hypotonic due to the addition of water to the rumen. We could not determine
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1 Quarterly Journal of Experimental Physiology (1977) 62, INFLUENCE OF RUMINAL AND PLASMA OSMOTIC PRESSURE ON SALIVARY SECRETION IN SHEEP. By A. C. I. WARNER and B. D. STACY. From C.S.I.R.O., Ian Clunies Ross Animal Research Laboratory, Prospect, P.O. Box 239, Blacktown, N.S.W. 2148, Australia. (Receivedfor publication 7th June 1976) The osmotic pressure of the rumen contents and also of the blood was altered by intraruminal administration of water or hypertonic solutions. It was found that alterations in osmotic pressure were accompanied by inverse changes in the flow rate of mixed saliva. Intravenous infusion of hypertonic solutions, causing elevation of the osmotic pressure of the blood without affecting that of the rumen, also caused a reduction of salivary secretion rate. The flow rates of both parotid and residual saliva were affected. When strongly hypertonic solutions of sodium or potassium salts were infused into the rumen, or sodium salts or urea were infused into the blood, the concentration of those substances increased in the saliva. Other treatments had little effect on salivary composition. In the course of measuring water and electrolyte absorption rates across the rumen wall of sheep, we diverted the saliva through an oesophageal fistula [Warner and Stacy, 1972]. We noticed that salivary flow was affected by the osmotic status of the animal. When solutes were infused into the rumen to raise the osmotic pressure of both rumen contents and blood salivation became slower compared with the rates when the rumen contents and blood were hypotonic due to the addition of water to the rumen. We could not determine from that work whether the stimulus affecting salivary secretion arose from the rumen or elsewhere; consequently in the work described here we also infused solutes intravenously to raise the blood osmotic pressure without affecting the rumen. We also used sheep with parotid fistulae in a few experiments to help determine which salivary glands were affected. METHODS Initial observations on salivary flow in sheep with oesophageal fistulae were made during the course of the absorption experiments previously described [Warner and Stacy, 1972]. Full experimental details can be found in that paper. Briefly, six Merino ewes were fitted with ruminal and oesophageal cannulae. Saliva was diverted through the oesophageal fistula and to prevent rumination or passage of saliva past the fistula a balloon was inserted into the oesophagus. The saliva was replaced by a synthetic solution of similar composition [Warner and Stacy, 1972] infused into the rumen at a rate of l.h 1, about the normal salivation rate in these sheep. The osmotic pressure in the rumen was varied over a wide range, lowering it by adding water, raising it by adding KCI, the potassium salts of volatile fatty acids, NaCl, a mixture of NaCl and KCl or of mannitol and urea, or glycerol in about 02 1 water, or leaving it unchanged. When solutes were added to the rumen they were also added to the synthetic saliva infusate at a concentration expected to maintain the rumen osmotic pressure constant. Eight samples of the rumen contents were taken at regular intervals between 1P0 and 5 5 h after water or solute loading; from the analyses of the samples for sodium, potassium and osmolality [Warner and Stacy, 1965] the average composition of the 133
2 134 Warner and Stacy rumen during the experimental period could be calculated. Mixed saliva was also collected hourly from the oesophageal fistula over this period and the average flow rate and composition were calculated. Salivary flow tended to be high for min following removal of the oesophageal cannula and insertion of the balloon. That procedure was therefore always carried out before the commencement of any treatment, i.e., at least 1 h before taking any samples for measurement; this time interval also allowed the attainment of a maximal response of salivary flow to the rumen infusion. An estimate of plasma osmotic pressure was obtained from a blood sample taken towards the end of the 5.5 h period. In a second series of experiments six Merino ewes, some the same as those mentioned above, were used. Salivary flow rates from the oesophageal fistula were measured after blood osmotic pressure was varied by intravenous administration of various substances. The solutions, all infused at 5 ml.min-1, included 75, 150 and 600 mmol.1-sodium chloride, 25 % sucrose in 75 mmol.1 -' sodium chloride and 2, 3 and 4 % urea in 5 % glucose. Finally, three sheep with unilateral Wright parotid fistulae [Denton, 1957] were infused with 1*8 mol.1 -' NaCl at 1*88 ml.mini for 60 min. Parotid saliva was collected at 5 min intervals from two of the sheep by continuous aspiration from a small plastic cup cemented to the skin around the skin tube; most of the skin tube of the third sheep had been accidentally torn off and saliva was collected by cannulation of the duct on the day of the experiment; results for this animal were not noticeably different from the others. The remaining saliva, i.e., all saliva except that secreted by the fistulated parotid, was collected from the oesophagus with the apparatus of Engelhardt and Sallmann [1972], and is here called 'oesophageal saliva'. Residual, i.e., non-parotid, salivary flow was calculated by subtracting the flow from the fistulated parotid from the oesophageal salivary flow rate, assuming equal flow from the two parotid ducts [Denton, 1957]. Blood samples were taken and infusions given by separate catheters implanted in the two jugular veins. Osmolalities and electrolyte concentrations were measured as described by Warner and Stacy [1965], plasma urea by the method of Wilson [1966] and plasma protein as described by Stacy and Warner [1968]. RESULTS Salivary Flow Rates In the initial experiments with intraruminal infusions, a clear relation existed between the average salivary flow rate and the average rumen osmotic pressure (Fig. 1). The changes in the composition of the rumen fluid were reflected in changes in the composition of the blood (Table I), due to the movement of both water and solutes across the rumen wall [see Warner and Stacy, 1972]. Consequently it was not surprising that salivary flow rate and plasma osmotic pressure were also related (Fig. 2). In order to alter the blood osmotic pressure without affecting the rumen various solutes were injected intravenously. Typical results are shown in Fig. 3. It can be seen that whatever the solute, a raised plasma osmolality was accompanied by a fall in salivary flow rate (Fig. 4). In the discussion that follows, reference is made to all the experiments carried out, not just those described in Fig. 3. When isotonic saline was infused (two experiments, two sheep, one in Fig. 3 (a)), there were negligible changes in plasma osmolality or sodium or potassium concentrations; salivary flow rate showed only normal fluctuations. When infusions of hypotonic and hypertonic saline were made in that order
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4 136 Warner and Stacy FIG. 1. Relation between salivary flow rate and rumen osmolality following the injection of water or solutes into the rumen. Different symbols represent different sheep. FIG. 2. The relation between salivary flow rate and plasma osmolality following the injection of water or solutes into the rumen. Different symbols represent different sheep.
5 Salivary secretion in sheep 137 (four experiments, two sheep, one in Fig. 3 (b)), there was little change in plasma osmolality despite a small (2 mmol.l-') drop in sodium concentration during the period of the hypotonic infusion. During the hypertonic infusion there was a rise in plasma osmolality averaging about 17 m-osmole.kg-', with a rise in FIG. 3. The effect of intravenous infusions of solutes on salivary flow rates and composition; all experiments were done on the one sheep. The horizontal bar represents the duration of the infusion; where a concentration is given it refers to NaCl; the arrow represents a priming dose. In Al-El, the histograms represent salivary flow, the solid line the plasma and the broken line the rumen osmolality. In A2-E2, the solid line represents the osmolality, the broken line the concentration of sodium and the dotted line the concentration of potassium in the saliva. sodium concentration of about 10 and a fall in potassium concentration of about 02 mmol.l-l. In the final period with no infusion into the blood, plasma composition started very slowly to return to normal. Salivary flow rate increased by an average of 37%Y. during the hypotonic infusion and decreased to 4000 of the resting rate during the hypertonic infusion, returning to about 70% of the resting rate in the final period.
6 138 Warner and Stacy When the order of the saline infusions was reversed (four experiments, two sheep, one in Fig. 3 (c)), the effects were similar, in reverse order, except that the persistent effects of the hypertonic infusion tended to counteract the effects of the hypotonic infusion, so that in only two experiments was the salivary flow rate higher during the hypotonic infusion than in the initial period. When sucrose was infused to give plasma osmolalities similar to those following infusion of hypertonic saline (three experiments, two sheep, one in Fig. 3 (d)), FIG. 4. The relation between salivary flow rate and the plasma osmolality during the last hour of each period (pre-infusion, first and second infusion and post-infusion) for all experiments similar to those in Fig. 3; different symbols represent different sheep. there was a decrease averaging 5% in plasma sodium concentration and 23 % in potassium concentration; in the only experiment in which it was measured, plasma protein decreased 16%. Salivary flow rate decreased to about 30% of its initial value, returning slowly to about that value by the end of the experiment. When urea was infused (six experiments, five sheep, one in Fig. 3 (e)), plasma osmolality rose during the infusion, returning to its initial value somewhat slowly. Plasma sodium fell by 5 %, potassium by 14% and protein by 8 % on average, and they were still below normal at the end of the experiment. Plasma urea rose erratically; in the four experiments in which 4% urea was infused
7 Salivary secretion in sheep 139 there were occasional values of plasma urea over 100 mg N/100 ml (about 35 mmol.lp'), and an average of about 80 mg N/100 ml. The plasma urea fell only very slowly following cessation of the infusion, and it was often over 40 mg N/100 ml at the end of the experiment. Salivary flow rate was reduced, on average, to 71 % of its initial value. In one of the six experiments no reduction at all was noted (mean flow rates before, during and after the infusion 323, 335 and 376 ml.h-' respectively), despite a high plasma osmolality (averaging 335 m-osmole.kg-' throughout the infusion period) and plasma urea concentration (averaging 107 mg N/100 ml); when the experiment was repeated with the same sheep, salivary flow was reduced to 50% of its initial value (mean flow rates before, during and after the infusion 215, 109 and 180 ml.h 1 respectively), average plasma osmolality being 327 m-osmole.kg 1 and urea concentration 85 mg N/100 ml in the infusion period. In the final experiments, in sheep with unilateral parotid fistulae, the ratio of the flow of single parotid to oesophageal saliva varied between sheep from 0 09 to 0 35 in the control period. This indicated that parotid saliva may have formed % of total saliva. Nevertheless, in all sheep, the intravenous infusion of hypertonic saline raised the plasma osmolality by m-osmole.kg -' and caused the flow of the fistulated parotid to be roughly halved; in two sheep the flow of oesophageal saliva fell in about the same proportion but in the third there was a much smaller fall. Average values may be seen in Table II. Recovery after stopping the infusion was slow, so that after two hours neither the plasma osmolality nor the salivary flow rates had fully returned to pre-infusion values. TABLE II. Parotid and residualt salivary flow rates and plasma osmolalities following intravenous hypertonic infusions; average of three sheep. Period Control* Infusion* Post-infusion* Plasma osmolality, m-osmole.kg Single parotid salivary flow rate, ml.min Oesophagealt salivary flow rate, ml.min1l Residualt salivary flow rate, ml.min *Periods were: Control, 30-0 min before start of infusion of 1-8 mol.h1 NaCl at 1-88 ml.minfor 60 min; Infusion, min after start of infusion; Post-infusion, min after end of infusion. Blood samples were collected at the end of each period. tdefined in text. In all experiments a tendency could be seen for individual sheep to have characteristic salivary flow rates. Because of this, and the uneven distribution of treatments among sheep (see e.g. Table I), statistical analyses have been avoided. Salivary Composition The composition of the mixed saliva fluctuated somewhat during the course of the experiments, particulary when large amounts of solutes were infused into
8 140 Warner and Stacy either the rumen or the blood, when differences of up to 25 mmol.l1 in either sodium or potassium concentration were found from one hour to the next. The average osmotic pressure of the saliva was always less than that of blood but large increases in blood osmolality were reflected in increases in salivary osmolality. Some of this increase was due to the entry into the saliva of the solute being infused. Table I and Fig. 3 show that the sodium and potassium concentrations in saliva reflected changes in plasma composition; salivary urea concentrations also followed the general trend of plasma urea concentrations at about two thirds the level. DISCUSSION In his review, Kay [1966] listed a number of stimuli in the mouth, oesophagus and rumen that affected salivary flow in sheep or cattle. He discussed several reports [see also Wilson, 1963] that distension of the rumen inhibited salivary flow. It seems unlikely that this effect played any significant part in the present experiments for two reasons. First, the rumen volume was expanded by addition of solutions of two different types, hypo- and hypertonic, and the magnitude of the expansion was similar (unpublished results). Ruminal distension was a factor common to all experiments, yet the two types of solution had opposite effects on the rate of salivation (Fig. 1, Table I). Second, although addition of hypertonic solutions caused distension of the rumen it also caused a rise in plasma osmotic pressure. Apparently the latter effect was primarily significant in bringing about a reduction in salivary flow because elevation of plasma osmotic pressure by intravascular administration of hypertonic infusions also resulted in similar reductions in salivary flow (cf. Figs. 2 and 4) despite the absence of any marked changes in the rumen (Fig. 3). This work seems to establish that plasma osmolality is one of the major determinants of salivary flow rate. Beal, Budtz-Olsen and Clark [1975] failed to find any effect of intravenous hypertonic sodium chloride infusions on parotid salivary flow of sheep, but their rates of infusion were only about a quarter of those used by us. On the other hand, Carr and Titchen [1972] found that hypertonic infusions, at a rate somewhat greater than in our experiments, caused a rapid inhibition of parotid salivation. It may also be noted that Bailey and Balch [1961b] found that a single large intraruminal dose of sodium chloride lowered the total salivation rate in cows, and Tomas and Potter [1975] found that sheep accustomed to a saline drinking water secreted less parotid saliva than those given rain water; in neither of those experiments was the plasma osmolality measured. More naturally, the solutes that enter the rumen during feeding raise its osmotic pressure [Warner and Stacy, 1968, 1975; Engelhardt, 1969; Bergen, 1972] to levels similar to those produced more artificially in this work (Table I). At the same time, the osmotic pressure of the blood is raised [Stacy and Warner, 1966; Carr and Titchen, 1972], again to levels similar to those found in the present work (Table I, Figs 2, 3, 4). It is now well-established that the rate of
9 Salivary secretion in sheep 141 salivation immediately after feeding is less than the rate immediately before feeding; indeed some [Bailey and Balch, 1961b; Bailey, 1961, 1966] found that the salivation rate in the immediately post-prandial period was the lowest for the day, though others [Meyer, Bartley, Morrill and Stewart, 1964; Putnam, Lehmann and Davis, 1966] found a later minimum. Several of these authors speculated about the cause of this diminution of flow; Kay [1966] in his review suggested ruminal distension as the primary cause. The present work suggests that a more important reason may have been the response to the increased plasma osmolality. Several workers [see Wilson, 1963] found that infusion of water into the rumen, or drinking, inhibited parotid secretion probably, as Wilson [1963] showed, as a result of ruminal distension; plasma osmolality was not measured. However, Carr and Titchen [1972] found that intravenous hypotonic infusions stimulated salivation; this was confirmed in the present work (Figs. 3, 4), which also showed (Figs. 1, 2) that hypotonic infusion into the rumen and the accompanying hypotonicity of the plasma could also stimulate salivation. A puzzling feature of some of our experiments (Fig. 3 c) was a stimulation of salivation by hypotonic intravascular infusions even when plasma osmolality was still raised following a preceding hypertonic infusion. It is plain that a considerable number of stimulants, chemical and mechanical, affect salivation in ruminants. The delineation of cause and effect in such natural phenomena as eating and drinking which involve several of these stimulants is far from easy. To the list of stimulants given by Kay [1966] must now, it seems, be added plasma osmolality, though its mechanism of action remains obscure. A similar balance of competing stimuli may be found in the factors affecting salivary composition. In the present work, any effects on salivary composition that might have derived from different rates of secretion [Kay, 1960; Bailey and Balch, 1961a] were presumably masked by the effects of electrolyte concentrations in the blood or perhaps of changing proportions in the secretions of the different salivary glands [Kay, 1960]. ACKNOWLEGMENTS The technical assistance of Messrs E. M. Rust and B. W. Wilson is gratefully acknowledged. The authors are grateful to the late Dr J. R. Goding for surgical assistance in the preparation of parotid fistulae. REFERENCES BAILEY, C. B. (1961). Saliva secretion and its relation to feeding in cattle. 4. The relationship between the concentrations of sodium, potassium, chloride and inorganic phosphate in in mixed saliva and rumen fluid. British Journal of Nutrition, 15, BAILEY, C. B. (1966). A note on the relationship between the rate of secretion of saliva and the rate of swallowing in cows at rest. Animal Production, 8, BAILEY, C. B. and BALCH, C. C. (1961a). Saliva secretion and its relation to feeding in cattle. 1. The composition and rate of secretion of parotid saliva in a small steer. British Journal of Nutrition, 15,
10 142 Warner and Stacy BAILEY, C. B. and BALCH, C. C. (1961b). Saliva secretion and its relation to feeding in cattle. 2. The composition and rate of secretion of mixed saliva in the cow during rest. British Journal of Nutrition, 15, BEAL, A. M., BUDTZ-OLSEN, 0. E. and CLARK, R. C. (1975). The effect of potassium chloride infusion on parotid salivary flow and composition in conscious sheep. Quarterly Journal of Experimental Physiology, 69, BERGEN, W. G. (1972). Rumen osmolality as a factor in feed intake control of sheep. Journal of Animal Science, 34, CARR, D. H. and TITCHEN, D. A. (1972). Factors contributing to the control of parotid salivary secretion in sheep. Proceedings of the Australian Physiological and Pharmacological Society, 3(2), 162. DENTON, D. A. (1957). The study of sheep with permanent unilateral parotid fistulae. Quarterly Journal of Experimental Physiology, 42, ENGELHARDT, W. v. (1969). Der osmotische Druck im Panseninhalt. Zentralblattffur Veterindrmedizin, Reihe A, 16, ENGELHARDT, W. v. and SALLMANN, H.-P. (1972). Resorption und Sekretion im Pansen des Guanakos (Lama guanacoe). Zentralblatt fur Veterindrmedizin, Reihe A, 19, KAY, R. N. B. (1960). The rate of flow and composition of various salivary secretions in sheep and calves. Journal ofphysiology, 150, KAY, R. N. B. (1966). The influence of saliva on digestion in ruminants. World Review of Nutrition and Dietetics, 6, MEYER, R. M., BARTLEY, E. E., MORRILL, J. L. and STEWART, W. E. (1964). Salivation in Cattle. 1. Feed and animal factors affecting salivation and its relation to bloat. Journal of Dairy Science, 47, PUTNAM, P. A., LEHMANN, R. and DAvIs, R. E. (1966). Feed intake and salivary secretion by steers. Journal of Animal Science, 25, STACY, B. D. and WARNER, A. C. I. (1966). Balances of water and sodium in the rumen during feeding: osmotic stimulation of sodium absorption in the sheep. Quarterly Journal of Experimental Physiology, 51, TOMAS, F. M. and POTTER, B. J. (1975). Influence of saline drinking water on the flow and mineral composition of saliva and rumen fluid of sheep. Australian Journal of Agricultural Research, 26, WARNER, A. C. I. and STACY, B. D. (1965). Solutes in the rumen of the sheep. Quarterly Journal of Experimental Physiology, 50, WARNER, A. C. I. and STACY, B. D. (1968). The fate of water in the rumen. 2. Water balances throughout the feeding cycle in sheep. British Journal of Nutrition, 22, WARNER, A. C. I. and STACY, B. D. (1972). Water, sodium and potassium movements across the rumen wall of sheep. Quarterly Journal of Experimental Physiology, 57, WILSON, A. D. (1963). The effect of diet on the secretion of parotid saliva by sheep. II. Variations in the rate of salivary secretion. Australian Journal of Agricultural Research, 14, WILSON, B. W. (1966). Automatic estimation of urea using urease and alkaline phenol. Clinical Chemistry, 12,
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