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They Are Designated Colligative. These Properties Include Osmotic Pressure, De- Pression of the Freezing Point, Vapor Tension, and Boiling Point of Solutions

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They Are Designated Colligative. These Properties Include Osmotic Pressure, De- Pression of the Freezing Point, Vapor Tension, and Boiling Point of Solutions THE NORMAL AND PATHOLOGICAL MOVEMENT OF WATER IN TISSUES AND ITS RELATION TO THE COLLIGA TIVE PROPERTIES OF SOLUTIONS AND TO INFLAMMATION BY EUGENE L. OPIE THE ROCKEFELLER UNIVERSITY Communicated May 26, 1966 A series of studies, each suggested by those that preceded, were first concerned with the movement of water in parenchymatous cells of liver, kidney, submaxillary glands, and other glandular organs. Evidence was soon obtained showing that these cells were isotonic as determined by the osmotic pressure they maintained, not with physiological salt solution (0.15 M), as at that time popularly assumed, but with sodium chloride in approximately twice this concentration. Cells of the liver or of the kidney acted as osmometers and measured the osmotic pressure which they maintained. When various electrolytes were tested, it was found that their osmotic pressures varied with the valence of the basic ions of the salts that were used, being, for example; 1 for monovalent sodium salts, 2 for calcium salt, 3 for lanthanum salts. Solutions of the salts of electrolytes manifest properties so bound together that they are designated colligative. These properties include osmotic pressure, de- pression of the freezing point, vapor tension, and boiling point of solutions. It is well established that any one of them provides data from which the others can be deduced by appropriate calculation.' The changes which occurred in liver or in kidney were found to be in accord with tables which record changes in the freezing point of graded solutions of salts of electrolytes, on the one hand, or of boiling points on the other. Visible necrosis of the skin of laboratory animals was produced by injection into the dermis, and the molar strength of solutions of various electrolytes needed to cause it was determined. This varied with the valence of the basic ions of the salts that were tested and followed a sequence which was the same as that of the iso- tonicity of liver or of kidney cortex immersed in corresponding solutions. The molar concentration of amino acids that produced necrosis followed the same order as osmotic pressure of liver in the same solutions. The relation of necrosis to the colligative properties of electrolytes suggested a study of the relation of inflammatory reactions to the molecular constitution of agents that cause them. Injection of injurious substances into the large serous cavities of the body, peritoneal and pleural, offered a method by which exudation of fluid, leucocytes, and plasma protein could be measured with considerable accuracy. The numerical results thus obtained give an adequate measure of the inflammatory reactions. The relations cited emphasize the dependence of normal and pathological changes upon the colligative properties of electrolytes and of organic compounds which direct the movement of water and of the compounds it may contain. With these relations in mind, it has seemed desirable to review the sequence of studies which were undertaken to measure the movement of water in cells and interstitial tissue under normal and under pathological conditions. 426 Downloaded by guest on September 29, 2021 VOL. 56, 1966 PATHOLOGY: E. L. OPIE 427 Osmotic Pressure of Parenchymatous Cells.-The attempt was made to determine gain or loss of fluid in tissues by changes in the specific gravity of particles of liver or of kidney tissue when immersed in various solutions immediately after their re- moval from the body.2 Reversible changes in liver and in kidney cells and in their mitochondria became evident, but the actual weight of tissue before and after im- mersion in various solutions was found to give more interpretable information.3 Immediately after removal from the living animal, slices of liver varying slightly, but approximately 0.5 mm in thickness, measuring 0.5 by 1.5 cm and weighing from 50 to 100 mg, were cut by a razor blade and rapidly weighed on a torsion balance before immersion and later at varied intervals. A similar procedure was applicable to tissue of the cortex of the kidney. When the slices were immersed in solutions of different substances, they took in or lost fluid in accord with the osmotic pressure which they maintained. Experiments showed that slices of tissue of secreting organs, such as liver, kidney, pancreas, and submaxillary glands, when immersed in solutions of sodium chloride of graded concentration were isotonic with solutions having approximately twice the molar concentration of the sodium chloride of the blood plasma, that is, 0.15 M. Evidence that this osmotic pressure of the tissue of glandular organs is maintained by their parenchymatous cells is of primary importance with relation both to the cells themselves and to the interstitial tissue which is their environment. Evidence assembled by Hastings4 and others showed that the extracellular fluid of the tissues had the electrolyte pattern of an ultrafiltrate of the blood plasma. Microchemical analysis brought confirmation when MaurerI withdrew fluid from the interstitial tissue by means of a micropipette. With this relation in view, it became evident that the osmotic pressure within liver cells was at a level slightly greater than twice that of the fluid about them. A large part of these experiments was made with tissue of the white rat. Similar determinations of the isotonicity of liver and of kidney cortex were made with tissues of animals of other mammalian species,6 and the concentrations of solutions of sodium chloride isotonic with them were as follows: White rat Mouse Guinea pig Rabbit Liver 3.4 M 3.4 M 3.8 M 3.2 M Kidney 2.1M 2.2M 2.7M When tissues of liver, kidney, pancreas, or salivary glands removed from the body were immersed in a solution of sodium chloride 0.3 M, water movement very quickly reached an equilibrium which was maintained during a period of approxi- mately 15 minutes following its immersion. Later, the level of isotonicity increased because the unfavorable environment caused by loss of sodium chloride had in- creased the permeability of the cells.7 Ringer's solution" was found to be a medium better adapted to the maintenance of the osmotic pressure of the parenchymatous cells of the liver. This solution, as later somewhat modified by Krebs,9 contained sodium, potassium, calcium, and magnesium chlorides and was buffered by sodium bicarbonate. Ringer had ad- justed the concentration of these components so that when used for perfusion, it maintained approximately normal the beat of the excised heart of an experimental animal. As a solution of a sodium chloride with twice the concentration of physi- Downloaded by guest on September 29, 2021 428 PATHOLOGY: E. L. OPIE PROC. N. A. S. ological salt solution (0.15 M) had been found to have approximately the same osmotic pressure as liver cells immersed in it, the osmotic pressure of the Ringer solution for the present purpose was doubled by the addition of sodium chloride. To reproduce conditions present during life, the medium was kept at 380C and a mixture of oxygen 95 per cent and carbon dioxide 5 per cent was passed through it during the period of immersion. With this closer approach to physiological condi- tions, the time during which the liver cells remained isotonic with the medium was increased from 15 minutes as with the sodium chloride solution (0.3 M) to ap- proximately 2 hours. Experiments showed that the osmotic pressure maintained by liver and other glandular cells above that of the fluid about them was dependent upon their func- tional activity.10 An injurious substance such as chloroform caused necrosis of cells of the liver and reduced the osmotic pressure they maintained to 0.15 M, ap- proximately that of the blood, but when the animal recovered, the higher osmotic pressure was regained. When the kidney cortex was similarly injured, as by potas- sium chromate, similar changes occurred. Tumors produced from liver cells by the compound dimethylamineazobenzene, or butter yellow, like most tumors, lost the functional activity of the cells from which they were derived. Those produced by this carcinogenic agent when immersed in graded sodium chloride solutions showed osmotic pressure reduced to that of the blood." It is noteworthy that liver tissue in the fetal period just before birth exhibited osmotic pressure approximately the same as that of the maternal blood serum.'2 It rose abruptly during the 24 hours after birth and then quite gradually during the next ten weeks increased to its normal level (approximately 0.3 M). Other examples of the relation of osmotic pressure of parenchymatous cells to their functional activ- ity might be cited. Hydration of Collagen Fibers and of Gelatin.-The ability of dense fibrous tissue to take up and hold water occurs under conditions (hydration) which differ from those associated with osmosis. The dense fibrous tissue of the corium of the skin, the tendons of muscles, and the wall of the aorta took up water when immersed in weak or in strong solutions of sodium chloride up to at least 0.75 M.'3 These tissues became swollen because their fibers took and held water. In striated muscle under the same conditions, water was held both by hydration of its fibrous frame- work and by osmotic interchange between the muscle cells and the fluid surrounding them. Striated muscle and heart muscle shortly after birth contained scant fibers and had approximately the same isotonicity as liver tissue. Densely fibrous tissue from the corium of the skin is much used commercially for the preparation of gelatin which is extractable by both acids and alkalis. Experi- mentsl4 showed that the quantity of water taken in by corium of the white rat was approximately the same as that of 20 per cent solidified gelatin prepared from the corium of the same animal.
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