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1 THE SITES AT WHICH PLASMA CLEARING ACTIVITY IS PRODUCED AND DESTROYED IN THE RAT. By G. H. JEFFRIES. From the Sir William Dunn School of Pathology, Oxford. (Received for publication 25th June 1954.) CLEARING activity appears in the plasma of an animal following the injection of heparin [Hahn, 1943]. The addition of heparin to blood in vitro, however, does not produce this activity. The sites at which heparin clearing activity is produced have been studied by Weld [1944], Swank and Levy [1952], and Anfinsen, Boyle and Brown [1952]. Their published results are conflicting. The experiments to be described were carried out to determine more precisely the sites at which plasma clearing activity is produced and destroyed in the rat. Both the plasma clearing activity which follows the injection of heparin, and that which follows the administration of olive oil [Jeffries, 1954], were studied. METHODS. Experiments were performed on Wistar strain albino rats weighing from 150 to 200 g. each. Plasma clearing activity was measured at 370 C. by adding chyle in excess of that which could be cleared by the plasma [French, Robinson and Florey, 1953]. Clearing activity is expressed as the decrease in optical density during a period of incubation. The site of production of the clearing activity induced by the injection of heparin was investigated by perfusing isolated organs and tissues with citrated blood to which heparin (Pularin-Evans containing 1000 i.u. per ml.) had been added immediately before perfusion; the final concentration varied from 2-5 to 0-01 i.u. per ml. of blood. The plasma obtained by centrifuging the perfused blood was tested for clearing activity. In some experiments perfusions were carried out with blood obtained by aortic cannulation of the same animal. In those experiments in which a study was made of the relation between the clearing activity induced and the heparin concentration in the perfused blood, isolated hind limbs from animals of the same weight were perfused with blood pooled from several animals. Perfusions were performed through a cannula in the afferent vessel of the isolated organ or tissue, and the effluent was collected either through a venous cannula or, in the case of the liver, from the open hepatic veins. All perfusions were commenced within 5 to 7 minutes VOL. XXXIX, NO

2 262 Jeffries of the cessation of the normal blood flow through the isolated tissue. The rate of perfusion for a particular organ or tissue was set at an arbitary constant. This rate for different tissues was not proportional to the normal blood flow through those tissues. Consequently, although the clearing activity of samples of plasma recovered from heparincontaining blood perfusates is expressed quantitatively in the text, the values given do not indicate the contribution which the particular tissue or organ may make to the plasma clearing activity of the intact animal. In each perfusion 5 to 10 ml. of blood was passed once through the isolated vascular bed. The temperature of the perfused blood and of the isolated preparation was maintained at 370 C. The perfusate was immediately cooled to 40 C. and the plasma was separated by centrifugation at this temperature. The hind limb of the anesthetized rat was completely isolated by division of the tissues of the upper thigh. The femoral vessels were ligated and cannulated with polythene tubing. The severed collateral vessels were clamped distally to prevent loss of perfused blood from the cut surface of the limb. Each isolated limb was perfused at a constant rate of 1 ml. of blood per minute. An area of skin and subcutaneous tissue, extending from the anterior aspect of the thigh to the upper abdomen, and receiving its blood supply from the femoral vessels, was partly isolated and perfused. The skin flap was dissected down from the abdominal wall after the communicating vessels at its cut edge had been ligated. The femoral vessels were then exposed, and the limb with the attached skin flap was isolated as previously described. The femoral vessels were cannulated as for the perfusion of the isolated limb, but the vascular area perfused was restricted to the skin flap. This was done by tying off all other proximal branches of the femoral vessels, and by tying off the femoral vessels themselves immediately distal to the origin of the large subcutaneous branches supplying the area of skin. Perfusion was performed at a rate of 0 5 ml. of blood per minute. The intact liver was isolated by division of its peritoneal attachments, after the portal vein had been cannulated. The perfusion was performed at a hydrostatic pressure of 5 to 10 cm. of blood and a rate of flow of approximately 1 ml. per minute. A restricted perfusion of the abdominal viscera drained by the portal vein was carried out. Blood was perfused into the cannulated thoracic aorta after the hepatic and renal arteries, the arteries to the dorsal abdominal wall and the lower abdominal aorta had been tied off. The perfused blood was collected from the cannulated portal vein. To determine the sites at which the plasma clearing activity which follows fat absorption is produced, 1 ml. of olive oil was administered to the rats by stomach tube under ether anesthesia, and the experiments were carried out on these animals 4 to 5 hours later. The isolated hind

3 Plasma Clearing Activity in the Rat limb of the fat-fed rat was perfused with citrated blood from a starved rat and the clearing activity of the plasma obtained from the perfusate was determined. As the circulating blood plasma of rats absorbing fat has clearing activity [Jeffries, 1954], it is necessary to ensure that the blood perfused through the isolated tissue is not contaminated with blood already present in the tissue at the commencement of perfusion. For this reason experiments with fat-fed rats were confined to the isolated hind limb preparation which could be perfused without difficulty. A total volume of 10 ml. of blood was passed, the initial i ml. of effluent being discarded. The sites at which plasma clearing activity is destroyed were determined by comparing the plasma clearing activity of blood from the aorta, the portal vein, the hepatic vein and the inferior vena cava. In animals which had received an injection of heparin (5 to 10 units per kg. body weight) or which had been fed fat, specimens of blood were obtained simultaneously from the aorta and from one of the veins mentioned above. Blood was obtained from the aorta, the portal vein and the lower inferior vena cava by direct cannulation of these vessels. Blood from the hepatic vein was collected indirectly by passing a cannula into the inferior vena cava up to the level of the hepatic veins, and tying off the vena cava above the liver and around the cannula between the hepatic and the renal veins. RESULTS. The Sites of Production of Heparin Clearing Activity in the Rat. (a) The Isolated Hind Limb.-When the isolated hind limb of the rat was perfused with blood containing added heparin in concentrations of from 2-5 to i.u. per ml., clearing activity appeared in the plasma of the perfusate. Clearing activity was not produced when blood containing no heparin was perfused. The relation between the plasma clearing activity of the perfusate and the heparin concentration of the perfused blood is shown in fig. 1. The 6 animals used in this experiment were of the same age and weight, and the hind limbs were perfused under the standard conditions described. At a heparin concentration of i.u. clearing activity was very slight. Activity increased to a maximum in the plasma of perfusates containing 01 i.u. of heparin per ml. of blood. (b) Skin and Subcutaneous Tissue.-Blood containing 1 i.u. of heparin per ml. was perfused through a restricted area of the skin and subcutaneous tissue of the ventral abdominal wall and thigh as described. The plasma of this perfused blood cleared added chyle. Fig. 2 shows the clearing activity obtained in a typical experiment. This clearing activity approached that which was produced when blood of a similar 263

4 264 Jeffries cj w a Time (minutes) FIG. 1.-The plasma clearing activity produced by perfusion of blood containing added heparin through the isolated hind limb. Heparin concentrations in the perfused blood were 1 i.u. per ml. (0), 0 1 i.u. per ml. (0), 0-05 i.u. per ml. (U), i.u. per ml. (El), i.u. per ml. (-), and 0 i.u. per ml. (X) o61 05 [ F _ I I I bo Time (minutes). FIG. 2.-The plasma clearing activit3 ''roduced by perfusion of blood containing 1 i.u. per ml. of added hepatii through an area of skin and subcutaneous tissue.

5 Plasma Clearing Activity in the Rat 265 heparin concentration was perfused through the whole isolated limb (see fig. 1). (c) The Abdominal Viscera drained by the Portal Vein.-Blood containing 1 i.u. of heparin per ml. was perfused through the partly isolated intestine and collected from the portal vein; the plasma of the perfusate showed clearing activity. Added chyle was cleared at a rate of 0 9 units of optical density per hour. (d) The Lung.-After the aorta had been cannulated and bleeding begun, 0 5 ml. of a 10 i.u. per ml. solution of heparin in 0-85 per cent sodium chloride was injected slowly into the inferior vena cava. The branches of the aortic arch to the upper extremities had been ligated prior to bleeding, so that the injected heparin could pass only through the heart chambers and the pulmonary circulation. Plasma from the aortic blood collected after the heparin injection cleared added chyle at a rate of 0 95 units of optical density per hour. (e) The Liver.-Clearing activity was not produced in the plasma when blood containing 1 i.u. of heparin per ml. was perfused through the isolated liver. This observation was confirmed in the intact animal. A solution of heparin (10 i.u. per ml.) in 0-85 per cent sodium chloride was injected into the portal vein of an anesthetized rat at a rate of 0.1 ml. per 20 seconds; the blood from the hepatic vein was collected and its plasma tested for clearing activity. No activity appeared in this plasma. The Site of Production of Plasma Clearing Activity during Fat Absorption. When the isolated hind limb of a rat absorbing fat was perfused with *citrated blood from a starved rat, the plasma of the perfusate showed clearing activity. Perfusions of the isolated hind limb of starved rats did not yield any clearing activity. In fig. 3 the clearing activity of 'the plasma from the perfused blood is compared with that of aortic 'blood from the perfused animal. The Destruction of Plasma Clearing Activity in vivo. Fig. 4 (a) shows the clearing activity of plasma samples obtained 10 and 20 minutes after the intravenous injection of 10 i.u. of heparin per kg. body weight. Fig. 4 (b) shows the clearing activity of plasma obtained from fat-fed animals 5 and 15 minutes after ligation of the thoracic duct. Each curve represents average figures from 4 animals. Both in animals which had received an injection of heparin and in those which had been fed fat, a fall in the clearing activity of the plasma occurred in 10 minutes.

6 266 Jeffries A ?2 0*t Time (minutes) FIG. 3.-The production of clearing activity by perfusion of citrated blood through the isolated hind limb of a fat-fed animal. Clearing activity of plasma of perfused blood (0); clearing activity of aortic blood of the perfused animal (0); clearing activity of plasma of unperfused blood from a starved animal (X). 31, -a 0 so (a) Time (minutes). (b) FIG. 4.-The rate of inactivation of plasma clearing activity in vivo. (a) Plasma clearing activity 10 minutes (0) and 20 minutes (0) after injection of 10 i.u. of heparin per kg. body weight. (b) Plasma clearing activity 5 minutes (0) and 15 minutes (0) after ligation of the thoracic duct of fat-fed animals. Each curve represents average figures from 4 animals.

7 Plasma Clearing Activity in the Rat 267 The Site of Destruction of Clearing Activity in vivo. The clearing activity of blood from the inferior vena cava, the portal vein and. the hepatic vein was compared with that of aortic blood in rats which had either been given an intravenous injection of 10 i.u. of heparin per kg. body weight 20 minutes before bleeding, or had been fed olive oil 4 to 5 hours previously. In each case the ph of the arterial and venous plasma was measured in order to take into account any differences in clearing activity which might have been caused by differences in ph. Blood from the inferior vena cava, uncontaminated by blood from the hepatic vein, and blood from the portal vein had a plasma clearing activity similar to that of aortic blood from the same animal. The plasma of blood from the hepatic vein, however, showed less clearing activity than aortic blood. This difference between aortic blood and blood from the hepatic vein occurred not only after the injection of heparin but also during fat absorption. Fig. 5 (a) and (b) shows the o ~~ I l I (a) Time (minutes). (b) FIG. 5.-The plasma clearing activity of blood from the aorta (0), and the hepatic vein (0) (a) of an animal injected with 10 i.u. per kg. body weight and bled after 20 minutes, and (b) of an animal fed 1 ml. oil 4j hours before bleeding. clearing activity of aortic blood and blood from the hepatic vein in two animals: (a) which had received an injection of 10 i.u. of heparin per kg. body weight 20 minutes before bleeding, and (b) which had been fed 1 ml. of olive oil 41 hours before bleeding. In the animal which had received the injection of heparin, the clearing activity of the blood from the hepatic vein was lower than that of aortic blood. There was no

8 268 Jeffries clearing activity in the blood from the hepatic vein of the fat-fed animal. The Destruction of Clearing Activity by the Isolated Perfused Liver of the Rat. When blood, obtained by aortic cannulation 10 minutes after the intravenous injection of 5 i.u. of heparin per kg. body weight, was perfused through the isolated liver of the same animal, there was a decrease in the clearing activity of the perfused blood. This fall in activity was comparable to that which occurred during the passage of active blood through the liver of the intact animal. DISCUSSION. It has been shown that clearing activity is produced rapidly when blood containing low concentrations of heparin passes through the blood vessels of the lung, the abdominal viscera excluding the liver, the hind limb, and the skin and subcutaneous tissue of the rat. Under similar conditions the liver did not produce clearing activity. In these experiments clearing activity was measured in vitro by incubating plasma with added chyle [French, Robinson and Florey, 1953]. Weld [1944] and Swank and Levy [1952] studied the clearing which occurred when lipawmic blood containing heparin passed through restricted areas of the circulation. They measured clearing as the decrease in the number of chylomicrons of the plasma which occurred during the passage of the blood through the tissue. This in vivo clearing corresponds to the clearing activity measured in vitro only if the chylomicrons of the circulating blood are removed by a lipolytic process in the plasma [Robinson and French, 1953]. Anfinsen et al. [1952] perfused plasma containing added heparin through isolated organs and tissues, and measured clearing activity in vitro by incubating the perfused plasma with lipaemic dog plasma. The demonstration of clearing activity production by the isolated hind limb confirms observations made by Weld [1944] and Swank and Levy [1952]. Anfinsen et al. [1952], who were unable to confirm Weld's results, suggested that when clearing occurred during perfusion of the hind limb this resulted from incomplete isolation of the limb from the general circulation, with leakage of blood through collateral vessels. This criticism, however, cannot be applied to the experiments which have been described. The failure to demonstrate production of clearing activity by the liver of the rat conflicts with results published by Weld [1944]. It is possible that during the passage of lipawmic blood through the liver, particulate fat may be removed by the liver or Kupffer cells. Alter-

9 Plasma Clearing Activity in the Rat 269 natively, the difference in results may be due to a species difference. Weld did not state which experimental animal he used in these perfusion experiments. The development of clearing activity when citrated blood from a starved rat is perfused through the isolated hind limb of a fat-fed animal indicates that this tissue contributes, at least in part, to the clearing activity which appears in the plasma of such animals in vivo. The clearing activity in the perfused blood was not due to contamination with active blood already present in the limb at the commencement of perfusion. The difference between the clearing activity of the plasma of aortic blood and that of blood from the hepatic vein, both in animals which have received an injection of heparin and in fat-fed animals, and the fall in clearing activity which occurs when heparinized blood is perfused through the isolated liver, indicate that the liver rapidly destroys clearing activity in vivo. This finding might explain the rapid fall in clearing activity which follows ligation of the thoracic duct in fat-fed animals, or the injection of small doses of heparin. SUMMARY. 1. Clearing activity has been produced by perfusing blood containing heparin in concentrations of from 2-5 to 0025 i.u. per ml. through the isolated hind limbs of rats. It is produced also by the lung, the abdominal viscera with the exception of the liver, and the skin and subcutaneous tissue. The experiments indicate that the liver does not produce clearing activity. 2. The appearance of clearing activity in blood perfused through the isolated hind limbs of rats fed olive oil 4 to 5 hours previously, indicates that clearing activity in such animals is produced in part by the hind limb circulation. 3. Both in rats which have received an injection of heparin and in fat-fed rats, clearing activity of the blood from the hepatic vein was less than that of the aortic blood. Blood from the portal vein, the inferior vena cava, and the aorta had similar clearing activity. 4. Perfusion of heparinized blood through the isolated liver resulted in a fall in its clearing activity. This loss indicates that this organ destroys clearing activity. ACKNOWLEDGMENTS. The author wishes to thank Professor H. W. Florey for his helpful advice, and Mr. H. W. Wheal and Mr. C. S. Crane for technical assistance.

10 270 Plasma Clearing Activity in the Rat REFERENCES. ANFINSEN, C. B., BOYLE, E., and BROWN, R. K. (1952). Science, 115, 583. FRENCH, J. E., IROBINSON, D. S., and FLOREY, H. W. (1953). Quart. J. exp. Physiol. 38, 101. HAHN, P. F. (1943). Science, 98, 19. JEFFRIES, G. H. (1954). Quart. J. exp. Physiol. 39, 77. ROBINSON, D. S., and FRENCH, J. E. (1953). Quart. J. exp. Physiol. 38, 233. SWANK, R. L., and LEVY, S. (1952). Amer. J. Physiol. 171, 209. WELD, C. B. (1944). Canad. med. Ass. J. 51, 578.

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