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Article

Digestion of Fat Does Not Differ in Growing Pigs Fed Diets Containing Fish Oil, Rapeseed Oil or Coconut Oil^{1 ,2}

Henry Jørgensen^*, Vince M. Gabert³, Mette S. Hedemann^* and Søren K. Jensen^*

^* Department of Animal Nutrition and Physiology, Danish Institute of Agricultural Sciences, Research Centre Foulum, 8830 Tjele, Denmark; and Department of Animal Sciences, University of Illinois, Urbana, IL 61801

³To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
We studied the digestion of fat and fatty acids in diets containing oils with different fatty acid composition. Four barrows (initial weight 35 kg) were fitted with a simple T-cannula at the terminal ileum. Three wheat starch and fish meal-based diets were formulated to contain either 150 g fish oil, rapeseed oil or coconut oil/kg. A basal diet, which did not contain oil, was also prepared. The diets were fed according to a 4 x 4 Latin square design. Each experimental period comprised 5 d adaptation to the diets, 3 d fecal collection and 2 d digesta collection. The apparent ileal and fecal digestibilities of fat were relatively high (88 - 93%). The ileal digestibilities of total, saturated and monounsaturated fatty acids did not differ among the diets. However, the digestibilities of polyunsaturated fatty acids (PUFA) in the fish and rapeseed oil diets were higher (P < 0.05) than in the coconut oil diet. The ileal digestibilities of 18:1, 18:2 and 18:3 in the rapeseed oil diet ranged from 94 to 97%. The ileal digestion of the unsaturated long-chain fatty acids 20:5(n-3) and 22:6(n-3) in the fish oil diet was nearly complete (97 - 98%). Apparent fecal digestibilities of saturated fatty acids (76 - 89%) were lower than apparent ileal digestibilities (89 - 94%). The digestibilities of fat and fatty acids were relatively high when pigs were fed diets containing fish oil, rapeseed oil or coconut oil. There were few differences in the digestibilities of saturated, monounsaturated and PUFA in the fish oil, rapeseed oil or coconut oil diets.

KEY WORDS: • pigs • dietary fat • digestibility • fatty acids

	INTRODUCTION

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Fats and oils are important dietary ingredients in animal production owing to their high energy value. Furthermore, the fatty acid pattern of the dietary lipids is reflected in the fatty acid profile of animal products (Jørgensen et al. 1996 ). However, the lipids used in domesticated animal diets are extremely diverse in chemical structure, which may influence digestibility and energy value. Differences in the fecal digestibility of fat for various sources of dietary fat were identified at the turn of the century in studies with humans (Atwater and Bryant 1900 , Merrill and Watt 1973 ). Fatty acids as a proportion of total fat and fat digestibility are the most important factors determining the nutritive value of fat (Wiseman et al. 1990 ).

Fat digestion occurs in the small intestine and absorption of fatty acids, such as mono- and diacylglycerols, is nearly complete at the distal ileum (Borgström 1993 ). However, the fatty acids which have not been absorbed in the small intestine will enter the cecum and large intestine. Microbial hydrogenation of unsaturated fatty acids has been shown to be substantial in the cecum and large intestine (Bayley and Lewis 1965 , Carlson and Bayley 1968 and Jørgensen et al. 1992 ). Therefore, the absorption of the individual fatty acids must be measured at the terminal ileum. In contrast, fecal digestibility of total fat is similar to the ileal digestibility of total fat (Jørgensen et al. 1992 ). Dietary fat from animal sources may have a lower digestibility and energy value than dietary fat from vegetable sources due to a higher content of saturated fatty acids (16:0 and 18:0). Saturated fatty acids may have a lower ileal digestibility than unsaturated fatty acids (18:1, 18:2 and 18:3; Jørgensen et al. 1992 and 1993, Øverland et al. 1994). Depending on the degree of saturation, fatty acids may have different rates of absorption. However, whether or not a difference in ileal digestibility is observed between saturated and unsaturated fatty acids when a diet containing coconut oil is fed compared to rapeseed oil or fish oil remains to be determined.

A recent study has examined the effect of the type of dietary fat on the exocrine pancreatic secretions in growing pigs, in which a significant effect of fat source on the secretion of carboxyl ester hydrolase was observed (EC 3.1.1.1; Gabert et al. 1996 ). Carboxyl ester hydrolase is a relatively nonspecific enzyme which hydrolyzes a variety of lipid substrates (Rinderknecht 1993 ), and its contribution to fat digestion has not yet been quantified. However, the apparent fecal digestibilities of fat, protein and energy were not affected by the inclusion of fish oil, rapeseed oil or coconut oil in the diet (Gabert et al. 1996 ). Nevertheless, there may have been some differences between the fat sources which were masked by the modifying and equalizing effects of the microflora in the cecum and large intestine (Sauer and Ozimek 1986 ).

The dietary source of fat and dietary fat level has been shown to affect the digestion of protein. Li and Sauer (1994) observed a significant increase in apparent ileal amino acid digestibilities as the level of canola oil in the diet was increased. Similar effects were demonstrated on the apparent fecal digestibility of protein when growing pigs were fed diets containing 4, 8 and 16% rapeseed oil (Jørgensen et al. 1996 ).

The objective of this study was to obtain further information on the influence of fatty acid composition of different dietary fats, namely fish oil, rapeseed oil and coconut oil, on fat and fatty acid digestibilities in growing pigs. Digestibility was determined at both the distal ileum and in feces in order to examine the modifying effects of bacteria in the cecum and large intestine on fatty acids in digesta. The digestibilities of protein and energy were also determined, and a basal diet which did not contain any supplemented oil was also prepared to determine the effect of including 150 g fat/kg diet from either fish oil, rapeseed oil or coconut oil.

	MATERIALS AND METHODS

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Animals and diets.

Four crossbred barrows (initial weight 35 kg) were obtained from the Danish Institute of Agricultural Science swine herd. The pigs were housed individually in pens and had free access to water and a commercial grower diet for 7 d. The pigs were fitted with a simple T-cannula at the terminal ileum, ~15 cm anterior to the ileo-cecal junction according to procedures adapted from Sauer et al. (1983) . The cannulas were modified according to Jørgensen et al. (1992) .

The protocol used in this experiment complied with the Guide for the Care and Use of Laboratory Animals (NRC 1985 ).

Four wheat starch-based diets (403 g/kg diet) were formulated to contain ~170 g protein/kg diet from fish meal (223 g/kg diet) and wheat bran (100 g/kg diet). The diets contained either 150 g fish oil, rapeseed or coconut oil/kg diet. The rapeseed oil was extracted from low glucosinolate and low erucic acid rapeseed which is commonly grown in Denmark. In this study, none of the essential fatty acids were limiting. However, whether or not essential fatty acids are limiting in the diets is not of concern for the determination of ileal fatty acid digestibilities. What is important is that the level of fat in the supplemented diets be high enough to allow an accurate digestibility determination. This is why the diets were supplemented with 15% fish oil, rapeseed oil or coconut oil. The inclusion level of the oils used was the same as the levels used in studies by Gabert et al. (1996) . A basal diet, which did not contain oil, was also prepared. In the basal diet, an additional 150 g wheat starch/kg diet was included. To increase the palatability of the diets, sucrose (100 g/kg diet) was included. Chromic oxide (2 g/kg diet) was included in the diets as a marker for the determination of the digestibilities of nutrients and energy. Vitamins, except for vitamin E, and minerals were supplemented to meet or exceed Danish standards for growing pigs (Andersen and Just 1983 ). Vitamin E was not supplemented to the diets because we were interested in determining the digestibility of tocopherols in the supplemented oils (results will be presented elsewhere). The chemical composition of the experimental diets is presented in Table 1 .

Analytical methods.

Digesta and feces were freeze-dried, pooled within pig and diet for each experimental period and ground with a mortar and pestle. Dry matter was determined according to AOAC (1990) methods. Protein (N x 6.25) was measured by the Kjeldahl method using a Kjell-Foss 16200 autoanalyzer (Foss Electric, Hillerød, Denmark). Gross energy was determined with an IKA-C 400 bomb calorimeter (IKA Werke, Janke & Knunkel, Staufen, Germany). Starch plus free sugars were measured according to procedures described by Christensen (1980) . The concentration of starch and free sugars was not determined in feces. Chromic oxide was measured using the method of Schürch et al. (1950) . Fat was extracted with diethyl ether after acid hydrolysis (Stoldt 1952 ). Determination of fatty acids in Stoldt fat extract was described by Engberg et al. (1993) .

Statistical analyses.

ANOVA was performed according to a 4 x 4 Latin square following procedures described by Steel and Torrie (1980) . Where appropriate, treatment means were compared using the Student-Newman-Keuls multiple range test (Steel and Torrie 1980 ). Treatment means were considered statistically different at P < 0.05. The calculations were performed with a statistical computer program (SAS/STAT Version 6.10; SAS Institute, Cary, NC).

	RESULTS

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The pigs remained healthy and consumed their meal allowances throughout each experiment. Postmorten examinations, performed at the conclusion of the experiment, revealed no intestinal adhesions or other abnormalitites.

The gross energy concentration of the fish, rapeseed and coconut oil diets were similar; however, due to the lower fat concentration (39 g/kg diet), the gross energy concentration of the basal diet was over 3 MJ/kg lower than the other diets, which had fat concentrations of 189 to 192 g/kg diet (Table 1) .

The fatty acid composition of the four diets varied considerably. The coconut oil diet contained a large amount of short-chain fatty acids (8:0, 10:0, 12:0 and 14:0), which contributed more than half of total fatty acids to the coconut oil diet. The rapeseed oil diet primarily contained medium-chain unsaturated fatty acids [18:1, 18:2 and 18:3 (n-3)]. The double low rapeseed oil used in this study contained less than half a percentage of erucic acid [22:1(n-9)], which has been greatly reduced through rapeseed breeding programs in Denmark. The fish oil diet contained a relatively high amount of long-chain PUFA [20:5(n-3) and 22:6(n-3)]. The fish oil diet also contained a large amount of 16:0 (151 g/kg fatty acids) and 18:1 (210 g/kg fatty acids). In addition, the fish oil diet contained large amounts of other fatty acids (201 g/kg fatty acids) which included 18:4(n-6), 22:1(n-11) and 20:1(n-9). The fatty acid composition of the basal diet was very similar to the fish oil diet, due to the fact that most of the dietary fat in the basal diet was supplied by fish meal.

The apparent ileal digestibilities of energy, dry matter and protein were not affected by the inclusion of fish oil, rapeseed oil or coconut oil in the diets (Table 2 ). Starch digestion was nearly complete by the end of the small intestine (>99.6%). Fat digestibility was not affected by the supplemented source of oil, and fat digestion was almost complete at the terminal ileum. Fat digestibility was higher (P < 0.05) in the diets supplemented with oil than in the basal diet. Furthermore, experimental period did not affect the ileal digestibilities of nutrients or energy.

Apparent fecal digestibility of fat was higher (P < 0.05) in the fish oil and rapeseed oil diets than in the basal diet (Table 3 ). In addition, experimental period did not affect the fecal digestibilities of nutrients or energy. The lowest digestibilities of 14:0 and 16:0 were observed when pigs were fed the coconut oil diet. Negative digestibilities, lowest –205.6%, were observed for 18:0 due to the low level in the diet, and the most negative values were observed when pigs were fed the basal diet. Fecal digestion of 18:1 and 18:2 was almost complete when pigs were fed the fish oil and rapeseed oil diets, and the digestibilities were higher (P < 0.05) than observed in the basal and coconut oil diets. Pigs fed the coconut oil diet had the lowest (P < 0.05) digestibility of 18:3. Fecal digestibilities of the long-chain fatty acids were very high (>91.6%). The long-chain fatty acid 20:5 was completely digested in all of the diets. In contrast, the digestibility of 22:6 was lower, and the lowest digestibility was determined when the pigs were fed the rapeseed oil diet.

The intake of saturated fatty acids differed among the experimental diets (Table 4 ). Pigs had the highest (P < 0.05) intake of saturated fatty acids (225.8 g/d) and the largest (P < 0.05) ileal flow (13.6 g/d) and fecal flow (25.1 g/d) of fatty acids when they consumed the coconut oil diet. When pigs were fed the basal diet, they had the lowest (P < 0.05) intake of saturated fatty acids, the lowest (P < 0.05) ileal flow of saturated fatty acids and the lowest (P < 0.05) fecal output of saturated fatty acids. In contrast, for monounsaturated fatty acids, pigs fed the rapeseed oil diet had the highest (P < 0.05) intake of monounsaturated fatty acids (180.1 g/d) and the highest (P < 0.05) ileal flow (10.3 g/d) of monounsaturated fatty acids. In addition, when pigs were fed the rapeseed oil diet, they had the highest (P < 0.05) intake of PUFA (103.1 g/d). The ileal flow of PUFA was higher (P < 0.05) when pigs were fed the rapeseed oil diet than when they were fed the basal diet or the coconut oil diet. However, the highest (P < 0.05) fecal flow of PUFA (2.3 g/d) was observed when pigs were fed the fish oil diet.

	DISCUSSION

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The dietary level of fat has been shown to affect the digestibility of amino acids (Li and Sauer 1994 ), and we hypothesized that there may be differences in protein digestibility between the basal diet and the diets with added fat or an effect of differences in fatty acid composition on protein digestion. In weaned pigs, different fat sources have been shown to have an effect on nutrient digestibility (Cera et al. 1989 ); however, the differences observed between fat sources decrease with age (Cera et al. 1989 ).

There was also no difference between the ileal and fecal digestibility of fat (Tables 2 and 3) ; when numerically compared, the maximal difference between the digestibilities was negative three percentage units which was observed in pigs fed the coconut oil diet. The next highest difference, 2.3 percentage units, was for pigs fed the rapeseed oil diet. The pigs fed the coconut oil diet were the only ones in which there was a net appearance or synthesis of fat in the cecum and large intestine. These findings are in agreement with previous results presented by Jørgensen et al. (1992) , suggesting essentially no net disappearance of long-chain fatty acids during transit of digesta through the cecum-colon.

However, there were differences in the ileal digestibilities of individual fatty acids and in the digestibilities of classes of fatty acids (Table 2) . Similar to the ileal digestibilities of fat, the ileal digestibilities of individual fatty acids were relatively high, indicating that most of the fat in the diets was digested and absorbed. However, observed digestibilities were largely affected by the concentration of individual fatty acids in ileal digesta, relative to the levels occurring in the diets. The low and negative digestibilities for 18:0 were likely due to the very low levels of 18:0 in the diets (Table 1) , and therefore the endogenous secretion of 18:0 decreased the apparent digestibility (Jørgensen et al. 1992 , 1993 ). The digestibility of 18:0 was much lower than determined in diets supplemented with animal fat (Jørgensen et al. 1992 ). The low and negative fatty acid digestibilities are not a reflection of analytical recovery and (or) mathematical errors, they are a result of having a lower fatty acid intake (level in the diet).

The apparent digestibility of fatty acids is influenced by both dietary fat (fatty acid level), the extent to which triacylglycerols are hydrolyzed (differences in the digestion of different sources of fat) and by the level of endogenous fatty acids. All of these factors must be taken into consideration when apparent digestibilities are used as opposed to true digestibilities. At low levels of fat intake, the amount of endogenous fatty acids present in ileal digesta can have a larger impact on apparent digestibilities than when higher levels of fat are fed (Jørgensen et al., 1992 and 1993 ). The lower the level in the diet, the less undigested fat there will be in ileal digesta and there will be proportionally more endogenous fat (fatty acids). Apparent ileal fatty acid digestibility measurements become more indicative of differences in fatty acid release (there is less influence of endogenous fatty acids) when a higher level of fat (fatty acids) is fed (Jørgensen et al., 1992 and 1993 ).

The highest ileal digestibilities for 18:1 and 18:3 (n-3) were observed when pigs were fed the fish oil and rapeseed oil diets. These high digestibilities were due in part to the high levels of 18:1 and 18:3 (n-3) in the fish oil and rapeseed oil diets. The highest digestibility of 18:2 was observed when pigs were fed the rapeseed oil diet which had the highest level of 18:2. The very high ileal digestibilities of the long-chain fatty acids indicated that they were almost completely digested.

The high ileal digestibility of PUFA determined when pigs were fed the rapeseed oil diet was most likely due to the high content of 18:2 and 18:3 (n-3) (Table 1) in rapeseed oil. The digestibility of the sum of fatty acids was higher than the digestibility of fat, suggesting that other lipids have a lower digestibility. Due to the very high ileal digestibilities of fat and fatty acids (Table 2) , the statistical differences are not likely biologically relevant. However, there is limited information on ileal fatty acid digestibilities in dietary fat sources and therefore, the digestibility values are very useful and this is why the experiment was conducted.

The digestibilities of fat observed in this study (Table 3) are similar to those reported by Jørgensen et al. (1992 ), 1996 for pigs fed diets containing a similar level of animal fat or rapeseed oil.

We determined fecal digestibilities to investigate how fat supplementation affects digestion and fermentation in the cecum and colon. There were no differences in the digestibilities of energy and protein, and the digestibilities were high, suggesting that the supplemented fats did not greatly affect digestion.

The diets fed in this study were formulated to have exactly the same composition as the diets fed in our previous study concerning the effect of dietary fat source on exocrine pancreatic secretion in growing pigs (Gabert et al. 1996 ). The fecal digestibilities of energy, dry matter, protein and fat determined in this study (Table 3) were slightly higher than fecal digestibilities measured in growing pigs surgically fitted with a pancreatic pouch re-entrant cannula (pouch method) or a catheter in the pancreatic duct (catheter method). The pigs in this study were under a similar feeding regimen and had a similar genetic background compared those used in our previous study (Gabert et al. 1996 ). This qualitative comparison, which has not been made before, may suggest that there was an effect of surgical intervention on digestion. However, before a definitive statement is made, more research is warranted which involves making a comparison within the same study, under the same conditions. Within the study, we did not observe differences in digestibility when animals were prepared for collection of pancreatic juice with the pouch or the catheter method (Gabert et al. 1996 ).

Biohydrogenation of fatty acids has been shown to occur in the cecum and colon in the pig (Bayley and Lewis 1965 , Carlson and Bayley 1968 , Jørgensen et al. 1992 ); therefore, fecal fatty acid digestibilities can be altered by the modifying and equalizing effects of the microflora in the hindgut (Sauer and Ozimek 1986 ). The negative three percentage unit difference between the fecal digestibility of fat (88.4%) and the ileal digestibility of fat (91.4%) when pigs were fed the coconut oil diet was likely due to the hydrogenation of mono- and PUFA by the microflora in the cecum and colon. Therefore, fecal fatty acid digestibilities are not reflective of ileal digestibilities. Compared to the ileal digestibilities of 18:0, the fecal digestibilities were highly negative, suggesting that additional 18:0 was synthesized by hydrogenation of mono- and polyunsaturated 18 carbon fatty acids. For 18:1, 18:2 and 18:3 (n-3), the fecal digestibilities were numerically higher than the corresponding ileal digestibilities (Tables 2 and 3) , which was likely a result of biohydrogenation of these fatty acids. There may also have been some degradation of fatty acids in the cecum and colon.

Biohydrogenation likely occurred for the long-chain fatty acid 20:5(n-3), fecal digestibilities (Table 3) suggest that the digestion of this fatty acid was essentially complete. However, this was not the case for 22:6(n-3); fecal digestibilities were lower than ileal digestibilities, suggesting that there may have been a net appearance of 22:6(n-3) in the cecum and large intestine.

The daily flow of fatty acids in ileal digesta was influenced by the fatty acid composition of the oils supplemented to the diets. When pigs were fed the coconut oil diet, as expected, they had the highest daily intake of saturated fatty acids which likely caused them to have the highest ileal flow of saturated fatty acids. The high fecal flow, which may have been due in part to the high ileal flow, was also a result of the biohydrogenation of mono- and PUFA. However, when pigs were fed all diets, the amount of saturated fatty acids excreted in feces was approximately twice the amount flowing into the cecum and colon (Table 4) . Although the disappearance of mono- and PUFA in the cecum and colon was high, it exceeded the increased amount of saturated fatty acids in feces of pigs when fed the basal, fish oil or rapeseed oil diets, which suggests that there were modifications in fatty acid chain length. The disappearance of mono- and PUFA in the cecum and colon of pigs when they consumed the coconut oil diet was 8.9 g/d less than the appearance of saturated fatty acids in the cecum and colon, indicating that synthesis of saturated fatty acids exceeded biohydrogenation. As a result of the high level of medium-chain mono- and PUFA in rapeseed oil, pigs fed the rapeseed oil diet had the highest intake and ileal flow of mono- and PUFA, respectively.

The present study suggests that type of fat (fish oil, rapeseed oil or coconut oil) included in the diet at a level of 150 g/kg diet does not affect fat, energy or protein digestibilities in growing pigs when measured at the terminal ileum or in feces. The supplemented fat sources were very digestible; ileal digestibilities exceeded 90%. The ileal analysis method should be used to determine the digestibilities of individual fatty acids because biohydrogenation occurs in the cecum and colon. The individual digestibilities of fatty acids, determined in ileal digesta, were usually high; however, the digestibilities were influenced by the dietary level of the fatty acid. If the concentration of a fatty acid in the diet is low, the measured digestibility will be low due to the influence of endogenous fat. The disappearance of mono- and PUFA in the cecum and colon and the net synthesis of saturated fatty acids in the cecum and colon do not fully account for the changes in the flow of fatty acids through the cecum and colon.

	ACKNOWLEDGMENTS

 
The authors thank Karl H. Jakobsen, Peter Sørensen, Benny Thomasen, Morten Smed and Liselotte Skovløkke for their technical assistance.

	FOOTNOTES

 
¹ Presented in part at the 47^th annual meeting of the Canadian Society of Animal Science, July 1997, McGill University, Montreal, Canada [Gabert, V. M., Jørgensen, H., Jensen, M. S. & Jensen, S. K. (1997) Apparent ileal fatty acid and tocopherol digestibilities determined in growing pigs fed diets containing fish oil, rapeseed oil or coconut oil (abs., p. 229)].

² Financial support was provided by the Danish Agricultural and Veterinary Research Council.

Manuscript received May 17, 1999. Initial review completed July 15, 1999. Revision accepted December 14, 1999.

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