment syndromes. , 1977, Bibliotheca anatomica.

[64]  Levick A two‐dimensional morphometry‐based model of interstitial and transcapillary flow in rabbit synovium , 1991, Experimental physiology.

[65]  K. Aukland,et al.  Protein concentration of interstitial fluid collected from rat skin by a wick method. , 1973, Acta physiologica Scandinavica.

[66]  A. C. Guyton,et al.  Some pressure and fluid dynamic characteristics of the canine epidural space. , 1977, The American journal of physiology.

[67]  P. D. Watson,et al.  Influence of venous pressure on plasma-lymph transport in the dog's paw: convective and dissipative mechanisms. , 1977, Microvascular research.

[68]  N. Staub,et al.  Interstitial fluid pressure gradient measured by micropuncture in excised dog lung. , 1984, Journal of applied physiology: respiratory, environmental and exercise physiology.

[69]  R. Reed,et al.  Transcapillary fluid balance in immature rats. interstitial fluid pressure, serum and interstitial protein concentration, and colloid osmotic pressure. , 1977, Microvascular research.

[70]  H. Granger,et al.  Interaction of Capillary, Interstitial, and Lymphatic Forces in the Canine Hindpaw , 1976, Circulation research.

[71]  J L Bert,et al.  A mathematical model of interstitial transport. II. Microvascular exchange in mesentery. , 1990, Microvascular research.

[72]  H. Bohlen,et al.  Microvascular pressures in rat intestinal muscle and mucosal villi. , 1977, The American journal of physiology.

[73]  C. Moyses,et al.  The Measurement of Fluid Filtration in Human Limbs , 1987 .

[74]  S. Williams,et al.  Dynamic measurement of human capillary blood pressure. , 1988, Clinical science.

[75]  G. Schmid-Schönbein,et al.  Microlymphatics and lymph flow. , 1990, Physiological reviews.

[76]  J. Friedman,et al.  The radial protein concentration profile in the interstitial space of the rat ileal mesentery. , 1986, Microvascular research.

[77]  F. A. Meyer,et al.  Macromolecular basis of globular protein exclusion and of swelling pressure in loose connective tissue (umbilical cord). , 1983, Biochimica et biophysica acta.

[78]  S. Mellander Comparative studies on the adrenergic neuro-hormonal control of resistance and capacitance blood vessels in the cat. , 1960, Acta physiologica Scandinavica. Supplementum.

[79]  J L Bert,et al.  A mathematical model of interstitial transport. I. Theory. , 1990, Microvascular research.

[80]  M. Intaglietta Vasomotor activity, time-dependent fluid exchange and tissue pressure. , 1981, Microvascular research.

[81]  J. Levick Flow through interstitium and other fibrous matrices. , 1987, Quarterly journal of experimental physiology.

[82]  R. M. Peters,et al.  Normal transcapillary pressures in human skeletal muscle and subcutaneous tissues. , 1981, Microvascular research.

[83]  P. Hutchins,et al.  Comparison of microvascular pressures in normal and spontaneously hypertensive rats. , 1977, Microvascular research.

[84]  E. Salathe,et al.  A mathematical analysis of fluid movement across capillary walls. , 1975, Microvascular research.

[85]  B. Zweifach,et al.  Transport between blood and peripheral lymph in intestine. , 1976, Microvascular research.

[86]  M. Intaglietta,et al.  Fluid exchange in tunnel and tube capillaries. , 1973, Microvascular research.

[87]  J. Levick Contributions of the lymphatic and microvascular systems to fluid absorption from the synovial cavity of the rabbit knee. , 1980, The Journal of physiology.

[88]  J. Levick,et al.  The effects of position and skin temperature on the capillary pressures in the fingers and toes , 1978, The Journal of physiology.

[89]  T Länne,et al.  Very rapid net transcapillary fluid absorption from skeletal muscle and skin in man during pronounced hypovolaemic circulatory stress. , 1989, Acta physiologica Scandinavica.

[90]  M Intaglietta,et al.  A microscope-television system for studying flow velocity in human skin capillaries. , 1977, The American journal of physiology.

[91]  J. Levick,et al.  An analysis of the permeability of a fenestra. , 1987, Microvascular research.

[92]  G. Nicolaysen,et al.  Interstitial fluid volume: local regulatory mechanisms. , 1981, Physiological reviews.

[93]  B. Haraldsson,et al.  On the steady-state relationship between the microvascular hydrostatic pressure and the transvascular filtration rate. Effects of heteroporosity. , 1987, Acta physiologica Scandinavica.

[94]  E. Starling On the Absorption of Fluids from the Connective Tissue Spaces , 1896, The Journal of physiology.

[95]  R. Reed,et al.  Interstitial compliance and transcapillary Starling pressures in cat skin and skeletal muscle. , 1985, The American journal of physiology.

[96]  H. Wiig,et al.  Hemodynamics and interstitial fluid pressure in the rat tail. , 1984, The American journal of physiology.

[97]  A. Shannon,et al.  The influence of the lymph node on the protein concentration of efferent lymph leaving the node. , 1977, The Journal of physiology.