Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T17:12:57.811Z Has data issue: false hasContentIssue false

Osmotic effects of ions diffusing in capillary plasma can explain Starling's osmotic force in plasma–ISF exchange

Published online by Cambridge University Press:  23 June 2011

William F. Brechue*
Affiliation:
Center for Physical Development Excellence, Department of Physical Education, United States Military Academy, West Point, NY10996, USA
Harold T. Hammel
Affiliation:
Department of Physiology, University of California, San Diego, CA, USA Department of Physiology and Biophysics, Medical Sciences Program, Indiana University School of Medicine, Indianapolis, IN47416, USA
*
*Corresponding author: [email protected]
Get access

Abstract

The exchange of water between plasma and interstitial fluid (ISF) along the length of a capillary is attributed to a balancing of the Starling forces, site-specific differences in hydrostatic and osmotic pressures that theoretically determine directional fluid movement. The osmotic forces for water movement are attributed to the osmotic effects of proteins, colloid osmotic pressure (COP). Several physiological inconsistencies question the role of proteins and COP in fluid flux. A reconsideration of Hulett's insights concerning the osmosis of water provides substantial evidence that the effect of COP does not cause osmosis, and therefore another force is needed to explain plasma–ISF exchange. Review of whole-body tissue and blood ion concentrations and/or ion differences across isolated tissue or secretory epithelia from a variety of species indicates that the diffusion of bicarbonate and strong ions within plasma is the dominant osmotic effect returning ISF to the capillary. Conceptually, as these ions diffuse along physiological gradients, they alter the chemical potential of water through which they are diffusing (solute–solvent drag), creating an osmotic effect on plasma water, and explain plasma–ISF exchange. Considering venous–arterial differences, diffusing and strong ions give rise to a net osmotic force (~35 Torr) in venous end capillary plasma water that is coupled to ISF through pores in the endothelium. More importantly, diffusing and strong ions provide an incremental osmotic force (~150 Torr) that is essentially matched to any change in metabolic rate (e.g. muscular work) when CO2 output and water production are increased. The proposed diffusing ion osmotic force does not negate the necessity for colloidal proteins in volume regulation. Proteins can have an essential effect on fluid exchange in plasma when blood flow is intermittent or changes in protein concentration in the ISF such that proteins exert a force against a distensible boundary (i.e. the endothelium and basement membrane) as they are reflected by it or diffuse through the membrane due to changes in permeability.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Starling, EH (1896). On the absorption of fluids from connective tissue spaces. Journal of Physiology London 19: 312326.CrossRefGoogle ScholarPubMed
2Schmidt-Nielsen, K (1983). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press, pp. 121.Google Scholar
3Hillman, SS, Zygmunt, A and Baustian, M (1987). Transcapillary fluid forces during dehydration in two amphibians. Physiological Zoology 60: 339345.CrossRefGoogle Scholar
4Lunde, PKM and Waaler, BA (1969). Transvascular fluid balance in the lung. Journal of Physiology 20: 118.CrossRefGoogle Scholar
5Sjogaard, G and Saltin, B (1982). Extra- and intracellular water spaced in muscle of man as rest and with dynamic exercise. American Journal of Physiology 243: R271R280.Google Scholar
6Mohsenin, V and Gonzalez, RR (1984). Tissue pressure and plasma oncotic pressure during exercise. Journal of Applied Physiology 56: 102108.CrossRefGoogle ScholarPubMed
7Lindinger, MI, McKeen, G and Ecker, GL (2004). Time course and magnitude of changes in total body water, extracellular fluid volume, intracellular fluid volume and plasma volume during submaximal exercise and recovery in horses. Equine and Comparative Exercise Physiology 1: 13101319.CrossRefGoogle Scholar
8Vengust, M, Staempfli, H, Viel, L and Heigenhauser, G (2006). Transvascular fluid flux from the pulmonary vasculature at rest and during exercise in horses. Journal of Physiology 570: 397405.CrossRefGoogle ScholarPubMed
9Duke-Elder, WS (1934). Physico-chemical factors affecting intra-ocular pressure. Physiological Reviews 14: 483513.CrossRefGoogle Scholar
10Maren, TH (1967). Carbonic anhydrase: chemistry, physiology, and inhibition. Physiological Reviews 47: 591781.CrossRefGoogle ScholarPubMed
11Maren, TH (1974). formation in aqueous humor: mechanism and relation to the treatment of glaucoma. Investigative Ophthalmology and Visual Science 13: 479484.Google Scholar
12Davson, H (1969). The intraocular fluids. In: Davson, (ed.) The Eye Volume 1. New York, NY: Academic Press, pp. 101.Google Scholar
13Hammel, HT and Brechue, WF (2000). Plasma–ISF fluid exchange in tissue is driven by diffusion of carbon dioxide and bicarbonate in presence of carbonic anhydrase. FASEB Journal 14: 3261.Google Scholar
14Brechue, WF and Hammel, HT (2002). Cause of plasma–ISF exchange in fish, birds, and mammals. FASEB Journal 16: A884.Google Scholar
15Hammel, HT and Scholander, PF (1973). Thermal motion and forced migration of colloidal particles generate hydrostatic pressure in solvent. Proceedings of the National Academy of Science 70: 124128.CrossRefGoogle ScholarPubMed
16Hulett, G (1902). Beziehung zwischen negativem Druck und osmotischem. Zeitscrift Physikalische Chemie 42: 353368.Google Scholar
17Hammel, HT (1994). How solutes alter water in aqueous solutions. Journal of Physical Chemistry 98: 41964204.CrossRefGoogle Scholar
18Hammel, HT (1998). Replacing Lewis's theory with Hulett's theory of altered chemical potentials of reacting constituents in solution. Recent Research Developments in Physical Chemistry 2: 77111.Google Scholar
19Hammel, HT (1999). Evolving ideas about osmosis and capillary fluid exchange. FASEB Journal 13: 213231.CrossRefGoogle ScholarPubMed
20Mysels, KJ (1978). Solvent tension or solvent concentration? Journal of Chemistry Education 55: 2122.CrossRefGoogle Scholar
21Mysels, KJ (1997). Vapor pressure lowering, osmotic pressure, and the elementary pseudo-gas model. Journal of Physical Chemistry B 101: 18931896.CrossRefGoogle Scholar
22Miller, FG and Knox, JH (1973). Apparent molal volumes of aqueous NaF, Na2SO4, KCl, K2SO4, MgCl2 and MgSO4 solutions at 0 °C and 50 °C. Journal of Chemical Engineering Data 18: 407411.Google Scholar
23Hammel, HT (2002). Osmotic effects on solvent of solute diffusing in solution. Recent Research Advances in Physical Chemistry 6: 747771.Google Scholar
24Michel, CC (1996). One hundred years of Starling's hypothesis. News in Physiological Science 11: 229237.Google Scholar
25Taylor, AE and Moore, TM (1999). Capillary fluid exchange. Advances in Physiology Education 22: S203S210.CrossRefGoogle Scholar
26Dill, DB, Edwards, HT and Consolazio, WV (1937). Blood as a physicochemical system. XI Man at rest. Journal of Biological Chemistry 118: 635648.CrossRefGoogle Scholar
27Henderson, LJ (1928). Blood: A Study in General Physiology. New Haven, CT: Yale University Press.Google Scholar
28Kowalchuk, JM, Heigenhauser, GJF, Lindinger, MI, Obminski, G, Sutton, JR and Jones, NL (1988). Role of lungs and inactive muscle in acid–base control after maximal exercise. Journal of Applied Phsyiology 65: 20902096.Google ScholarPubMed
29Kowalchuk, JM, Heigenhauser, GJF, Lindinger, MI, Sutton, JR and Jones, NL (1988). Factors influencing hydrogen ion concentration in muscle after intense exercise. Journal of Applied Physiology 65: 20802089.CrossRefGoogle ScholarPubMed
30McKenna, MJ, Heigenhauser, GJF, McKelvie, RS, MacDougall, JD and Jones, NL (1997). Sprint training enhances ionic regulation during intense exercise in men. Journal of Physiology 501: 687702.CrossRefGoogle ScholarPubMed
31Stainsby, WN and Eitzman, PD (1988). Roles of CO2, O2 and acid in arteriovenous [H+] difference during muscle contractions. Journal of Applied Physiology 65: 18031810.CrossRefGoogle ScholarPubMed
32Brechue, WF, Stainsby, WN and O'Drobinak, DM (1990). Ion flux during intense repetitive contractions in isolated skeletal muscle. FASEB Journal 4: A1213.Google Scholar
33Brechue, WF, Gropp, KE, Ameredes, BT, O'Drobinak, DM, Stainsby, WN and Harvey, JW (1994). Metabolic and work capacity of skeletal muscle of PFK-deficient dogs studied in situ. Journal of Applied Physiology 77: 24562467.CrossRefGoogle ScholarPubMed
34Tyrrel, JV (1961). Diffusion and Heat Flow in Liquids. London: Butterworth.Google Scholar
35Guyton, AC (1963). A concept of negative interstitial pressure based on pressure in implanted perforated capsules. Circulation Research 12: 399414.CrossRefGoogle ScholarPubMed
36Curry, FE, Hu, X, Adamson, RH, Liu, B and Weinbaum, S (2000). Starling forces opposing filtration when albumin is present at equal concentration in vessel and tissue. FASEB Journal 14: 31.18.Google Scholar
37Olson, KR (1992). Blood and extracellular fluid volume regulation: role of the renin-angiotensin system, kallikrein-kinin system, and atrial natriuretic peptides. In: Hoar, WS, Randall, DJ and Farrell, AP (eds) Fish Physiology Vol. XII, Part B. The Cardiovascular System. San Diego, CA: Academic Press, pp. 135232.Google Scholar
38Gillen, CM, Lee, R, Mack, GW, Tomaselli, CM, Nishiyasu, T and Nadel, ER (1991). Plasma volume expansion in humans after a single intense exercise protocol. Journal of Applied Physiology 71: 19141920.CrossRefGoogle ScholarPubMed
39Mack, GW, Yang, R, Hargens, AR, Nagashima, K and Haskell, A (1998). Influence of hydrostatic pressure gradients on regulation of plasma volume after exercise. Journal of Applied Physiology 85: 667675.CrossRefGoogle ScholarPubMed
40Maren, TH (1988). The kinetics of synthesis related to fluid secretion, pH control, and CO2 elimination. Annual Review of Physiology 50: 695717.CrossRefGoogle Scholar
41Maren, TH (1991). The links among biochemistry, physiology, and pharmacology in carbonic anhydrase systems. In: Botre, F, Gros, G and Storey, BT (eds) Carbonic Anhydrase. From Biochemistry and Genetics to Physiology and Clinical Medicine. Weinheim: VCH, pp. 186207.Google Scholar
42Brechue, WF (1994). Topical carbonic anhydrase inhibitors: physicochemical properties and aqueous humor dynamics. Roumanian Chemical Quarterly Reviews 2: 301312.Google Scholar
43Tinker, JP, Coulson, R and Weiner, IM (1981). Dextran-bound inhibitors of carbonic anhydrase. Journal of Pharmacology and Experimental Therapeutics 218: 600607.Google ScholarPubMed
44Brechue, WF, Kinne-Saffran, E, Kinne, RKH and Maren, TH (1991). Localization and activity of renal carbonic anhydrase in CA-II deficient mice. Biochimica Biophysica Acta 1066: 201207.CrossRefGoogle ScholarPubMed
45Brechue, WF and Maren, TH (1993). A comparison between the effect of topical and systemic carbonic anhydrase inhibitors on aqueous humor secretion. Experimental Eye Research 57: 6778.CrossRefGoogle ScholarPubMed
46Ridderstralle, Y, Wistrand, PJ and Brechue, WF (1994). Membrane-associated CA activity in the eye of the CA-II deficient mouse. Investigative Ophthalmology and Visual Science 35: 25772583.Google Scholar
47Gros, G, Moll, W, Hoppe, H and Gros, H (1976). Proton transport by phosphate diffusion in a mechanism of facilitated CO2 transfer. Journal of General Physiology 67: 773790.CrossRefGoogle Scholar
48Gutknecth, J, Bisson, MA and Tosteson, DC (1977). Diffusion of carbon dioxide through lipid bilayer membranes. Effects of carbonic anhydrase, bicarbonate, and unstirred layers. Journal of General Physiology 69: 779794.CrossRefGoogle Scholar
49Maren, TH, Haywood, JR, Chapman, SK and Zimmerman, TJ (1977). The pharmacology of methazolamide in relation to treatment of glaucoma. Investigative Ophthalmology 16: 730742.Google ScholarPubMed
50Brechue, WF and Maren, TH (1993). Carbonic anhydrase inhibitory activity and ocular pharmacology of organic sulfamates. Journal of Pharmacology and Experimental Therapeutics 264: 670675.Google ScholarPubMed
51Vogh, BP and Maren, TH (1975). Sodium, chloride, and bicarbonate movement from plasma to cerebrospinal fluid in cats. American Journal of Physiology 228: 673683.CrossRefGoogle ScholarPubMed
52Vogh, BP, Godman, DR and Maren, TH (1987). Effect of AlCl3 and other acids on cerebrospinal fluid production: a correction. Journal of Pharmacology and Experimental Therapeutics 242: 3539.Google Scholar
53Rawls, JA, Wistrand, PJ and Maren, TH (1963). Effects of acid–base changes and carbonic anhydrase inhibition on pancreatic secretion. American Journal of Physiology 205: 651657.CrossRefGoogle ScholarPubMed
54Gregory, DS (1990). Tomolol reduced IOP in normal NZW rabbits during the dark only. Investigative Ophthalmology and Visual Science 31: 715721.Google Scholar
55Brechue, WF, Krumin, DK and Godman, DG (1993). Combination of carbonic anhydrase and β-blockade abolishes circadian rhythm of IOP. Investigative Ophthalmology and Visual Science 34: 931.Google Scholar
56Maren, TH and Vogh, BV (1990). Timolol appears to dissociate flow and Na+ entry to the aqueous humor. Investigative Ophthalmology and Visual Science 31: 182.Google Scholar
57Maren, TH (1984). The general physiology of reactions catalyzed by carbonic anhydrase and their inhibition by sulfonamides. In: Tashian, RE and Hewitt-Emmett, D (eds) Biology and Chemistry of the Carbonic Anhydrases. New York: Annals of the National Academy of Science, pp. 568579.Google Scholar
58Conroy, CW and Maren, TH (1989). The permeability of hydrophobic membranes to 22Na salts and 14CO2 in low dielectric media. Biophysical Chemistry 34: 177184.CrossRefGoogle ScholarPubMed
59Duhm, J and Becker, BF (1978). Studies on Na+-dependent L+ cotransport and bicarbonate-stimulated L+ transport in human erythrocytes. In: Staub, RW and Bolis, L (eds) Cell Membrane Receptors for Drug and Hormones. New York, NY: Raven, pp. 281299.Google Scholar
60Weith, JO (1970). Effects of monovalent anions on sodium permeability of human red cells. Acta Physiologica Scandinavica 79: 7687.CrossRefGoogle Scholar
61Soleimani, M and Aronson, PS (1989). Ionic mechanism of Na+ cotransport in rabbit renal basolateral membrane vesicles. Journal of Biological Chemistry 264: 1830218308.CrossRefGoogle Scholar
62Krapf, R (1988). Basolateral membrane H/OH/HCO3 transport in rat cortical thick ascending limb: evidence for an electrogenic NaHCO3 cotransporter in parallel with a Na/H antiporter. Journal of Clinical Investigation 82: 234241.CrossRefGoogle ScholarPubMed
63Curci, S, Debellis, L and Fromter, E (1987). Evidence for a rheogenic sodium bicarbonate cotransporter in the basolateral membrane of oxyntic cells of frog gatric fundus. Pflugers Archiv European Journal of Physiology 408: 497504.CrossRefGoogle Scholar
64Jentsch, TJ, Keller, SK, Koch, M and Wiederholt, M (1984). Evidence of coupled transport of bicarbonate and sodium cultured bovine corneal endothelial cells. Journal of Membrane Biology 81: 189204.CrossRefGoogle ScholarPubMed
65Boron, WF (1985). Intracellular pH-regulating mechanism of the squid axon. Journal of General Physiology 85: 325345.CrossRefGoogle ScholarPubMed
66Gross, E, Pushkin, A, Abuladze, N, Fedotoff, O and Kurtz, I (2002). Regulation of the sodium bicarbonate transporter kNBC1 function: role of Asp (986), Asp (988), and kNBC1-carbonic anhydrase II binding. Journal of Physiology 544: 679685.CrossRefGoogle Scholar
67Alvarez, BV, Loiselle, FB, Supuran, CT, Schwartz, GJ and Casey, JR (2003). Direct extracellular interaction between carbonic anyhdrase IV and the human NBC1 sodium/bicarbonate co-transporter. Biochemistry 42: 1232112329.CrossRefGoogle Scholar
68Loiselle, FB, Morgan, PE, Alvarez, BV and Cadey, JR (2004). Regulation of the human NBC3 Na+/ cotransporter by carbonic anhydrase II and PKA. American Journal of Physiology Cell Physiology 286: C1423C1433.CrossRefGoogle ScholarPubMed
69Vince, JW and Reithmeier, RAF (1998). Carbonic anhydrase II binds to the carboxyl-terminus of human band 3, the erythrocyte Cl/ exchanger. Journal of Biological Chemistry 273: 2843028437.CrossRefGoogle Scholar
70Sterling, D, Reithmeier, RA and Casey, JR (2001). A transport metabolon. Functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers. Journal of Biological Chemistry 276: 4788647894.CrossRefGoogle ScholarPubMed
71Mount, DB and Romero, MF (2004). The SLC26 gene family of multi-functional anion exchangers. Pflugers Archive 447: 710721.CrossRefGoogle Scholar
72Alvarez, BV, Vilas, GL and Casey, JR (2005). Metabolic disruption: a mechanism that regulates bicarbonate transport. The EMBO Journal 24: 24992511.CrossRefGoogle ScholarPubMed
73Brechue, WF and Stager, JM (1990). Acetazolamide alters temperature regulation during submaximal exercise. Journal of Applied Physiology 69: 14021407.CrossRefGoogle Scholar
74Brechue, WF, Stager, JM and Lukaski, HC (1990). Body water and electrolyte responses to acetazolamide in humans. Journal of Applied Physiology 69: 13971401.CrossRefGoogle ScholarPubMed
75Kowalchuk, JM, Heigenhauser, GJF, Sutton, JR and Jones, NL (1992). Effect of acetazolamide on gas exchange and acid–base control after maximal exercise. Journal of Applied Physiology 72: 278287.CrossRefGoogle ScholarPubMed
76Dell, RB, Lee, CE and Winters, RW (1971). Influence of body composition on the in vivo response to acute hypercapnia. Pediatric Research 5: 523538.CrossRefGoogle Scholar
77Astrand, PO, Rodahl, K, Dahl, HA and Stromme, SB (2003). Textbook of Work Physiology. 4th edn.Champaign, IL: Human Kinetics.Google Scholar
78Taylor, CR, Maloiy, GMO, Weibel, ER, Langman, VA, Kamau, JMZ, Seeherman, HJ et al. (1981). Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic mammals. Respiration Physiology 44: 2537.CrossRefGoogle ScholarPubMed
79Weibel, ER, Taylor, CR, Weber, J-M, Vock, R, Roberts, TJ and Hoppler, H (1992). Variations in function and design: testing symmorphosis in the respiratory system. Respiration Physiology 87: 325348.CrossRefGoogle ScholarPubMed
80Kearns, CF, McKeever, KH, John-Adler, H, Abe, T and Brechue, WF (2002). Relationship between body composition, blood volume, and maximal oxygen uptake. Equine Veterinary Journal Supplement 34: 485490.CrossRefGoogle Scholar
81Dobson, GP, Parkhouse, WS, Weber, JM, Stuttard, E, Harman, J, Snow, DH et al. (1988). Metabolic changes in skeletal muscle and blood in greyhounds during 800 m track sprint. American Journal of Physiology 255: R513R519.Google ScholarPubMed
82Rose, RJ, Hodgson, DR, Kelso, TB, McCutcheon, LJ, Reid, TA, Bayly, WM et al. (1988). Maximum oxygen uptake, O2 debt, and deficit and muscle metabolites in thoroughbred horses. Journal of Applied Physiology 64: 781788.CrossRefGoogle ScholarPubMed
83Brechue, WF, Barclay, JK, O'Drobinak, DM and Stainsby, WN (1991). Differences between VO2 maxima of twitch and tetanic contractions are related to blood flow. Journal of Applied Physiology 71: 131135.CrossRefGoogle ScholarPubMed
84Lundvall, JS, Mellander, S, Westling, H and White, T (1972). Fluid transfer between blood and tissues during exercise. Acta Phsyiologica Scandinavica 85: 258269.CrossRefGoogle ScholarPubMed
85Greenleaf, JE, Van Beaumont, W, Brock, PJ, Morse, JT and Mangseth, GR (1979). Plasma volume and electrolyte shifts with heavy exercise in sitting and supine positions. American Journal of Physiology 236: R206R213.Google ScholarPubMed
86Miles, DS, Sawka, MN, Glaser, RM and Petrofsky, JS (1983). Plasma volume shifts during progressive arm and leg exercise. Journal of Applied Physiology 54: 491495.CrossRefGoogle ScholarPubMed
87McKeever, KH, Hinchcliff, KW, Reed, SM and Robertson, JT (1993). Plasma constituents during incremental treadmill exercise in intact and spenectomized horses. Equine Veterinary Journal 25: 233236.CrossRefGoogle Scholar
88Kjellmer, I (1964). The effect of exercise on the vascular bed of skeletal muscle. Acta Physiologica Scandinavica 82: 1830.CrossRefGoogle Scholar
89Kjellmer, I (1964). An indirect method for estimating tissue pressure with special reference to tissue pressure in muscle during exercise. Acta Physiologica Scandinavica 62: 3140.CrossRefGoogle ScholarPubMed
90Drahota, Z (1961). The ionic composition of various types of striated muscle. Physiologica Bohemoslovia 10: 160165.Google Scholar
91Nose, H, Mack, GW, Shi, X and Nadel, ER (1988). Shift in body fluid compartments after dehydration in humans. Journal of Applied Physiology 65: 318324.CrossRefGoogle ScholarPubMed
92Lindinger, MI, Heigenhauser, GJF, McKelvie, RS and Jones, NL (1990). Role of nonworking muscle on blood metabolites and ions with intense intermittent exercise. American Journal of Physiology 258: R1486R1494.Google ScholarPubMed
93Sreter, FA and Woo, G (1963). Cell water, sodium, and potassium in red and white mammalian muscle. American Journal of Physiology 205: 12901294.CrossRefGoogle Scholar
94Folkow, B, Haglund, U, Jodal, M and Lundgren, O (1971). Blood flow in calf muscle of man during heavy rhythmic exercise. Acta Physiological Scandinavica 81: 157163.CrossRefGoogle ScholarPubMed
95Lundvall, JS (1972). Tissue hyperosmolality as a mediator of vasodilatation and transcapillary fluid flux in exercising skeletal muscle. Acta Phsyiologica Scandinavica 379(Suppl.): 1142.Google ScholarPubMed
96Jacobsson, S and Kjellmer, I (1964). Accumulation of fluid in exercising skeletal muscle. Acta Physiologica Scandinavica 60: 286292.CrossRefGoogle ScholarPubMed
97Senay, LC (1972). Changes in plasma volume and protein content during exposures of walking men to various temperatures before and after acclimatization to heat: separation of the roles of cutaneous and skeletal muscle circulation. Journal of Physiology (London) 224: 6181.CrossRefGoogle Scholar
98Artuson, G and Kjellmer, I (1964). Capillary permeability in skeletal muscle during rest and activity. Acta Physiologica Scandinavica 62: 457463.Google Scholar
99Brechue, WF and Stainsby, WN (1994). Lactate and acid–base exchange during brief intense contractions of skeletal muscle, in situ. Journal of Applied Physiology 77: 223230.CrossRefGoogle ScholarPubMed
100Beekely, MD and Brechue, WF (2002). Inhibition of carbonic anhydrase has no effect on muscle contractile properties nor rate of fatigue in situ. FASEB Journal 16: A776.Google Scholar
101Stainsby, WN and Renkin, EM (1961). Autoregulation of blood flow in resting skeletal muscle. American Journal of Physiology 190: 117121.CrossRefGoogle Scholar
102Johnson, PC (1964). Autoregulation of blood flow. Circulation Research 15(Suppl. 12): 29.Google Scholar
103Jones, RD and Berne, RM (1968). Autoregulation: factors affecting vascular resistance in isolated, perfused skeletal muscle. Circulation in Skeletal Muscle. Oxford: Pergamon Press, pp. 231241.CrossRefGoogle Scholar
104Senay, LC and Pivarnik, JM (1985). Fluid shifts during exercise. Exercise and Sports Science Reviews 13: 335387.CrossRefGoogle ScholarPubMed
105Maren, TH (1968). Renal carbonic anhydrase and the pharmacology of sulfonamide inhibitors. Handbook of Pharmacology: Diuretics. Heidelberg: Springer.Google Scholar
106Wolbach, RA (1955). Renal regulation of acid–base balance in chickens. American Journal of Physiology 181: 149156.CrossRefGoogle Scholar
107Hober, R (1942). Effect of sulfonamides on renal secretion. Proceedings of the Society of Experimental Biology and Medicine 49: 8790.CrossRefGoogle Scholar
108Maren, TH, Wadsworth, BC, Yale, EK and Alonso, LG (1954). Effects of Diamox on electrolyte metabolism. Bulletin of the Johns Hopkins Hospital 95: 277321.Google ScholarPubMed
109Brown, JB and Brechue, WF (1998). Renal response to carbonic anhydrase inhibition is modulated by aldosterone in humans. FASEB Journal 12: A681.Google Scholar
110Garg, LC (1992). Actions of adrenergic and cholinergic drugs on renal tubular cells. Pharmacological Reviews 44: 81102.Google ScholarPubMed
111Diamond, JM and Bossert, WH (1967). Standing-gradient osmotic flow: a mechanism for coupling of water and solute transport in epithelia. Journal of General Physiology 50: 20612083.CrossRefGoogle Scholar