reaching the upper small intestine where pancreatic juice can act [Garton,
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1 Q. Jl exp. Physiol. (1969) 54, LIPID DIGESTION IN THE SHEEP: EFFECT OF BILE AND PAN- CREATIC JUICE ON THE LIPIDS OF INTESTINAL CONTENTS. By W. M. F. LEAT and F. A. HARRISON. From the Agricultural Research Council Institute of Animal Physiology, Babraham, Cambridge. (Received for publicotion 16th August 1968) The effect of bile and pancreatic juice on the pattern of lipids in the intestinal digesta of the sheep has been examined using animals suitably prepared with chronic intestinal fistulae. The major lipid of digesta collected anterior to the common bile duct was the free fatty acid fraction composed mainly of palmitic and stearic acids. Digesta collected immediately posterior to the common bile duct contained, in addition, polyunsaturated fatty acids and lecithin, indicating that these lipids originated in the mixed secretions of bile and pancreatic juice. In the mid jejunum the major phospholipid was lysolecithin derived from the hydrolysis of lecithin by pancreatic enzymes. In the duodenum and jejunum the free fatty acids were associated mainly with the particulate matter of digesta, but in the ileum the free fatty acids were more evenly distributed between the particulate and aqueous phases. Negligible amounts of monoglyceride were present in digesta of the small intestine. Diversion of bile and pancreatic juice from the intestine resulted in the disappearance of lysolecithin and a decrease in the content of unsaturated fatty acids in the digesta of the jejunum. The digestion of lipids in the sheep intestine is discussed in relation to the possible role of bile and pancreatic juice. It is suggested that a major function of pancreatic juice is to provide, by interaction with biliary lecithin, the lysolecithin required for optimum micelle formation and lipid absorption. IN fat digestion in non-ruminant animals one of the major functions of pancreatic juice is to facilitate the hydrolysis of the water insoluble triglyceride molecule to monoglycerides and free fatty acids (FFA) which then form water soluble micelles with bile salts [Hofmann and Borgstr6m, 1962]. In the ruminant animal, however, because of lipolytic activity by rumen micro-organisms most of the dietary fat is already in the form of FFA before reaching the upper small intestine where pancreatic juice can act [Garton, 196]. Nevertheless it has been shown that both bile and pancreatic juice are necessary for optimum fat absorption in the sheep [Heath and Morris, 1964]. Whilst the function of bile in the sheep is apparent, that of pancreatic juice is more obscure. The FFA of abomasal contents are mainly saturated in character, as a result of hydrogenation in the rumen, but there is an increase in unsaturation in the fatty acids of the small intestinal contents [McCarthy, 1962]. It has been suggested, on the basis of in vitro experiments, that the source of these unsaturated acids may be biliary and pancreatic secretions [Leat, 1965]. The object of the present investigation was first to examine the spectrum of lipids normally present in the intestinal digesta of the sheep, and then to determine any changes occurring in this lipid pattern when bile and pancreatic juice were diverted from the intestine. It was hoped that the 187
2 188 Leat and Harrison function of pancreatic juice in the ruminant animal would then become more apparent. A preliminary account has been published [Leat and Harrison, 1967]. METHODS AND ANIMALS Animals and diets. - Clun Forest sheep aged 1-2 yr from the Institute flock were used. They were housed indoors and unless otherwise stated were fed once daily at 9 hr 1 g chaffed hay + 2 g crushed oats. Cystic duct 7 Hepatic duct Pancreas/ 7f Pancreatic duct ~~~Common bile duct <~~~anl 3X Dudenu m Cannula3nnua Cannula 4 Catheter in common bile duct Cannula 1 Abomasu m Fig. 1. Diagram of double re-entrant duodenal-fistula preparation [from Harrison and Hill, 1962]. Surgical procedures. Wether sheep 'Gabriel' and ewe 'Jonquil' were prepared with a rumen cannula and two duodenal re-entrant cannulae, cannulae 1-2 in the first part of the duodenum adjacent to the pylorus and cannulae 3-4 posterior to the point of entry of the common bile duct at the iliac flexure of the duodenum, [Harrison and Hill, 1962; see fig. 1]. Digesta collected from cannula 1 was essentially abomasal in character whereas that from cannula 3 contained in addition bile and pancreatic juice. Wether sheep 'Hubert' and ewe 'Giaconda' were each prepared with (a) a rumen cannula (b) a Thomas fistula, i.e. a cannula opposite the entrance of the common bile duct into the duodenum [Hart and Thomas, 1945] and (c) two intestinal re-entrant cannulae, cannulae 1-2 being in the jejunum about 365 cm (12 ft) from the common bile duct and cannulae 3-4 being in the lower ileum about 15 cm (5 ft) from the ileocaecal valve. In the sheep the pancreatic duct enters the common bile duct about 1 cm from the bile papilla and mixed bile and pancreatic secretion enters the intestine through the sphincter of Oddi. Using the method described by Taylor [196] for the collection of pancreatic juice in the sheep, mixed bile and pancreatic secretion could be diverted from the intestine through a catheter introduced into the common bile duct via the
3 Lipid Digestion in the Sheep 189 Thomas fistula. Digesta could then be collected quantitatively from the intestinal cannulae with or without the contribution of mixed bile and pancreatic secretions. Design of experiments. Expt (Giaconda and Hubert). In a 1 hr experiment intestinal contents were quantitatively collected from cannulae 1 (CI) and 3 (C3) respectively. Approximately 5 ml amounts of digesta were collected and, after thorough mixing, 1 per cent was retained on ice to form a representative hourly sample. The major part of the digesta was then rapidly returned to cannulae 2 and 4 respectively. At the end of each hour aliquots of the Cl and C3 digesta were taken and the remaining bulked material returned to the appropriate cannula after warming to body temperature. Expt (Giaconda and Hubert). The basic design of the experiment was the same as described for Expt. 1. However, at the beginning of the 5th hr the common bile duct was catheterized and mixed bile and pancreatic secretion was diverted from the intestine and collected into a bottle strapped to the sheep. After 4 hr of drainage the catheter was removed and bile and pancreatic juice allowed to flow into the intestine again. Expt (Gabriel and Jonquil). In the first part of the experiment intestinal contents were collected from cannula 1 and returned to cannula 4, samples being taken as described in Expt. 1 At the same time the secretions of the duodenum mixed with the bile and pancreatic juice were collected from cannulae 2 and 3. In the second part of the experiment cannulae 1 and 2 were reconnected and digesta was collected from cannula 3 and returned to cannula 4 after sampling. In other experiments the order of procedure was reversed. Expt Another sheep was fed ad lib, for 14 days prior to killing, a diet of hay and crushed sheep nuts mixed with 1 per cent chromic oxide as a marker. The animal was anaesthetized with pentobarbitone sodium ('Nembutal', Abbott) the abdomen opened rapidly and the small intestine clamped at several randomly selected points. The clamps were then replaced by ligatures and, after killing the sheep, the loops of small intestine were removed. The distance of each loop from the abomasum was measured and the contents taken for analysis. Treatment of digesta. - The intestinal contents were centrifuged at 4 C in graduated tubes to separate the particulate and supernatant fractions for analysis and to determine the proportion of each fraction. Samples not extracted immediately were stored at - 2 C. Chemical Analysis. - Analysis of lipids included thin layer and gas liquid chromatography and was carried out as described previously [Leat, 1966, 1967]. Chromic oxide was estimated by the method of Christian and Coup [1959]. RESULTS Table I shows the composition of digesta collected from the duodenal, jejunal and ileal re-entrant cannulw of various sheep over periods of time ranging from 4-11 hr. Ninety-two, 78 and 43 per cent of the free fatty acids in the digesta of duodenum, jejunum and ileum respectively were associated with the particulate fraction. Phospholipids were distributed more evenly between the particulate and aqueous phases. The major lipids found in the particulate free digesta from duodenum, jejunum and ileum were free fatty acids (3, 56 and 68 per cent respectively) and phospholipids (7, 36 and 2 per cent respectively). The ph of the intestinal contents increased from abomasum to ileum. Fig. 2 shows a thin layer chromatogram of the phospholipids of the particulate free digesta from various parts of the digestive tract of the sheep.
4 19 Leat and Harrison Co I I I o4 MO H Co o o 3- o cq,qq -4 1 r-4 -H + XoI? IVI * -Hc. -H Cs Co H z H.5 cz 1- C) P, cq F- c -H -H I?G - I1 m-h - Cg v z v H N cd 2 m~ ;, Co Hw Ca Ca~ r Odc isoi - _~ es * * * z O -H E-4 H Co &) to,-i o= CO Q. 1 CO - d - -H -d Cec H -H O to O s o o t Co v # ~ -H : + e~~~ m _~ w4 _ X V~
5 --77 ~7 front cephalin a_" ~~~~~~~~~~~~~~~~lecithin sphingomyelin lysolecithin origin F R Di D2 J II S Fig. 2. Thin layer chromatogram of the phospholipids of particulate-free digesta from various regions of the sheep intestine. See text for further details. F, food; R, rumen; Dl, duodenum anterior to cormmon bile duct (cbd); D2, duodenum posterior to cbd; J, jejunum; Il, ileum; 5, standards. Solvent system :-chloroform: methanol: water: acetic acid (.O : 25 : 4 : 1 by vol.) Detection by molybdenum blue reagent (Dittmer and Lester, 1964).
6 192 Leat and Harrison ~~~~~~C66 4 -: t:.4-z o m ~ ~~~~~~~~~~~~~~~~~~~~~~~~~~~~ i P4~~~~~~~~~~~~~~1 _Ic o 1 C Dco X~~~~~~~~~~a _N r ~~~ P4 rn -4 r- _ LX rmaqo4-4c b w t;o z _ o I 14Z 14z *XH 4 14D 4 m C I o.,- Ce (6 o cbxx6 > - P O4 C Z E- O- 3 Cs 6 - GE-4 14D X : > X X C 4) EH ~~~~A
7 Lipid Digestion in the Sheep 193 There were three main phospholipids in rumen contents, all staining positively with ninhydrin. They had Rf values of -58, 45 and *37 and accounted for 46, 34 and 2 per cent respectively of the lipid phosphorus. The same pattern was seen in duodenal contents anterior to the common 8 7- ~6-6 so g \5 ph E I I IOII 12 Time Our) Fig. 3. Sheep Giaconda: effect of diverting bile and pancreatic juice (5th-8th hr) on the lipids of the particulate free digesta of the jejunum. See text for further details. O, free fatty acids; * *, phospholipids; -, ph. bile duct, suggesting that little if any degradation of these phospholipids occurred in the omasum and abomasum. The most predominant phosphatides in duodenal digesta collected posterior to the common bile duct were lecithin (48 per cent) and lysolecithin (27 per cent), although the pattern of phospholipids was largely unchanged. In jejunal digesta lysolecithin was quantitatively the most important phosphatide (8 per cent) and the phospholipid of Rf -58 detected anterior to the common bile duct had been replaced by one of Rf -28. The pattern of neutral lipids in digesta from the rumen, jejunum and ileum was qualitatively similar and confirmed that the major lipid was free fatty acid; the presence of monoglyceride could not be demonstrated unequivocally. Table II gives the fatty acid composition of the lipids of these digesta samples. The free fatty acids of digesta anterior to the common bile duct and of the ileum contained a high proportion of saturated acids but those
8 194 Leat and Harrison of the upper small intestine were more unsaturated, the difference being most pronounced immediately posterior to the common bile duct. Of note is the higher content of branched fatty acids in the phospholipid fraction compared with the corresponding free fatty acids. 4 a 4._ CY% E 3 21._ "f.. a Time (hr) Fig. 4. Sheep Giaconda: effect of diversion of bile and pancreatic juice (5th-8th hr) on the individual free fatty acids of jejunaldigesta. O,C18:1; * *,C18:2; A A C18:. Expt. 2. Fig. 3 shows the effect on the lipids of jejunal digesta of - diverting bile and pancreatic juice from the intestine. In the absence of the mixed secretions, the ph of the digesta and the concentrations of free fatty acids and phospholipids fell. However, when bile and pancreatic juice were allowed to re-enter the intestine the FFA and phospholipid concentrations rose to higher values than found in the initial control period. Fig. 4 shows the changes in individual free fatty acids in more detail: during the absence of bile and pancreatic juice C18:2 acid disappeared and the concentrations of C18: and C18:1 acids decreased. Thin layer chromatography of digesta lipids showed that diversion of bile and pancreatic juice had no qualitative effect on the spectrum of neutral lipids but a marked effect on that of phospholipids (fig. 5). During the initial 4 hr control period lysolecithin was the major phospholipid (8 per cent) but on diversion of bile and pancreatic juice between hr 5-8
9 ḳs,.i!. t_ :. w.nw. 7, *y.'. i :'..:t' 7s ::: w.6; si,,, j>-znea, %, Lipid Digestion in the Sheep 195 * wi.x W- X :''$: " ':,:;t ES'!+t: X"' ::e S; D'* '; >, i :: i': j, l:: :.: x. v I I....v',E' RE &. XA;i Ao.X ',:,,,,: ',!:' : =. ^ _v A! W. : _ :._t,r,_ 'SF _g _- '* {._.. m e w:'..n :,..t 'L Fs iz.w..'gilll ; r Xk w r i; S front cephalin lecithin ',-.,.,>._ -q_. a_ :H :.s. '=I, _ 9.* :r _r. -_gas in_xn. - _ v _ lyvolecithin %,...,;. origin Hr S BPJ Fig. 5. Sheep Giaconda: effect of diverting bile and pancreatic juice (5th-8th hr) on the phospholipids of the particulate free digesta of the jejunum. See text and fig. 3 for further details. Thin layer chromatography as described in fig. 2. S, standard; BPJ, mixed secretion of bile and pancreatic juice. lysolecithin disappeared and the phospholipid pattern characteristic of digesta anterior to the common bile duct appeared. The major phospholipids of the diverted mixed secretions were lysolecithin (8 per cent) and lecithin (17 per cent). When bile and pancreatic juice were allowed to flow again into the intestine at hr 8, lecithin (51 per cent), lysolecithin
10 196 Leat and Harrison (28 per cent) and phospholipid Rf 28 (5 per cent) reappeared but the phospholipid Rf -58 persisted. Changes also occurred in the phospholipids of digesta collected from the ileal cannula. There was a four-fold increase in the concentration of phospholipids after hr 8, the main components being lecithin and lysolecithin. The phospholipid Rf -58 was detected after hr 8 although not present before this time. Table III shows the volume and fatty acid content of the mixed secretions of bile and pancreatic juice; it is seen that at least g fatty acid are secreted daily into the duodenum of the sheep. TABLE III. FATTY ACID CONTENT OF MIXED SECRETIONS OF BILE AND PANCREATIC JUICE. Volume of *Fatty acid Weight Period of secretion content Sheep (kg) collection (hr) (ml./kg/hr) (g/day) Secretion Giaconda Bile + pancreatic juice Hubert VP Hubert ,, Gabriel Bile +pancreatic juice +duodenal secretions Jonquil of Jonquil IV * Component fatty acids (per cent) C16:, 39 5; C16:1, 7.8; C18:, 12.4; C8s:1, 3; C18:2, 7-6; minor acids, 2-7. Expt Fig. 6 shows the lipid content of digesta at various distances along the small intestine related to a unit weight of chromic oxide. There was a secretion of free fatty acids, phospholipids and cholesterol into the duodenum, the free fatty acid and phospholipid concentrations in the upper small intestine being respectively twice and four times that found in the abomasum. Fig. 7 shows the changes in free fatty acids in more detail and indicates that both saturated and unsaturated fatty acids were secreted into the duodenum. DIscusSION The results reported here confirm previous findings in ruminants [see Garton, 196] that most of the fat passing from the abomasum into the upper duodenum is in the form of saturated free fatty acids, mainly palmitic and stearic acids. In the lower duodenum, however, the fatty acids of digesta become more unsaturated, containing larger amounts of C18:1, C18:2 and C188: fatty acids. This secretion of unsaturated fatty acids into the small intestine of the ruminant has also been noted previously in the goat [McCarthy, 1962], the sheep [Felinski, Garton, Lough and Phillipson, 1964; Ward, Scott and Dawson, 1964; Leat, 1965] and the cow [Leat and Hall, 1968]. Our results indicate that, in addition, there was a secretion of saturated free fatty acids,
11 Lipid Digestion in the Sheep 197 phospholipids and cholesterol into the lumen of the small intestine. The most marked increase in the concentration of these lipids occurred in the distal duodenum immediately posterior to the common bile duct, suggesting that a major source of these lipids was the mixed secretion of bile and pancreatic juice. Immediately distal to the common bile duct, the major intestinal phospholipid was lecithin, but 3 cm (1 ft) further down the intestinal 2r 15OF x u E - E 1 E 51_ ph Ab 7 Distance from abomasum (ft) Fig. 6. Variation in the concentration of digesta lipids along the small intestine of the sheep. O, free fatty acids; *, phospholipids; -- -, ph; Ab = abomasum. tract lysolecithin predominated. These findings can be explained by the observation that when sheep bile and pancreatic juice are incubated together in vitro the biliary lecithin is rapidly degraded to lysolecithin by pancreatic enzymes, with concomitant release of both saturated and unsaturated fatty acids [Leat, 1965]. The in vivo experiments reported here indicate that when bile and pancreatic juice were diverted from the intestine, lysolecithin and C18:2 fatty acid disappeared from intestinal contents but reappeared when these secretions were allowed to re-enter the intestine. This confirms a previous suggestion that the mixed secretion VOL. LIV, NO
12 198 Leat and Harrison of bile and pancreatic juice is the major source of lysolecithin and unsaturated fatty acids in digesta of the small intestine of the sheep [Leat, 1965]. Pancreatic juice also appeared to degrade the digesta phospholipids arriving from the abomasum. The phospholipid Rf -58 found in the contents of the rumen and upper duodenum was replaced in jejunal digesta by one of Rf -28. Diversion of bile and pancreatic juice resulted in the disappearance of phospholipid Rf -28 in jejunal contents and the reappearance of phospholipid Rf -58. The chromatographic and staining properties of these 3r o la x._u - u E._ 21F I o a- Ea Distance from abomasum (ft) Fig. 7. Changes in the concentration of the individual free fatty acids of digesta along the small intestine of the sheep. A A, C16:; A * C18:; O, C18:1; *- O C18:2. Ab =Abomasum. two phospholipids suggest that phospholipid Rf -58 is phosphatidylethanolamine and phospholipid Rf -28 is its lyso-derivative. The incomplete hydrolysis of phospholipids observed when bile and pancreatic juice were allowed to flow into the intestine after a 4 hr drainage period may be a result of the decrease in the enzyme content of pancreatic juice known to occur on drainage [Taylor, 1962]. The calculated amount of fatty acids passing daily through the duodenum and jejunum of sheep Gabriel and Giaconda, 15-8 g and 11-5 g respectively, was in reasonable agreement with the intake of dietary fatty acids (a maximum of 14 g daily). Most of the fatty acids were absorbed before reaching the lower ileum. Sheep Jonquil was a more nervous animal and did not usually eat its food completely; this could account for the reduced flow
13 Lipid Digestion in the Sheep 19'3 rate of digesta, and hence the lower calculated daily values. The combined secretions of bile and pancreatic juice would add at least 3 g fatty acid to the duodenal contents daily, which is 2 per cent of the dietary intake. These values are a minimum sinoe if the diverted bile is not returned to the duodenum, as was the case in our experiment, bile secretion decreases [Harrisorn, 1962]. Adams and Heath [1963] have calculated on the basis of biliary return that 7-1 g fatty acid are secreted daily into the duodenum in bile. The flow of digesta from the ileal cannule was on average about 6 per cent of that from the jejunal cannulke; the hourly flow rates from the ileum (-597 ml./hr) were more variable than those from the jejunum ( ml./hr). Because of this large variation it was not possible to determine whether diversion of bile and pancreatic juice had any consistent effect on the flow of digesta from jejunal and ileal cannulwe. In duodenal contents, and to a lesser extent in jejunal contents, the free fatty acids were associated mainly with the particulate matter, whereas in ileal digesta they were distributed more evenly between the particulate and supernatant fractions; preferential attachment of FFA to solid particles in ruminal and jejunal contents has been noted by Ward et at., [1964] and Lennox, Lough and Garton [1968] respectively. This unequal distribution of FFA does not appear to be a function of ph, since titration of duodenal contents to a ph comparable with that of the ileum did not result in any redistribution of FFA. However, when duodenal contents were adjusted to ph 6-5 and then incubated in vitro for 3 hr about 2 per cent of the FFA attached to the food particles passed into the aqueous phase. This would suggest that the fatty acids do not pass readily into the micellar phase until that part of the food particles responsible for binding the FFA, for example protein, is digested. Mono- and diglycerides are minor constituents of the digesta lipids of the rumen and abomasum [Garton, Lough and Vioque, 1959; Bath and Hill 1967]. Our experiments have shown in addition that insignificant amounts of monoglyceride were present at the site of fat absorption in the small intestine and it must be concluded that monoglycerides are of minor importance in fat absorption in the ruminant animal. However, the lysolecithin formed by the interaction of bile and pancreatic juice is itself a powerful detergent and, since it forms micelles readily [Barton and Glover, 1965], it may replace monoglyceride in function. Lysolecithin has been detected in the intestinal contents of man [Borgstrom, 1957], the sheep [Leat, 1965; Lennox et al., 1968] and the cow [Leat and Hall, 1968] but any role that it might play in fat absorption in non-ruminant animals has been overshadowed by the importance assigned to monoglyceride. Although it cannot be concluded from Expt. 3 that lipid absorption in the sheep takes place in the mid-small intestine, it does seem that phospholipids together with saturated and unsaturated fatty acids are absorbed concomitantly, suggesting that an aggregate of these lipids is involved. Savary [1966] has shown that unsaturated fatty acids increase the solubility of saturated fatty acids in bile salt micelles and this might explain
14 2 Leat and Harrison the improved absorption of stearic and palmitic acids in chicks noted in the presence of unsaturated fatty acids [Young and Garrett, 1963]. The unsaturated fatty acids released from bile in the small intestine of the sheep may therefore expand the lysolecithin-bile salt micelle and increase the solubility and absorption of the saturated fatty acids formed in the rumen. This enterohepatic circulation of unsaturated fatty acids could therefore improve fat absorption and also tend to conserve the polyunsaturated fatty acids that have escaped hydrogenation in the rumen. It is now possible to offer some explanation for the findings of Heath and Morris [1964], who showed in the sheep that a lymph lipid concentration of u-equiv/ml. fell to 14-7,u-equiv/ml. when pancreatic juice was diverted from the intestine and to 1.5,u-equiv/ml. when bile was diverted. A decrease in the concentration of lymph lipid on diversion of bile would be expected since bile contributes at a minimum 3 g fatty acids daily in addition to providing the bile salt and phospholipid required for optimum micelle formation. Pancreatic juice contributes negligible amounts of lipid but provides the enzyme necessary to degrade lecithin to lysolecithin. When bile alone is infused into the duodenum in the absence of pancreatic juice, lecithin appears undegraded at both jejunal and ileal cannulae [Leat and Harrison, unpublished observations], suggesting that biliary lecithin is not absorbed as efficiently as lysolecithin. However, the neutralizing ability of the bicarbonate in pancreatic juice may also be important. In the absence of pancreatic juice the ph of the intestinal contents of the sheep decreased and this could result in decreased ionization and hence decreased solubility of the fatty acids in micelles [Hofmann, 1965]. The experiments reported here, however, suggest that in the sheep a major function of pancreatic juice is to convert biliary lecithin to lysolecithin which then forms the micelles necessary for optimum absorption of fatty acids. ACKNOWLEDGEMENTS We thank Mrs G. V. Thompson, S.R.N., S.C.M., Miss G. H. Needham and Miss J. Baker for their invaluable assistance. Fig. 1 is reproduced by permission of the Editorial Board of the Journal of Physiology. REFERENCES ADAMs, E. P., and HEATH, T. J. (1963). 'The phospholipids of ruminant bile', Biochim. Biophys. Acta, 7, BARTON, P. G., and GLOVER, J. (1965). In The Biliary System, p ed. Taylor, W. Oxford: Blackwell Scientific Publications Ltd. BATH, I. H., and HILL, K. J. (1967). 'The lipolysis and hydrogenation of lipids in the digestive tract of the sheep', J. agric. Sci. Camb., 68, BORGSTROM, B. (1957). 'Studies of the phospholipids of human bile and small intestinal content', Acta chem. scand., 11, 749. CHRISTIAN, K. R., and Coup, M. R. (1959). 'Measurement of feed intake by grazing cattle and sheep. VI. The determination of chromic oxide in faeces', N.Z. Ji Sci. Technol., 36,
15 Lipid Digestion in the Sheep 21 DITTMmER, J. C., and LESTER, R. L. (1964). 'A simple, specific spray for the detection of phospholipids on thin layer chromatograms', J. Lipid Res., 5, FEIJNSKI, L., GARTON, G. A., LOUGH, A. K., and PHILLIPSON, A. T. (1964). 'Lipids of sheep lymph: transport from the intestine', Biochem. J., 9, GARTON, G. A. (196). 'Lipid metabolism in herbivorous animals', Nutr. Abst. Rev., 3, GARTON, G. A., LOUGH, A. K., and VIOQUE, E. (1961). 'Glyceride hydrolysis and glycerol fermentation by sheep rumen contents', J. gen. Microbiol., 25, HARRISoN, F. A. (1962). 'Bile secretion in the sheep', J. Physiol., 162, HARRISON, F. A., and HILL, K. J. (1962). 'Digestive secretions and the flow of digesta along the duodenum of the sheep', J, Physiol., 162, HART, W. H., and THOMAS, J. E. (1945). 'Bicarbonate and chloride of pancreatic juice secreted in respcnse to various stimuli', Gastroenterology, 4, HEATH, T. J., and MORRIS, B. (1964). 'The role of bile and pancreatic juice in the absorption of fat in ewes and lambs', Br. J. Nutr., 17, HOFMANN, A. F. (1965). 'Clinical implications of physicochemical studies on bile salts', Gastroenterology, 48, HOFMANN, A. F., and BORGSTROM, B. (1962). 'Physico-chemical state of lipids in intestinal content during their digestion and absorption', Fed. Proc., 21, LEAT, W. M. F. (1965). 'Possible function of bile and pancreatic juice in fat absorption in the ruminant' Biochem. J., 94, 21-22P. LEAT, W. M. F. (1966). 'Fatty acid composition of plasma lipids of newborn and maternal ruminants', Biochem. J., 98, LEAT, W. M. F. (1967). 'Plasma lipids to newborn and adult ruminants and of lambs from birth to weaning', J. agric. Sci. Camb., 69, LEAT, W. M. F., and HALL, J. G. (1968). 'Lipid composition of lymph and blood plasma of the cow', J. agric. Sci. Camb., 71, LEAT, W. M. F., and HARRISON, F. A. (1967). 'Effect of bile and pancreatic juice on the intestinal lipids of the sheep', Biochem. J., 15, 13P. LENNOX, A. M., LOUGH, A. K., and GARTON, G. A. (1968). 'Observations on the nature and origin of lipids in the small intestine of the sheep', Br. J. Nutr., 22, MCCARTHY, R. D. (1962). In Use of Radioisotopes in Animal Biology and Medical Sciences, Vol. 2, ed. M. Fried. London: Academic Press Inc. SAVARY, P. (1966). 'Sur la solubilization micellaire des acides palmitique, stearique et ole`que dans les solutions d'acides biliaires conjugu6s', Biochem. Biophys. Acta, 125, TAYLOR, R. B. (196). 'A method for collection of pancreatic juice in the conscious sheep', Res. vet. Sci., 1, TAYLOR, R. B. (1962). 'Pancreatic secretion in the sheep', Res. vet. Sci., 3, WARD, P. F. V., SCOTT, T. W., and DAWSON, R. M. C. (1964). 'The hydrogenation of unsaturated fatty acids in the ovine digestive tract', Biochem. J., 92, YouNG, R. J., and GARRETT, R. L. (1963). 'Effect of oleic and linoleic acids on the absorption of saturated fatty acids in the chick', J. Nutr., 81,
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